Beasts of The Earth Animals, Humans, and Disease

= Beasts OF THE Earth
ALSO BY E. FULLER TORREY
Surviving Manic-Depression (2002, senior author)

The Invisible Plague: The Rise of Mental Illness from 1750 to the Present
(2002, senior author)
Out of the Shadows: Confronting America’s Mental Illness Crisis (1997)
Schizophrenia and Manic-Depressive Disorder (1994, senior author)
Freudian Fraud (1992)
Criminalizing the Seriously Mentally Ill (1992, senior author)
Frontier Justice: The Rise and Fall of the Loomis Gang (1992)
Nowhere To Go: The Tragic Odyssey of the Homeless Mentally Ill (1988)
Care of the Seriously Mentally Ill (1986, 1988, 1990, senior author)
Surviving Schizophrenia: A Family Manual (1983, 1988, 1995, 2001)
The Roots of Treason: Ezra Pound and the Secret of St. Elizabeths (1983)
Schizophrenia and Civilization (1980)
Why Did You Do That? (1975)
The Death of Psychiatry (1974)
Witchdoctors and Psychiatrists (1972, 1986)
Ethical Issues in Medicine (1968, editor)
Beasts
=
Earth
OF
THE
Animals, Humans, and Disease
E. Fuller Torrey, M.D.

Robert H. Yolken, M.D.
Rutgers University Press

New Brunswick, New Jersey, and London
Library of Congress Cataloging-in-Publication Data
Torrey, E. Fuller (Edwin Fuller), 1937–

Beasts of the earth : animals, humans, and disease / E. Fuller Torrey, Robert H. Yolken.
p. ; cm.
Includes bibliographical references and index.
ISBN 0-8135-3571-9 (hardcover : alk. paper)
1. Zoonoses—Popular works.
[DNLM: 1. Zoonoses—Popular Works. 2. Disease Outbreaks—Popular
Works. 3. Disease Transmission—Popular Works. WC 950 T694b 2005] I. Yolken,
Robert H. II. Title.
RA639.T676 2005
616.9'59—dc22
2004011751
A British Cataloging-in-Publication record for this book is available from the British Library
Copyright © 2005 by E. Fuller Torrey, M.D., and Robert H. Yolken, M.D.
All rights reserved
No part of this book may be reproduced or utilized in any form or by any means, electronic
or mechanical, or by any information storage and retrieval system, without written permis-
sion from the publisher. Please contact Rutgers University Press, 100 Joyce Kilmer Avenue,
Piscataway, NJ 08854 – 8099. The only exception to this prohibition is “fair use” as defined
by U.S. copyright law.
Design by John Romer
Manufactured in the United States of America

To our wives, Barbara and Faith
And God made the beasts of the earth according to their
kinds and the cattle according to their kinds, and everything
that creeps upon the ground according to its kind. And God
saw that it was good.
GENESIS 1 : 24 –25
And I saw, and behold, a pale horse, and its rider’s name was
Death, and Hades followed him; and they were given power
over a fourth of the earth, to kill with sword and with famine
and with pestilence and by wild beasts of the earth.
REVELATION 6 : 8
Contents
Acknowledgments ix
Introduction xi
1 The Smallest Passengers on Noah’s Ark 1
2 Heirloom Infections: Microbes before the
Advent of Humans 14
3 Humans as Hunters: Animal Origins of
Bioterrorism 23
4 Humans as Farmers: Microbes Move into the
Home 33
5 Humans as Villagers: Microbes in the Promised
Land 48
6 Humans as Traders: Microbes Get Passports 56
7 Humans as Pet Keepers: Microbes Move into
the Bedroom 68
8 Humans as Diners: Mad Cows and Sane Chickens 97
9 Microbes from the Modern Food Chain: Lessons from
SARS, Influenza, and Bird Flu 112
10 The Coming Plagues: Lessons from AIDS, West Nile
Virus, and Lyme Disease 124
11 A Four-footed View of History 139
= vii
viii = Contents
Notes 145
Glossary 171
Appendix 173
Index 175
Acknowledgments
We are grateful to the following for helping to make this book possible:
Museo del Prado, Madrid, for permission to use a detail of
Bosch’s Garden of Earthly Delights for the cover.
Mr. Jordi Masia for arranging a visit to the remarkable Al-
tamira caves, which helped us understand the relationship
between Paleolithic people and animals.
Barbara Torrey and Dr. Robert Taylor for insightful and
constructive comments on the manuscript.
Judy Miller for superb editing, organization, attention to
detail, and the index.
Adi Hovav and Audra Wolfe at Rutgers University Press for
their belief in the book during its conception and for mid-
wifing its birth, Marilyn Campbell and Nicole Manganaro
for excellent technical support, and Bobbe Needham for
carefully copyediting the newborn manuscript.
= ix
Introduction
T his book is about human infectious diseases and the microbes that cause
them. As the recent resurgence of AIDS, tuberculosis, and influenza has
shown, infections are still major causes of illness and death in our society. We
are also discovering that infectious agents may play a role in many chronic
ailments such as cancer, heart disease, and schizophrenia. The microbes that
cause infectious diseases are thus very much part of our daily lives.
The vast majority of these microbes has been, and continues to be, trans-
mitted to humans from other animals. A few diseases, heirloom infections
such as those caused by herpes and hepatitis viruses, first infected our primate
ancestors, and their microbes descended through early hominids to Homo
sapiens. A large number of diseases, such as measles and tuberculosis, resulted
from microbes transmitted to humans following the domestication of animals.
Many other diseases, such as AIDS, SARS, mad cow disease, monkeypox, and
bird flu have been transmitted from animals to humans in recent years as the
relationship between animals and humans has changed. Each change in this
relationship is accompanied by a risk of additional animal microbes being
transmitted to humans.
We have become accustomed to thinking of animals as our friends, not
as sources of human disease. Through the influence of Aesop, the Brothers
Grimm, Beatrix Potter, and Walt Disney, it has become increasingly difficult
to appreciate that the animal represented by Donald Duck was the origin of
an influenza pandemic that killed twenty million people, that Mickey Mouse
may be spreading deadly hantavirus, that Clarabelle Cow is the source of pri-
ons that cause mad cow disease, and that Pluto may be carrying leishmaniasis.
We do not associate Bambi with Lyme disease, Big Bird with West Nile virus,
Rocky Raccoon with rabies, or Garfield with toxoplasmosis. Even Barney, the
dinosaur beloved of small children, is almost certainly a carrier of Salmonella
bacteria, as all reptiles are.
In the past two hundred years, we have entered another period in which
= xi
xii = Beasts of the Earth
the relationship between animals and humans is changing in important ways.

The changes include our personal relationship to animals as pets and ways of
processing animals for our food supply. The present period of changing ani-
mal-human relationships may represent the most profound alteration in this
relationship since animals were domesticated ten thousand years ago. One of
the consequences of this changing relationship has been the emergence of
new diseases that are transmitted to humans from animals.
Concurrent with the changing animal-human relationship have been
changes in technology and in ways humans interact with each other. Chang-
ing sexual mores, the use of injections, increased urbanization, and increased
access to air travel and other forms of transportation may all promote the
spread of microbes from person to person. These changes magnify the effects
of transmission of microbes from animals to humans, making it more likely
that an infection of a single individual will become perpetuated as a chain of
human infections.
It is important to appreciate the complexity of the animal-human rela-
tionship. On the one hand, animals have fulfilled many important human
material and, as we have discovered more recently, psychological needs. On
the other hand, animals have also been the source of many of the most impor-
tant human diseases. These are the two sides of the beasts of the earth.
= Beasts OF THE Earth
1=
C H A P T E R
The Smallest Passengers

on Noah’s Ark
So, naturalists observe, a flea
Has smaller fleas that on him prey;
And these have smaller still to bite ’em;
And so proceed ad infinitum.
Jonathan Swift, 1733
H uman diseases that are transmitted from animals are big news. Consider,
for example, the following items reported in the United States during a
single month, June 2003: 79 cases of human monkeypox, spread by pet prairie
dogs; 7 cases of SARS (severe acute respiratory syndrome) among the 8,398
cases worldwide, spread by palm civets or other animals; the season’s first hu-
man case of West Nile virus disease, spread from birds by mosquitoes; the sea-
son’s first human case of Eastern equine encephalitis, spread from horses and
other animals by mosquitoes; the first case of hantavirus infection, spread by
mice and other rodents, in which two members of one family were infected;
2,820 new cases of Lyme disease, spread from deer by ticks, for the first half of
the year; 19,482 new cases of AIDS, originally spread from primates, for the
first half of the year; and a report of the first cow in North America infected
with bovine spongiform encephalopathy (mad cow disease), which causes an
almost invariably fatal disease when transmitted to humans.1
All of these are animal-associated diseases, caused by microbes, that may
affect humans. In medical terms, they are called zoonoses. (Terms that may
be new to readers are listed in the glossary.) Numerous news stories in recent
years about such diseases have questioned whether zoonoses are becoming
more numerous. The Washington Post, for example, published a front-page
story on June 15, 2003, under the headline “Infections Now More Wide-
spread: Animals Passing Them to Humans.” Is there evidence to support an
= 1
2 = Beasts of the Earth
increasing incidence of animal-associated human diseases? As we shall see,

there is.
In reading such news items, it is difficult to remember that humans are a
relatively inconsequential part of the interaction between microbes and ani-
mals. Theologically, humans are said to be created in the image of God, but
biologically we are merely one species in class Mammalia, phylum Craniata.
There are 4,500 other species of mammals, encompassing everything from
aardvarks, bats, cats, and rats to zebras, and including other primates. Anthro-
pocentrally, we consider humans the most important animal species, yet all
mammalian species combined constitute less than one-tenth of 1 percent of
the estimated thirty million living animal species.2 From the point of view of a
microbe looking for an animal to parasitize, humans are at best an incidental
hors d’oeuvre at a microbe’s feast of life.
Where Do Microbes Come From?

The key to understanding animal-associated diseases is to understand mi-
crobes, referred to scientifically as microorganisms. They can be divided
into microparasites, consisting of bacteria, viruses, fungi, and protozoa, and
macroparasites, which include such organisms as helminths and tapeworms;
macroparasites are comparatively unimportant as causes of serious human
diseases. Prions, a newly discovered and poorly understood type of protein,
will be discussed in chapter 8.
Stephen Jay Gould said bacteria are “the dominant form of life on
Earth—and always have been, and probably always will be.” 3 There are esti-
mated to be between three hundred thousand and one million different spe-
cies.4 Ancestors of modern bacteria were the first form of life on earth, ap-
pearing approximately 3.5 billion years ago. (See the appendix for a time line
of the evolution of life.) They are so primitive that bacterial cells do not even
have nuclei; the genes simply float in the cells’ cytoplasm and come together
when the bacteria divide. Bacteria are also remarkably hardy, as was recently
illustrated by the reported revival of bacteria that had lain quiescent in a salt
crystal for 250 million years.5
Bacteria had existed for more than two billion years when other life forms
came into being, and bacteria immediately colonized them. When fungi,
plants, and animals emerged one billion years ago; when animal life diver-
sified in the Cambrian explosion 570 million years ago; when land plants
appeared 425 million years ago; when reptiles appeared 300 million years
ago; when dinosaurs appeared and the continents drifted apart 200 million
years ago; when mammals appeared 155 million years ago; when primates
T h e S m a l l e s t Pa s s e n g e r s o n N o a h ’s A r k = 3
appeared 60 million years ago; when hominids separated from primates

6 million years ago; and when anatomically modern Homo sapiens emerged
130,000 years ago, bacteria were already ancient, adapted, and ready to take
possession of these newly emerging life forms.
And take possession they did. The human mouth and large intestine
each contain an estimated four hundred different species of bacteria. The
total number of bacteria in the human large intestine has been estimated to be
between one and ten trillion bacteria per milliliter.6 Bacteria are also found in
the human eye, ear, nose, stomach, small intestine, and genital tract and on
the skin. It has been said that we have ten times as many bacteria as human
cells in our bodies,7 and that the bacteria account for a significant amount
of the body weight.8 Studies have shown that, although newborn infants are
usually free from bacteria at birth, they are almost immediately colonized
by bacteria and show the same distribution of normal flora as adults within
a few weeks of birth.9 All animals are similarly colonized, and all are carriers
of bacteria.
Another measure of the importance of bacteria is that they have in-
corporated themselves into the genome of humans and other animals. This
revelation was a surprising offshoot of the human genome sequencing pro-
ject, in which it was reported “that between 113 and 223 genes have been
transferred from bacteria to humans (or to one of our vertebrate ancestors)
over the course of evolution.” 10 Although subsequent analysis suggested that
the actual number of transferred bacterial genes may be lower, that such trans-
fers have occurred at all has led to a new appreciation of the importance of
bacteria for humans and a reanalysis of the human relationship to bacterial
ancestors. Many scientists suspect that the mitochondria found in all mam-
malian cells may also have originally come from bacteria that infected cells
of our ancestors.
In contrast to those of bacteria, the origins and functions of viruses are
poorly understood. A virus is not a living cell but merely one or two strands
of DNA or RNA surrounded by a protein or lipoprotein coat, and it can re-
produce itself only by getting into a living cell. Some researchers believe that
viruses are degenerate forms of ancient bacteria, perhaps originally derived
from plants. Others contend that viruses are pieces of animal genes that es-
caped from their cells, a kind of “rebel human DNA.” A British astronomer
has even suggested that viruses fell to earth from outer space.11
What is clear is that viruses are ubiquitous and have a complex and inti-
mate relationship with humans and other animals. There are more than five
thousand species of viruses known, and all of them, especially the RNA type,
are unstable, undergo constant mutations, and are able to integrate their ge-
netic material into other cells. Lewis Thomas, in his lyrical work The Lives of
a Cell, described viruses as “more like mobile genes”: “We live in a dancing
matrix of viruses; they dart, rather like bees, from organism to organism, . . .
tugging along pieces of this genome, strings of genes, . . . passing around he-
redity as though at a great party.” 12 At least one type of RNA viruses, the en-
dogenous (internal) retroviruses, not only can integrate themselves into the
human genome but may also be passed on from generation to generation, just
as inherited genes are (see chapter 2).
The third important type of microbe is protozoa. In popular parlance,
bacteria, viruses, and protozoa together are called germs. Protozoa are also
commonly referred to as parasites, although this is simply linguistic conven-
tion, since many bacteria and viruses are also parasites but are not referred
to as such. Protozoa evolved from bacteria approximately two billion years
ago. Like bacteria, protozoa are one-celled organisms, but unlike bacteria,
they are more complex and have nuclei and other intracellular components
such as mitochondria. Since they are very ancient, protozoa, like bacteria,
also colonized other forms of life as these emerged, including humans and
other animals.
That humans and other animals have been heavily colonized with bac-
teria, viruses, and protozoa since the beginning of our existence has been
known for more than a century. American humorist Mark Twain, in an essay
that he instructed not be published until after his death, wrote a satire about
microbes on Noah’s ark:
Noah and his family . . . were saved, yes, but they were not comfortable,
for they were full of microbes. Full to the eyebrows; fat with them, obese
with them; distended like balloons. It was a disagreeable condition, but
it could not be helped, because enough microbes had to be saved to sup-
ply the future races of men with desolating diseases, and there were but
eight people on board to serve as hotels for them. . . . There were typhoid
germs, and cholera germs, and hydrophobia germs, and lockjaw germs,
and consumption germs, and black-plague germs, and some hundreds
of other aristocrats, specially precious creations, golden bearers of God’s
love to man. . . . The great intestine was the favorite resort. There they
gathered, by countless billions, and worked, and fed, and squirmed, and
sang hymns of praise and thanksgiving; and at night when it was quiet
you could hear the soft murmur of it. The large intestine was in effect
their heaven.13
The fact that microbes cause human disease is thus not new. This discovery of
the microbe-human disease relationship has been called “one of the greatest
achievements of all time.” 14 What is new is an increasing appreciation of the
fact that many, if not most, of these microbes were originally transmitted to hu-
mans from other animals. And that this transmission is continuing to occur.
How Microbes Get Ahead in Life

All living organisms undergo continuous evolution, a process that is inherent
in life itself. This is clearly visible for simpler forms of life, such as bacteria,
viruses, and protozoa, which evolve more rapidly than complex forms of life
such as mammals. But all living things evolve, as noted by Hans Zinsser in his
classic Rats, Lice, and History: “Nothing in the world of living things is per-
manently fixed. Evolution is continuous, though its progress is so slow that the
changes it produces can be perceived only in the determinable relationship of
existing forms, and in their paleontological and embryological histories.” 15
One of the most common ways in which microbes evolve is by invading
tissues of animals, including humans. In doing so, microbes are placed in a
situation where they must evolve or die. Infectious diseases of animals and hu-
mans, therefore, are merely manifestations of microbes trying to get ahead in
life. As Jared Diamond noted in Guns, Germs, and Steel: “Diseases represent
evolution in progress, and microbes adapt by natural selection to new hosts
and vectors. . . . In that new environment, a microbe must evolve new ways to
live and to propagate itself.” 16
Humans and other animals, from a microbe’s point of view, are merely
vessels that are useful for reproducing and evolving. If a human or other ani-
mal becomes diseased as part of that process, the disease is incidental, that is,
an epiphenomenon. It is not in the best interest of most bacteria, viruses, and
protozoa to kill their host, because if they do so they may die as well. Arno
Karlen, in Man and Microbes, described this process by noting that “the ulti-
mate adjustment between host and parasite is not murder but mutuality. . . .
Infectious disease, then, is not nature’s tantrum against humanity. Often it is
an argument in what becomes a long marriage.” 17
The outcome of this marriage, however, is not as clearly defined as it
was once thought to be. For many years, it was believed that microbes and
humans slowly learn to live with each other as microbes evolve toward a be-
nign coexistence with their hosts. Thus, the bacterium that causes syphilis
was thought to be extremely virulent when it initially spread among humans
in the sixteenth century, then to have slowly become less virulent over the fol-
lowing three centuries. This reassuring view of microbial history has recently
been challenged by Paul Ewald and others, who have questioned whether
microbes do necessarily evolve toward long-term accommodation with their
hosts. Under certain circumstances, Ewald argues: “Natural selection may . . .
favor the evolution of extreme harmfulness if the exploitation that damages
the host [i.e., disease] enhances the ability of the harmful variant to compete
with a more benign pathogen.” 18 The outcome of such a “marriage” may
thus be the murder of one spouse by the other. In eschatological terms, this
1. Heirloom Infections Heirloom infections are microbes
that were transmitted from prehistoric
animals to early primates, then to
early hominids, and eventually to
dinosaur early primate humans. Examples: human
herpesviruses, hepatitis A and B,
malaria.
early
hominid human human
2. Direct Transmission Microbe transmitted from animal to
human by direct contact by bite,
scratch, cuts in skin, inhalation of
droplets, and so on. No human-to-
human transmission. Examples:
rabies, cat-scratch disease, anthrax.
cat human
3. Indirect Transmission Microbe transmitted from animal to
human indirectly by contamination of
food or water. No human-to-human
transmission. Examples: BSE (mad
cow disease), Escherichia coli 0157
strain.
cow beefburger human
4. Vector Transmission Microbe transmitted from animal to
human via another animal, or vector.
Rare human-to-human transmission,
e.g., by blood transfusion. Examples:
Lyme disease, West Nile virus.
bird mosquito human
5. Animal to Human to Human
Microbe transmitted from animal to
human on an ongoing basis but then
also transmitted from human to
human. Examples: influenza, SARS.
duck human human
human
6. Now Human to Human Only Microbe transmitted from animal to
human in the past, but has undergone
mutations and adapted specifically to
humans. Now transmitted only person
cow human human to person. Examples: measles, AIDS,
typhoid fever.
human
Figure 1-1: Types of Animal-to-Human Transmission of Microbes

view argues that a microbe such as HIV or SARS virus may be truly capable of
eradicating the human race.
Microbes are remarkably resourceful in finding ways to move from ani-
mals to humans. As shown in figure 1.1, the transmission of microbes from
animals to humans may occur in a variety of ways. Some transmissions from
early animals to hominids took place in the distant past, before Homo sapiens
had even evolved, and then the microbes were passed down from hominids to
humans (panel 1); these are called heirloom infections (see chapter 2). Direct
transmission occurs when animals pass microbes directly to humans (panel 2),
such as when a cat scratches a human, causing cat-scratch disease; when a dog
bites a human, causing rabies; or when a person inhales aerosolized mouse
droppings and gets hantavirus infection. Indirect transmission occurs when
there is an intermediary between the animals and the humans (panel 3), such
as when a cow becomes infected with bovine spongiform encephalopathy
(mad cow disease) and after death passes the prion to humans by way of beef-
burgers, or when an infected cow transmits the toxic strain of Escherichia coli
bacteria by way of contaminated food or water. Another mode of transmission
is when the microbe hitchhikes on another animal, called a vector, such as a
mosquito, tick, flea, or fly (panel 4). Examples of this include the West Nile
virus, which uses mosquitoes to move from birds to humans; the bacteria that
causes Lyme disease, which uses ticks to move from deer to humans; and
the plague bacteria, which uses fleas to move from rats to humans. Whatever
mode of transportation the microbe chooses, the objective is always the same:
Be fruitful and multiply.
When animal microbes are transmitted to humans for the first time, most
of the microbes either die or pass harmlessly through our bodies without our
being aware of them. A few microbes cause infections in humans that may
result in symptoms of illness or even in death. In most such cases, the microbe
cannot be passed from human to human, as illustrated in the examples in pan-
els 2, 3, and 4 in figure 1.1. Occasionally, however, the microbe adapts itself
to humans, usually by undergoing minor changes in its genetic makeup called
mutations, and is then able to spread from human to human (panel 5). Trans-
mission of the microbe from animal to human continues to take place, but
human-to-human transmission also occurs; influenza and SARS are examples.
Finally, in a few cases, after the microbe has been adapted to humans
for a long period of time, it changes its genetic makeup so much that it is
no longer transmitted from animals to humans but only from humans to hu-
mans (panel 6). Examples are measles, which originally was transmitted to
humans from cattle; AIDS, which was originally transmitted from primates;
and typhoid fever, which was originally transmitted from birds. This type of
animal-to-human transmission differs from an heirloom infection in that the
original transmission occurred after Homo sapiens had evolved, that is, within
the past 130,000 years.
Being resourceful, many microbes have developed multiple modes of
transmission. The protozoa that causes sleeping sickness (trypanosomiasis),
for example, is transmitted among horses as a venereal disease, among hu-
mans by using flies as a vector, and among rats by using fleas as a vector.19 In
the course of evolving, microbes often develop new methods of moving from
one animal to another. A recent example of this is the virus that causes SARS,
which apparently found ways to move from palm civets or other animals to
humans and then from human to human.
All microbes are continuously trying to spread themselves, crossing both
geographic and species barriers. Humans are therefore subjected to a con-
tinuing barrage of bacteria, viruses, and protozoa coming from other animals.
Given this continuous exposure, it is remarkable that we do not suffer more
than we do from animal-associated diseases.
There are three major determinants that influence the outcome of en-
counters between a microbe and a potentially new host such as a human:
genes, the immune system, and the virulence of the microbe. Genetic expres-
sion varies from person to person and plays an important role in determining
whether or not a microbe will cause illness. For example, half the people in the
world are infected with the bacteria Helicobacter pylori. However, the bacteria
causes disease, such as gastric ulcers or stomach cancer, in fewer than one in
five of the Helicobacter carriers. One factor that determines whether the bac-
teria will cause disease is whether the person has certain genes (specifically
the babA2, cagA, or vacA genotypes).20 Having these genes does not guarantee
that Helicobacter will cause disease, but it increases the odds that it will. Such
genes are called predisposing genes, and there are probably dozens, or even
hundreds, of such genes for all human diseases that are caused by microbes.
Another example is Mycobacterium tuberculosis, which infects large num-
bers of individuals. However, only one out of ten people infected with this
bacteria develops tuberculosis. It is now known that carrying certain genes,
such as NRAMP-1 or a specific type of vitamin D receptor (VDR) gene, pre-
disposes a person to develop clinical tuberculosis.21
Genes may predispose individuals to diseases caused by microbes, but
they may also be protective. The best-known example of this is the protec-
tion provided against malaria by the gene associated with sickle-cell disease.
Individuals who carry the sickle hemoglobin gene are more resistant to infec-
tion by Plasmodium falciparum, protozoa that cause the most severe form of
malaria. Another example of a protective gene is PTR-1, a gene that limits the
damage induced by protozoa that causes leishmaniasis, a disease spread by
dogs (see chapter 7).22
Many of the genes that predispose or protect an individual in encounters

with microbes do so by affecting the person’s immune system, the second
determinant of the outcome. This is an extraordinarily complex system that
consists of lymphocytes and other white blood cells, cytokines, and antibodies
against microbes. Anything that weakens the immune system makes a per-
son more susceptible to infection; conversely, anything that strengthens the
system makes a person more resistant. The former is illustrated by individu-
als with AIDS who become increasingly susceptible to all infections as their
lymphocytes become fewer in number.
The third major determinant that influences the outcome of encounters
between microbes and potentially new hosts is the strength, or virulence, of
the microbe. Bacteria, viruses, and protozoa all have strains that are more
lethal or less lethal; this variation is commonly called virulence. A well-known
example of this is the influenza virus: Some strains cause only a mild illness;
other strains, such as the one that caused the 1918 influenza pandemic, are
highly lethal.
Occasionally, different kinds of microbes join forces to cause disease. In
mice, for example, the mouse hepatitis virus is harmless by itself, and the
protozoan Eperythrozoon coccoides is harmless by itself, but when they infect
mice together, the mice develop severe hepatitis and die.23 Such co-infections
are also known to occur in humans; for example, the hepatitis D virus is harm-
less by itself but can cause severe disease when the person is also infected with
the hepatitis B virus.
Encounters between microbes and their potential hosts thus resemble
battle scenes from Star Wars. The outcome of such battles depends in part
on the numbers and strength (virulence) of the invading microbes and in
part on the strength of the defensive forces (genes that afford resistance) and
its special weapons (the immune system). Traitors within the defensive forces
(predisposing genes) may tip the scales in favor of the invaders. Cells of the
immune system may also act as Trojan horses, carrying microbes to previously
uninfected parts of the body. These battles occur continuously in humans and
in all other animals.
As humans, it is understandable that we focus attention on the effects
of microbes on ourselves. However, it is important to keep in mind that mi-
crobes similarly affect all other animal species, sometimes with catastrophic
results. An example was the rinderpest virus epidemic among African animals
in the closing years of the nineteenth century. The virus, which was endemic
among cattle in India, was brought to Africa for the first time in 1889, when
the Italian army imported cattle from India to feed its troops in Ethiopia and
Somalia. Rinderpest quickly infected African domestic cattle, sweeping across
the continent within seven years and virtually wiping them out in many areas.
Since cattle were the main source of food for African groups such as the Ma-
sai, widespread human famine followed. As one Masai man described the epi-
demic, the corpses of cattle and people were “so many and so close together
that the vultures had forgotten how to fly.” 24 The rinderpest epidemic also
spread to wild animals related to cattle, causing especially widespread mortal-
ity among buffalo, wildebeests, giraffes, bushpigs, eland, and kudu.
The African rinderpest epidemic was an example of the spread of a mi-
crobe from one animal to another of the same species (Indian to African
cattle) and to other species in the same animal order (cattle, buffalo, wilde-
beests, etc., all of which are artiodactyls). A more recent example of such an
epidemic was the death of at least 30 percent of North Sea grey seals by the
phocine distemper virus. This virus had been endemic among harp seals in
the Arctic region, but the harp seals migrated to the North Sea after commer-
cial overfishing depleted Arctic fish stocks.25
Less commonly, microbes may spread from one species to a species in a
different animal order. An example of this was the spread to seals of canine
distemper virus, which was endemic among dogs. Dogs are members of the
carnivore order of mammals, while seals are members of the pinniped order.
The canine distemper virus is thought to have been introduced to Antarctic
seals by contact with infected sled dogs used on Antarctic explorations.26 Ca-
nine distemper virus also caused a devastating epidemic among seals in the
Caspian Sea. The origin of the virus became clear when it was learned that
people who lived nearby had thrown dogs that had died from a local outbreak
of canine distemper into the sea, where they were eaten by the seals.27 Another
carnivore-to-pinniped transmission (cat to sea otter) recently occurred along
the northern California coast. The protozoan Toxoplasma gondii, excreted by
cats, washed into the sea with groundwater runoff from streams that drained an
area with large numbers of cats, with the resultant death of many sea otters.28
As a general rule, then, when microbes spread, they are most likely to
spread to other members of the same species or to members of closely re-
lated species. Thus, humans are most likely to become infected by microbes
coming from other humans, then by microbes coming from other primates,
then by microbes coming from other mammals, and so on. The more closely
related the animals, the more likely it is that microbes will be exchanged be-
tween them.
Also, as interested as we are as humans in the transmission of microbes
from other animals to ourselves, we need to keep in mind that microbes move
freely in both directions. Humans have inadvertently transmitted to primates
human microbes that cause polio, tuberculosis, malaria, and influenza, and
probably pneumonia, meningitis, and measles.29 There are also documented
instances of the spread of antibiotic-resistant staphylococcus bacteria from hu-
mans to cats, dogs, and horses, causing infections in these animals.30
At the same time that existing microbes are spreading among related and
unrelated animal species, new microbes continue to evolve. This occurs when
the genetic structure of existing microbes undergoes slight modifications. A
recent example of this was mutations of the feline panleukopenia virus (FPV),
a cat virus first described in the early twentieth century. In the 1940s, a new
viral disease of minks was noted; the cause was subsequently found to be mink
parvovirus (MPV), which was a mutation of FPV. Then, in the 1970s, a new
disease of domestic dogs was described, and its causative agent, named canine
parvovirus (CPV), was also shown to be a mutation of FPV. Genetic mapping
studies have shown that FPV, MPV, and CPV differ by changes in only a few
nucleotides.31 The FPV virus had been evolving, spreading by mutations from
one species of animal to another and causing new diseases.
How Many Human Infections

Come from Animals?
How many human infections are caused by microbes that spread from other
animals? Researchers at the University of Edinburgh recently compiled a list
of 1,415 microbes known to cause diseases in humans. Of these, 868, or 61 per-
cent, are known to be currently transmitted from other animals to humans.32
Significantly, this list did not include microbes that were transmitted from
other animals to humans in the recent past, such as the HIV virus from chim-
panzees, which probably occurred in the last fifty years, or in the more distant
past, such as the measles virus from cows, which occurred approximately ten
thousand years ago. If all examples of past animal-to-human microbe trans-
missions are included in the list, it seems likely that at least three-quarters of
all human infections are caused by microbes that originally came from ani-
mals. Most of the other one-quarter of human infections are almost certainly
heirloom infections, transmitted from animals to hominids before modern
humans evolved.
From which animals do microbes that cause human diseases come? Ac-
cording to the Scottish researchers, the largest number come from dogs and
cats (carnivores, 43 percent) and from domestic livestock, primarily horses,
cattle, sheep, goats, and pigs (ungulates, 39 percent). Additional microbes
that cause human diseases come from rodents (23 percent), other primates
(13 percent), birds (10 percent), marine mammals (5 percent), and bats (2 per-
cent). The total adds up to more than 100 percent because some microbes
may be transmitted to humans from more than one animal; rabies, for ex-
ample, may come from dogs, cats, raccoons, and bats. In fact, this study con-
cluded that “over a quarter of pathogens of humans and domestic mammals
have a very broad host range and are capable of infecting human, domestic
and wildlife hosts.” 33
In addition to asking how many infectious diseases are caused by mi-
crobes transmitted from animals, researchers have also asked how many of the
emerging human infectious diseases are caused by microbes transmitted from
animals. By “emerging,” researchers mean diseases caused by microbes “that
have appeared in a human population for the first time, or have occurred
previously but are increasing in incidence or expanding into areas where they
had not . . . been reported” in the past twenty years.34 SARS and avian influ-
enza (bird flu) are examples of such emerging diseases. This question has
been raised because of an increasingly broad consensus among specialists in
infectious diseases that “in the past few years, emergent disease episodes have
increased in the United States and globally. . . . Nearly all these emergent
disease episodes have involved zoonotic infectious agents.” 35
In an attempt to quantify emergent diseases, the Scottish researchers
made a list of 175 microbes that are known to cause emerging infectious dis-
eases in humans. Of these, 132, or 75 percent, are transmitted from animals.36
Viruses account for 44 percent of these animal-associated emergent human
infections, bacteria for 30 percent, protozoa for 11 percent, and helminths
and fungi together for the remaining 15 percent. RNA viruses are especially
prominent, since their mutation rate is significantly higher than that of other
microbes, and they can therefore adapt more quickly to new hosts.37 The
importance of animal-associated microbes as the cause of emerging human
diseases has thus been clearly established. In 2004, the director of the Cen-
ters for Disease Control and Prevention, Dr. Julie Gerberding, noted that “11
of the last 12 emerging infectious diseases that we’re aware of in the world,
that have had human health consequences, have probably arisen from animal
sources.” 38 As summarized by a report from the Institute of Medicine: “The
significance of zoonoses in the emergence of human infections cannot be
overstated.” 39
The available data on zoonoses probably underestimate their contribu-
tion to human diseases. One reason for this is “the inherent bias of humans in
studying themselves in preference to other species,” according to the Scottish
research group that catalogued these diseases.40 Much more is known about
microbes that affect humans than about those that affect other animals; as the
latter become better known, the animal origins of additional human diseases
likely will become evident.
Knowledge about the origins of microbes in general will very probably
increase rapidly in the coming years. We now have the ability to determine
the nucleic acid sequences of viruses, bacteria, and protozoa and to com-
pare those sequences with the sequences of related microbes. This enables
researchers to create phylogenetic trees for microbes, arranging the microbes’

ancestors just as is done for human family trees. As a general rule, the greater
the difference in the nucleic acid sequence between two related microbes,
the longer ago they diverged from a common ancestor. Various “molecular
clocks” are used to estimate that time interval.41
Finally, in the ongoing war between microbes and humans, microbes
have a definite advantage. In any war, the winner’s victory partly depends on
its having been able to perceive its enemy’s defenses, then adapting its forces
to exploit weaknesses in those defenses. Bacteria and viruses can reproduce
and create a new generation of themselves in a few minutes, protozoa, in a few
days. Humans, by contrast, need twenty years to reproduce and create a new
generation. If speed of evolution and adaptability is to be the deciding factor
in the ongoing war between microbes and humans, the future of the human
race is not bright. Clearly, we need to continue developing other weapons in
the human arsenal, including anti-infective drugs, vaccines, and measures to
prevent infections, if we are to survive. As noted by Richard Krause, former
director of the National Institute of Allergy and Infectious Diseases, microbes
were on earth for more than two billion years before humans arrived, “and it
is likely that they will be here 2 billion years after we depart.” 42
2=
C H A P T E R
Heirloom Infections
Microbes before the Advent of Humans
Belief in a golden age has provided mankind with solace in times of de-
spair. . . . The very belief in its existence implies the conviction that perfect
health and happiness are birthrights of men. Yet, in reality, complete
freedom from disease and from struggle is almost incompatible with the
process of living.
Rene Dubos, Mirage of Health
I f there ever was a Garden of Eden, it certainly was not free from disease.
Adam may have been carrying the herpesviruses that cause cold sores and
shingles, and Eve could have had hepatitis B. Mosquitoes in the garden may
have been carrying the microbes that cause malaria and yellow fever. And the
serpent that proffered Eve the forbidden fruit was almost certainly carrying
Salmonella bacteria, as reptiles had been doing for millions of years. One
hopes that Eve washed the apple before eating it and offering it to Adam.
Given that bacteria, viruses, and protozoa had existed for millions of years
before animals evolved, it is not surprising that the earliest known animals
were infected with microbes. Evidence of staphylococcus infection of a rep-
tile bone has been dated to approximately two hundred million years ago,
a viral infection in a bird fossil to ninety million years ago, and a bacterial
abscess in a dinosaur jaw to at least seventy-five million years ago.1 As mam-
mals evolved from reptiles, primates from mammals, hominids from primates,
and Homo sapiens from hominids, all were exposed to the existing bacteria,
viruses, and protozoa.
Often, microbes that infected earlier species of animals were passed along
to later species as the later species evolved. Thus, as hominids evolved from
14 =
Heirloom Infections = 15
primates, they carried with them bacteria, viruses, and protozoa that had in-
fected primates. These infections have been called heirloom infections, since
they are similar to possessions from our parents and grandparents that many
of us carry with us from generation to generation.2
Most microbes that cause heirloom infections are harmless, living unob-
trusively on our skin or in our intestines for our entire lives. Such microbes are
called commensals, and many are useful to us, such as intestinal bacteria that
help us digest food. Commensal microbes rarely cause disease except when
their distribution changes or when the host’s defense mechanisms change. Ex-
amples of such circumstances are treatment with antibiotics, which changes
the distribution of microbes, or AIDS, in which the body’s immune defenses
are markedly reduced. In many cases, if we leave human heirloom infections
alone, they will leave us alone.
Human heirloom infections include protozoa commonly found in hu-
man intestines. One study reported that among twelve human intestinal
protozoa, eleven are also found in the intestines of monkeys.3 Similarly, the
protozoa Trichomonas vaginalis, which may cause a mild vaginal infection in
women, has been isolated from both wild and captive monkeys, in which the
symptoms are also mild.4
The consequences of having inherited microbes from our ancestors are
also illustrated by the appearance of similar microbes in humans everywhere
on earth. This is especially true of harmless commensal microbes; as noted
by one researcher: “Isolated human tribes have the same commensals as those
living in well populated areas.” 5 Thus, the types of bacteria in the noses of
humans who live in remote villages in Papua New Guinea are remarkably
similar to the microbes found in the noses of people who live in New York
and Paris.
Herpes and Hepatitis Viruses

Although most human heirloom infections are harmless, some may cause
disease. Examples are infections with human herpesviruses and some of the
viruses that cause hepatitis.
All members of the herpesvirus family are thought to have evolved from a
common herpesvirus ancestor that originated approximately 400 million years
ago. This ancestor virus split into two ancestral lines. One of these evolved into
the herpesviruses that today infect fish (e.g., channel catfish virus) and am-
phibians such as frogs (e.g., ranid herpesvirus 1). When birds and mammals
evolved, the other ancestor herpesvirus split approximately 180 million years
ago into three main families, labeled alpha, beta, and gamma. These families
in turn further divided, so that, for example, approximately 8 million years

ago, herpes simplex virus 2, which is a common cause of genital infections,
split off from herpes simplex virus 1, which may cause cold sores. As described
by researchers: “The overall scheme of herpesvirus evolution . . . places the
development of herpesviruses in much the same timeframe as that of the ver-
tebrates.” 6 The simultaneous evolution of microbes such as viruses with other
life forms is referred to as coevolution, indicating that the two evolved together.
Since all forms of life are continuously evolving, coevolution of microbes and
animals is also continuous in what is essentially a phylogenetic pas de deux. It
is a Darwinian dance that is never ending.
Today, there are eight known human herpesviruses, and it is likely that
there are additional, undiscovered ones. They are divided into the alpha, beta,
and gamma families that were established 180 million years ago. Since her-
pesviruses have been coevolving with other mammals and birds, herpesviruses
also infect other species. Table 2.1 lists the known human herpesviruses with
the diseases caused by them; it also includes selected examples of herpes-
viruses that occur in other animals.
Human herpesviruses have some common characteristics. All of them,
for example, establish lifetime infections in their hosts. They may remain
quietly latent for long periods of time, causing no symptoms, and then sud-
denly flare up, as occurs with infections of herpes simplex viruses 1 and 2 or
varicella-zoster virus. The herpesviruses are also noteworthy for the variety of
illnesses they may cause in a single animal species. In humans, for example,
they may cause cold sores, childhood rashes, mononucleosis, and various
forms of cancer.
Members of each family of herpesviruses are more closely related to
each other than to members of another family; thus, herpes simplex virus 1 of
humans is more closely related to canine herpesvirus 1 of dogs or feline
herpesvirus 1 of cats than it is to human cytomegalovirus or Epstein-Barr virus.
As noted in chapter 1, the more closely related the animal species, the more
likely it is that a virus from one species will be transmitted to another species.
This is illustrated by the herpes B virus of macaque monkeys. In monkeys,
the herpes B virus is transmitted either sexually or orally and produces a mild
infection similar to that produced by herpes simplex 1 and 2 in humans.
However, when humans are bitten by monkeys infected with the herpes B
virus, the virus may be transmitted to humans, causing a severe, and often
fatal, infection of the brain (encephalitis). Transmission of herpesviruses from
dogs, cats, or other animals more distantly related to humans is not known to
occur.
Another important principle illustrated by herpesviruses is that, even
though the heirloom infections they cause have existed in humans since
Table 2.1. Herpesviruses of Humans and Other Animals

Animals
Type of Virus Infected Symptoms
Alpha herpesviruses
Herpes simplex virus 1* Humans Cold sores, occasional brain
infections
Herpes simplex virus 2 Humans Genital infections, infections
of newborns
Varicella-zoster virus Humans Chickenpox (varicella),
shingles (herpes zoster)
Herpes B virus Monkeys
Simian agent 8 Baboons
Spider-monkey Monkeys
herpesvirus
Canine herpesvirus 1 Dogs
Feline herpesvirus 1 Cats
Equine herpesvirus 1 Horses
Bovine herpesvirus 1 Cattle
Marek’s disease virus Birds
Infectious Birds
laryngotracheitis virus
Beta herpesviruses
Human cytomegalovirus Humans Usually asymptomatic but can
cause congenital infections
in fetus and immune-
compromised individual
Human herpesvirus 6 Humans Childhood rash (exanthem
subitum)
Human herpesvirus 7 Humans No disease yet known
Murine cytomegalovirus Mice
(continued)
Table 2.1. (continued)

Animals
Type of Virus Infected Symptoms
Gamma herpesviruses
Epstein-Barr virus Humans Mononucleosis, Burkitt’s
lymphoma, nasopharyngeal
carcinoma
Human herpesvirus 8 Humans Kaposi’s sarcoma, often
associated with HIV infection
Herpesvirus saimiri Monkeys
Murine herpesvirus 68 Mice
*Human viruses appear in italics.
Source: Adapted from D. J. McGeoch, S. Cook, A. Dolan et al., “Molecular Phylogeny and Evolutionary
Timescale for the Family of Mammalian Herpesviruses,” Journal of Molecular Biology 247 (1995): 443– 458.
Homo sapiens evolved, these infections may change as humans change. For
example, herpes simplex virus 2, which is transmitted sexually, has mark-
edly increased in incidence in recent years as human sexual practices have
changed. Similarly, human herpesvirus 8 was unknown until the AIDS epi-
demic but has been recognized as the cause of Kaposi’s sarcoma, a form of
cancer that occurs with greatly increased frequency when a person’s immune
system is markedly weakened.
Other examples of human heirloom infections are hepatitis A and hepa-
titis B viruses. (Hepatitis C is almost certainly also an heirloom infection, but
its origin has not been studied as extensively.) Hepatitis A is a common cause
of acute human hepatitis in the United States. The virus is usually spread
by person-to-person contact or by contaminated food or water, especially in
places where sanitary conditions are poor.
Outbreaks of hepatitis A have also occurred among animal handlers who
work closely with chimpanzees and other primates. We therefore know that
hepatitis A can spread from primates to humans, and it is suspected that it can
also spread from humans to primates. Recent analyses of hepatitis A strains in
primates and humans have shown that they are closely related, suggesting a
common viral ancestor.7
Hepatitis B is caused by a virus unrelated to the virus that causes hepa-
titis A. It affects 5 percent of the human population and causes cirrhosis and
cancer of the liver, resulting in approximately one million deaths per year
worldwide. It is transmitted by sexual contact, the sharing of needles, and
blood transfusions, and from mothers to infants via blood contact during the
delivery process.
The family to which the hepatitis B virus belongs, hepadnaviruses, in-
cludes related viruses that affect birds, squirrels, woodchucks, and several pri-
mates. The virus most closely related to the human hepatitis B virus is found
in woolly monkeys, suggesting that the human and primate viruses may have
descended from a common ancestor.8 Hepatitis B virus can be transmitted
experimentally from humans to other primates such as chimpanzees, but it is
not known whether transmission can also occur from primates to humans.
Malaria and Yellow Fever

Malaria is a classic heirloom infection that has affected primates since they
evolved approximately sixty million years ago. It causes approximately two
million human deaths each year worldwide, half of them of children under
five. But its devastation is even broader, because millions of other people with
chronic malaria suffer from periodic fevers and severe anemia, with resulting
lack of energy.
Malaria has also changed the course of history. According to Richard
Fiennes, an expert in tropical diseases: “The results of malarial infection on
the evolution and history of civilized man have been incalculable.” Fiennes
claims that malaria “may well have been a major cause of the decline and fall
of the Greek and Roman empires” and “has been responsible for the devital-
ization of whole populations.” 9 Malaria is thus one of the oldest and one of
the deadliest human diseases.
Four species of Plasmodium protozoa (malaria parasites)—vivax, ovale,
malariae, and falciparum—infect humans, and at least twenty-five other spe-
cies infect reptiles, birds, rodents, and other mammals. A major reason these
protozoa have been so successful is that they learned to use blood-sucking
mosquitoes as vectors to move from host to host. This was much more ef-
ficient than traveling on their own, and over millions of years these protozoa
developed a complex life cycle in which one part of their reproductive stage
occurs in mosquitoes.
The protozoa that cause human malaria descended from primates through
various hominids to Homo sapiens. Vivax, ovale, and malariae separated from
related primate protozoa approximately twenty-five to thirty million years ago,
whereas falciparum separated from a chimpanzee protozoan five to ten mil-
lion years ago.10
Since that time, the Plasmodium species that infect humans have changed
genetically so that, with the possible exception of malariae, they can no longer
naturally infect other primates. On the other hand, three Plasmodium spe-
cies found in primates have, on rare occasions, been naturally transmitted by
mosquitoes from primates to humans.11 Thus, malaria is both an heirloom
infection, transmitted millions of years ago from primates to hominids and
eventually to humans, and also a contemporary although rare zoonosis still
being transmitted from primates to humans.
Yellow fever, like malaria, is both an heirloom infection and an ongoing
zoonosis. In humans, it varies from being a mild febrile illness to being a se-
vere illness with high fever, internal hemorrhaging, jaundice, kidney failure,
and death. It was brought to the Americas with African slaves. In Philadel-
phia in 1793, a yellow-fever epidemic killed 10 percent of the population and
shut down the U.S. government, which was temporarily housed in that city.
In Memphis in 1878, it halved the population and caused twenty thousand
deaths in the Mississippi Valley.12
Yellow fever has often altered the course of history. In Haiti, for example,
the 1801 uprising of African slaves was successful because yellow fever killed
twenty-seven thousand French troops while leaving untouched the African-
born slaves, who were relatively immune because of their exposure earlier
in life. Napoleon, discouraged by the loss of his Haitian colony, gave up his
American ambitions and sold his remaining territory, the Louisiana Purchase.
The combination of yellow fever and malaria also affected the colonization
of Africa, since “about half of the European missionaries died [from these dis-
eases] during their first year in Africa. . . . For this reason, they often shipped
their gear [to Africa] in a coffin.” 13 Yellow fever was also a major reason for the
failure of the French to build a canal between the Atlantic and the Pacific at
the Isthmus of Panama in the nineteenth century. The control of the disease
through control of the mosquitoes was one reason for the eventual success of
the U.S. builders of the canal in the early part of the twentieth century.
The yellow-fever virus has apparently been endemic in African monkeys
for millions of years and causes no apparent disease in them. Like the malaria
protozoa, the yellow-fever virus evolved ways of using mosquitoes as vectors to
move from host to host. And as with malaria, control of the disease is through
eradication of the mosquitoes that carry it.
Urban yellow fever is an heirloom infection in that monkeys are no lon-
ger involved in its transmission. The virus simply moves from human to hu-
man, carried by mosquitoes that breed in still water. Jungle yellow fever, by
contrast, involves transmission from monkeys to humans and primarily affects
individuals who live near forested areas.
Endogenous Retroviruses
A special type of heirloom infection involves endogenous retroviruses. These
are retroviruses in the same large family as HIV, the virus that causes AIDS,
and HTLV, a virus that causes a type of leukemia and a neurological disorder.
Endogenous retroviruses are able to integrate themselves into the sperm and
egg cells and thus be passed down from generation to generation. Such inte-
grations have occurred many times in the history of Homo sapiens and our
progenitors. One period of integration was approximately thirty-five million
years ago, after New World monkeys split off from the other primates but be-
fore Homo sapiens became distinguished from other primates. It was during
this period that the integration of a virus known as Human Endogenous Retro-
virus W (Herv-W) took place. We know this because humans share a num-
ber of Herv-W genetic sequences with all the Old World primates, including
rhesus monkeys, gibbons, apes, and chimpanzees, but not with New World
monkeys such as macaques or squirrel monkeys.
Integrations of other retroviruses into the human genome have occurred
at more recent times in primate evolution. One type of retrovirus has been
found in humans, chimpanzees, and gorillas but not in orangutans and gib-
bons, suggesting that this integration occurred after the split of these species
approximately ten million years ago. Other integrations appear to have oc-
curred even more recently. One type of retrovirus, known as Herv-K, is found
mostly in humans. One strain of Herv-K occurs in some humans but not oth-
ers, indicating that the original attack of this retrovirus and its integration into
the genome occurred after the separation of different groups of Homo sapiens
approximately one hundred thousand years ago.
Interestingly, in all of these cases the infectious retroviruses that originally
attacked our ancestors appear to have disappeared from the face of the earth.
Such viruses live on only in our genes and in the genes of our primate cousins.
It is possible that the process is still going on, and that we will genetically pass
on to future generations the retroviruses that are currently infecting human
populations, such as HIV, HTLV-1, and HTLV-2.
The persistence of these retroviruses in the primate genome—for mil-
lions of years, in some cases—has led scientists to ask whether the viruses
have persisted because they offer some protective advantage. In fact, some of
the retroviruses have been commandeered by the human genome to perform
important functions; for example, one of the retrovirus proteins appears to be
important in the formation of the human placenta. Other parts of these retro-
viruses are used to control the expression of primate genes, particularly those
involved in the regulation of the immune response to microbes. This appar-
ently allows humans and other primates, which have relatively slow rates of
procreation, to respond more rapidly to environmental changes. For example,
it is possible that the presence of these retroviruses in our genomes protects
us from infection with many other retroviruses to which we are exposed. This
may be why we do not apparently become infected with retroviruses from
monkeys, cats, mice, rats, chickens, and many other animals with which we
are in contact. However, the recent emergence of HIV and HTLV-1 indicates
that such protection is not total.
The aberrant expression of endogenous retroviruses in our genome has
been suspected, but not proven, to be associated with a number of human
diseases, including multiple sclerosis, schizophrenia, and systemic lupus, and
with problems during pregnancy, including preeclampsia. It thus may be that
the protection these endogenous retroviral heirloom infections offer us comes
at a price. Our ability to understand and control the expression of these heir-
loom infections would represent a major accomplishment in the field of hu-
man health.
Hominids, then, have been continuously infected with microbes ever
since they began evolving from their primate ancestors. Many of these mi-
crobes had also infected the mammalian ancestors of primates and even the
premammalian ancestors, such as reptiles and birds. Human diseases such as
herpes infections, hepatitis A and B, malaria, yellow fever, and endogenous
retroviral infections are thus heirloom infections, part of our birthright as
humans.
Most worrisome about heirloom infections is what we do not know.
Most microbes that are part of the human legacy are harmless, and we live
with them in negotiated peace. The emergence of human herpesvirus 8 as a
cause of Kaposi’s sarcoma in individuals with AIDS, when the immune sys-
tem has been devastated, has given us pause. How many other unknown mi-
crobes that we carry as our heritage may do harm under changing biological
circumstances?
3=
C H A P T E R
Humans as Hunters
Animal Origins of Bioterrorism
Unlike the remaining living primates, man evolved as a carnivorous pred-
ator dependent on his mental and physical prowess to kill other animals
for food. This entailed the development of complicated social relationships
between the hunters, their prey, and competing predators.
Juliet Clutton-Brock, Domestic Animals from Early Times
E arly hominids had little contact with animals other than themselves.
The ancestors of Homo sapiens, after breaking away from other African
apes approximately six million years ago, subsisted on a diet mostly of insects,
fruits, and leaves and apparently did little hunting of animals.
The best measure of what early hominids ate is probably what modern
chimpanzees eat. Jane Goodall, who studied these animals in Tanzania, ob-
served them eating more than fifty types of fruit, thirty types of leaves and leaf
buds, blossoms, seeds, bark, nuts, ants, termites, caterpillars, honey, and larval
grubs of bees, wasps, and beetles. Chimpanzees occasionally also eat birds’
eggs and meat from other animals, including baboons, monkeys, and young
bushbucks or bushpigs, but these are not mainstays of their diet. Goodall es-
timated that one chimpanzee eats the equivalent of approximately one-half
a prey animal in a one-year period, and during ten years of observation, she
observed chimpanzees killing other animals only twice.1
Even when Australopithecus afarensis walked upright on the African
plains approximately three million years ago, the dietary practices of early
hominids had not changed much. An analysis of the teeth of “Lucy,” the best-
studied member of this group, suggests she ate fruit “in quantities when it was
in season, . . . a great many berries and seeds and roots and tubers, and a good
= 23
deal of dirt and sand along with these things.” 2 These hominids undoubtedly
supplemented their diet with small animals when they could catch them, but
meat was not a major part of their diet.
It was not until approximately one million years ago that human ances-
tors became accomplished hunters. By then, hominids had evolved through
Homo habilis and Homo erectus, had begun using stone tools, and had do-
mesticated fire. This last was an important antecedent for meat eating, since
cooking makes meat more palatable. The importance of dietary meat also
increased at this time because the climate became cooler and drier in the
preglacial era. During this period, “plant foods became more sparse,” while
“grazing animals on open grassy savannahs proliferated.” 3 The development
of language made hunting large animals easier, for it could be carried out co-
operatively by groups of individuals as they communicated with one another.
Evidence for a hominid shift from being primarily herbivorous to being
increasingly carnivorous comes from archeological research at prehistoric liv-
ing sites. Animal bones have been found with “distinctive cut-marks and ham-
mer indentations characteristic of butchering and marrow extraction,” ac-
cording to Tony McMichael’s Human Frontiers, Environments and Disease:
Anthropologists think that early humans probably came to rely on meat
for around one-quarter of their daily calories. Meat intake not only pro-
vided energy; it supplied the full range of amino acids (the building
blocks of proteins) and some important micronutrients (such as trace
elements and vitamin B12) that were deficient in a vegetarian diet. In
those precarious dietary circumstances, a modest meat intake would have
significantly aided survival. It would also have consolidated cooperative
hunting and food sharing. . . . The evidence, while still contentious,
points increasingly to a Pleistocene in which early humans became seri-
ous hunters and big meat-eaters.4
By the late Paleolithic period, humans had become highly dependent

on meat for sustenance. Recent study of bone chemistry of Neanderthals
“overwhelmingly points to the Neanderthals behaving as top-level carnivores,
obtaining almost all of their dietary protein from animal sources; . . . protein
from plants was insignificant.” 5 The importance of dietary protein at this time
can also be measured by the size of humans. According to experts on Paleo-
lithic nutrition, “Homo sapiens sapiens, who enjoyed an abundance of animal
protein thirty thousand years ago, were an average of six inches taller than
their descendants who lived after the development of farming,” when meat
consumption declined.6
Given this immense meat consumption, why didn’t Paleolithic humans
all succumb to heart attacks? One reason is that free-living animals have a
much lower fat content in their muscles than do domesticated animals, and its
Humans as Hunters = 25
composition is different; “wild game contains over five times more polyunsatu-
rated fat per gram than is found in domestic livestock.” 7 Thus, even though
Paleolithic humans were eating large quantities of meat, it contained much
less fat, and healthier forms of fat, than meat from domesticated animals.
In addition to hunting animals for meat, Paleolithic humans used an-
imals for their skins and bones. Animal skins were early humans’ primary
source of protection from the cold. This became especially important during
the four glacial periods between six hundred thousand and fifteen thousand
years ago. At their peak, ice covered all of northern Europe as far south as
central Germany and France, and the landscape was cold tundra, with little
vegetation except during the summer months. The availability of skins of bi-
son, aurochs (wild cattle), deer, ibex, wild sheep, bear, beaver, foxes, and other
mammals largely determined whether humans survived or not. Humans also
needed the bones of animals for making tools. Awls, harpoons, fish hooks,
scrapers, and needles were fashioned from animal bones for at least seventy
thousand years and were essential for hunting, fishing, butchering the catch,
and sewing clothing.
In addition, at some point during the last hundred thousand years, Homo
sapiens developed self-awareness. This may have been a consequence of the
evolution of the frontal lobes of the brain or, as argued by Richard Klein in
The Dawn of Human Culture, a genetic mutation.8 From that time onward,
animals became incorporated into humans’ philosophic view of the world and
their place within it. Animals thus began to play a major role in the creation
myths of many cultures and continue even now to be incorporated into the
ancestor stories and social structure of family and group organizations. An
example of this is the role of animals in totems and clan identification among
Native Americans along North America’s northwest coast. One may argue that
the use of animals as symbols for fraternal organizations, colleges, and sports
teams is an extension of this group identity.
The late Paleolithic period, therefore, witnessed a major revolution in
the relationship between humans and other animals. Following their diver-
gence from chimpanzees, hominids had interacted minimally with other ani-
mals for five million years. Then, over a period of one million years, humans
evolved increasingly as hunters, culminating in the late Paleolithic period,
when hunting became the major human activity.
Thus emerged humans as hunters. For millions of years, hominids had
merely watched other animals from afar. The new relationship required hunt-
ers to pursue and kill the animals. Knowledge of the animals’ habits increased
chances of success in the hunt, and for this reason it has been said that “the
study of animal behavior is among the oldest of human endeavors.” 9 Animals
took on new meaning for Paleolithic humans. Bison and horses, viewed on
the plains, became the Paleolithic equivalent of a McDonald’s golden arch.

A passing gazelle may have evoked the same reaction that a sign for Kentucky
Fried Chicken does today.
The relationship between Paleolithic humans and animals is most clearly
illustrated by the animal paintings, drawings, and etchings by Paleolithic art-
ists in caves of southern France and northern Spain. In France’s Chauvet cave,
discovered in 1994, some of the paintings are thirty-two thousand years old.
One panel shows four horses running side by side, another depicts ten lions
moving toward some bison, and yet another has two rhinoceroses squared off
to fight. France’s Lascaux cave has a panel with five deer swimming across a
river and, elsewhere, a remarkable deer with nine-point antlers, painted with
red ocher from iron oxide. But Lascaux cave is best known for its Hall of the
Bulls, a fifty-foot-long semicircular frieze painted seventeen thousand years
ago. The animals are aurochs, the wild ancestors of contemporary cattle, and
the artist needed scaffolding to paint them on the ceiling. One bull is six-
teen feet long. Picasso, after visiting Lascaux, commented: “We have invented
nothing!” 10
In Spain’s Altamira cave, the ceiling of the main hall, which has been
called the Sistine Chapel of Paleolithic art, is one thousand square feet and
covered with animals and geometric figures. Most prominent are “21 mag-
nificently painted bison outlined and shaded in black, red bodies engraved in
the glistening, creamy limestone. They crouch, lie down, shake their manes,
charge across the ceiling, heads turned, tails flying, drilled eyes dark as coal.” 11
The bison were engraved to emphasize eyes or other parts of their bodies. The
artists took advantage of the natural rock contours of the ceiling so that one
bison, whose head is turned to look back, appears three-dimensional because
its head is painted on a rock outcropping. As described by one observer: “The
figure develops in harmony in its surfaces; it leaps as if real and alive from the
rugged surface of the rock. The fur, the beards, the manes of the bisons attain
an almost tactile reality.” 12
Some of the bison appear so freshly painted and lifelike that in 1880,
when Marcelino de Sautuola first published the results of his discovery of the
cave, his claims that the paintings were Paleolithic in origin were derided.
One skeptic, at an 1886 scientific meeting, claimed that “they are merely the
expression of a mediocre follower of the Modern School,” referring to emerg-
ing Impressionism.13 It was not until 1902, after Sautuola had died, that the
Altamira paintings were finally accepted as authentic.
This, then, was the new relationship between animals and humans. The
Paleolithic cave paintings include no hills, no mountains, no natural scenery
at all. Nor do they include any humans except for occasional stick figures in
pursuit of the animals. The paintings represent Paleolithic humans’ new and
special relationship with animals—reverence, perhaps even worship. Sitting
quietly in the main hall of Altamira cave, one is deeply impressed by the ani-
mals and by the people who painted them. It is an animal apotheosis. But with
this new relationship came new diseases.
Taenia and Trichinosis

The animals Paleolithic humans killed, skinned, butchered, and ate were
infected with an assortment of microbes, as all animals are. Since humans
and the other animals had lived relatively separate lives for millions of years,
humans had little previous exposure to most of these microbes. Their expo-
sure now resulted in new infections, some harmless and some harmful, for
Paleolithic humans. This can be illustrated by two macroparasite infestations,
taenia and trichinosis, and five microbial diseases: anthrax, brucellosis, Q fe-
ver, tularemia, and glanders. All are examples of direct infection, as described
in chapter 1, and all probably infected humans for the first time during the
Paleolithic era. Such infections were part of the price humans began paying
for their new relationship with animals. Humans hunted the animals, and the
animals’ microbes hunted the humans.
Recent studies have established that humans were first infected with
Taenia tapeworms in Africa during the Paleolithic period. The source of the
human infections was undercooked meat from wild cattle (aurochs) or wild
boars.14 Taenia saginata and Taenia solium infect humans when they ingest
Taenia eggs in uncooked or undercooked beef or pork. In most cases, tape-
worms cause no clinical symptoms, but in some individuals they cause ab-
dominal pain, nausea and vomiting, and weight loss. A serious complication
of Taenia solium is cysticercosis, in which numerous cysts go to the brain or
eye, causing seizures or impaired vision. In developing countries, cysticercosis
of the brain is the most common cause of acquired epilepsy, and even in Los
Angeles, “neurocysticercosis was found in 10 percent of patients with seizures
who went to an emergency room.” 15
Trichinosis is caused by Trichinella spiralis, a roundworm. Humans be-
come infected when they eat uncooked or undercooked meat that contains
cysts containing worm larva. Most humans have no symptoms unless they in-
gest a very large number of cysts; in such cases the cysts can infect the person’s
heart muscle or brain, and deaths from trichinosis have been reported. Wild
boars, horses, and bears are all infected with Trichinella spiralis and could
have been a source of infection for Paleolithic hunters.
Numerous other macroparasites are known, but most are of little or

no clinical significance for humans. It seems likely that Paleolithic hunters
would have encountered most of them as they skinned, butchered, and ate
the animals of the African plains. Studies of the fossilized human excrement
(coprolites) of early hunters have often found evidence of macroparasites.16
Anthrax, Brucellosis, and Q Fever

Anthrax, brucellosis, and Q fever are microbial diseases that were originally
transmitted to early humans from wild ruminants, specifically the ancestors
of cattle, sheep, and goats. These microbes have thus infected humans for
thousands of years; in recent years, they have become prominent as possible
agents for bioterrorism.
The Egyptians, Greeks, and Romans knew anthrax well. It achieved a
unique place in history in 1877, when Robert Koch described it as the first
microbe to be specifically linked to a disease. Anthrax spores live in the soil,
where they are ingested by cattle and other grass-eating animals. The infected
animals die, and their meat, hides, hair, and even bones can then spread the
spores to humans.
The most common clinical form of human anthrax disease is the cu-
taneous form that produces black skin ulcers; untreated, it causes death in
25 percent of cases. Less common but much more serious is the systemic form
in which anthrax spores are inhaled, producing initial flulike symptoms and
almost always progressing to death within in a few days. Anthrax continues to
occur among farm animals in many parts of the world, including the United
States. An outbreak among cattle in North Dakota in 2000, for example, re-
sulted in 157 animal deaths.17
Brucellosis is also an ancient disease; Hippocrates described it as Medi-
terranean fever. It continues to be widespread in the Mediterranean area even
today; worldwide, approximately one-half million cases are reported each
year, although it is rare in the United States. It is transmitted to humans from
infected cattle or goats through butchering or by ingesting infected meat or
unpasteurized milk, cream, or cheese. In animals it is an important cause of
abortions, and in humans it is manifested by a relapsing fever (brucellosis is
also called undulant fever), weakness, and muscle and joint pain. Untreated,
it causes death in approximately 5 percent of cases.
Q fever acquired its name as an abbreviation for query fever by an Aus-
tralian researcher investigating an outbreak of fever among slaughterhouse
workers. Like anthrax and brucellosis, it is spread from cattle, sheep, and goats
to humans and does not spread from person to person. It is caused by a rickett-
sial type of bacteria and causes no symptoms in animals but may cause high
fevers, pneumonia, hepatitis, or infection of the heart muscle in humans.
Tularemia and Glanders

Tularemia and glanders are also microbial diseases that were originally trans-
mitted from animals to humans during the Paleolithic period. Tularemia
comes from rabbits and squirrels, while glanders comes from horses and
mules.
The bacteria that causes tularemia is transmitted to humans most often
during the butchering and eating of infected rabbits or squirrels. Less often it is
acquired from ticks or flies that have previously bitten an infected animal. Clini-
cally, tularemia causes ulcers, enlarged lymph nodes, and occasionally pneu-
monia. The mortality rate in untreated cases is approximately 10 percent.
Glanders is caused by bacteria carried by horses and mules. It can be
acquired by eating the meat of infected animals, by butchering them, or
merely through close contact with them, as has occurred among stable work-
ers. In both horses and humans, glanders can cause skin ulcers (called farcy in
horses), abscesses in internal organs, and pneumonia. Cases in humans have
been described in which the person died less than three weeks after infection,
“literally covered with pustules and ulcers.” 18
Glanders was known to the Greeks and remained an important disease
until the gasoline engine replaced horses for transportation. For example, dur-
ing the Civil War, Union and Confederate forces collected as many as 30,000
horses in large supply depots, and glanders spread quickly among them. At a
Confederate depot in Lynchburg, Virginia, only 1,000 out of the 6,875 horses
stabled there were said to be fit for service.19 At a Union depot in Washington,
D.C., 331 glanders-infected horses had to be shot in a single day.20 The short-
age of horses because of glanders created major problems for the armies on
both sides. At the Battle of Chancellorsville in 1863, “more than one-fourth of
the Confederate cavalry was without mounts.” 21
By the close of the Civil War, glanders had become widespread among
horses on both the Union and Confederate sides. It had also presumably
spread to many soldiers and was, along with typhoid, measles, tuberculosis,
and other diseases, an additional source of mortality. When the Union and
Confederate forces broke camp at the end of the war, they left behind many
sick horses and mules “for the common people, both black and white. . . . Un-
intentionally they opened a floodgate of disease upon the countryside.” Other
soldiers returned home accompanied by their sick animals in what has been
called “a Civil War legacy.” 22
Paleolithic Microbes in the Modern Age

A recent synopsis of the biological and chemical agents most likely to be used
for bioterrorism listed twelve microbes, including those that cause anthrax,
brucellosis, Q fever, tularemia, and glanders23 — legacies of animals hunted
by Paleolithic peoples. It is interesting to speculate why some microbes that
have infected humans for the longest time should be useful as agents of bioter-
rorism. All of them except brucellosis can be aerosolized and thereby spread
through the air, all are hardy bacteria that can survive for long periods, and
all are capable of causing disease in a wide variety of animals in addition to
humans.
Anthrax is the best known and most feared among these. In October 2001,
the United States became transfixed by anthrax when it was sent by mail to
members of Congress and to a company in Florida. Inadvertently released
from its envelope at a mail-sorting facility in Washington, D.C., anthrax killed
two postal workers and caused illness in two dozen others. Anthrax is espe-
cially feared because its spores can be aerosolized, released into the air, and “if
released in a fine-particle mist, . . . can ride air currents for 50 miles or more.”
A 1993 U.S. government assessment estimated that “if 220 pounds of aerosol-
ized anthrax spores were released over Washington, D.C., between 130,000
and three million people would die.” 24 Japanese troops are alleged to have
used anthrax in this manner in China in the 1930s.
The microbe causing Q fever is also considered especially appropriate for
bioterrorism because it spreads mainly by being blown through the air. For
example, an outbreak in Switzerland infected 415 residents who lived along
a road over which infected sheep were merely driven to pasture.25 Thus, re-
leased into the air, Q fever could sicken thousands of people. Tularemia is of
special interest to bioterrorists for the same reason—it also can be aerosolized
and thereby spread by inhalation.
All five of these Paleolithic-era microbes have been, and presumably still
are, under study by military researchers in the United States and elsewhere.
All of them are also of interest to bioterrorists and have been used as agents of
germ warfare.
The Germans used glanders, for example, in World War I to kill horses
and mules destined for the Allied forces in Europe, where the animals were
widely used for carrying supplies to the lines. Although technically still neu-
tral, by 1915 the United States had become a principal source of war supplies
for Britain and France, including thousands of horses and mules. The Ger-
mans evolved a plan to sabotage these equine supplies by infecting them with
glanders before they were shipped abroad.
Brooklyn-born Anton “Tony” Dilger, the son of German immigrants, co-
ordinated the plan. Trained in medicine at Johns Hopkins University in Balti-
more, Dilger went to Germany before the war and was recruited as a German
operative. In 1914 he returned to the United States and set up a laboratory
in a house in Chevy Chase, Maryland, where he grew glanders bacteria in
cultures.
To infect the horses and mules awaiting shipment to Europe, the Ger-
mans recruited Edward Felton, a stevedore in Baltimore. Dilger supplied
glanders in small glass bottles that had “a piece of steel in the form of a needle
with a sharp point . . . stuck in the underside of the cork, and the steel needle
extended down in the liquid where the germs were.” The Germans told Fel-
ton where to find the horses, and he recruited fellow stevedores to help him.
According to testimony he later gave in court:
I had about ten or twelve men working on these matters with me. We
would work at it sometimes at night and sometimes in the daytime. A
good many of the men were also doing other work and they made this
extra money on the side. . . . We used rubber gloves and would put the
germs in the horses by pulling out the stopper and jabbing the horses with
the sharp point of the needle that had been down among the germs. We
did a good bit of the work by walking along the fences that enclosed the
horses and jabbing them when they would come up along the fence or
lean over where we could get at them. We also spread the germs some-
times on their food and in the water they were drinking.26
Felton and his associates infected more than three thousand animals
awaiting shipment to Europe, and these animals probably infected others. It
was claimed that “several hundred military personnel were also affected.” 27
The Germans regarded the sabotage efforts as so successful that “Dilger later
went to St. Louis to establish a second lab there for the inoculation of Eu-
rope-bound horses and mules raised in Western states.” 28 Germany may have
extended its glanders program to Spain, Argentina, and other countries that
were also supplying horses and mules to the Allied forces.29
The entry of the United States into the war in 1917 put an end to these
German sabotage efforts. Dilger moved to Mexico, where, under an alias, he
was said to be “the overseer of all German intelligence in Mexico.” 30 Dilger
later moved to Spain, where he died suddenly during the final months of the
war. “It was whispered that he knew too much. It was a deadly poison that
removed him—at least so it was intimated by a former German agent.” 31
The use of glanders in germ warfare was probably tested in extensive

biowarfare research carried out by the Japanese in the 1930s and possibly in
Soviet research during the Cold War. There are also allegations that Soviet
forces used glanders to infect horses of resistance forces in Afghanistan during
the 1982–1984 war.32 In the United States, glanders has continued to be a
subject of military research. Between November 1944 and September 1945,
six cases of human glanders occurred among thirteen researchers working
on the microbe at the army research facility at Fort Dietrich, Maryland.33 In
March 2000, a researcher at that facility developed severe glanders and had
to be placed on a respirator before he was properly diagnosed and treated.34
Thus, these ancient animal microbes that first infected Paleolithic hunters
remain relevant today, primarily as agents of human destruction.
4=
C H A P T E R
Humans as Farmers
Microbes Move into the Home
Directly or indirectly, every creature survives at some expense to others.
It stays alive only if it creates proteins; to do so, it must take in proteins
or the amino acids from which proteins are built. The ways one creature
makes another’s protein its own range from predation to parasitism, but
all are paths to the same end.
Arno Karlen, Man and Microbes
N obody fully understands why humans domesticated crops and farm ani-
mals when they did. Changes in climate are only part of the explanation.
Perhaps the continuing evolution of the human brain also played a role, al-
lowing people to plan ahead and work together in ways that had not previously
been possible. Whatever the reasons, the Neolithic revolution, as it is com-
monly called, changed the relationship between humans and other animals
more profoundly than any other event in history.
By the beginning of the Neolithic period, hominids had spread broadly
across the earth. They migrated from Africa into the Middle East and Asia
approximately 1.7 million years ago and into Europe by 1 million years ago.1
Homo sapiens, the only species of Homo that survived and that from which
modern humans descend, spread widely around the earth beginning approx-
imately one hundred thousand years ago and by the Neolithic period had
reached Australia and South America. Whereas the total hominid population
of eastern Africa had probably been no more than fifty thousand individuals
before they began dispersing, by the Neolithic period the widely scattered
humans numbered approximately five million.2
The climate in many areas of the earth became more hospitable to agri-
= 33
culture as the glaciers started to recede approximately fifteen thousand years

ago. As the earth slowly warmed, grasslands and forests increasingly replaced
the tundra across much of Europe, the Middle East, and Asia. One area espe-
cially rich in agricultural potential was the Fertile Crescent, which stretches
for almost one thousand miles from what are now Israel and Palestine through
Lebanon, Jordan, Syria, and southeastern Turkey into Iraq and Iran.
Growing wild in the Neolithic grasslands of the Fertile Crescent were
ancestor grasses of wheat, barley, rye, lentils, and chick-peas.3 According to
Steve Olson in Mapping Human History: “Of the fifty-six grasses with the
largest seeds, thirty-two grow in the Middle East, including wheat and barley.
No other part of the world has more than a few such plants.” 4 The upper
reaches of the Tigris and Euphrates rivers, which cover part of northern Iraq
and southeastern Turkey, were especially rich in the Neolithic founder crops
and have been called “the cradle of agriculture.” 5 There is evidence that ag-
riculture developed independently in other areas of the world as well, includ-
ing Southeast Asia, northern China, Africa, Papua New Guinea, Mexico, and
Peru. The Fertile Crescent, however, was unique in having a wide variety of
cultivatable plants, as well as wild olives, figs, grapes, dates, and apples.6
Agriculture, of course, did not develop at a single site or at a single time.
Over hundreds, perhaps thousands, of years, humans picked the wild plants,
harvested the edible parts, and discarded the seeds nearby. Inevitably some
of the seeds grew into new plants. The cereal grains were ground, baked, and
mixed with water to make an edible gruel. When gruel is allowed to stand,
it uses bacteria to ferment and change into a type of beer. This development
almost certainly added both impetus and enthusiasm to the agricultural
revolution.
Neolithic people valued most the foods that they could store and that
were good sources of calories—cereals such as wheat, barley, millet, rye, corn,
and rice, as well as tubers such as potatoes, yams, and manioc (cassava).7 Once
a plant became well established as a source of food among one group of Neo-
lithic farmers, its use spread to other parts of the world.
The use of increasingly sophisticated tools also encouraged the develop-
ment and spread of agriculture during the Neolithic period. Recent experi-
ments using a flint-bladed sickle demonstrate that one person could gather
enough wild wheat in one hour to produce a kilo of grain. Experiments with
a polished stone axe head report that “three men managed to clear 600 square
yards of silver birch forest in 4 hours. . . . More than 100 trees were felled with
one axe-head, which had not been sharpened for about 4,000 years.” 8 Thus,
Neolithic farmers were able to clear forested areas to enlarge the size of their
gardens.
H u m a n s a s Fa r m e r s = 35
Domestication of Animals
At the same time that Neolithic people were domesticating plants, they were
domesticating animals. The sequence of these two developments has been de-
bated, but they probably occurred simultaneously and influenced each other.
Using an animal to pull a plow, for example, doubled the area that could be
cultivated by human power alone.9 Similarly, the parts of cultivated crops that
could not be used by humans could be fed to domesticated goats, pigs, and
cattle.
For animals to become domesticated, according to Francis Galton, they
must possess six characteristics: They must be “hardy” and able to adapt; they
must be social; they must be “comfort-loving” and appreciate what humans
have to offer them; they must be “useful” to those domesticating them; they
must breed easily; and “they should be easy to tend.” Only one animal does
not follow these rules: “With the exception of the domestic cat, all domestic
mammals are derived from wild species that are social rather than solitary in
their behavior.” 10
The first animal Homo sapiens domesticated was the dog, approximately
fourteen thousand years ago. Domestication may have occurred first in China
or Japan, although once domesticated, dogs spread quickly throughout the
settled world.11 The process of domestication has been widely debated: Did
humans domesticate wolves, or did wolves domesticate themselves?
Proponents of the first position argue that taming wolf pups is compara-
tively easy. In this scenario, early humans kept and bred those pups that were
especially placid and submissive and then learned to use the tamed wolves
to help hunt deer and other mammals and to warn of approaching enemies
at night. The experiments of Soviet biologist D. K. Belyaev support this sce-
nario. Belyaev, working with silver foxes, selected for breeding those foxes that
showed the most “consistently tame behavior toward humans.” Twenty years
after the selective breeding began, “the results were astonishing.” Belyaev’s
“tame-selected foxes were not just tame; they acted for all the world like do-
mestic dogs. They approached familiar persons and licked their hands and
faces. They barked like dogs. They even sought the attention of strangers by
whining and wagging their tails. Their annual molting cycle was disrupted,
and the females began to come into heat twice a year, like dogs, and unlike
both foxes and wolves.” 12
Proponents of the alternate theory call attention to the evolution of both
early humans and wolves “as social hunters” and point out that “during the
glacial phases of the Upper Pleistocene, they had the same ubiquitous distri-
bution and they preyed on the same herds of large mammals.” 13 According
to this scenario, wolves began hanging around human campsites to scavenge

garbage and gradually became less fearful. These wolves were not being se-
lected by humans but rather were selecting themselves: “These were animals
that chose to hang around humans, and in so doing to isolate themselves from
their wild counterparts by their own volition.” 14 Over time, being social and
hierarchical in nature, the wolves would have accepted the human social or-
der as their own in exchange for food. As Stephen Budiansky summarized this
scenario in The Covenant of the Wild: “In an evolutionary sense, domesticated
animals chose us as much as we chose them.” 15 Rudyard Kipling portrayed
such a scene in his 1912 Just So Stories, in which he has a woman throw a
“roasted mutton-bone” to “Wild Thing out of the Wild Woods”:
Wild Dog gnawed the bone, and it was more delicious than anything he
had ever tasted, and he said, “O my Enemy and Wife of my Enemy, give
me another.”
The Woman said, “Wild Thing out of the Wild Woods, help my
Man to hunt through the day and guard this Cave at night, and I will give
you as many roast bones as you need.” 16
Sheep and goats were the next animals to become domesticated. The
wild ancestors of both lived in the Fertile Crescent, especially in the Zagros
Mountains in what is now western Iraq. Domestication would not have been
difficult, since both sheep and goats follow a dominant leader. They also have
relatively placid natures, breed easily in captivity, and eat a wide variety of
shrubs and grasses. Evidence that suggests the domestication of sheep has
been found at a site in northern Iraq that dates to almost eleven thousand
years ago. Goat domestication in this area apparently began about ten thou-
sand years ago.17 The problem with fixing such dates with any certainty is
one of definitions. Does the simple herding of wild goats or sheep qualify as
domestication? Or confining them to fenced areas? Breeding them while in
captivity, or breeding selectively so as to enhance certain characteristics?
Goats were an especially valuable commodity in the ancient world and
continue to be so today in many parts of the developing world. As Juliet Clut-
ton-Brock notes: “The goat can provide both the primitive peasant farmer and
the nomadic pastoralist with all his physical needs, clothing, meat, and milk as
well as bone and sinew for artifacts, tallow for lighting, and dung for fuel and
manure.” 18 In addition, goat’s milk can be made into cheese, its wool used for
clothing, and its skins used for both clothing and water containers. It is thus
not surprising that the five-thousand-year-old man discovered in 1991 in a gla-
cier in the Alps was wearing a jacket and leggings made of goat- and deerskins.
Goats may have also been helpful to Neolithic farmers in clearing land for
planting by eating shrubs and low-hanging trees. Since goats eat plants that
sheep and cows will not, they are very hardy and adaptable and can be raised
in a wider variety of environments, including those that are semi-desert.
Humans next domesticated pigs and cattle. Their ancestors, wild boars
and aurochs, were widely distributed across the Middle East, Asia, and Eu-
rope, so domestication could theoretically have occurred in many places over
a broad geographic area. DNA analyses from contemporary animals, however,
suggest that for both pigs and cattle, “modern livestock derived from a small
number of animals domesticated in just a few places 8,000 to 10,000 years
ago.” 19
Domesticated pigs are relatively easy to maintain. They eat almost any-
thing, produce two litters a year, and provide a steady supply of protein as
ham, pork, and bacon. Although ancient Semitic peoples and modern-day
followers of Jewish and Islamic rituals shun pigs as unclean for food, they
are highly valued in many Asian and Pacific Island cultures. In some parts of
Papua New Guinea, for example, pigs are the major means for counting one’s
wealth, and it is not uncommon for a woman to suckle a piglet at her breast
alongside her own child.
In contrast, the circumstances that led early humans to domesticate wild
aurochs as cattle are difficult to imagine, for the animals were not only six feet
high but “fierce, swift and agile.” 20 They would certainly have been more
difficult than pigs or goats to herd from village to village and, if left to roam
freely, would have trampled the grain in the gardens and fields.
Nevertheless, Neolithic humans discovered the immense value of domes-
ticated aurochs. Cattle can provide meat, milk, butter, and cheese as food.
Their horns are useful as weapons and their dried hides make good shields,
both valuable in warfare. The hides can also be used for making shoes and
clothing. Cattle dung can be burned as fuel, used as fertilizer, and used in
pastes for the building of huts, and cattle fat can be burned as tallow. Cattle
may also be used to thrash grain by walking on it, pull carts, and turn wheels
to bring water from wells. Frederick Zeuner, in A History of Domesticated
Animals, claimed that, after dogs, “the domestication of cattle was the most
important step ever taken by man in the direction of exploitation of the ani-
mal world.” 21 Given these contributions, it is not surprising that many societ-
ies have revered, even worshipped, cattle.
Horses were domesticated next, approximately five thousand years ago, in
Turkestan, Ukraine, and southern Russia, where wild horses were abundant.22
In contrast to pigs and cattle, DNA analyses of modern horses suggest that they
were domesticated at multiple places and at different times.23 Horses were
probably originally domesticated as an additional source of meat, but their
value as transportation soon became apparent.
The successful domestication of goats, sheep, pigs, cattle, and horses—
referred to as the “Big Five” 24—was an enormous advantage for Neolithic

people, providing them with a reliable supply of food, clothing, and transpor-
tation. Selective breeding rapidly produced groups of animals with special
characteristics, and “both the Babylonian and the Ancient Egyptian civiliza-
tions had developed definitive breeds of dogs, cattle, and sheep by the begin-
ning of the second millennium b.c.” 25
The idea of domesticating animals spread quickly across the world and
in some cases was accomplished independently. Oxen, yaks, water buffalo,
gaur, banteng, reindeer, camels, donkeys, elephants, and alpacas were domes-
ticated for tasks such as carrying loads; pulling plows, wagons, or sleds; or
turning wheels to pump water from wells. Ducks, geese, and turkeys were do-
mesticated for food; cats, as we will see later, were domesticated by Egyptians
to keep rodents away from the grain or simply as pets. The Egyptians, in fact,
were so enthusiastic about domesticating animals that they also tried, though
unsuccessfully, to domesticate antelopes, gazelles, hyenas, and monkeys.26
Enter the Microbes

Peoples of the Neolithic period, then, profoundly and permanently altered
the relationship between animals and humans. Animals that early hominids
had watched from afar for millions of years, and Paleolithic humans had
hunted for thousands of years, now grazed peacefully in the backyard. In the
past, animals and humans had essentially been equals; after domestication,
that was no longer true. As James Serpell observed in In the Company of Ani-
mals: “This essentially egalitarian relationship disappeared with the advent of
domestication. The domestic animal is dependent for survival on its human
owner. The human becomes the overlord and master, the animals his servants
and slaves.” 27 This new relationship between animals and humans was sym-
bolized by how humans depicted animals. As one art historian observed: “The
altered relationship to the animal world of man as hunter and man as farmer
was inevitable and seems to account for differences between the command-
ing bulls and bison of Lascaux . . . and the tiny, toy-like horned animals found
on Neolithic sites such as Hăbăşeşti, or the heads attached to Neolithic and
Bronze Age pots” several centuries later.28
A consequence of the domestication of animals was a marked increase
in intimacy between animals and humans. Sheep, goats, pigs, and cows were
often housed immediately adjacent to, or under the same roof as, Neolithic
farmers. In agrarian areas of the developing world, it is still not unusual to find
several animals sharing one-room living quarters with an extended human
family. Even in Western nations, the separation of living quarters for farm
animals and humans is a relatively recent phenomenon.
Following domestication, therefore, animals not only entered the home

but also became part of the family. According to Keith Thomas: “Sheep or
pigs were not usually given individual names, but cows always were, . . . like
Marigold or Lily.” Furthermore, “shepherds know the faces of their sheep as
well as those of their neighbors.” 29 Such animals were usually the family’s
most valuable possessions, as well as its main sources of milk and meat. The
animals were nursed when they were sick and midwifed, as needed, when
giving birth. The extent of the intimacy between domesticated animals and
humans is also symbolized by humans’ drinking of the milk of goats and cows.
As Joanna Swabe has pointed out: “The practice of drinking cow’s milk, par-
ticularly by human babies, . . . created an intense bond between humans and
other animals; by seeking the milk of another species to nourish their young,
humans were effectively using cattle as wet-nurses.” 30
The new relationship between animals and humans led to many new hu-
man diseases. The animals Neolithic people domesticated were carrying a va-
riety of bacteria, viruses, and protozoa that had evolved with the animals over
thousands, even millions, of years. Putting the previously wild animals into
pens and other enclosures facilitated the dissemination of microbes within
each species. Placing different animal species, such as sheep and goats, within
the same enclosures encouraged the spread of microbes across species, some-
times producing new and different strains of the microbes.
Many of the microbes inevitably spread from the domesticated animals to
humans. They spread when Neolithic people ingested the meat or milk prod-
ucts of the animals. They spread through the air when animals were housed
within human dwellings. They spread through animal feces, which were de-
posited close to human dwellings, used as building material, burned as fuel,
and spread as fertilizer on Neolithic farmers’ crops, and which contaminated
water supplies being used by humans. The microbes spread when dogs or other
domesticated animals licked or bit people. They spread by being carried by
flies, ticks, mosquitoes, fleas, or other vectors from the domesticated animals
to humans living close by. And they spread when humans had sexual contact
with animals, as has occasionally occurred throughout history and is depicted
in prehistoric art.31 Indeed, in the years following the initial domestication of
animals, humans were heavily exposed to a multitude of animal microbes to
which they had previously been exposed only minimally or not at all.
Ulcers, Whooping Cough, and Smallpox

We are still learning the microbial consequences of the domestication of ani-
mals, and as the genomes of additional microbes are characterized by nucleo-
tide sequencing in coming years, we will gain a more complete picture. What
is already clear is that many important human diseases can be traced to bacte-
ria, viruses, and protozoa that were first transmitted from animals to humans
during the Neolithic revolution.
Peptic ulcers in humans are an example. They are caused by an erosion
of the lining of the stomach or the duodenum, the first segment of the small
intestine. The main symptoms are abdominal pain, usually sharply localized
to the midabdomen. Untreated, ulcers are a common cause of gastrointesti-
nal bleeding, which makes people vomit blood or pass blood in their feces.
Ulcers, especially of the duodenal variety, can also perforate the wall of the
intestine, thereby allowing infectious organisms into the abdominal cavity,
causing generalized infection (peritonitis). Bleeding or perforated ulcers may
cause death.
Throughout most of the twentieth century, the causes of peptic ulcers
were widely believed to be “hurry, worry and curry.” 32 Psychotherapy was
commonly recommended for patients with ulcers as a means of reducing
stress. In 1982, however, Australian researchers proved that most peptic ulcers
are caused by a spiral-shaped bacteria, Helicobacter pylori, which had long
been known to be present in human stomachs but whose significance had not
been appreciated.33 This discovery has profoundly changed our understand-
ing of peptic ulcers.
Approximately 50 percent of the world’s population is infected with He-
licobacter pylori, making it “one of the most common bacterial infections in
humans.” 34 It spreads from person to person in childhood, more quickly in
crowded households.35 The bacteria may possibly also be spread by contami-
nated water or by flies. We are not certain why it causes peptic ulcers in some
individuals and not in others, but genetic predisposition, as described in chap-
ter 1, certainly plays some role.
The origins of Helicobacter pylori are still under debate. Some observers
have suggested that it is an heirloom infection and has infected hominids for
millions of years, while others suggest that it was transmitted from animals to
humans in the more recent past. Many animals carry spiral-shaped bacteria
that are closely related to Helicobacter pylori. Dogs, cats, horses, cows, pigs,
sheep, and some primates are thought to carry Helicobacter pylori itself.36 Sug-
gestions that it spreads from animals to humans have come from studies of
abattoir workers and employees of meat-processing plants, who have an un-
usually high incidence of infection.37
The leading animal candidate as the origin of human Helicobacter pylori
is the sheep. In rural Sardinia, it has been reported that 98 percent of shep-
herds are infected with this bacteria, an infection rate more than twice that
of Sardinians who are not shepherds.38 Helicobacter pylori is also commonly
present in sheep’s milk, which shepherds often drink raw.39 Studies in Sar-
dinia have shown that children in rural areas who are exposed to dogs, many
of which are used to herd sheep, have a higher rate of Helicobacter pylori
infection than children not exposed to dogs.40 Additional support for the as-
sociation of Helicobacter pylori with sheep comes from studies of shepherds in
Poland and from studies in South America that show that children exposed to
sheep have a higher rate of infection.41
The emerging hypothesis regarding the origin of Helicobacter pylori,
then, is that “sheep were the ancestral host of the bacteria and that it entered
the human population after domestication of sheep.” 42 Sheep have been very
closely tied to humans since domestication, as illustrated by the widespread
imagery of sheep and shepherds in the Bible.
Another example of a human disease that was probably originally trans-
mitted from animals to humans after animals were domesticated is whooping
cough, or pertussis. Before public health measures improved and use of a vac-
cine became widespread in the first half of the twentieth century, whooping
cough was one of the most feared childhood diseases. Even today it results in
approximately thirty-five thousand deaths per year worldwide, most of them
in infants.
The bacteria that causes human whooping cough, Bordetella pertussis, is
very closely related to a bacteria (Bordetella parapertussis) that occurs in both
humans and sheep, and also to a bacteria (Bordetella bronchiseptica) that oc-
curs in pigs, dogs, cats, rabbits, rats, horses, and some primates, occasionally
including humans. For many years, it was assumed that Bordetella pertussis
came originally from the sheep bacteria, but recent studies have shown that
this is not the case.43 Instead it now seems likely that human whooping cough
came from pigs.44
Pigs are reservoirs for many human diseases in addition to whooping
cough. For example, the nipah virus is carried by pigs and also affects dogs,
cats, horses, and bats. In 1998 –1999, an outbreak of encephalitis in Malaysia
killed 105 of the 265 people infected with this virus, most of whom had come
in close contact with pigs. The outbreak was brought under control by killing
one million pigs, but smaller outbreaks have since occurred in Singapore and
Bangladesh. Pigs also play a crucial role in the evolution of new strains of the
influenza virus (see chapter 9).
One of the most important diseases that appears to have been transmit-
ted to humans following the domestication of animals is smallpox. Intimately
associated with the history of the New World, smallpox first devastated the
Aztecs and Incas in Mexico and Peru, then wiped out entire tribes of North
American Indians. Smallpox also figures prominently as a potential microbe
for bioterrorism and was one of the first microbes so used; in 1763 British offi-
cer Lord Jeffrey Amherst ordered his troops to give smallpox-infected blankets
to Native Americans to deliberately infect them.45
The origins of smallpox have long been debated. The virus that causes
it is a member of the orthopoxvirus family. This family includes the monkey-

pox virus, which affects many rodents and which recently infected pet prairie
dogs in an outbreak in the United States (see chapter 7). Recent research,
however, suggests that the smallpox virus did not come from the monkeypox
virus.46 The orthopoxvirus family also includes the cowpox virus, which not
only affects cows but also is especially common in members of the cat fam-
ily and may cause mild infections in humans.47 A third closely related virus
is the buffalopox virus, which infects water buffalo, cattle, and occasionally
humans.48 Water buffalo were first domesticated in Southeast Asia,49 and it is
perhaps significant that, approximately three thousand years ago, the earliest
recorded cases of smallpox also appeared in this region.50 Ongoing molecular
research should soon provide a definitive answer regarding the animal origins
of the smallpox virus.
Regardless of the origin of human smallpox, it was the relatedness of the
smallpox virus to another member of the orthopoxvirus family, the vaccinia
virus, that allowed the development of immunizations that have essentially
eliminated naturally occurring cases of smallpox from the face of the earth.
The recent fears concerning the spread of smallpox by means of bioterrorism
have highlighted the importance of vaccinia in terms of providing protection
to the general population.
Tuberculosis
Of all microbes bequeathed to humans as a consequence of animal domes-
tication, the deadliest was the bacterium that causes tuberculosis. Currently,
tuberculosis kills nearly two million people each year worldwide, and it has
“probably killed 100 million people over the past 100 years.” 51 It was for good
reason that John Bunyan, in 1680, called tuberculosis “the captain of all these
men of death.” 52
Even though almost all cases of human tuberculosis are now spread from
person to person, humans were probably first infected by contact with domesti-
cated animals. Robert Koch in 1882 identified the tuberculosis bacterium that
infects humans as Mycobacterium tuberculosis. A closely related member of the
same family is Mycobacterium bovis, which causes an important disease of cattle
and which can also infect sheep, goats, pigs, rabbits, cats, and other animals.
Molecular studies have shown that these two bacteria are almost identical.53
For many years it was believed that Mycobacterium tuberculosis, the cause
of human disease, had evolved from Mycobacterium bovis when cattle were
domesticated. Recent studies, however, suggest a more complex story: Both
bacteria evolved from a common ancestor.54 The studies have also shown that
the Mycobacterium bovis strains that infect cattle and goats differ from each
other—the goat strain has a molecular structure more closely related to hu-
man Mycobacterium tuberculosis than has the cattle strain.55 The authors of
one study concluded: “Considering the results shown here, it is tempting to
speculate that the immediate missing-link ancestor of Mycobacterium tuber-
culosis . . . may be the goat M. bovis strains and not the cattle M. bovis strains,
as was proposed previously.” 56 This hypothesis would also be consistent with
the fact that goats can become infected with human Mycobacterium tubercu-
losis but cattle cannot.57
The ancestors of both Mycobacterium tuberculosis and Mycobacterium
bovis, then, may have been bacteria carried by wild bezoar goats in the Fertile
Crescent. The bacteria would have evolved into the human strain as humans
domesticated goats, sharing living quarters with them, eating their meat, and
drinking their milk.
The sharing of living quarters between humans and animals was an espe-
cially important facet of the evolution of human tuberculosis. Mycobacteria
are unusual microbes insofar as they do not usually cause disease except when
humans or other animals are crowded together. This has been clearly dem-
onstrated in cattle: “It is a universal experience that the incidence of bovine
tuberculosis increases in proportion to the density of the cattle population,
i.e., to the size of the herds and the space allotted to the cattle when they are
kept indoors.” 58 This phenomenon has also been observed in American buf-
falo; when roaming unconfined in a large national park, they were found to
be virtually free of bovine tuberculosis, whereas buffalo confined and mixed
with cattle were reported to be heavily infected.59 Similarly, monkeys that live
in the wild are free of tuberculosis, whereas “the monkey in captivity is the
most susceptible of all animals to tuberculosis.” 60 The events that led to the
evolution of human tuberculosis, then, were not only the domestication of
goats and other animals, but also the crowding together of the animals and
humans into the confined spaces of homes.
The King’s Evil

The earliest claim for the origins of human tuberculosis has been from hu-
man remains in Germany approximately seven thousand years old. Definite
tuberculosis was diagnosed in a mummified corpse in Egypt approximately
three thousand years old; ancient Egypt may even have had a large sanitarium
for treating the disease.61 Tuberculosis was also widespread in ancient Greece
and Rome and spread in ancient times to North America, probably by way of
the Bering land bridge; proof lies in the discovery of Mycobacterium tubercu-
losis in a Peruvian mummy dated to before the arrival of Columbus.62
One manifestation of tuberculosis is enlargement of lymph glands in the

neck, commonly called scrofula. Beginning in the Middle Ages in France
and England, it became widely believed that a king’s touch could heal scrof-
ula. People widely referred to scrofula as “the king’s evil,” and by the reign of
Henry VII in the late fifteenth century, the ceremony of touching scrofulous
individuals had become highly ritualized, with “prayers recited by priests,
stroking of both sides of the face with both hands by the king, hanging a gold
piece about the patient’s neck, and closing prayers and a blessing.” 63 In 1606,
Shakespeare included a description of this ceremony in Macbeth:
Strangely visited people,

All swoln and ulcerous, pitiful to the eye,
The mere despair of surgery, he cures;
Hanging a golden stamp about their necks,
Put on with holy prayers.
(Act 4, scene 3)
Easter Sunday, Pentecost, and the Feast of Michaelmas were especially fa-
vored times. Given the exposure of kings to scrofulous individuals, it is not
surprising that Henry VII, his eldest son, Arthur, and his grandson, Edward
VII, are all thought to have died from tuberculosis.64 Their deaths played a
major role in the history of England. The death of Arthur in 1502, before he
could inherit the throne, resulted in the ascendancy of his brother, Henry
VIII, who eventually led England out of the Catholic Church when the pope
refused to grant him a divorce from his first wife, Catherine. The death of
Edward VII in 1553 led to the ascendancy of his Catholic half-sister Mary,
whose attempts to reinstitute the Catholic Church in England led to much
civil strife and retribution, earning her the appellation “Bloody Mary.” Reli-
gious strife continued in England until Mary’s death and the ascendancy of
her Protestant, and more tolerant, half-sister Elizabeth in 1558.
In the seventeenth century, tuberculosis appears to have markedly in-
creased in incidence. By 1650, it was thought to account for 20 percent of
deaths in England and Wales, with approximately one-quarter of the entire
European population being infected.65 Between 1662 and 1682, King Charles
II is recorded to have touched ninety-two thousand individuals with scrofula.
At a ceremony of touching in 1684, seven persons were trampled to death
while attempting to reach the king.66
Seventeenth-century England presented ideal conditions for the spread
of tuberculosis. In the previous century, the population of London had tripled,
so crowding was endemic; many people lived several to a room. Recurring
visitations of the plague, including the 1665 epidemic that killed one-quarter
of London’s population, weakened people’s immune systems, so they had less
resistance to infections. It was a chaotic century, both socially and politically,

with civil war and an unstable monarchy.
Tuberculosis continued to ravage Europe during the eighteenth and
nineteenth centuries as the industrial revolution brought additional urbaniza-
tion and household crowding. In colder seasons, people crowded around the
fire and kept windows tightly shut, thereby exposing everyone in the house to
microbes carried by any one of them. Many houses had no windows to open.
In 1696 in England, and later in France, the government instituted a tax on
glass windows, which were still considered luxuries; many landlords simply
bricked up the windows rather than pay the tax.67
The death rate from tuberculosis continued to climb, especially in cities
and in crowded institutions. By 1780 in England, more than one person in
every hundred died from tuberculosis each year.68 In an English orphanage,
169 out of 172 children were diagnosed with scrofula; in Paris, tuberculosis
was found to be the cause of death in more than one-third of all cases brought
to autopsy.69
“Blood Was Its Avatar”

At about this time, tuberculosis began to be romanticized. Individuals afflicted
with “consumption,” as it was called, were thought to be endowed with “a pe-
culiar quality of spirituality, even with creative genius.” 70 This view prevailed
especially among the literati of that period.
Poet John Keats was one of many writers and artists who became infected.
When he was fourteen, Keats’s mother died from tuberculosis after he had
spent many weeks caring for her. At twenty-three, Keats nursed his brother,
who was also dying from tuberculosis. Just over a year later, Keats coughed up
blood for the first time; trained as a physician, he immediately knew its mean-
ing. He said to a friend: “I know the color of that blood; —it is arterial blood;
—I cannot be deceived in that color; that drop of blood is my death warrant.
I must die.” Percy Bysshe Shelley, who also had tuberculosis and was Keats’s
close friend, wrote to him: “This consumption is a disease particularly fond
of people who write good verse as you have done.” 71 Shortly thereafter Keats
wrote Ode to a Nightingale, in which “youth grows pale, and specter-thin,
and dies”:
Darkling I listen; and for many a time
I have been half in love with easeful Death.72
One year later, Keats died at the age of twenty-five.

During the 1820s in Germany, Johann Wolfgang von Goethe was com-
pleting Faust, and in Scotland, Sir Walter Scott was publishing a new novel
almost every year; both had suffered from tuberculosis. In 1827, young Fred-
eric Chopin’s sister developed fulminating tuberculosis and, eight years later,
he too began showing the symptoms of the disease that eventually led to his
death. In Paris during the 1840s, two young women who would become op-
eratic heroines died from tuberculosis. One, Alphonsine Plessis, was a well-
known courtesan who became the subject of an 1848 novel and eventually, as
Violetta, the heroine of Giuseppe Verdi’s 1853 opera La Traviata. The other
young woman also became the subject of a novel, Scene da “La Vie de Bo-
hème,” later adapted by Giacomo Puccini as La Bohème. At the end of the
opera, a thin, pale, and consumptive Mimi asks Rudolfo, “Am I still beauti-
ful?” He replies: “As beautiful as dawn.” 73
In England at this time, the closing scenes in the Brontë family trag-
edy were being played out. By the late 1840s, the two youngest children had
died from tuberculosis at the family parsonage in Haworth, and the other four
were to follow. Branwell died in 1848, followed by Emily, who had recently
completed Wuthering Heights. A few months later Anne, who had published
Agnes Gray, died in 1849. Charlotte, author of Jane Eyre, was the last to die,
in 1855. One can visit their home today and see the table they sat around
together as they wrote. From their front porch, the view of the Yorkshire hills
must look as it did then; goats graze quietly on the hillside, unaware of the role
their ancestors may have played in such human tragedies.
In the United States, where Edgar Allan Poe was publishing poems and
short stories, his wife and foster mother had both died from tuberculosis, and
Poe himself was infected. In “The Masque of the Red Death,” Poe described
tuberculosis as “a thief in the night. . . . Blood was its Avatar and seal.” When
the “Red Death” appears, the hour is sounded by “the brazen lungs of the
clock,” and after everyone has died, “the life of the ebony clock went out.” 74
In New England at about this time, Ralph Waldo Emerson and Henry David
Thoreau were sharing a house; both had tuberculosis, which Emerson sur-
vived but Thoreau did not.
In the late nineteenth century, Fyodor Dostoyevsky in Russia wrote about
tuberculosis in The House of the Dead. Dostoyevsky’s wife had died from the
disease, as Dostoyevsky did later. Russian playwright Anton Chekhov suffered
from tuberculosis for many years and eventually died from it. Like Chekhov,
Robert Louis Stevenson suffered from tuberculosis for most of his life. He
described the experience of having tuberculosis as being “like an enthusiast
leading about with him a stolid, indifferent tourist.” 75 At one point, Steven-
son’s doctors splinted his right arm to his chest to try to keep his tuberculous
right lung quiescent; Stevenson then learned to write with his left hand. In
1880, Stevenson was hospitalized in Davos, Switzerland, at a tuberculosis
sanitarium; there he wrote much of Treasure Island.76
Thirty years later, the wife of Thomas Mann was hospitalized at Davos for
the treatment of her tuberculosis. While visiting his wife in 1912, Mann himself
was diagnosed with the disease. He remained at Davos only long enough to make
notes for his novel about a tuberculosis sanitarium, The Magic Mountain.
Late nineteenth-century tuberculosis affected artists as well as writers.
Edvard Munch’s mother died from tuberculosis when he was five, and his
sister died from the disease when he was fourteen. He portrayed his despair
in several paintings, including The Dead Mother, Death in the Sickroom, and,
according to some critics, The Scream.
The scourge of tuberculosis continued to follow writers into the twen-
tieth century. Franz Kafka, Katherine Mansfield, Thomas Wolfe, and George
Orwell all died from it, the last shortly after completing Nineteen Eighty-Four.
Terminally ill with the disease, D. H. Lawrence wrote in The Ship of Death:
“Piecemeal the body dies, and the timid soul / has her footing washed away,
as the dark flood rises.” 77
In the latter half of the twentieth century, following the discovery of strep-
tomycin and other antituberculosis drugs, there was hope of controlling, per-
haps even eradicating, this ancient scourge. In the 1980s, increasingly wide-
spread drug-resistant strains of the bacteria, along with the AIDS epidemic,
extinguished this hope. As the immune system of AIDS patients loses its abil-
ity to fight infections, Mycobacterium tuberculosis is a major invader; thus,
38 percent of new cases of tuberculosis in sub-Saharan Africa now occur in
individuals with AIDS.78
Tuberculosis remains a major threat in the United States as well. In Min-
nesota in 1992, a man with untreated tuberculosis infected forty-one patrons
and employees of a bar he frequented.79 In Maryland in 1993, a university
student with untreated tuberculosis infected thirty-three friends and acquain-
tances; investigators concluded that she had been “more infectious than the
average child with measles.” 80 Tuberculosis has become an especially promi-
nent problem among individuals who are homeless and living in public shel-
ters; in Seattle in 2002, thirty such cases were diagnosed.81
5=
C H A P T E R
Humans as Villagers
Microbes in the Promised Land
Nor is it a new thing for man to invent an existence that he imagines to be
above the rest of life; this has been his most consistent intellectual exertion
down the millennia. As illusion, it has never worked out to his satisfaction
in the past, any more than it does today. Man is embedded in nature.
Lewis Thomas, The Lives of a Cell
P aleolithic hunters were remarkably isolated. For hundreds of thousands

of years, they lived in small, extended family bands, often moving season-
ally to follow the migrations of animals they hunted. According to Karlen’s
Man and Microbes, the hunters “lived in bands of probably a few dozen, per-
haps a hundred at most, . . . seldom exceeding a density of one person per
square mile.” 1 Because of their sparse distribution, contact between groups
was infrequent. During an entire lifetime, an individual would probably have
interacted with no more than a few hundred other individuals.
Neolithic farmers at first were also widely scattered. However, as the do-
mestication of grains and animals progressed, a reliable supply of food was
increasingly available in a single location. Individual families began settling
closer to each other in hamlets and small villages, often living in homes clus-
tered together and farming the surrounding fields. Such villages afforded mu-
tual protection against wild animals, which would have been attracted to the
domesticated animals. The villages also offered some protection against other
human groups that might try to steal their grain or animals. Most villages con-
sisted of three hundred people or less. During an entire lifetime, an individual
would probably have interacted at most with only a few thousand others.
Over time, some of the villages grew to become towns. By nine thousand
years ago, Zawi Chemi Shanidar in northern Iraq, Jericho in Israel, and Cat-
48 =
Humans as Villagers = 49
alhöyük in Turkey had all achieved town status. Jericho, for example, had a
population of approximately two thousand people and had a wall around it
for protection. In Catalhöyük, the homes were substantial: “The living rooms
had built-in furniture consisting of benches and platforms, as well as hearths
and ovens, all made from earth and plaster. Groups of rooms, each with a
storeroom, were centered around shrines.” 2
A relatively stable food supply and settled population made it easier to
raise children, and so beginning approximately ten thousand years ago, hu-
mans began proliferating more quickly. It has been estimated that the world’s
population was no greater than five million when domestication of grains
and animals began. Within four thousand years, the world’s population had
increased tenfold, to approximately fifty million.3 Towns grew accordingly,
and a few merged with other nearby towns to create the first urban centers
of eighty to one hundred thousand people. During an entire lifetime, an
individual living in such an urban area may have interacted with as many as
ten thousand others.
The urbanization of Neolithic people occurred first in Mesopotamia,
which was watered by the Tigris and Euphrates rivers. Uruk, Ur, Lagash, Kish,
and Erech were significant centers of population; Erech’s walls encompassed
two square miles.4 In Egypt, urban centers such as Memphis and Thebes de-
veloped in the Nile Valley; in what is now Pakistan, along the Indus River,
Mohenjo-Daro and Harappa became important centers of population. By ap-
proximately 4,500 years ago, each of these three river valleys “probably con-
tained about three-quarters of a million people.” 5
A Microbial Feast
From the viewpoint of bacteria, viruses, and protozoa, village life offered many
advantages. Closed and dark houses kept out sunlight, a powerful enemy of
microbes. The houses also promoted the recirculation of stale air, so that
microbes could move freely among human respiratory tracts, especially in
crowded rooms. Permanent houses also promoted the accumulation of trash,
garbage, and feces, which attracted mice, rats, mosquitoes, and flies, some of
which moved permanently into the human dwellings. As Karlen described
conditions: “The gardens of Babylon and temples of Egypt were emblems of
urban glory, but the alleys in their shadows were choked with garbage. Homes
reeked with fetid air and smoke. Vast amounts of human and animal wastes
accumulated; water was drawn from contaminated wells, food harvested from
tainted fields. Dirt and refuse drew every germ-bearing scavenger that flew,
crept, or crawled.” 6 Mosquitoes, flies, and other vectors fed on both humans
and domesticated animals nearby. For microbes, which for millions of years
had chased nomadic animals and hominids across open spaces, it was like
sitting at a banquet table.
Predictably, the bringing of people together into villages, towns, and ur-
ban areas resulted in increasing microbial-caused infections. Studies of early
settlements, for example, reveal that “the percentage of individuals displaying
signs of infection doubled in the transition from hunting and gathering to
intensive maize cultivation; . . . rates of infection were positively correlated
with the size and permanence of the communities.” 7
The main reason increasing microbial infections follow an increasing
density of people is that many microbes cannot exist without a minimum
density of people or other animals. For example, “a strain of ear-nose-throat
bacteria that persists for an average of four months may be sustained by a
group of only 70 persons, while one that persists for only one month may
require up to 500 persons if continuing transmission is to be achieved.” 8 A
sufficient population density is especially necessary for microbes that induce
permanent immunity following initial infection. In such cases, there must
be enough susceptible individuals who have never been infected to keep the
microbe circulating; once it infects everyone, it simply dies out.
For such reasons, many infectious diseases increased in incidence as
humans moved closer together in ever-increasing groups. Tuberculosis and
smallpox are well-known examples, and evidence of both has been found in
mummies from ancient Egypt. Less known are microbes that began to infect
humans only when a sufficient number of people lived together.
Examples of this that everyone has experienced are human rhinoviruses,
the most frequent causes of common colds. For many years, it was assumed
that rhinoviruses had been originally transmitted to humans from horses, but
more recently it has been shown that human rhinoviruses originated from
bovine counterparts in cattle.9 After transmission to humans, the rhinoviruses
underwent mutations and specifically adapted to humans, as discussed in
chapter 1. Thus, human rhinoviruses are no longer thought to be transmit-
ted to humans from cattle but rather to circulate only among humans. To do
this, they need a large group of people to act as a reservoir for the viruses and
to keep the viruses from dying out. Such conditions exist only in towns and
urban areas. Thus, human colds are a product of humans’ both having domes-
ticated cattle and then moving into villages and towns.
Measles
The best example of a microbe that requires a large number of people to
survive is the measles virus, which was also originally transmitted to humans
from cattle. Like human rhinoviruses, the measles virus no longer spreads
from animals to humans but is instead transmitted exclusively from humans

to humans. Since it confers permanent immunity following an initial infec-
tion, measles can exist permanently only where at least 250,000 people live in
contact with each other.10 That is the minimum number required to ensure
that there will always be a sufficient number of uninfected individuals to keep
a chain of infection going. Since most people who are not yet infected in
such populations are children, measles is usually a childhood illness. When
measles is introduced into isolated populations of less than 250,000 people, by
contrast, the disease may sweep through not-previously-infected members of
all ages, but then dies out until it is introduced again from outside.
Measles is widely regarded as a benign infection; for most persons in-
fected, it is. However, for a minority, it may be deadly; measles kills about two
million people a year worldwide, and between 1840 and 1990, killed about
two hundred million.11 The lethal potential of measles arises from two sources.
First, measles cripples the body’s immune system. In doing so, it is similar to
the HIV virus that causes AIDS.12 With the immune system impaired, other
infectious agents can freely replicate, and this occurs even more rapidly in
individuals who have poor nutrition or existing concurrent diseases. Thus, it
is possible for individuals with measles to die from pneumonia, tuberculosis,
typhoid, or other infections. This also explains why the mortality rate from
measles may be as high as 10 percent in developing countries, compared to
one-tenth of 1 percent in developed nations.
The other reason measles can be deadly is that it invades the brain. It
apparently does this as a matter of course, since a study of electroencephalo-
grams (EEGs) in children with uncomplicated measles showed that half of
them had EEG changes.13 In some individuals, the measles virus causes an
acute or chronic infection of the brain (encephalitis). Before the introduction
of measles vaccine in 1963, acute measles encephalitis affected approximately
four thousand children in the United States each year, leaving one-quarter of
them with deafness, blindness, seizures, mental retardation, or other brain
damage.14 In some cases, measles encephalitis may not become symptomatic
for several years after the original infection and may then progress to coma
and death.
The measles virus belongs to the morbillivirus family and is a direct off-
spring of the rinderpest virus of cattle. Studies of the molecular structure of
measles virus have shown it to differ very little from its rinderpest parent and
to be more closely related to rinderpest than are any of the other morbilli-
viruses.15 Other members of the morbillivirus family that are more distantly
related to the measles virus of humans are the canine distemper virus of dogs
and other canines, pest-des-petits virus of sheep and goats, phocine distemper
virus of seals, and distemper virus of dolphins.
The measles virus is thought to have evolved from the rinderpest virus
after the domestication of cattle. Rinderpest is endemic in cattle and, when

introduced to previously uninfected herds, can cause a severe epidemic. In the
1740s, rinderpest killed one-half of the cattle in France; in the 1890s, it devas-
tated both cattle and related wild animals in Africa, as noted in chapter 1.
After humans domesticated animals, as we have seen, cattle and humans
lived closely together; people milked their cows, helped them give birth,
butchered them, and ate their meat. Drawings from Mesopotamia depict
cows being milked, and paintings from ancient Egyptian tombs show differ-
ent breeds of cattle. Until comparatively recently, in much of the world cattle
and humans lived under the same roof; according to Thomas in Man and the
Natural World, even in recent times in some areas of western Europe, it was
said “that cows gave better milk if they could see the fire.” Even people who
themselves did not own cattle were exposed. “In the towns of the early mod-
ern period animals were everywhere, and the efforts of municipal authorities
to prevent the inhabitants from keeping pigs or milking their cows in the street
proved largely ineffective.” 16
Because the measles virus needs a population reservoir of at least 250,000
people to survive, measles as a disease did not exist before the rise of the urban
centers in the Tigris-Euphrates, Nile, and Indus river valleys approximately
five thousand years ago. Measles almost certainly existed after that time in
the ancient world, but definitive descriptions are lacking because of its confu-
sion with smallpox, chickenpox, rubella (German measles), scarlet fever, and
other diseases that cause a rash. There are claims that measles was described
in ancient Greece, Rome, Egypt, and China, but the first unequivocal descrip-
tion of the disease was provided by Al-Razi (Rhazes) in tenth-century Persia.
This brilliant Muslim physician, whose full name was Abu Bakr Muhammad
ibn Zakariyya of Ray, differentiated measles from smallpox and prescribed a
treatment for both. Despite al-Razi’s work, measles and smallpox continued
to be confused for several hundred years more. However, by the seventeenth
century, the two were definitely viewed as separate diseases, as illustrated by
this quotation from English essayist Thomas Fuller: “Therefore the [measles]
Pestilence can never breed the Small-Pox, nor the Small-Pox the Measles, . . .
anymore than a Hen can a Duck, a Wolf a Sheep, or a Thistle Figs.” 17
“La Pequena Lepra”

The lethal potential of measles has been demonstrated many times in recent
centuries when it has been introduced to previously unexposed populations.
Mortality has been especially high in populations that suffer from poor nu-
trition and when measles has occurred in association with other diseases.
Since measles suppresses the immune system, any concurrent disease be-
comes more virulent.
A dramatic illustration of the effects of measles plus smallpox followed
the arrival in the Americas of European explorers who inadvertently brought
with them both viruses, along with other infectious diseases. Smallpox struck
first and was rapidly followed by measles. For example, in 1529, “a measles
epidemic in Cuba killed two-thirds of the natives who had survived small-
pox.” 18 In 1530, measles spread to Mexico and Peru, in 1531 to Honduras,
and in 1532 to Nicaragua and Guatemala, killing up to half the inhabitants.
A missionary wrote: “The Indians die so easily that the bare look and smell
of a Spaniard caused them to give up the ghost.” 19 Measles was known as “la
pequena lepra” (the little leprosy) in contrast to “la gran lepra” of smallpox,
which had preceded it.20
The devastation caused by these two diseases significantly altered the his-
tory of the New World. As noted by Karlen in Man and Microbes: “The toll
of smallpox and measles was ten thousand here, a hundred thousand there,
whole cities and tribes wiped out, cultures and languages lost. Corpses lay scat-
tered in fields and heaped in silent villages.” 21 Before the arrival of Europe-
ans, the native populations of Mexico and Peru were between twenty-five and
thirty million each; by the end of the sixteenth century, only approximately
10 percent of the population remained.22 Confronted by the immunity of the
Spaniards to these diseases (because they had been infected in childhood),
the remaining natives accepted smallpox and measles as the white god’s judg-
ment on themselves and rapidly converted to Catholicism. The Aztec and
Inca civilizations, among the most advanced in the world when the Europe-
ans arrived, essentially ceased to exist as organized societies.
Elsewhere in the Americas, the effect of measles on the indigenous popu-
lation was similar, if less well documented. In Florida, a measles epidemic
in 1531 killed about half the native population; a second epidemic in 1596
killed one-quarter of those who remained.23 In 1837, measles broke out on the
North American plains among two thousand Mandan Indians who were un-
der siege by their Sioux enemies. According to McNeil: “Their numbers were
reduced from about 2,000 to a mere 30 – 40 survivors in a matter of weeks; and
those survivors were promptly captured by enemies so that the Mandan tribe
ceased to exist.” 24 Canadian Indians similarly suffered. In 1819 and 1820, a
measles epidemic killed “whole bands” of Chippewas; “one-third of the native
population in the vicinity of Fort Chipewyan . . . is believed to have perished
from an epidemic of dysentery accompanied by measles.” 25
The lethal effect of measles in combination with influenza was tragi-
cally illustrated when the two diseases simultaneously struck Alaska in 1900.
According to studies of the epidemic, “a quarter of western Alaska’s Eskimo
population perished,” with many villages virtually wiped out.” At Ugavig, 60

of 132 inhabitants died. At Dog Fish Village on the Yukon River, 20 of 27
residents died. The Eskimos called it the “Great Sickness,” and as a mission-
ary described the epidemic: “Many were the wretched sights to be seen as
the plague progressed. We used to go slopping along in the mud under a
constant downpour of rain, through the stricken village of tents and cabins
with our rumbling dead cart hauling out the unfortunate victims, while all
around in the dark could be heard the fatal cough and groans of the sufferers.
It was dismal work indeed. The very dogs ceased to howl, some forever, as the
poor things overlooked in the general misery starved to death in their chains.”
And in another village: “At one place some passing strangers heard the crying
of children, and upon examination found only some children left with both
parents dead in the tent.” 26
On St. Paul Island, isolated in the Bering Sea, influenza arrived by ship
on June 11, 1900. It infected virtually all the two hundred Aleut inhabitants
and caused seven deaths. Two months later, measles arrived by another ship.
It also infected virtually every inhabitant, so that “on 9 September only two
Aleuts were not bedridden; . . . deaths continued almost daily until 3 Octo-
ber.” Altogether, measles killed 10 percent of a population already weakened
by influenza.27
There are many other examples of isolated human populations devas-
tated by measles when initially exposed. In Iceland, an 1846 epidemic killed
2,026 people, 3 percent of the population. Another epidemic in 1882 killed
1,700 more. Measles first arrived in southern Greenland in 1951; out of a
population of 4,262, all except 5 individuals were affected, and 77 died.28
In the South Pacific, measles arrived in then-isolated Sydney in 1834 and
again in 1854, 1860, and 1867. The last epidemic was well documented; “in
only a handful of months measles carried off more than 700 young children.”
This epidemic also illustrates the importance of poor nutrition and lower so-
cioeconomic status as contributors to measles mortality. Among the poorest
Sydney families, the mortality among children was approximately 30 percent,
whereas among the wealthiest families, the mortality was less than 1 percent.29
Perhaps the best-known epidemic of measles swept through Fiji in 1875.
The king of Fiji and his family had traveled to Australia to participate in the
signing of a treaty with Britain, making Fiji a British colony. While in Austra-
lia, the king and his son were infected with measles, which was subsequently
transmitted to other members of the group en route home. When the king
arrived in Fiji, he was greeted by local chiefs, many of whom had traveled
from the outer islands. Two days of discussions and celebrations followed,
after which the chiefs returned home.
Within two months, measles had spread throughout Fiji, with lethal re-
sults. According to one account: “The attacks have been so sudden and com-
plete that every soul in the village is down with it at once, and no one able to
procure food or if procured cook it for themselves or others. . . . People have
died of starvation and exhaustion in the midst of plenty.” 30
It was estimated that “not less than 40,000 Fijians died from the measles
in the following four months out of a population of approximately 150,000,
thus depleting the population by at least 27 percent.” 31
Among European settlers in the United States, measles was also a sig-
nificant problem among rural populations that had not been exposed to the
disease in childhood. During the Civil War, young men from rural areas were
brought together with inevitable results: “Training programmes were so thor-
oughly disrupted by measles epidemics that companies, battalions and even
whole regiments were disbanded temporarily and the men sent home.” 32
Knowledgeable Civil War commanders, aware that measles could devas-
tate their troops, took only “seasoned” regiments into battle. When one Con-
federate general was asked to forward troops for battle, he promised to send
them “as soon as [he could] have them put through the measles; a process
which they are now undergoing—one-half of them now being sick.” General
Robert E. Lee also astutely noted the effects of measles on his troops: “We
have a great deal of sickness among the soldiers, and now those on the sick-list
would form an army. The measles is still among them, though I hope is dying
out. But it is a disease which though light in childhood is severe in manhood,
and prepares the system for other attacks. The constant rains, with no shelter
but tents, have aggravated it.” 33
Measles favored neither side in the Civil War. Among Union forces,
76,318 cases, with 5,177 deaths, were recorded. At a Confederate camp in
North Carolina, “4,000 cases of measles developed among 10,000 troops.” 34
The most famous Civil War victim of measles was, however, a fictional
one. In Margaret Mitchell’s novel Gone with the Wind, Scarlett O’Hara’s first
husband went off to war three weeks after their marriage. Less than two months
later, Scarlett received a telegram informing her that her husband “had died
ignominiously and swiftly of pneumonia, following measles, without ever hav-
ing gotten any closer to the Yankees than the camp in South Carolina.” 35
Measles, then, is an example of a microbe that was originally transmitted
from animals to humans but that became a problem only when humans came
together in villages, towns, and urban centers. Other microbes also found ur-
ban living to their liking, spreading more easily from person to person. Some
of the microbes became so successfully established in the new urban centers
that they found new and even faster ways to spread themselves. Today Uruk
and Thebes, tomorrow the world.
6=
C H A P T E R
Humans as Traders
Microbes Get Passports
It is obvious that the equilibrium of human communities and of the ani-
mals kept by man has been drastically altered during the small number of
generations since man was living as a highly successful nomadic predator
animal. It is this disequilibrium which has imparted to infectious disease
such an important role.
Richard Fiennes, Man, Nature, and Disease
F or millions of years, microbes that were attached to mammals traveled

neither very far nor very fast. Most hominids and other animals spent
their lives in relatively circumscribed areas, and when they eventually mi-
grated out of Africa, they traveled slowly. Since there were few opportunities
for microbes to spread widely to nonimmune populations, microbe-caused
disease epidemics were probably rare occurrences.
As Neolithic farmers settled into villages, and towns grew into urban cen-
ters, trade and warfare increased the opportunities for travel for humans, other
animals, and the microbes that accompanied them. As early as nine thousand
years ago, Catalahöyük in Turkey was a center of trade.
By the time the Mesopotamian civilizations flowered along the Tigris
and Euphrates rivers, trading over long distances had become commonplace.
Artisans of Mesopotamia produced pottery, leather goods, tools, and jewelry
made from copper, silver, and gold, which were offered in trade. In exchange,
Mesopotamians imported copper ore from Oman, gold and silver from Tur-
key, shells from India, lapis lazuli from Afghanistan, and cedar from Lebanon.
Food was traded, including dates from Bahrain and wine from the shores of
the Mediterranean. Domesticated animals were also commonly traded, and
56 =
H u m a n s a s Tr a d e r s = 57
this was a major reason they spread so rapidly throughout the civilized world.
The long-distance trade was often highly organized; 4,500 years ago, for ex-
ample, Mesopotamia maintained a “colony” in Turkey to oversee its imports
and exports.1
The speed with which humans, other animals, and microbes could travel
increased substantially with the domestication of horses and camels and the
introduction of ships. A journey that once had taken a week’s walking could
be completed in two days on horseback. At approximately the same time that
horses were becoming widely used for travel, Egyptian merchant trading ships
began plying the Mediterranean, later to be joined by Greek and Phoenician
ships. From Lebanon came glass, textiles, metals, timber, and wine. From
Egypt came linen, papyrus, gold, and ivory. From Cyprus came copper. From
Arabia came dates, amber, and other resins. By the time of the Roman Em-
pire, domesticated cattle were widely traded throughout the Near East and
Europe, and Rome imported a thousand tons of wheat per day from North
Africa.2
The movement of humans, domesticated animals, and microbes by trade
routes was supplemented by warfare-associated travel. Disputes between
neighboring groups of hominids had certainly always existed, but horses and
ships elevated sporadic fighting to the level of warfare. Sargon the Great led
military campaigns from Mesopotamia into Syria and Turkey more than four
thousand years ago; five hundred years later, Persians invaded and destroyed
the cities of the Indus Valley in Pakistan. When chariots were invented and
attached to horses approximately four thousand years ago, power shifted to the
Hittites and other horse-raising groups from the Asian steppes.
With the use of camels, horses, and ships, the pace of the world acceler-
ated. Along established trade routes, increasing numbers of people, animals,
and microbes interacted with each other in crowded bazaars and caravansa-
ries. Warfare brought famine, rape, and the forcible resettlement of large num-
bers of slaves and animals as spoils of war. Before the introduction of ships,
“dispersal of disease over long distances was slow and required a larger host
population to remain intact until it reached a new population,” but with ships
the passengers “could act as a disease reservoir with reasonably swift dispersal”
of the disease.” 3 Bacteria, viruses, and protozoa that had remained relatively
localized for millions of years found themselves in new environments and in
contact with large numbers of susceptible humans and other animals.
The consequences of this unprecedented human movement were pre-
dictable. Ancient heirloom infections like hepatitis, malaria, and yellow fever
and more recent diseases like measles, smallpox, and tuberculosis, which had
come from animal domestication, began spreading more widely. Epidemics
followed.
The first suggestion of epidemics in human history comes from Mesopo-

tamia, where there is “a stone inscription describing epidemics and invoking
the Goddess of Epidemics.” 4 Among these are the biblical “ten plagues” that
led to the release of the Hebrews from their Egyptian enslavement; a “pes-
tilence” that killed 70,000 Israelis in three days;5 and a disease said to have
killed 185,000 Assyrians overnight.6
Epidemics were also recorded by the ancient Greek writers. The most
noteworthy, as we will see in chapter 11, was the plague of Athens, which
reached its height around 430 b.c.e. The epidemic was thought to have arisen
in Ethiopia and to have affected Egypt before moving to the port of Piraeus and
then to the rest of the Athens city-state. Recent excavations carried out during
the building of the Athens subway confirmed the existence of the plague: A
mass grave was uncovered that contained the remains of many plague victims,
who had apparently been buried in great haste.7 This discovery appears to
confirm the observation of Thucydides, who wrote: “All the funeral ceremo-
nies which used to be observed were now disorganized, and they buried the
dead as best they could. Many people, lacking the necessary means of burial
because so many deaths had already occurred in their households, adopted
the most shameless methods.” 8 The cause of the plague in Athens has been
the subject of intense speculation but has never been conclusively identified.
However, the effects of the plague are clear: It resulted in the death of approxi-
mately one-third of the population of Athens.
Even allowing for an apocryphal element in some of these accounts, it
seems evident that epidemics of disease periodically swept the Middle East
and eastern Mediterranean region in an era in which human travel was in-
creasing, both in numbers and speed. Medical speculations have been legion
regarding which human disease caused which ancient epidemic. The results
are quite unsatisfactory because the descriptions of most of these epidemics
are too fragmentary to allow for specific attribution. Among diseases that have
been suggested are measles, smallpox, influenza, typhoid, typhus, glanders,
and plague. The last is least likely since rats, which carry plague, had not yet
arrived in the Middle East.
The Arrival of Rats

Mice and rats are rodents, along with squirrels, chipmunks, marmots, gerbils,
hamsters, guinea pigs, woodchucks, beavers, and porcupines. Mice and rats
originally evolved in central Asia, India, and Pakistan and were confined to
that region for millions of years. At Bhimbetka in northern India, there is
an ancient but undated rock drawing of several rats being carried in a bag.
Mice and rats diverged approximately ten million years ago; DNA differences
between them, in fact, are ten times greater than DNA differences between
chimpanzees and humans.9
Rats migrated from their ancient homeland rather late in history. The
Greeks and Romans had no word for them, and, according to Hans Zinsser’s
Rats, Lice, and History, “most scholars agree that there is no reliable mention
of rats—as such—in classical literature.” 10 When the rats finally did migrate,
they carried with them Yersinia pestis, the bacteria that causes human plague.
Plague is transmitted from rats to humans by using fleas as vectors; the fleas
bite infected rats, then bite humans, and thereby transmit the bacteria.
Yersinia pestis is unusual insofar as it is, in microbial terms, a relative
newcomer. It evolved from, and is almost identical to, Yersinia pseudotubercu-
losis, a bacteria that is widely distributed among rodents, other mammals, and
birds. In humans, Yersinia pseudotuberculosis causes a mild intestinal disease.
According to recent molecular studies, Yersinia pestis evolved from Yersinia
pseudotuberculosis sometime within the past few thousand years, “shortly be-
fore the first known pandemics of human plague.” 11
What causes a comparatively harmless bacteria like Yersinia pseudo-
tuberculosis to undergo changes in genetic structure and evolve into a closely
related but highly malignant Yersinia pestis? Such changes may occur when
a bacteria infects an animal species it has not previously infected. They may
also occur when two different microbes infect a single mammal at the same
time, resulting in an exchange of genetic material between the microbes.
This is the same mechanism that makes some strains of influenza so deadly,
as we will see in chapter 9. There is some evidence that Yersinia pseudotuber-
culosis may have undergone malignant transformation as part of a simulta-
neous infection of a mammal with Salmonella typhi, a related bacteria that
causes typhoid fever.12 The transformation of Yersinia pseudotuberculosis into
the plague bacteria almost certainly took place in central Asia, since Yersinia
pestis even today is endemic among marmots and gerbils of that region; it does
not cause apparent disease in them, although it does cause disease in rats. The
transformation to Yersinia pestis may therefore have occurred when Yersinia
pseudotuberculosis made the jump from marmots and gerbils to rats.
The evolution of one species of bacteria into a closely related species
with different properties presumably occurs frequently in nature. In the case
of Yersinia pestis, we would not even be aware of its existence had it remained
a microbe of rodents living remotely from humans, as rats once did. However,
once humans began to travel, rats traveled with them. Rats joined caravans
of traders going back and forth between the Middle East and China, passing
directly through the rats’ ancient homeland. And rats in large numbers came
aboard ships and traveled by sea. The most common rat at that time was the
black rat (Rattus rattus), originally a tree dweller known for its remarkable
climbing ability. It is said to easily climb up “slick-painted drainpipes, eleva-
tor cables, or telephone wires” and “can gnaw a hole in a ceiling while at the
same time gripping tightly an electric wire.” 13 The black rat thus had no dif-
ficulty entering and exiting ships on mooring lines. As trade increased, so did
the distribution of the black rat.
Once rats arrived in a new area or disembarked at a new port, they spread
rapidly because they are so prolific. They can breed at four to six months of
age, have a gestation period of only twenty days, and have four or five litters
each year, with up to ten rat pups in each litter. By one estimate, a single rat
can theoretically produce as many as fifteen thousand descendents in a year.14
This rapid rate of reproduction also means, in evolutionary terms, that rats
can quickly adapt to new conditions and climates.
The first definite appearance of rats in the Mediterranean region was
not until the sixth century c.e. The rats, infected with Yersinia pestis, prob-
ably arrived by ship, since plague first appeared in port cities of Egypt. From
there, it spread quickly to Constantinople, where “panic, disorder, and mur-
der reigned in the streets. . . . There were too many corpses to bury. The roofs
were removed from the city’s fortified towers, and bodies were stacked in them
like cordwood. Soon the towers filled, and the stench became unbearable.
People kept dying, up to 10,000 each day, and there was no place to put the
corpses. Rafts were loaded with the dead, rowed out to sea, and set adrift.
When this bout of plague ended, 40 percent of the city’s people had died.” 15
Contemporary descriptions leave little doubt about the diagnosis: “They had
a sudden fever; . . . not many days after, a bubonic swelling developed. . . .
With some the body broke out in black postules . . . and these did not survive
even one day.” 16 The swellings, or bubos, were enlarged lymph nodes and are
characteristic of plague.
This was the plague of Justinian, named after the emperor of the eastern
Roman Empire who ruled from Constantinople.
The Black Death

In the centuries following the plague of Justinian in the sixth century c.e.,
periodic outbreaks recurred but on a smaller scale. The black rat continued
to spread by land and by sea, increasing significantly in Europe with the re-
turning Crusaders. When rats reached Ireland, the Irish called them “French
mice.” 17 By the thirteenth century, rats had become so abundant that they
threatened food supplies.
In central Germany, the town of Hamelin was infested. According to leg-
end, a mysterious piper appeared and offered to rid the town of rats for a cer-
tain sum. The townspeople accepted the proposal, and the piper thereupon
played his pipe and led the rats into the Weser River, where they drowned.
When the town refused to pay him, the piper returned the next day, played his
pipe again, and this time led the town’s children to a mountain cave, where
all but two disappeared.
By the fifteenth century, rat catchers had become valued citizens in Eu-
rope and were organized into guilds. In some areas, they wore multicolored
(pied) uniforms and carried flags with pictures of rats on them. Some rat catch-
ers became wealthy, since they were paid a bounty for each rat they caught; in
addition, rat skins were used to make inexpensive coats, gloves, and trim for
collars. Shakespeare alludes to rats several times, as when Hamlet plunges his
sword through a drapery, thinking that Claudius hides there, and cries: “How
now! A rat? Dead, for a ducat, dead!” 18 It was also at this time that Cervantes
wrote in Don Quixote de la Mancha: “I begin to smell a rat.” 19 In later centu-
ries, rat catchers were immortalized in literature, as in Goethe’s poem “The
Rat Catcher,” and in paintings by Vischer and Rembrandt.
The Black Death, or Great Pestilence as it was known at the time, began
in 1338 at Issyk Kul, in what is now Krygyzstan in central Asia. Plague broke
out in a trading community and spread south into India, east into China, and
west toward the Middle East along the caravan routes. By 1346, it had reached
the shores of the Mediterranean and Black seas. In Aleppo and Gaza, five
hundred people died each day, and rumors reached Europe that “all of India
was said to be depopulated, whole territories covered by dead bodies, other
areas with no one left alive.” 20
On April 27, 1348, three ships arrived in Genoa from Caffa, a major
Genoese trading port on the Black Sea (now Feodosiya, Ukraine). According
to a contemporary writer, the ships were “carrying horrible disease from the
East.” 21 Simon Boccanegra, the Genoese doge who would later be immortal-
ized by a Verdi opera, turned the ships away. Another ship from Caffa arrived
in Messina, Sicily, “with dead and dying men at the oars.” 22 Soon the plague
had swept ashore at every Mediterranean port, carried by the fleas on the dy-
ing rats and men.
In contrast to the sixth-century plague, the fourteenth-century plague
spread throughout Europe because black rats had by then become widespread.
A favorite place for them to live was in the thatch roofs of dwellings used by
all except the wealthiest people. When rats died, their infected fleas dropped
onto the people who lived below. As has been noted, “the distribution and
density of the rat population governs the distribution and intensity of the hu-
man disease.” 23 Carried by ships, plague spread up the Arno to Florence and
up the Rhone to Avignon; then it continued inland.
Italy, with three of the four largest cities in Europe, was hardest hit. Siena,
Parma, Verona, Genoa, and Naples lost half their populations. Giovanni Boc-
caccio in his 1353 Decameron described the plague in Florence:
Many dropped dead in the open streets, both by day and by night, whilst
a great many others, though dying in their own houses, drew their neigh-
bors’ attention to the fact more by the smell of their rotting corpses than
by any other means. And what with these, and the others dying all over
the city, bodies were here, there and everywhere. . . . Tedious were it to
recount, how citizen avoided citizen, how among neighbors was scarce
found any that shewed fellow-feeling for another, how kinsfolk held aloof,
and never met, or but rarely; enough that this sore affliction entered
so deep into the minds of men and women, that in the horror thereof
brother was forsaken by brother, nephew by uncle, brother by sister, and
oftentimes husband by wife: nay, what is more, and scarcely to be be-
lieved, fathers and mothers were found to abandon their own children,
untended, unvisited, to their fate, as if they had been strangers. . . . It was
come to this, that a dead man was then of no more account than a dead
goat would be today.24
Italian poet Francesco Petrarch, whose beloved Laura died from the plague,
asked: “Is it possible that posterity can believe these things? For we, who have
seen them, can hardly believe them.” 25
At Avignon in southern France, when graveyards filled up, bodies “were
thrown into the Rhone until mass burial pits were dug for dumping the
corpses.” 26 Avignon was the seat of the papacy from 1309 to 1377, and Pope
Clement VI, on orders of his physicians, sat quietly between two huge blaz-
ing fireplaces until the plague had passed. King Philip VI asked the medical
faculty at the University of Paris what was causing the plague; they replied that
it was caused by an unusual alignment of the planets, and this belief became
widespread. In many French, Swiss, and German cities, Jews were blamed for
the plague and were persecuted; in Strasbourg, an estimated nine hundred
Jews were burned to death on February 14, 1349.27
Month after month, the Great Pestilence rolled northward into England,
Ireland, Scotland, and Scandinavia, eventually reaching even Iceland and
Greenland. Off the coast of Norway, a ship ran aground because its entire
crew had died.28 Monasteries, hospitals, and prisons, where many people
lived closely together, were especially affected, since infected fleas could
move quickly among their inhabitants. In Montpellier in France, only 7 of
140 Dominicans survived.29 At a monastery at Ivy Church in England, only 1
of 13 monks lived.30 And at a monastery in Kilkenny, Ireland, a monk watched
each of his brothers die until he was the only one left. Before he, too, died,
he wrote:
Now I, brother John Clyn, of the Order of Minor Friars and the commu-
nity of Kilkenny, have written in this book these notable events that have
occurred in my time, which I have learned from the evidence of my own
eyes or upon reliable report. And lest [these] notable events should per-
ish with time and fade from the memory of future generations, . . . while
waiting among the dead for the coming of death, I have set them down
in writing just as I have truthfully heard and examined them. And lest the
writing should perish with the writer and the work with the workman, I
leave the parchment for the work to be continued in case in the future
any human survivor should remain, or someone of the race of Adam
should be able to escape this plague and continue what I have begun.31
In these small communities, it must have seemed as if the end of the world
had truly arrived.
Historians disagree regarding the number of people who died during the
Great Pestilence from 1348 to 1350, with most estimates ranging from one-
quarter to one-third of Europe’s population. There are also disagreements re-
garding the relative role of other diseases, especially anthrax and typhus, in
increasing the mortality. It seems certain, however, that plague was the main
cause of death, since there are many classic descriptions of the symptoms,
especially enlarged lymph nodes (bubos) in the groin or armpit, depending
on whether the initial fleabite was on the person’s leg or arm.
The effect of the Great Pestilence on European society was profound.
Norman Cantor called it “the greatest biomedical disaster in European and
possibly in world history” and discussed at length the social and economic
disruption it brought about.32 A shortage of labor led directly to the Peasants’
Revolt of 1381 and the subsequent decline of serfdom. The fact that a dispro-
portionate number of monks and priests died undermined the Church; if this
was God’s will, he was indeed a mysterious God. The plague also provided
impetus to the development of public health, since it was the first time that
quarantines were used; arriving ships were forced to lie at anchor for forty
days (quarant is the French word for “forty”) until it was certain there was no
plague on board.
During the 1350s, the Great Pestilence slowly diminished, but smaller
epidemics of plague continued to recur in Europe and throughout the world.
Outbreaks in Venice between 1575 and 1577 and again from 1630 to 1631
are said to have killed one-third of the population. England had major out-
breaks in 1563, 1593, 1603, and 1625, but these were eclipsed by the Great
Plague of London in 1665, when half the population, including King Charles
II and his entire court, fled the city. Of those who remained, approximately
one-third died. This outbreak of plague was noteworthy in being documented
by Samuel Pepys in his Diary and later fictionalized by Daniel Defoe in his
Journal of the Plague Year. The Great Plague of London was also memorable
because of widespread beliefs that venereal disease and smoking provided
some immunity from the plague. It has been speculated that “the modern use
of tobacco in Britain . . . may have derived from its supposititious efficacy as a
prophylactic against bubonic plague, for the menace of plague and the terror
inspired by its rumored approach persisted among the population until late
in the nineteenth century.” 33 Strong odors were also believed to be protec-
tive and gave rise to the wearing of eau de cologne, based on an eighteenth-
century formula from Cologne, Germany, among those who could afford it.
Plague in the United States

Plague entered the United States on January 2, 1900, by way of infected rats
on a steamship that arrived in San Francisco. The ship had come from Hono-
lulu, which, along with Hong Kong, Kobe, and other Pacific ports, was expe-
riencing plague.
The 1900 epidemic had begun in 1894 in central Asia. A change in wom-
en’s fashions had made the fur of marmots more valuable, so Manchurian
hunters began trapping and selling them.34 Since Yersinia pestis is widespread
among marmots, some of the hunters contracted plague. It spread to Hong
Kong, and then in 1896 to India.
San Francisco’s first deaths occurred in Chinatown, adjacent to the docks.
The year 1900 was, ironically, the Year of the Rat on the Chinese calendar.
Over the following eight years, 280 San Francisco residents were infected with
plague, with 172 reported deaths.35 It was suspected that others died, but many
Chinese families surreptitiously buried their dead so that the bodies would
not be desecrated by autopsy. The main reason mortality was not greater was
that a French bacteriologist, Alexandre Yersin, had identified the bacteria that
caused the disease and correctly surmised that it was being spread by rats.
Therefore, public health authorities in San Francisco implemented a cam-
paign to kill the city’s rats.
That Chinese immigrants made up the majority of people affected by
the plague in San Francisco (because they lived closest to its point of ori-
gin) led to anti-Chinese sentiment. It fed a growing xenophobia among white
Americans, who feared that immigrants from foreign countries were bringing
diseases with them. A similar anti-Jewish sentiment arose in Baltimore in the
late nineteenth century following a cholera epidemic in which poor Jewish
immigrants were severely affected. This association of immigrants with infec-
tious diseases was a major impetus to the immigration restriction movement,
culminating in the Immigration Restriction Act of 1921, which established
quotas of immigrants by country of origin, and subsequently to the Johnson-

Reed Act of 1924, which virtually abolished immigration from some nations.
By the time plague had come under control in San Francisco in 1908,
Yersinia pestis had spread beyond the city. Rats carried it across the bay to
Oakland, and from there it moved into the countryside, infecting squirrels,
chipmunks, prairie dogs, and other rodents. During the twentieth century,
plague moved slowly but progressively eastward, so that by the end of the
century, it had been reported in rodents in the Dakotas, Nebraska, Kansas,
Oklahoma, and Texas.36 There is no reason to believe that this eastward march
is not continuing.
Presently, there are only approximately ten reported human cases of
plague each year in the United States, with most occurring in California,
Arizona, New Mexico, and Colorado. In 2002, a couple from New Mexico
who were visiting New York City were diagnosed with plague, setting off fears
of terrorism.37 The fears proved unfounded but were based on the fact that
plague can be spread by droplets as well as by fleas; thus, aerosolized, it is a
potential agent for use by bioterrorists. So traumatic was the news of the two
cases of plague in New York that the New York Times on November 8, 2002,
felt the need to publish an editorial reassuring people that “we have antibiot-
ics to quell the germ, and good supportive care.”
What is the future of plague? Since the disease is permanently estab-
lished in rats and other rodents throughout the world, its eradication is out of
the question.
Rats are extremely hardy, with the brown rat (Rattus Norvegicus), which
became widespread in the eighteenth century, even more difficult to exter-
minate than the black rat (Rattus rattus). Brown rats are excellent swimmers;
they can “tread water for three days, . . . survive being flushed down a toilet
and have been found alive in a block of ice.” Both black rats and brown rats
can also “chew through metal, wood and concrete” with their sharp incisors.38
In many cities, black and brown rats coexist; both can be affected by, and thus
carry, the plague.
Periodic outbreaks of plague should therefore be expected. In 2003, for
example, an outbreak of plague affected eleven people in Oran, Algeria;39
ironically, this city was the setting for Albert Camus’s The Plague, a fictional
account of such an epidemic.
In the United States, conditions favorable to plague exist in many cities.
Even in affluent Beverly Hills, for example, rats have become abundant, using
the city’s “fruit trees, bird feeders, swimming pools and dog-food bowls.” Ac-
cording to a news story in September 2002, “over the past two months a half
dozen restaurants have temporarily closed along Santa Monica Promenade
because of rats” and a “well-to-do doctor . . . found five rats swimming in his
marble pool on a recent Saturday afternoon.” 40 In New York City, there are
an estimated twelve rats for every person;41 the city’s Department of Health
has posted on its Web page the symptoms of plague and its proper treatment.42
Yersinia pestis could arrive in eastern port cities by ship, or eventually by its
continuing spread across the country, carried by squirrels, prairie dogs, and
other rodents.
The immediate threat of a plague epidemic in the United States is mini-
mal because the plague bacteria continues to be sensitive to some antibiotics.
As long as antibiotics are started early in the course of illness, anyone infected
with plague should recover. If, on the other hand, Yersinia pestis should mu-
tate either through natural evolution or by terrorism-related modifications, it
could become antibiotic resistant. Plague could again become not just a fatal
disease but a synonym for disaster.
Mice and Hantavirus Infection

In contrast to rats, mice migrated out of central Asia much earlier in human
history. By the time Neolithic farmers began settling in permanent dwell-
ings approximately ten thousand years ago, four species of mice had already
spread to the Middle East and North Africa.43 One of these, the common
house mouse (Mus musculus) moved into dwellings and became humans’
first houseguest. Thus, it is not surprising that mice are described in the Old
Testament and were well known to the Greeks and Romans.
As humans spread around the world, mice accompanied them. And like
all animals, mice brought along their microbes. Hantaviruses are microbes
carried by many species of mice, rats, voles, and other rodents. The hanta-
viruses and rodents have adapted to each other over millions of years, so the
microbes cause no apparent illness in the rodents. A recent summary of these
viruses notes that “each virus has adapted to a single or a small group of rodent
hosts with which it has a commensal relationship, being transmitted from
adults to young animals and causing lifelong persistent infections.” 44 As part
of this lifelong infection, hantaviruses are chronically shed in the rodents’
saliva, urine, and feces.
The importance of rodent-carried hantaviruses became clear during the
Korean War. Over 3,000 UN troops developed Korean hemorrhagic fever;
more than 300 died, including 121 Americans. It was eventually shown that
the disease was caused by a hantavirus carried by a Korean field mouse, and it
is thought that the troops had been exposed by sleeping on the ground in areas
with large numbers of mice.
Hantaviruses became prominent in the United States in 1993, with an
outbreak of hantavirus pulmonary syndrome among young adults in the Four

Corners area of the Southwest. Within two weeks, nineteen individuals were
affected, twelve of whom died. The disease begins with fever, headache,
muscle aches, and a cough. The lungs are primarily affected, and death can
come quickly if the lungs fill with fluid. Since the disease was first recognized
in 1993, 353 cases have been reported in the United States, including 132
deaths.45
The virus that has caused most cases of hantavirus pulmonary syndrome
in the United States is carried by deer mice and has been designated the
Sin Nombre (without a name) virus. Studies have shown that approximately
10 percent of deer mice shed the virus, which may then become airborne in
microscopic particles when, for example, a person sweeps up mouse drop-
pings.46 Exposure to deer mice and their droppings has been a common de-
nominator in most cases of hantavirus pulmonary syndrome caused by Sin
Nombre virus.
Since the Sin Nombre virus has infected mice for millions of years, it has
presumably caused occasional past cases of human disease but was not rec-
ognized as such. Why, then, did it become visible in the United States only
in 1993?
The primary reason for the outbreak in 1993 was ecological. The south-
western United States experienced a severe drought in the years that preceded
1992, then had abundant precipitation during the winter of 1992–1993. This
led to a record number of wild piñon nuts, which deer mice eat, in the spring
of 1993. The deer mice, therefore, proliferated rapidly, increasing tenfold
between 1992 and 1993.47 And when the piñon nuts ran out, the mice in-
vaded the dwellings of people who lived in the area, thus exposing many more
people to the virus than would have been exposed under normal climatic
conditions.
The Sin Nombre hantavirus disease outbreak has focused attention on
hantaviruses in general. At least seventeen different hantaviruses have been
identified, nine of which are found in the United States. Each is adapted to
one or more rodents, and their potential for causing human diseases is under
investigation.
The hantavirus disease outbreak has also served as an unpleasant re-
minder that animals carry thousands of microbes currently unknown to us.
When ecological conditions change, either naturally or through human in-
tervention, such microbes may produce outbreaks of diseases not previously
recognized.
7=
C H A P T E R
Humans as Pet Keepers

Microbes Move into the Bedroom
Our domesticated animals have become less an integral part of our
struggle for survival and more surrogates in our need for social fulfillment.
As such, they become even more intimately part of our extended families.
They enjoy our medical system and become potential vectors of pathogens
at levels previously known only in members of our own species.
Larry Martin, “Earth History”
D uring the ten thousand years since humans began domesticating ani-
mals, we have kept them primarily to supply our material needs. Their
meat, milk, and eggs have been our major source of protein; their wool, skins,
and fur have been our most important sources of clothing; and until the inven-
tion of the gasoline-powered engine, they were the main source of transporta-
tion for people and goods. They have also helped plow fields, herd sheep, turn
waterwheels, guard the home, protect grain supplies from rodents, and track
wild animals during the hunt. By supplying our material needs, animals have
played a critical role in advancing human civilization.
Using animals to supply our emotional needs, by contrast, is relatively
new. The keeping of pets has always existed on a small scale but has been
widespread for only the past three hundred years and especially prominent in
Western culture for only the past fifty years. This is bringing about a funda-
mental change in the way humans and other animals interact and exchange
microbes.
Occasional pet keeping probably dates to the time when Paleolithic hunt-
ers brought home infant offspring of their kill as curiosities or playthings for
their children. Twentieth-century anthropological accounts of remaining
68 =
Humans as Pet Keepers = 69
hunter-gatherer societies include descriptions of such pet keeping. Ancient

Egyptians also were enthusiastic pet keepers, especially families in the up-
per classes. Some dogs wore collars with names inscribed, such as “Ebony”
or “Cooking-Pot.” 1 Cats, known in Egyptian as “miu,” were associated with
the goddess of fertility, and, according to one historian, by the fourth century
b.c.e., “the status of cats . . . seems to have been roughly equivalent to that
of cows in present day India. Many people owned pet cats, and the death of
one sent the entire family into mourning, shaving their eyebrows as a mark
of respect.” 2
Pet keeping among the aristocracy has been widespread over the centu-
ries. As James Serpell noted in his In the Company of Animals: “Throughout
history the world’s ruling classes have almost invariably demonstrated a power-
ful affinity for pets, and this affinity has often been the excuse for mind-bog-
gling displays of gratuitous self-indulgence.” As examples, Serpell cites the
Roman emperor Hadrian, who had “monumental tombstones erected over
the graves of his favorite dogs”; the Han Chinese emperor Ling, who gave his
dogs “the rank of senior court officials . . . and a personal bodyguard of hand-
picked soldiers”; and the Japanese shogun Tsunayoshi, who owned a hundred
thousand dogs and “passed a law that all dogs must be treated kindly and only
spoken to in the politest of terms.” 3
Pet keeping by aristocrats was also popular in mediaeval Europe. Accord-
ing to sociologist Joanna Swabe: “From the late middle ages onwards, the
practice of keeping ‘toy’ dogs became increasingly fashionable in aristocratic
circles. . . . Mediaeval noble women, for example, were inclined to carry such
dogs around with them and feed them scraps from the table. . . . By the six-
teenth century, the practice of keeping lap-dogs had become extremely popu-
lar within English high society.” One writer chastised “these kind of people,
who delight more in dogs that are deprived of all possibility of reason, than
they do in children that be capable of wisdom and judgment.” 4
The status of pets among the English aristocracy reached its apogee in
the early seventeenth century. James I, who became king in 1603, kept many
pet dogs and “was accused in 1617 of loving his dogs more than his subjects.” 5
His ill-fated mother, Mary Queen of Scots, was also fond of dogs. Reportedly,
following her execution, her headless body was seen to move, causing great
consternation among those gathered to witness the event. This movement was
found to have been caused by her little dog, which, unknown to her execu-
tioners, had been resting beneath her capacious clothing.
Elizabeth, daughter of James I, “was notorious for preferring her pets to
her children.” James’s son, Charles I, who ascended to the throne in 1625,
“only parted with his own dog after receiving sentence of death in 1649,” and
his son, Charles II, “was notorious for playing with his dog at the Council
table.” Aristocrats of the era emulated the royal family, so that “hounds were
often better fed than the servants, and they were sometimes better housed.” 6
But the popularity of dogs as pets did not extend to the middle or lower
classes. Shakespeare usually referred to dogs in derogatory terms as, for ex-
ample, “whoreson dog,” “thou damn’d, inexecrable dog,” and “you bawling,
blasphemous, incharitable dog.” 7 Thomas Brooks in 1662 referred to dogs
as “vermin,” and in paintings of this period dogs often symbolized “gluttony,
lust, coarse bodily functions and general disruptiveness.” 8
The Rise of Dogs and Cats

Dogs and cats are the most popular pets in most parts of the world today. Both
animals are a manageable size, relatively easy to maintain and train, playful,
and seemingly intelligent. Also, as noted by Joanna Swabe, “both species are
particularly communicative and possess an extensive range of facial expres-
sions, typical body and tail postures, sounds and so forth that humans believe
they can understand.” 9
In seventeenth-century Europe, the keeping of pet dogs began to slowly
spread from the aristocracy to the middle class. Dogs were increasingly given
personal names, allowed in the home, and even taken to church, where large
dogs could function as foot warmers.10
One measure of the increase in dogs as pets is the number of breeds avail-
able. All dogs are descended from the common wolf; different breeds develop
as the result of selective breeding of dogs with unusual physical characteristics
caused by mutations, such as a curly tail or long hair, or specific behavioral
traits, such as the ability to herd sheep. In 1800 in England, there were only
fifteen breeds of dogs; by 1900 the number had increased to sixty, and by
the year 2000, to more than four hundred.11 Pet dogs had become so com-
mon in France by the mid–nineteenth century that the government put a tax
on nonworking dogs; at that time, there were one hundred thousand dogs in
Paris alone. By the end of the nineteenth century, dog-care books had become
widely available, dog shows were becoming popular, and a pet cemetery had
opened in Paris, guaranteeing for fifty francs a private plot for the deceased
dog for ten years.12
Cats, by contrast, became popular as pets much more slowly. In the an-
cient world, they had been kept as pets in Egypt and possibly Cyprus, but
elsewhere until the eighteenth century, people used cats to control rodents
but rarely viewed them as pets. During the Middle Ages, they were associated
with witches and Satan, both of which were believed capable of transform-
ing themselves into cats. Witches were also thought to ride on the backs of
giant cats to their nocturnal Sabbats, where they participated in orgies with
demons and devils. As these beliefs became widespread, people treated cats
with increasing cruelty, especially on Christian holidays. “Lent was a particu-
larly hard time for medieval cats. They were killed and buried in Oldenburg,
Westphalia, Belgium, Switzerland and Bohemia; burnt on Shrove Tuesday
in the Vosges, and in Alsace at Easter. In the Ardennes they were thrown into
bonfires or roasted in the ends of long poles, or in wicker baskets on the first
Sunday in Lent.” 13
Keeping cats as pets began among writers and intellectuals in eighteenth-
century England and France. In England, Samuel Johnson kept a pet cat,
Thomas Gray wrote an “Ode on the Death of a Favorite Cat, Drowned in a
Tub of Gold Fishes,” and Christopher Smart, in his poem “On Jeoffrey, My
Cat,” praised his cat as “the servant of the Living God, duly and daily serving
him.” In France, novelist Francois Chateaubriand wrote: “What I like about
the cat is his character, independent and almost heartless. . . . The cat lives
alone, he has no need of society.” Chateaubriand especially admired the cat
for “that indifference with which he passes from salon to gutter,” according to
Kathleen Kete’s The Beast in the Boudoir. The cat, Kete observes, “became a
trope of intellectuals, . . . a sign for the literary life, a signature.” 14 By the end
of the eighteenth century, cats had achieved some gentility, so that in 1792,
a Mrs. Griggs in London reportedly “bequested £150 per annum so that a
trusted black servant could continue to care for her eighty-six cats.” 15
The association of pet cats with writers and intellectuals continued well
into the nineteenth century. In England, Shelley and Wordsworth wrote lov-
ingly of cats; in France, Baudelaire, in his poem “The Cat,” merged the ani-
mal with his mistress;16 and in America, Poe wrote with his pet tortoiseshell
perched upon his shoulder. By that time, cats were more widely accepted as
pets and had become associated with children. A French writer noted that
“the cat is the nurse’s favorite and the baby’s earliest friend.” 17 An 1836 U.S.
essay described children at play, “dressing themselves, or perhaps a favorite
dog or kitten, in the most ludicrous and fanciful attire.” 18 And cats took their
place in nursery rhymes:
Great A, little A, bouncing B,
Cat’s in the cupboard, and can’t see me.
In the latter half of the nineteenth century, the keeping of cats as pets increased
markedly, and for the first time they began to challenge dogs in popularity. Ad-
vertisers used cats extensively to attract attention to their products, including
“soap, thread boxes, games, hosiery, stove cleaner, shoe polish, rat poison, oils
and cigar boxes.” Among the last, cigars with the Me-ow label first appeared
in 1886, Tabby cigars in 1894, White Cat in 1908, and Pussy in 1910. In 1914,
Kellogg’s advertised cornflakes with a picture of a young girl eating her cereal
while holding her cat; the accompanying slogan read: “For Kiddies, Not Kit-
ties.” Procter and Gamble advertised Ivory soap with a picture of twelve black
cats and one white cat and the slogan “Ivory Soap: 99 and 44/100 percent
pure.” 19 The use of black cats in advertising was especially eye-catching, since
they had been viewed for centuries as symbols of witchcraft.
The increasing acceptance of cats as pets can also be measured by their
presence in art. Before 1700, cats were depicted only rarely in paintings and,
when included, usually represented malevolent forces. An example is Lorenzo
Lotto’s “Annunciation,” painted in 1534, which shows an angel announcing
the coming Christ child and a cat running away from the angel, indicating the
banishment of evil. In the eighteenth century, cats were occasionally included
in paintings, and in the nineteenth century they became commonplace, as,
for example, in two Renoir paintings of young women holding cats.
By the end of the nineteenth century, then, dogs and cats had both be-
come firmly established as pets in Western cultures. In England, “domestic
animals added to the comfort of the home,” while in France “bourgeois Pa-
risians insistently associated petkeeping with modernity.” 20 The first cat show
was held in London’s Crystal Palace in 1871, and by the end of the century
such shows had spread throughout Europe and America. An 1892 article in
the Atlantic Monthly illustrates how far cats had come from being burned as
Lenten offerings: “Of late years there has been a rapid and promising growth of
what disaffected and alliterative critics call the ‘cat cult,’ and poets and painters
vie with one another in celebrating the charms of this long-neglected pet.” 21
Contemporary Pet Keeping

The increase in pet keeping in the past half century is unique in human his-
tory. In the United States and Europe, more than half of all homes have one
household animal and a substantial number have several. U.S. homes have an
estimated 55 million dogs, 64 million cats, 31 million caged birds, 7 million
reptiles, 87 million aquarium fish, and more than 12 million other “small ani-
mals.” 22 American dogs are said to annually deposit two million tons of feces
on streets, in yards, and sometimes in homes. In the Netherlands, it has been
estimated that “cats produce 100,000 tons of waste per annum,” and cat litter
“makes up five per cent of Dutch refuse.” 23
Pet keeping may still be on the increase. Between 1994 and 1998, for
example, the sale of cat food rose 11 percent in both the United States and
western Europe. The two largest U.S. suppliers of pet food and pet acces-
sories, PETsMART and Petco, reported increased sales of 8 and 11 percent,
respectively, in 2002, and Petco announced that it planned to add sixty new
stores to the six hundred it already owned.24
In other parts of the world, pet keeping is growing even faster. Between
1994 and 1998, cat-food sales rose by 20 percent in Asia and 48 percent in
Latin America.25 As the middle class expands in many developing countries,
pet ownership is increasing proportionately. Even China, where pets have
been considered bourgeois and “running dog” has been a popular expletive,
is experiencing a “boom in pet ownership.” Pet dogs and cats are the newest
Chinese symbol of success, and it has been projected “that China in 2050 will
have more than 500 million cats and dogs.” 26
Numbers, however, reveal only part of this contemporary change in ani-
mal-human relationships. Equally important is the increased contact, and in-
deed intimacy, between humans and their pet animals. Many pets, especially
dogs and cats, are increasingly considered family members and cared for al-
most as if they were human. We indulge pets today in ways that would have
been unimaginable in past years.
For example, a 1999 poll of pet owners reported that 16 percent of house-
hold dogs sleep on top of their owner’s bed, and an additional 2 percent sleep
in the bed. The same survey reported that “67 percent of America’s cats are al-
lowed to sleep on their owner’s beds or anywhere they want”; in a 2003 survey
of cat owners, 75 percent answered “frequently” when asked how often they
“kiss the cat or allow it to lick you”; and 11 percent of dog owners “say they
feel closest to their pets while exchanging kisses.” 27
The increasing intimacy between pet owners and their pets reflects pets
having become members of the family. As one pet owner explained: “When
I was growing up, a dog was just an add-on to the family, but it really wasn’t
like a person. But now, with many people, dogs have become much more
like a member of the family.” That pets have become family members is also
suggested by the 58 percent of pet owners who include their pet in family or
holiday portraits, the 55 percent who call themselves their pet’s “mom” or
“dad,” and the 39 percent who “have more pictures of their pets than of their
spouse or significant other.” 28
The close relationship between pets and their owners also shows up in
the number of pets that owners take along on trips. One survey reported that
“nearly half of all dog owners questioned said they had taken their pets on
overnight trips in the past year”; some hotels include pet attractions such as
a “personalized welcome package for Whiskers,” “a veterinarian-approved
room-service menu,” “homemade biscuits each morning” for dogs, and a
“Yappy Hour” for “social critters.” 29 A newsletter for people who like to travel
with their pet is called “Bone Voyage.” People who cannot take their pets
along but feel guilty leaving them behind can house them at deluxe pet ho-
tels, now available in many cities. A pet hotel in Washington, D.C., charges
$230 per day for a suite “replete with expansive views, 24-hour attendants and
tasteful décor accented with original artwork.” 30
Since pets are family members, no expense for their care is considered
too great. Americans spend $19 billion on veterinary care, including pet spe-
cialists in cardiology, dentistry, ophthalmology, psychotherapy, and radiology.
Surgical procedures such as hip replacements and kidney transplants, costing
as much as $15,000, have become routine.31 And if your pet is in danger of
dying, you can take some tissue to have it cloned. In 2004, a company called
Genetic Savings and Clone announced that it would clone cats for $50,000
each and expected to soon be able to clone dogs as well.32
Specialty pet foods and supplies are also big business. Available for pur-
chase are heated dog beds made with designer fabrics, $4,500 dog houses,
Irish knit sweaters, jogging suits, National Football League team jerseys, rain-
coats, fleece boots, and pet pajamas.33 In Israel, gas masks can be purchased
in various sizes for both dogs and cats.34 Hallmark now markets a death-of-pet
card that says, “In sympathy, in your loss of your loving friend,” while Internet
pet suppliers offer cremation urns, caskets, and memorial stones “to honor
your pet until you meet again at the ‘Rainbow Bridge.’” 35 When the costs
of veterinary care, pet food, and pet supplies are combined, Americans now
spend some $47 billion per year on their pets, more than the gross national
product of Costa Rica, Guatemala, Ecuador, Ivory Coast, Ethiopia, Croatia,
Bulgaria, or Lebanon.36
The new relationship between U.S. pet owners and pets is also reflected
in the courts. In New York and other cities, there is “a growing group of
homeowners and renters who argue that they should be able to keep their
pets even if community or building rules forbid them.” One New York law-
yer “has handled nearly 40 such cases since 2000.” In most cases, pet own-
ers argue that their pet is necessary for emotional support. In 2003, the New
York City Bar Association began offering a course that “included material on
emotional support animals.” Also that year, the federal Department of Trans-
portation relaxed rules that prohibited airline passengers from keeping pets
with them on airplanes. Pets may now accompany passengers who have letters
from their doctors or therapists saying that “the pet is necessary for emotional
support.” 37
Viewing pets as integral members of human families is also reflected by
legislation introduced in Colorado in 2003 to legally upgrade the status of
dogs and cats from “property” to “companions.” The purpose, said the spon-
sors of the legislation, would be to “allow lawsuits against veterinarians or
animal abusers for up to $100,000 for loss of companionship and emotional
suffering” if a pet is injured or killed.38 The proposed legislation has not yet
been enacted.
The Benefits of Pets

The increasingly close relationship between pets and their owners is partly
due to an increasing realization that pets may be beneficial to humans. An
obvious example is the use of dogs to assist individuals who are blind or deaf
and those with severe physical disabilities such as muscular dystrophy and ce-
rebral palsy. Dogs trained to help the latter, according to a recent survey, can
be taught to “open and close doors, turn switches on and off, pull a person up
from a sitting or lying down position, assist a person in and out of baths and
pools, help pull on clothing, procure and pick up objects, pull wheelchairs,
help with shopping, carry parcels, and drag a person to safety in case of fire or
other emergency.” A study that compared forty-eight disabled individuals who
were given service dogs to forty-eight individuals who were not given dogs
reported that, at the end of one year, the former had significant improvements
in self-esteem, psychological well-being, school attendance, and part-time
employment. Equally important, the disabled individuals with service dogs
markedly decreased their use of both paid and unpaid human assistants.39
There is also increasing evidence that pets can reduce loneliness and de-
pression, especially in individuals who are socially isolated. A survey of 1,992
homosexual and bisexual men reported that “persons with AIDS who owned
pets reported less depression than persons with AIDS who did not own pets.”
The benefit was most significant among individuals who were the most iso-
lated and had the fewest close friends.40
Anecdotal data to support such findings are abundant. In New York, a
thirty-six-year-old bond salesman claimed that when separated from his black
Labrador, he “became a miserable human being in every way that you can
think of ”; his wife agreed, saying that without the dog, her husband was “de-
pressed and very difficult to live with.” 41
Pets have also been widely used in nursing homes and in institutions for
individuals with psychiatric disabilities, where much of their beneficial value
has been phrased in terms of companionship: “When older people withdraw
from active participation in daily human affairs, the nonhuman environment
in general and animals in particular can become increasingly important. Ani-
mals have boundless capacity for acceptance, adoration, attention, forgive-
ness, and unconditional love. Although the potential for significant benefits to
a great variety of people exists through association with companion animals,
the potential seems greatest in the elderly, for whom the bond with animal
companions is perhaps stronger and more profound than at any other age.” 42
Studies have shown, for example, that individuals with Alzheimer’s disease are
less agitated and more social when they have companion animals.43
Surveys that ask pet owners why they have pets usually elicit answers that
include feelings of security, being loved, being needed, and not being judged.
In one study, divorced women who owned dogs said that “whereas husbands
may come and go, and children may grow up and leave home, a ‘dog is for-
ever’; . . . pets never withhold their love, they never get angry and leave, and
they never go out looking for new owners.” 44 A study of single women con-
cluded that “a pet can help to diminish feelings of loneliness, particularly
for women living alone, and compensate for the absence of human compan-
ionship.” 45 Similarly, more than half of homeless individuals who kept a pet
reported that “relationships with their pets were their only relationships with
other human beings.” As one writer summarized it: “There is no psychiatrist
in the world like a puppy licking your face.” 46
In addition to the psychological benefits of companionship, pets may pro-
vide medical benefits. Cat and dog owners, compared to nonowners, have
been reported to have lower resting heart rates and blood pressures and to
handle conditions of experimental stress better when their pet is present.47
Two studies of patients with severe cardiac problems reported that the pres-
ence of a pet in the home increased the survival rate of such patients. In
one of the studies, the benefits were found only when the pet was a dog; a
cat provided no beneficial effect.48 Part of the cardiac benefit in such studies
undoubtedly accrues from the necessity of walking the dog, thus affording the
owner more exercise.
Companion animals have also been shown to increase the general well-
being of adults and to decrease their use of physician services. In one study,
adults who acquired a new dog or cat, followed for ten months, reported “a
highly significant reduction in minor health problems”; the benefit lasted the
entire ten-month period for the dog owners but was present only for the first
month for cat owners.49 Similarly, physician use was measured for 938 Medi-
care enrollees who were undergoing stressful life situations. Those who owned
a dog did not see their doctors more often under stressful circumstances, but
owning a cat or other pet afforded no such benefit.50
It is noteworthy that most studies that report beneficial effects from own-
ing a pet have focused on adults. Few studies have reported benefits of pet
ownership for children, except in two major arenas. One is children who
have autism, childhood schizophrenia, or other severe psychiatric disabilities;
such children have been shown to relate better to companion animals than to
adults. For this reason, dogs or other animals are sometime used as “cothera-
pists” in psychotherapy for such children.51
The other major benefit of animal exposure for children is a possible
decrease in the likelihood of their getting asthma, hay fever, or other aller-
gies. Some studies have reported that children who are raised on farms have
a lower incidence of allergic disorders, but other studies have not replicated
these findings. One of the positive studies found that the benefit was greatest
when animal exposure started early in life. The benefit was also dose depen-
dent; more exposure produced greater benefit. Thus, small children who were
“exposed to stables, farm milk, or both in their first year of life” had the lowest
incidence of allergies. “Furthermore, amount and duration of exposure also
seemed to play an important part in conferring protection against develop-
ment of hay fever and allergic sensitization. For asthma, even short exposure
times conferred protection.” 52 Another study found that exposure to dogs and
cats in the first year of life decreased children’s chances of later developing
asthma or other allergies. Significantly, however, the benefit was seen only if
the child was exposed to two or more animals, suggesting that the benefit was
not acquired from casual contact alone.53 Against such possible decrease in
allergies with childhood exposure to animals must be weighed the findings
that both dogs and cats induce allergies in some children.
Diseases Transmitted by Dogs

Given the increasing number of pet animals and the increasing intimacy be-
tween pets and their owners, it is inevitable that an increasing exchange of
microbes is also taking place. As noted by William McNeil in Plagues and
People: “It appears obvious that the sharing of infection increases with the
degree of intimacy that prevails between man and beast.” 54
Bites are the most common mode of transmission to humans of microbes
from both dogs and cats. “Several million” people in the United States are
bitten by dogs and cats each year, “resulting in approximately 300,000 vis-
its to emergency departments, 10,000 hospitalizations, and 20 deaths, mostly
among young children.” 55 Because cats have such sharp teeth, their bites
cause deep puncture wounds and are more likely than dog bites to become
infected. A study of infected human wounds from dog and cat bites reported
that the median number of different types of bacteria cultured from a single
human wound was 5.0 for dogs and 6.5 for cats; however, individual bites from
dogs had as many as sixteen different types of bacteria, and from cats, thirteen
different types. Most of the bacteria remain localized to the wound, although
occasionally they may enter the general circulation and cause serious prob-
lems in joints (arthritis), the heart (endocarditis), or the brain (meningitis).56
Apart from dog bites, the risk of transmission of serious diseases from dogs
to humans appears relatively low. One reason for this is that dogs and humans
have had a close relationship for more than ten thousand years, and during
that time humans have been exposed to most microbes carried by dogs. It is
thus unlikely that there will be many microbial surprises from dogs compared
to cats or other pets to which humans have had comparatively less exposure.
Diseases known or strongly suspected to be transmissible from dogs to humans
are these: bordetellosis, brucellosis, campylobacteriosis, cryptosporidiosis, cu-
taneous larva migrans, dirofilariasis, echinococcus, giardiasis, leishmaniasis,
leptospirosis, Lyme disease (by ticks), rabies, and toxocariasis. Apart from in-
fected dog-bite wounds, the most important dog-associated disease for indi-
viduals in the United States is toxocariasis.
The bacterial infection bordetellosis is caused by Bordetella bronchisep-
tica, a close cousin of the bacteria that causes pertussis (whooping cough). It
is carried by both dogs and cats and is occasionally transmitted to humans, es-
pecially children or adults who are immunocompromised. Symptoms include
fever, malaise, joint pains, and/or respiratory problems. It can be treated with
antibiotics.
Brucellosis is a bacterial disease usually transmitted to humans from
cows and other farm animals (see chapter 3). Dogs, however, may also be a
reservoir. In humans, it causes fever, malaise, and enlarged lymph nodes. In
beagles, it is an important cause of abortions.
The bacterial disease campylobacteriosis “has emerged as the most com-
mon infectious diarrhea in the United States.” 57 It is carried by a variety of
wild and domestic animals, with dogs and cats responsible for approximately
6 percent of human cases.58 The diarrhea may be severe and accompanied by
fever. Exposure to dogs or cats with diarrhea increases one’s risk of getting this
disease. It can be treated with antibiotics.
Responsible for cryptosporidiosis, Cryptosporidium parvum is a protozoon
carried by both dogs and cats and may be transmitted by fecal contamination
of food or water. In humans, it causes diarrhea and occurs most commonly in
children. Since this parasite is also carried by other animals, the role of dogs
and cats in causing this disease is not yet clear. The parasite is a major cause of
intestinal disease in individuals who are immunocompromised, such as those
with HIV infection.
Cutaneous larva migrans is caused by a type of hookworm carried by
dogs and occurs mostly in southern states. Humans may get it by walking
barefoot in areas contaminated by dog feces. Once beneath the skin, it causes
redness, itching, and swelling of the local area and may slowly spread. It is
usually self-limited but may be treated.
Dirofilariasis, caused by the dog heartworm, Dirofilaria immitis, is trans-
mitted from dog to dog by mosquitoes, and humans are occasionally acciden-
tal hosts. The larvae migrate to the heart and lungs. It is usually asymptom-
atic, but the worms sometimes form lung nodules that may be mistaken on
X-rays for an embolus or lung cancer.
Echinococcus is caused by a tapeworm carried by dogs. When ingested
by humans through food or water contaminated with dog feces, the tapeworm
may go to the liver or lungs, causing large cysts that may require surgical exci-
sion. The disease is rare in the United States, except in southwestern states
and Alaska.
Giardiasis is caused by the protozoon Giardia lamblia, also a common
cause of human diarrhea and usually gotten from contaminated water. It is
carried by a variety of animals, including dogs and cats, but rarely causes
symptoms in them. Although pet-to-human transmission has not yet been
proven, it is strongly suspected.
Dogs, wolves, foxes, and other canids are the natural carriers for protozoa
that cause leishmaniasis. Leishmaniasis affects five hundred thousand people
each year in South America, Asia, and the Middle East. It causes fever with
enlarged lymph nodes and is often confused with malaria. A mild skin form of
leishmaniasis has infected hundreds of U.S. military personnel in Iraq during
the war, where it is widely referred to as the “Baghdad Boil.” 59 An especially
disfiguring form of the disease, espundia, occurs in South America and causes
“the nose and mouth parts [to] literally rot away.” 60 Sandflies carry the proto-
zoa from dogs to humans and in some cases from humans to humans; in Italy,
Spain, and Brazil, as many as one-quarter of all dogs are infected.61
Leishmaniasis is thought to be rare in the United States. However, in
1999, twenty-one foxhounds at a hunt club near New York City died from it,
although the outbreak was apparently not transmitted to humans.62 Subse-
quent studies have confirmed the occurrence of visceral leishmaniasis in dogs
in twenty-one states, thus showing that it is much more widespread than was
previously thought and has the potential to cause human disease. In 2000, the
Institute of Medicine called visceral leishmaniasis “one of the most important
emerging parasitic diseases” and “a major public health problem” because of
its increasing incidence in Europe among drug users and immunocompro-
mised individuals with AIDS.63
Leptospirosis is caused by a spirochetal bacteria. It may be transmitted
to humans by the infected urine of many animals, but most commonly of
rats and dogs. It usually occurs in outbreaks when drinking water has been
contaminated with the urine of rats or dogs; in 1998, 375 cases of leptospirosis
occurred among triathlon participants in the Midwest.64 Affected individuals
may develop a fever, malaise, severe headache, or mild jaundice. In its severe
form, it affects the kidneys and liver and is called Weil’s disease. It can be
treated with antibiotics.
Lyme disease is transmitted from deer to humans by ticks. Occasionally,
humans become infected by ticks carried by dogs or cats.
Rabies from infected dogs continues to be a major problem in countries
in which rabies vaccine is not routinely given to dogs. In China, for example,
rabies from dog bites killed 1,297 people in a nine-month period in 2003,
more people than died from SARS or AIDS.65 In the United States, rabies
among dogs and cats is rare; the major carriers of the virus are bats and rac-
coons, as we will see later in this chapter.
Toxocariasis is “the most common zoonotic infection associated with pet
animals in the United States.” 66 It is caused by the roundworms Toxocara ca-
nis from dogs or Toxocara cati from cats. The former are more common, and
virtually all puppies shed this parasite in their first weeks of life. Deposited in
children’s outdoor play areas or sandboxes, the parasite eggs remain alive for
months and may be ingested by children, especially those who eat dirt. Most
infected children show no symptoms but may have a high blood count of
eosinophil cells. However, in some cases, the parasite migrates to the lungs or
liver, causing cough, wheezing, fever, or an enlarged liver (visceral larva mi-
grans). In other cases, it migrates to the eye (ocular larva migrans) and “causes
hundreds of cases of unilateral blindness and less permanent forms of ocular
disorders in children each year in the USA.” 67 This parasite may also cause
some cases of epilepsy, but this has not been proven. Toxocariasis may be pre-
vented by properly disposing of dog and cat feces, keeping unused sandboxes
covered, and treating puppies and kittens with deworming medications.
Multiple Sclerosis
Foremost among diseases for which a link between dogs and humans has been
suggested but never proven is multiple sclerosis, a chronic disease of the brain
that affects approximately 300,000 persons in the United States and 2.5 mil-
lion worldwide. It begins most commonly between ages twenty and thirty-five,
with symptoms such as double vision, clumsiness, weakness of the arms or
legs, or changes in sensation. In 10 percent of cases it remains benign for most
of the person’s life, in 70 percent it relapses and remits as it slowly progresses,
and in 20 percent it rapidly progresses to total disability and death.
Infectious agents have been suspected for more than a century to be one
of the causes of multiple sclerosis. One reason for this is reports of clusters of
cases, which often occur in infectious diseases. Multiple sclerosis also has a
striking geographic distribution, with a much higher incidence at latitudes
distant from the equator. In addition, there is evidence—based on studies
of people who migrate from a country with a high incidence to a country
with a low incidence or vice versa—that whatever causes multiple sclerosis
gets into the brain before age fifteen and then remains latent for ten years
or more. Most important, individuals with multiple sclerosis often have in-
creased antibodies to various viruses and increased immunoglobulins, both of
which are measures of infection, in their cerebrospinal fluid. The infectious
agent that has been studied most actively is the measles virus; other suspects
have included various herpes viruses, rubella, influenza, parainfluenza, and
a retrovirus.
One reason animals have been proposed as possible sources of the infec-
tious agent is because multiple sclerosis–like diseases occur in several animal
species. As early as 1952, it was suggested that “dogs or cats may be suspected
as reservoirs of the [infectious] agent.” Animal theories received support in
1977 with a report that three sisters, ages twenty-three to thirty, had all devel-
oped multiple sclerosis shortly after their pet dog experienced a severe neu-
rological illness.68
This report triggered an outpouring of research studies to ascertain
whether individuals with multiple sclerosis had been more exposed to dogs
compared to individuals who did not have the disease. One researcher who
reported a positive association claimed that this “discovery is of monumental
importance, analogous to the discovery of the link between cigarette smoking
and cancer.” An editorial in a leading neurological journal called 1977 “the
year of the dog,” and the possible link between multiple sclerosis and dogs was
widely reported by the media.69
A quarter of a century later, the possible relationship of multiple sclerosis
and dogs is still unresolved and continues to stir lively debate among neu-
rologists. At least twenty-one studies have been carried out on dog exposure.
In seven of them, individuals with multiple sclerosis had significantly more
exposure to dogs than the controls; in the remaining studies, no significant
association was found, but in none of them did the controls have significantly
more dog exposure. In some studies, only small dogs or dogs kept in the house
appeared to be risk factors.70
Several of the studies inquired specifically about exposure to sick dogs
before the onset of human multiple sclerosis. This is of special interest be-
cause dogs may be infected with the canine distemper virus, which is closely
related to the human measles virus. Some researchers have claimed that epi-
demics of canine distemper in dogs have been followed by outbreaks of mul-
tiple sclerosis in humans, including outbreaks in the Faroe Islands; Iceland;
Newfoundland; Key West, Florida; and Sitka, Alaska.71 In Sitka, for example,
an outbreak of distemper occurred among dogs in 1965. Between 1967 and
1970, five individuals with a multiple sclerosis–like illness were diagnosed,
the only such cases diagnosed in Sitka between 1949 and 1979.72 Based on
such observations, several research groups have tested individuals with mul-
tiple sclerosis to see whether they have increased antibodies to the canine dis-
temper virus. A 1997 summary of such studies concluded that “the evidence
for an etiologic role for canine distemper virus in MS [multiple sclerosis] is
at best equivocal.” 73
Such studies have many methodological problems, and the results re-
main controversial. Dogs are so widely distributed as pets that almost everyone
has owned or been exposed to them at the homes of relatives and neighbors.
The issue of timing of exposure also continues to be problematic; since there
is probably a latent period of several years between exposure to the dog and
disease onset, one must measure dog exposure at various times in the past
and follow humans for an extended period of time to ascertain whether they
develop the disease.
Diseases Transmitted by Cats

Since cats have been widely used as pets for less than two hundred years, hu-
man exposure to feline microbes has occurred for a relatively short period.
Diseases transmitted from cats to humans are these: bordetellosis, campylo-
bacteriosis, cat scratch disease, cryptosporidiosis, giardiasis, Lyme disease (by
ticks), plague (by fleas), rabies, toxocariasis, and toxoplasmosis. Except for in-
fected cat-bite wounds, discussed earlier, the most important cat-associated
diseases for individuals in the United States are cat-scratch disease, toxocaria-
sis, and especially toxoplasmosis. (Discussion of several of the diseases listed
can be found in the section on dog-associated diseases.)
There are approximately twenty-two thousand cases of cat-scratch disease,
including two thousand hospitalizations, each year in the United States.74
The cause of cat-scratch disease eluded investigators for many years. How-
ever, recent studies show that it is caused by a bacteria, Bartonella henselae,
transmitted to humans by the scratch or bite of a cat or, occasionally, by cat
fleas. It usually affects children and is most commonly acquired from young
or stray cats. A sore (papule) at the site of inoculation is followed by enlarged
lymph nodes and mild fever. Most cases are self-limited, but a few progress to
involve other organs, including the heart, lungs, liver, eyes, and brain. It can
be treated with antibiotics, although the response to the medication varies.
Plague is a bacterial disease (Yersina pestis) that in the United States mostly
occurs among rodents in southwestern states (see chapter 6). Cats may become
infected by contact with infected rodents. In New Mexico between 1977 and
1988, 119 cases of plague in cats were reported. Cats occasionally transmit it to
humans, usually by carrying plague-infected fleas. Of the 297 cases of human
plague in the United States between 1977 and 1998, 23 were believed to have
been transmitted by cats; in 5 of those cases, the outcome was fatal because of
a failure to properly diagnose the person and begin antibiotics.75
Toxoplasmosis is caused by a protozoa, Toxoplasma gondii, which over
millions of years has adapted to cats and other felids. Cats rarely show symp-
toms, but when first infected they may pass up to twenty million cysts per day
in their feces. The cysts are extremely hardy and may remain infective in soil
or sand for up to eighteen months. If the cysts are ingested by other animals,
they may go to muscle tissue and remain there. If that animal is in turn eaten
by a felid, the cysts complete their complex life cycle in the cat. A special situ-
ation occurs when Toxoplasma is ingested by a mammal that is pregnant. In
such situations, the microbe may infect the placenta or cross the placenta and
infect the fetus. This is a major cause of spontaneous abortions among sheep
and may also cause severe problems for the human fetus.
Humans become infected with Toxoplasma gondii by inhalation or in-
gestion. Inhalation of cysts may occur in anyone who is exposed to cat feces,
such as when they are deposited in litter boxes, under chairs, in gardens, in
loose soil around the house, or in children’s sandboxes. The feces become dry
within two days, lose their color and odor within two weeks, and can no longer
be distinguished from the surrounding soil or sand. Cysts from infected cats
may become airborne and thus inhaled when the dried feces are disturbed,
as when a person changes the cat litter, digs in the garden, or plays in the
sandbox.
Sandboxes (called “sandpits” in many countries) should be regarded as
common sources of Toxoplasma infection for children, since studies have
shown many of them to be highly contaminated with cat feces. In one study
of three public sandboxes in urban parks, a total of 176 cat defecations took
place over a four-week period, mostly at night.76 Since a single infected cat
can deposit millions of cysts per day, and since the cysts can remain infective
in moist sand or soil for as long as eighteen months, it seems likely that many
children playing in such sandboxes become infected.
A second major route by which humans may become infected with Toxo-
plasma is by eating undercooked meat from animals that became infected by
ingesting cysts from cat feces. The muscles of these infected animals contain
microscopic cysts that can be transmitted to humans or other animals if the
muscle is eaten. This is a common mode of infection in countries such as
France, Germany, Turkey, Pakistan, Sudan, and Ethiopia, where undercooked
meat is widely consumed. The effectiveness of transmitting Toxoplasma by

undercooked meat was demonstrated in a study of a children’s institution in
France: Given “barely cooked beef or horse meat” and “undercooked lamb
chops,” 100 percent of the children demonstrated antibodies to Toxoplasma
at the end of one year.77
Humans may also become infected with Toxoplasma by drinking contam-
inated water or milk or by ingesting unwashed fruits or vegetables that have
been exposed to flies or cockroaches carrying Toxoplasma cysts. Houseflies
have been shown to infect food with Toxoplasma for up to two days after the
flies have had contact with infected cat feces. Cockroaches may excrete Toxo-
plasma in their feces for up to ten days after ingesting infected cat feces.78
What are the chances of humans becoming infected with Toxoplasma
from these various sources? In the United States, studies have shown that ap-
proximately 1 percent of cats are actively infected, and thus shedding cysts, at
any one time. Studies of how many cats have ever been infected, as measured
by the presence of antibodies against Toxoplasma, have shown the number to
be approximately one-third.79 The infection rate is lower in cats kept indoors
and higher in stray cats, since the latter rely more on hunting for their food
and thus are more likely to ingest infected rodents. Cats excrete cysts only at
the time they acquire their initial infection. In young cats, this is most likely
to take place when they become old enough to begin hunting for themselves;
thus, excretion of cysts is much more likely to occur in cats at this stage of
development. A study of pregnant women in Norway attempted to assess the
relative importance of various factors for becoming infected with Toxoplasma.
It reported that the women who became infected had a significantly greater
exposure to cat litter boxes, undercooked meats, and raw fruits and vegetables;
thus, multiple sources of infection appear to be important.80
The number of humans who have been infected by Toxoplasma gondii, as
measured by their having antibodies, varies geographically depending on cat
exposure and dietary habits. A national survey in the United States reported
that 23 percent of people are infected.81 By contrast, a survey of pregnant
women in Paris, where undercooked meat is highly valued, reported that 84
percent of them had been infected.82 High rates have also been reported in
countries where cats are numerous and exposure to their feces is thought to
be common.83
Clinically, the best-studied form of human toxoplasmosis is the congeni-
tal form, which occurs when Toxoplasma infects a pregnant woman who has
not previously been infected. In the United States, “approximately one out
of every 1,000 pregnant women becomes infected, resulting in anywhere
from 400 to 4,000 cases of congenital toxoplasmosis each year.” 84 In approxi-
mately 60 percent of such cases, the parasite infects the mother but causes no
symptoms and does not affect the placenta or fetus. In the other 40 percent,
Toxoplasma affects the placenta and fetus, causing spontaneous abortion or
stillbirth in approximately 5 percent of cases and congenital toxoplasmosis at
birth in an additional 10 percent. The symptoms of congenital toxoplasmosis
may include changes in head size (hydrocephaly or microcephaly), cysts in
the brain, mental retardation, deafness, seizures, cerebral palsy, enlargement
of the liver and spleen, and damage to the retina.
The remaining 25 percent of children infected with Toxoplasma in utero
appear normal at birth but develop symptoms later. In most cases, this form of
toxoplasmosis involves infections of the eyes (retina and choroid), which may
produce scarring or impaired vision. Symptoms in these delayed-onset cases
peak in the person’s second and third decade of life. Much of the damage in
congenitally transmitted toxoplasmosis can be prevented by timely treatment
with appropriate antibiotics if the correct diagnosis is made.
Acquired toxoplasmosis occurs when Toxoplasma infects a nonpregnant
person for the first time, most commonly a child or young adult. It may cause
no symptoms or manifest as headache, fever, and enlarged lymph nodes,
symptoms often misdiagnosed as a cold, flu, mononucleosis, or other disorder.
In some cases, acquired toxoplasmosis may proceed to a relapsing or chronic
stage and cause more serious symptoms. Such symptoms may include infec-
tion of the liver (hepatitis), heart muscle (myocarditis), brain (encephalitis),
lungs (pneumonia), or eye (retinochoroiditis). In one study of seventy cases of
acquired toxoplasmosis, these more serious symptoms occurred in twenty-six
patients.85
In addition to the congenital and acquired forms of toxoplasmosis, a third
form occurs in individuals with an impaired immune system, including those
receiving chemotherapy for cancer and those infected with HIV. Infection
of the brain with toxoplasmosis occurs in approximately 30 percent of AIDS
patients who have had a previous primary infection and causes up to 10 per-
cent of deaths in these patients.86 The cerebral toxoplasmosis may cause eye
disease and a variety of neurological and psychiatric symptoms, including sei-
zures, cranial nerve palsies, focal neurological signs, and altered mental status
such as confusion, delusions, and hallucinations.87 The toxoplasmosis in such
immunocompromised individuals is a reactivation of latent Toxoplasma that
has lain dormant in the body, often for many years.
The activation of latent toxoplasmosis in individuals with AIDS has led
to a realization that “Toxoplasma gondii is among the most prevalent causes of
latent infection of the central nervous system (CNS) throughout the world”
and has raised questions about what else it might be doing in human brains.88
In sheep, pigs, and cattle, Toxoplasma causes neurological symptoms. Studies
of mice and rats have shown that infection with Toxoplasma decreases their
memory and learning ability.89 Of special interest are the studies of Joanne
Webster and her colleagues in England, which show that Toxoplasma-infected
rats become more active and lose their natural aversion to the smell of cats,
behaviors that increase the chances that such rats will be eaten by cats. Since
this would return the Toxoplasma gondii cyst to cats, where it can effectively
complete its life cycle, this altered behavior has been used as an example of
evolutionarily derived manipulation by the parasite.90
In humans, Toxoplasma may cause mental retardation, and there has
been speculation that it may also cause some cases of epilepsy, Guillain-Barré
syndrome, and brain tumors such as meningiomas.91 Also of interest are stud-
ies suggesting that toxoplasmosis infections in otherwise normal individuals
may produce subtle changes in personality traits, impairment in psychomotor
skills, and a lowering of IQ.92
Recent research has also focused on the possibility that Toxoplasma
gondii may play a role in the causation of severe psychiatric disorders. Such
research was stimulated by observations that AIDS patients who have reacti-
vated toxoplasmosis have delusions, hallucinations, and other manifestations
of disordered thought processes. There are also reports of such psychiatric
symptoms in individuals with acquired toxoplasmosis; in a review of 114 such
cases, “psychiatric disturbances were very frequent” in 24 of them.93
Nineteen studies have been carried out that assess antibodies to Toxo-
plasma gondii in individuals with schizophrenia and other severe psychiat-
ric disorders; all except one of the studies reported that patients had more
antibodies than control groups had.94 A study of mothers who gave birth to
individuals who later developed schizophrenia and other psychoses reported
that the mothers, in blood taken just prior to delivery, had more antibod-
ies to Toxoplasma than mothers whose offspring did not develop these disor-
ders.95 Finally, two studies have ascertained that individuals with a diagnosis
of schizophrenia or bipolar disorder were more likely to have owned a cat
during childhood than individuals without such diagnoses.96 Studies relating
Toxoplasma infection to severe psychiatric disorders are ongoing, including
studies to assess whether treatment for Toxoplasma results in clinically appar-
ent improvement for some individuals with these diseases.
Another human disease for which there has been speculation regarding
the possible role of cats is rheumatoid arthritis. This is a disease of joints, af-
fecting women more often than men and usually becoming manifest after
the age of forty. It is widely accepted that some individuals have a genetic
predisposition to rheumatoid arthritis and that there are abnormalities in such
persons’ immune systems. Some researchers have also suspected that an infec-
tious agent triggers the disease, and a variety of microbes has been proposed.
If rheumatoid arthritis is triggered by an infectious agent, could the agent
be transmitted from animals? The first group to ask that question was Nor-
man Gottlieb and his colleagues at the University of Miami. In a 1974 study,
they compared pet histories for the five years preceding the onset of illness for
105 individuals with rheumatoid arthritis, 105 individuals with other forms of
arthritis, and 95 individuals with nonarthritic illnesses. They found that “the
rheumatoid group had significantly greater exposure to one or more dogs, cats,
or birds (combined) than did the arthritic controls.” When the pets were ana-
lyzed individually, the presence of a pet dog or any sick animal in the home
of an individual with rheumatoid arthritis was statistically significant. There
were also “more cats and birds in the homes of patients who developed RA
[rheumatoid arthritis], but differences were not statistically significant.” 97
In 1996, Colin Bond and Leslie Cleland at the University of Adelaide,
Australia, followed up the Gottlieb study. They compared the animal expo-
sure histories for 122 individuals with rheumatoid arthritis and 114 individu-
als with other arthritides, mostly osteoarthritis. They asked about a broad array
of animals, including dogs, cats, rabbits, guinea pigs, mice, parakeets, cocka-
toos, parrots, pigeons, fish, ducks, sheep, cattle, pigs, goats, and horses. Their
most significant finding was that individuals with rheumatoid arthritis had
a statistically significant greater exposure to cats, especially in the five years
before puberty. Exposure to parakeets also achieved significance, but expo-
sure to none of the other animals was significantly different between the two
groups.98 No additional studies on animal exposure in rheumatoid arthritis
have been reported since this study.
Other Pets
Although dogs and cats are the most popular choices as pets, fish, rabbits,
birds, and small rodents are also widely kept.
Aquarium fish can be found in more than twenty million homes in the
United States. They are considered to be “relatively harmless” in terms of
human disease risk.99 The most common disease transmitted by fish is a skin
infection caused by mycobacteria, and it occurs most often when persons
cleaning the fish tank have cuts on their hands.
Rabbits, when raised domestically rather than caught in the wild, are also
considered “exceptionally free of most transmittable zoonoses” and can be
trained to make good pets.100 If improperly restrained, rabbits will sometimes
inflict painful scratches with their back feet, and the scratches may become
infected. Wild rabbits, however, should not be kept as pets, since they may
carry tularemia (see chapter 3). Approximately one hundred cases of human
tularemia occur in the United States each year from wild rabbits. Especially
ironic was a case in which a father gave the rabbit feet from a wild rabbit to his
two children as good luck charms; both children developed tularemia.101
Caged birds are commonly kept as pets but present some risks to their
owners. Allergic reactions, including asthma attacks, are relatively common
in owners. Caged birds may also spread salmonellosis, giardiasis, influenza
(see chapter 9), and Newcastle disease, an influenza-like syndrome caused by
a paramyxovirus. One of the most serious diseases they may transmit is psit-
tacosis.
Psittacosis, also known as parrot fever, is caused by a bacteria, Chlamydia
psittaci, and may be carried by almost all bird species, including parrots, para-
keets, cockatiels, canaries, and finches. A study of pet birds in Florida found
that 20 percent of them were infected.102
Psittacosis is often asymptomatic in birds, and it is believed that some birds
carry the bacteria throughout their lifetime. Situations that cause stress, such
as crowding birds in cages and transporting them, may cause latent bacteria
to become active and cause symptomatic disease. The symptoms of psittacosis
in birds vary by species, as well as by strain of bacteria, but include inflamma-
tion of the eyes, nasal discharge, diarrhea, lethargy, and ruffled feathers. Some
infected birds may die, especially if they are subjected to stress; others recover
but have periodic relapses; and others recover completely.
Chlamydia psittaci is transmitted from birds to humans most commonly
when humans inhale droplets of dried bird excreta that have become air-
borne. Birds excrete bacteria in their eyes, nasal secretions, and feces and may
carry it on their feathers. Studies have shown that one may become infected
merely by being in the same room with an infected bird, and infections have
been reported among multiple family members infected from a single bird,
as well as among individuals visiting a bird park.103 “Kissing or nuzzling the
bird, handling the bird, and feeding the bird” have been shown to increase the
chances of transmission.104 Intimate exposure to pet birds markedly increases
transmission, as demonstrated by the odd case of “a man who developed life-
threatening psittacosis after administering ‘mouth to beak’ resuscitation to his
ill, newly purchased parrot.” 105 There are suggestions that Chlamydia psittaci
may occasionally be transmitted from person to person, although this has not
been proven.106
Human psittacosis is varied in its manifestations, from being asymptom-
atic to being a fatal disease.107 Classically, the infected person develops in-
fluenza-like symptoms of chills, fever, headache, muscle aches, and malaise.
This may be followed by coughing, chest pain, shortness of breath, and pneu-
monia. The pneumonia caused by Chlamydia psittaci may be severe;108 it may
also look similar to pneumonia caused by another member of the Chlamydia
family, Chlamydia pneumonia. Occasionally, Chlamydia psittaci also infects
other organs, including the heart, liver, kidney, joints, and brain. Before the
availability of antibiotics, the mortality rate from human Chlamydia psittaci

infections was over 20 percent, but it is now less than 1 percent.109
The most worrisome aspect of Chlamydia psittaci, however, is what other
human diseases it may be setting off. In the animal kingdom, it has been im-
plicated in causing pneumonia, arthritis, diarrhea and inflammation of the
intestine, and abortions.110 In humans, Chlamydia psittaci may be responsible
for some cases of temporal arteritis and temperomandibular joint syndrome,
but this has not yet been established and the cases may represent cross-reac-
tions to another closely related Chlamydia.111 As is true for other members of
the Chlamydia family, there is a general belief among researchers that we are
just beginning to understand how many human diseases these bacteria may
cause.
Small rodents raised domestically, such as hamsters, gerbils, guinea pigs,
mice, and rats, can also make good pets. Since they have been used in labora-
tory research for many years, we know a great deal about diseases they may
carry. They are not without risk, however, and may induce allergies in some
people. They may also carry a variety of infectious agents, although those
causing the most serious diseases, such as plague, typhus, and hantavirus in-
fection, occur in wild rodents but not generally in rodents raised for sale.
One important microbe that pet rodents may carry is the virus that causes
lymphocytic choriomeningitis (LCM). LCM virus is a member of the arena-
virus family, which also contains the lethal Lassa fever virus and several vi-
ruses that cause viral hemorrhagic fevers. Hamsters and mice do not show any
signs of illness following infection with the LCM virus, suggesting that these
species have carried the virus for a long period of time. They may transmit the
virus to a human who handles the animal or is simply around its cage, since
the virus, shed in the rodent’s urine and feces, may become airborne.
In most cases, LCM causes a relatively mild illness, with fever, headache,
muscle aches, eye pain, and nausea and vomiting. However, in approximately
one-third of human cases, LCM also causes meningitis or encephalitis, with
severe headache, stiff neck, and other neurological symptoms. LCM infec-
tions are rarely fatal but occur in humans more frequently than was previously
thought. One study of a rural population in northern Germany, where mice
are relatively common, reported that 9 percent of the population had been
exposed to LCM, as measured by their having antibodies against it.112
Pet hamsters have caused outbreaks of human LCM. In one outbreak in
New York State, fifty-seven cases of LCM meningitis occurred in a four-month
period, with the victims ranging in age from three to seventy. The highest in-
fection rates occurred in households in which hamsters were kept in open
wire cages in living rooms or other common living areas.113 Family outbreaks
have also been described, including one in which the husband developed
meningitis; his mother-in-law, encephalitis; and his wife and daughter, lesser
degrees of illness—all four had handled the family’s pet hamster.114 A hospital
outbreak of LCM infection occurred among personnel who visited a room
that housed a copy machine and cages of hamsters being used for research.
Another outbreak occurred among personnel in a research laboratory using
hamsters; two of the seven affected individuals required hospitalization.115
LCM infections in humans may be more serious, at least occasionally.
When the illness infects pregnant women, it may cross the placenta and has
been documented to cause miscarriages and death of the newborn.116 LCM
virus is also known to cause lymphomas in animals and to increase animals’
susceptibility to tumors.117
Increasing Exposure to Pets and Farm Animals

In addition to an increasing number of pet animals in the United States,
there also appears to be an increasing number of feral animals, especially
cats. These animals were originally obtained as pets but later ran away or were
abandoned. Most feral cats live in wooded areas or vacant buildings. There
are also estimated to be approximately two million feral pigs in the United
States, predominantly in Texas and other southern states.118
The number of feral cats in the United States may be as high as sixty mil-
lion but is really unknown.119 As one observer noted, “Counting cats is only
slightly less difficult than herding them.” 120 In general, however, most esti-
mates of the number of cats in the United States—pet and feral—are at least
one hundred million, or one cat for every three persons. Feral animals pose
special problems in the transmission of animal microbes, because they “come
in contact with both domestic animals and wildlife [and] they can act as con-
duits for pathogen exchange between otherwise isolated host populations.” 121
It is not necessary, however, to own pet animals to be exposed to them.
Children in the United States are exposed to animals at petting farms and
petting zoos, which have become increasingly popular in recent years. A Web
site devoted to them describes the merits of taking children to places such
as Old MacDonald’s Petting Zoo, Happy Times Farm, and Country Critters
Petting Zoo, which claims to have the “cutest critters in town.” Most petting
zoos include goats, sheep, rabbits, ducks, pigs, calves, donkeys, ponies, and
other farm animals, but some also include more exotic animals. For example,
WOW Animals in Sunland, California, advertises “50 species of mammals,
birds, reptiles, amphibians and invertebrates.” 122
In many areas, a petting farm or a petting zoo will come to you. Mobile
Menagerie in Gilbert, Arizona, suggests that you “reserve a bunch of cute
critters for your party or event.” Zoo-to-You in Leesburg, Virginia, will bring a
“baby zoo” (ducks, chicks, bunnies, and a goat or lamb) or a “full zoo” (plus
sheep, donkeys, and llamas) to your child’s birthday party for only $200 (baby
zoo) or $550 (full zoo) plus a mileage fee.123 Other events advertised as ap-
propriate for inclusion of a petting zoo are company picnics, church festivals,
and school fairs or carnivals. In what was probably a first, the University of
Louisiana at Lafayette in 2002 put a petting zoo in the parking lot of its foot-
ball stadium to increase attendance at one of its home games. According to
a news report: “That game drew 20,512 fans, about a third more than their
average attendance of 15,056.” 124
The number of children exposed to animals at petting farms or petting
zoos is impressive. A popular petting farm near Philadelphia, Pennsylvania,
for example, claimed to attract 1,500 to 2,000 persons each day. Most visitors
are young children, and most of them have direct contact with the animals by
petting or holding them, often to have their picture taken. This petting farm
came under scrutiny by public health authorities in late 2000, when fifty-one
cases of severe diarrhea occurred among its visitors. All except four of those
who became sick were ten years old or younger. Among them, sixteen had to
be hospitalized and eight developed kidney failure with a hemolytic uremic
syndrome; of these, one child required a kidney transplant. The cause of the
outbreak was found to be the 0157 strain of Escherichia coli bacteria (see
chapter 8), which was carried by cows at the farm. Children who became sick
had spent more time with the animals, were less likely to have washed their
hands after doing so, and were more likely to have purchased and eaten food
from the petting farm’s concession stand.125
There are no general data available on how frequently children become
ill after visits to petting farms or petting zoos. The Pennsylvania outbreak,
however, was not unique. Similar outbreaks caused by the same strain of bac-
teria have been reported in Washington, Wisconsin, England, and Canada;
the Canadian outbreak involved 159 visitors.126 On May 6, 2002, Inside Edi-
tion aired a program that featured outbreaks of illness at petting zoos. As part
of the story, the producers visited eight petting zoos in Florida; none of the
eight informed visitors that they might get sick from the animals, but three of
the petting zoos had signs warning that the animals could get sick from the
visitors.127
Exotic Pets
Throughout history and in many cultures, individuals have kept exotic ani-
mals as pets. Some ancient Egyptians attempted to tame gazelles, hartebeests,
and hyenas, and Moghul emperors in India kept cheetahs as pets. Australian
aborigines tamed wallabies, and North American Indians occasionally kept

pet bears. Indeed, even a president of the United States, John Quincy Adams,
is alleged to have “kept a pet alligator in the East Room bathtub” of the White
House.128
What is new is not the keeping of exotic pets but rather its rapidly increas-
ing incidence. One estimate is that the sale of exotic pets in the United States
is now a billion-dollar-a-year industry.129 The combination of animals available
on the Internet and overnight delivery service has made almost any animal
available to any person. Purchasing exotic animals may be seen as an effective
way to assert one’s individuality, as the National Alternative Pet Association
also implies on its Web site: “Is your pet unconventional? Do people put you
down because your pet isn’t a socially acceptable cat, dog or goldfish? . . . Let’s
help people understand and love our misunderstood alternative pets.” 130
Ferrets are a good example of an exotic pet that has risen rapidly in popu-
larity. They have been used for hundreds of years as rat hunters, leading to use
of the term “to ferret something out.” In the United States, there are an esti-
mated “5 to 7 million pet ferrets in approximately 4 to 5 million households
nationwide.” 131 A Web site, www.ferretstore.com, sells clothing for pet fer-
rets, including lace hats, raincoats, sweaters, T-shirts, tuxedo shirts, and Santa
Claus suits. Ferrets, however, have been known to severely injure small chil-
dren and can be infected with influenza, rabies, tuberculosis, leptospirosis,
listeriosis, salmonellosis, campylobacteriosis, and cryptosproidiosis, although
only influenza has been proven so far to have been transmitted to humans.132
Ferrets have become so commonplace that many people no longer con-
sider them exotic. To own a truly exotic pet these days, one must purchase an
animal such as an African pouch rat, bushbaby, bushy-tailed jird, capybara,
coatimundi, degus, desert jerboa, fennec fox, fire-bellied toad, gundi, hedge-
hog, kinkajou, miniature Sicilian donkey, porcupine, serval, sloth, or wallaby.
All of these and many others are available for purchase through exotic pet Web
sites. If money and space are not limiting factors, one may choose to own large
exotic animals. In October 2003, New York City police removed a 425-pound
Bengal tiger and an alligator from an apartment in Harlem.133 Also available
for sale on the Internet are buffalo ($2,000), chimpanzees ($55,000), giraffes
($60,000), jaguars ($5,000), kangaroos ($6,000), reindeer ($2,700), and spot-
ted leopards ($3,900).134 Since it is difficult to imagine a buffalo or reindeer
as a companion animal, it seems reasonable to assume that individuals who
purchase such animals do so to satisfy other needs.
The recent increase in keeping exotic animals as pets has occurred not
only in the United States but also in Europe, Asia, South America, and Africa.
The international aspect of this phenomenon is illustrated by a news account
of a German family that for thirty-three years kept a pet eel in the bathtub.
“‘He’s part of our family,’ said Hannelore Richter of Bochum, whose husband
caught the eel on a fishing trip in 1969 and took it home for supper.” However,
plans changed when “their children fell in love with it.” The family said they
had “trained it to swim into a bucket when somebody needs to bathe.” 135
What most exotic pet Web sites and pet stores do not advertise, however,
is that exotic pets come with exotic and not-so-exotic diseases. All exotic ani-
mals should be regarded as high-risk pets because of their potential for trans-
mitting disease-causing microbes to their human owners. Iguanas, raccoons,
and prairie dogs are exotic pets that illustrate this problem.
Pet iguanas are part of what has been called “an explosion of pet rep-
tile ownership in the United States.” 136 Lizards, snakes, turtles, and alligators
have also increased in popularity. Between 1991 and 2001, the number of
U.S. households with reptiles doubled to 1.7 million.137 A federal inspector
reported in 2004 that he was seeing shipments of monitor lizards arriving “al-
most weekly” and that “it was not uncommon to get shipments of 1,000 baby
boas from Colombia or pythons from Indonesia.” 138 One 2003 news account,
for example, described a Connecticut couple, the Boykos, who kept three five-
foot-long alligators in their home as pets. When authorities tried to confiscate
the alligators, Mr. Boyko protested. “We didn’t have kids,” he explained. “We
had gators.” 139
Iguanas are found in Central and South America and raised for export
on farms in Colombia and El Salvador. U.S. imports of iguanas increased
thirtyfold between 1986 and 1993 to almost eight hundred thousand per
year.140 Like all reptiles, iguanas have been infected with salmonella bacteria
for millions of years and are asymptomatic carriers of this microbe. As we will
see, infection with salmonella usually causes diarrhea, nausea, vomiting, and
abdominal cramping, although in small children and individuals who have
compromised immune systems the illness can be much more severe. A 1993
study of reptile-associated salmonella infections in New York State found ap-
proximately seven hundred cases; in 83 percent of cases the reptile was an
iguana.141 If these figures are representative of the United States as a whole,
there were approximately sixteen thousand iguana-associated cases of human
salmonella infection that year.
The most serious cases of iguana-associated salmonella infections in the
United States have been reported in very young children. For example, in
Wisconsin in 1998, a five-month-old boy died suddenly at home from septice-
mia due to Salmonella marina; a family pet iguana was found to be infected
with the same microbe.142 Salmonella-related deaths attributed to iguanas
were also reported for a three-week-old infant in Indiana and a newborn baby
in New York.143 The importance of a compromised immune system was il-
lustrated in Massachusetts in 1997, when “an 8-year-old boy with a congenital
immune deficiency developed severe vomiting, abdominal cramps, bloody

diarrhea and headache” attributed to salmonella infection from two iguanas
purchased three days before the onset of the boy’s illness.144 Adults are less
likely to develop severe forms of salmonellosis from reptiles but may do so; in
Connecticut in 1995, for example, a forty-year-old man developed osteomy-
elitis, a chronic bone infection, from a salmonella infection he acquired from
the family’s iguanas.145
In reviewing such cases, the manner of transmission of salmonella from
iguanas to family members is a cause for concern. In most instances, the
young children had no direct contact with the iguanas; rather, the infection
was transmitted to them by family members. In some cases, it was established
that “the infant’s mother fed the iguana and cleaned its cage” and “reported
handwashing after these activities.” 146 In one case, the infant’s father and pet
iguana did not even live with the boy, “but his father reported pacifying his
son by allowing him to suck his fingers during visits to the child’s house.” 147
Other children have become infected at the homes of babysitters who owned
iguanas or at a birthday party at a home in which iguanas were kept.148
Raccoons have attractive masklike faces and ringed tails and are sold on
Internet pet sites as exotic pets. They are also the major reservoir for rabies in
the United States. In the Middle Atlantic and New England states, rabies is
epidemic among them.
Rabies is caused by a virus spread by exposure to the saliva or bite of an
infected animal. Once infected, a person experiences muscle spasms, confu-
sion, hallucinations, coma, and death in almost every case. This inevitable
course can be reversed only by treating the infected person with rabies vac-
cine and prophylactic immune globulin after the exposure occurs but before
symptoms begin. In the United States, such rabies prophylaxis is given approx-
imately forty thousand times each year at an annual cost of $60 million.149
The present epidemic of raccoon rabies in the northeastern United
States began in 1977 when, according to one account, “several members of
[President] Carter’s cabinet and personal staff missed going ‘coon hunting’
over the weekend, [so] they had some raccoons imported into Virginia from
Georgia.” 150 More than 3,500 raccoons were translocated for hunting, some
of which had rabies.151 In 1977, raccoons accounted for just 2 percent of all
rabid animals in the Middle Atlantic states, but by 1983 they accounted for
84 percent.152 Dogs and cats, by contrast, accounted for less than 2 percent.
Bats, skunks, foxes, coyotes, woodchucks, and beavers may also become in-
fected with rabies; a reportedly rabid beaver “exhibited aggressive behavior by
charging canoes and kayaks” on a river.153
As the epidemic of raccoon rabies has spread in northeastern states, there
has also occurred an inevitable increase in the number of individuals exposed
to sick raccoons; these individuals must therefore undergo injections of rabies

vaccine and prophylactic immune globulin. In one case, “a baby raccoon was
passed between two families and handled by many neighborhood children,
exposing 16 persons.” In another, “a science teacher encouraged a student to
bring his pet raccoon to school.” In Florida, a pet raccoon “accounted for the
prophylaxis of 172 persons at a cost of more than $64,000.” 154 In New Hamp-
shire, a cat infected by a rabid raccoon exposed 665 people, and in New York
a goat infected by a rabid raccoon exposed 438 people.155
In February 2003, the first human case of rabies from a raccoon was re-
ported. A twenty-five-year-old man in northern Virginia died after two weeks
of hospitalization. Molecular studies established that the rabies virus had
come from a raccoon, despite the man’s having had no known exposure to
pet or wild raccoons.156 It is still not known how he became infected. While
attempts are made to bring rabies under control by animal immunization,
the increased popularity of pet raccoons has led to new health hazards to
humans.
Prairie dogs, foot-long rodents related to squirrels and marmots, became
popular as exotic pets in the 1990s. Although no figures are available on the
total number of pet prairie dogs in the United States, “officials estimate that
20,000 prairie dogs a year are exported from Texas alone to be sold as pets.” 157
They also became popular as pets in Japan until they were banned from
that country because they carry not only monkeypox, but also tularemia and
plague.158
In June 2003, an outbreak of monkeypox occurred in Midwestern states
among individuals who had had contact with pet prairie dogs. Symptoms of
monkeypox include a high fever, cough, enlarged lymph nodes, and a rash
that looks like smallpox. This is not surprising, since the virus that causes
monkeypox is in the orthopoxvirus family and closely related to the virus that
causes smallpox. Monkeypox outbreaks in Africa have had mortality rates of
up to 10 percent. In the U.S. outbreak, one-quarter of the eighty-six cases
required hospitalization, but there were no deaths.
Since monkeypox had never been reported anywhere except in Africa
before June 2003, an immediate investigation was undertaken by health au-
thorities to ascertain its origin. They discovered that the infected prairie dogs
had come from an animal distributor in Illinois who had housed prairie dogs
in close proximity to Gambian pouch rats and other rodents imported from
Africa; several of these rodents were found to be carriers of the monkeypox
virus.
Gambian pouch rats, which are the size of small cats, have hamsterlike
pouches and have also become popular in the United States as exotic pets.
An Internet Web site describes them as “very intelligent, . . . [with] the abil-
ity to bond/show deep affection to their human companions. . . . When the

pouches are full it gives the pouch rat an absolutely adorable, yet comical face.
If you like rodents, especially rats, they are sure to captivate your heart.” 159 No
information is available on the number of Gambian pouch rats imported into
the United States each year, but the shipment from Africa that included the
infected rats consisted of “about 800 small mammals of nine different species,
including . . . rope squirrels, tree squirrels, Gambian pouch rats, brushtail
porcupines, dormice, and striped mice.” 160
It is not yet known whether the 2003 U.S. monkeypox outbreak was
fully contained. Squirrels, not monkeys, are the natural reservoir of the virus
in Africa; the disease acquired its name because it often kills monkeys. It is
known that in the U.S. outbreak, monkeypox spread to a pet rabbit in one of
the homes. Attempts to trace all of the possibly infected prairie dogs proved
difficult because, in addition to having been sold in pet stores, they were ex-
changed at pet “swap meets,” at which no sales records are kept.
Public health officials are concerned about the possible spread of mon-
keypox to pet hamsters, gerbils, or other pet rodents. Even worse, if an in-
fected pet prairie dog had been released in the wild, it could have transmitted
the disease to squirrels, chipmunks, rats, and wild prairie dogs, which would
permanently establish the disease among U.S. wildlife, similar to what oc-
curred with the plague bacteria a century earlier.
The 2003 U.S. monkeypox outbreak did have one beneficial effect: It
focused public attention on the widespread and largely unregulated sale of
exotic animals as pets. Several states subsequently banned the sale of prairie
dogs, and the federal government restricted the importation of some African
rodents. Perhaps the definitive word on the prairie-dog outbreak appeared in
an editorial in the June 11, 2003, New York Times: “Domestic life is not appro-
priate for any creature of the wild, whether it is a lion cub or a Gambian rat.
And prairie dogs are appropriate pets only for people who own a prairie.”
8=
C H A P T E R
Humans as Diners
Mad Cows and Sane Chickens
Man occupies a unique position in the pecking order of nature. Not only
is he able to use anything that he wants as a source of food, but under
ordinary circumstances he need not fall prey to any living creature of
another species. . . . There is only one significant exception to his biologi-
cal dominance, but a very large one. Like any other living thing, man can
become the victim of microorganisms, and in fact these account for a large
percentage of his diseases.
Rene Dubos, Mirage of Health
H umans have been infected with animal microbes since we first began
to eat animal meat in the Paleolithic period. Paleolithic man acquired
many animal macroparasites, such as taenia and trichinosis, as well as bacteria
that cause such diseases as brucellosis, tularemia, and glanders. Humans have
thus been exposed to animal microbes over thousands of years by eating ani-
mals’ meat and drinking their milk, and through animal fecal contamination
of food and water. In biblical times, many of the Mosaic laws that governed
food consumption and animal care, as detailed in Deuteronomy and Leviti-
cus, were attempts to limit the spread of food-borne and other diseases from
animals to humans.
Until recently, human exposure to animal microbes through meat, milk,
or contamination was a local affair. Cattle and chickens were raised on fam-
ily farms, then slaughtered and eaten locally. Fruits and vegetables were also
homegrown, and most families prepared their own food and ate meals at
home. In recent years, however, the human food chain has changed mark-
edly. Cattle and chickens are commonly raised by large agribusinesses, killed
in mechanized slaughterhouses, and distributed to hundreds, even thousands,
= 97
of food outlets in surrounding states. Fruits and vegetables are imported from
distant states and, increasingly, distant countries where standards of sanitation
and food processing are less stringent than our own. Families that prepare
their own meals are becoming progressively fewer; instead, families buy pre-
cooked and prepared foods, order in, or eat out.
Much of the increase in food-borne illnesses in the United States in
recent years has been associated with ordering in and eating out. Many of
the jobs in restaurant kitchens pay low wages and offer few or no sick-leave
benefits, making it more likely that employees will come to work even when
sick because they cannot afford not to. Many restaurant employees are also
immigrants from countries where a large percentage of people suffer from
intestinal diseases. According to one study, although fewer than 1 percent of
individuals among the general public host a disease-carrying intestinal para-
site, “in restaurants that have triggered food-borne outbreaks, up to 18 percent
of food handlers have been shown to suffer intestinal infections.” Contami-
nation of food by an infected food handler can occur in a myriad of ways, as
illustrated by a worker “who used his bare hands and arms to stir 76 liters of
butter-cream frosting, an unconventional culinary technique.” 1
Some increase in food-borne illnesses has come about because of chang-
ing dietary patterns. For example, raw fish, in the form of sushi or sashimi,
has become popular in the United States. Fish carry more than fifty types of
parasites, most of which are killed with adequate cooking. The most common
infections spring from a worm called Diphyllobothrium latum, which causes
a persistent infection characterized by diarrhea, weight loss, and anemia.
Recently, there have been several cases of infection due to another parasite
called Anisakis simplex. This parasite can cause abdominal pain and intestinal
obstruction, sometimes leading to a misdiagnosis of intestinal tumors. The
consumption of raw shellfish can also result in infection with hepatitis A or
Norwalk-type viruses. We can avoid all these infections by not eating raw or
undercooked seafood.
Changes in the human food chain have brought about many new oppor-
tunities for animal microbes to cause food-borne illnesses. Not all food-borne
illnesses, of course, are caused by microbes that come from animals, but the
vast majority of them are. Exceptions include food-borne diseases due to con-
tamination with organisms from human feces, the cause of the outbreak of
hepatitis A among more than five hundred restaurant patrons who in 2003 ate
contaminated green onions at a restaurant in Pennsylvania.2
A measure of the importance of animal microbes in causing food-borne
illnesses in the United States is the Emerging Infections Program’s Foodborne
Diseases Active Surveillance Network, maintained by the Centers for Dis-
ease Control and Prevention (CDC).3 CDC estimates that seventy-six million
Humans as Diners = 99
Americans contract food-borne illnesses each year, and it maintains ongoing

surveys of ten microbes thought to be important causes of these illnesses.
Nine of the microbes surveyed by CDC come from animals; they are Campy-
lobacter, Listeria, Salmonella, Escherichia coli 0157, Yersinia, Shigella, Cryp-
tosporidium, Cyclospora, and hemolytic uremic syndrome. The origin of the
tenth, Vibrio, is not known.
Typhoid Mary, Salmonella, and Chickens

In 1915, New York health authorities banished Mary Mallon, an Irish immi-
grant cook, to a cottage on a small island off Manhattan, because she was in-
fected with the bacteria Salmonella typhi. Although asymptomatic herself, she
had caused nine typhoid outbreaks, with fifty-four cases and four deaths, by
inadvertently infecting the food and water other people ingested. By the time
she was banished, Mary Mallon was widely known to the public as Typhoid
Mary. She remained on the island until she died in 1938.
Salmonella typhi is unusual in being one of the only serotypes among
the over 2,500 known salmonella serotypes that have specifically adapted to
humans. Although Salmonella typhi almost certainly was originally transmit-
ted to humans from reptiles or birds, which are thought to be the origin of all
salmonella, it acquired an ability to be transmitted directly from human to
human, usually by contaminated food or water. That is why Mary Mallon’s
profession as a cook made her so dangerous.
Typhoid epidemics occurred frequently in U.S. cities in the nineteenth
century. In Philadelphia, for example, an 1899 epidemic killed 948 people.
During the Spanish-American War, typhoid was rampant among U.S. troops
and killed seven times more soldiers than were killed by bullets.4 Even today,
Salmonella typhi causes twelve million illnesses worldwide each year and is
an important cause of death in such countries as Indonesia, Nigeria, and In-
dia. Salmonella typhi thus continues to serve as an important reminder of
what salmonella serotypes can do if they adapt to humans.
Fortunately, the vast majority of the known serotypes of salmonella have
not yet adapted to humans and cause human disease only when they are ac-
quired from infected chickens or eggs. Salmonella bacteria are the single larg-
est cause of death among the known causes of food-borne illness in the United
States.5 Of the estimated 76 million Americans who develop food-borne ill-
nesses each year, 325,000 are hospitalized and approximately 5,000, mostly
elderly, die. Between 1976 and 1995, the incidence of salmonella infections
increased eightfold in the United States, and even more sharply in England
and other industrialized countries.6
Clinically, food-borne salmonella infections may vary from mild to severe.

After an incubation period of one-half to three days, the infected person devel-
ops fever, abdominal pain, and severe diarrhea, which, untreated, may last for
four to five days. Occasional cases develop complications such as pneumonia,
endocarditis of the heart valves, pyelonephritis of the kidney, osteomyelitis of
bones, arthritis of joints, or an abscess in virtually any organ. Such complica-
tions occur most commonly in the elderly, with death rates from salmonella
in nursing homes estimated to be forty to seventy times higher than in the
general population.7 Newborn children are also at high risk from complica-
tions of salmonella infections, and outbreaks of salmonella infections have
occurred in newborn nurseries with devastating consequences.8 Overall, the
outcome of salmonella food-borne infections is estimated as follows: 94 per-
cent of individuals recover without medical care; 5 percent visit a physician;
0.5 percent are hospitalized; and 0.05 percent die.9
A disturbing recent development in human salmonella infections are
reports of increasing antibiotic resistance to some salmonella serotypes. Sal-
monella Newport, for example, has been found to be “resistant to at least nine
of 17 antimicrobials tested,” including the antibiotic most commonly used
to treat serious infections in children. A summary of such cases noted that
“antimicrobial-resistant salmonella infections have been associated with an
increased hospitalization rate, morbidity, and mortality.” 10 A study in Den-
mark, for example, reported that individuals infected with a salmonella sero-
type resistant to quinolone antibiotics had “a mortality rate 10.3 times higher
than the general population.” 11 It is likely that the increase in resistance to
antibiotics is due to the widespread administration of antibiotics to animals
in the food chain.12 Given the broad human exposure to salmonella bacteria,
antibiotic-resistant strains pose a significant risk of future major outbreaks of
disease. This development provides another example of how the management
of animals used as food can affect human health.
Episodes of food-borne salmonella infections in which many people be-
come sick are much more likely to come to public attention than are individ-
ual infections. In fact, nobody really knows how many cases of salmonellosis
occur each year, because most cases are relatively mild and attributed simply
to “food poisoning.” It has been estimated that twenty to one hundred cases
of salmonella infection go unreported for every reported case.13 Examples
of salmonella outbreaks include 688 inmates in the South Carolina prison
system who in February 2001 developed severe abdominal cramps, nausea,
vomiting, and diarrhea after eating tuna salad made with eggs contaminated
with Salmonella enteritidis. Four months later in North Carolina, fifty-one
persons became similarly affected after eating contaminated eggs. These were
merely two of the 677 multiple-person outbreaks of salmonellosis reported in
the United States between 1990 and 2001. These outbreaks alone resulted in
23,366 illnesses, 1,988 hospitalizations, and thirty-three deaths.14
The variety of egg products that have been linked to salmonellosis out-
breaks is impressive. Scrambled eggs were the cause of outbreaks at a British
prison15 and at a restaurant chain’s breakfast bar.16 Egg sandwiches led to an
outbreak at a wedding reception, and scotch eggs produced an outbreak in a
hospital.17 Hollandaise and béarnaise sauces produced illness in seventy-three
individuals who had eaten at a Tennessee restaurant one evening.18 Home-
made ice cream sickened sixty-three out of seventy-five individuals at a charity
bridge tournament, while an almond parfait dessert caused illness in 381 con-
ference attendees at a hotel.19 All five children in one family became ill with
salmonellosis after eating chocolate mousse; the mousse had been prepared
by one of the children at school “in a domestic science lesson.” 20
In fact, Salmonellosis outbreaks have been linked to almost every prod-
uct in which eggs are used—omelets, eggnog, Caesar salad, custard, me-
ringue pies, French toast, tartare sauce, asparagus egg sauce, quiche, lasa-
gna, and stuffed pasta. One of the larger Salmonella enteritidis outbreaks,
affecting more than four hundred people in the Midwest, was caused not
directly by eggs but rather by an ice cream mix that had become contami-
nated with the bacteria “by hauling it in a tanker improperly cleaned after
carrying a load of unpasteurized liquid eggs.” 21
Although Salmonella enteritidis has been the principal salmonella sero-
type implicated in recent outbreaks caused by eggs, other serotypes may also
lead to outbreaks. Salmonella heidelberg, for example, was the cause of an
outbreak among 121 patients in a California hospital; they had all eaten tapi-
oca pudding to which raw egg whites had been added. Salmonella heidelberg
was also the cause of “a large outbreak of salmonellosis occurring among 700
University of Utah students who attended a sorority luncheon.” 22
Salmonella typhimurium is, after Salmonella enteritidis, the salmonella
serotype that causes the most egg-related outbreaks of disease. For example,
187 students at a college in Washington state became ill after eating chocolate
meringue pie contaminated with this bacteria.23 And in a politically note-
worthy outbreak, many of the seven hundred guests at a social function in
England’s House of Lords became sick after eating “a variety of dishes made
with mayonnaise containing fresh shell eggs” contaminated with Salmonella
typhimurium.24
Accounts of egg-related salmonella infections often note that the eggs
were undercooked or added raw, as in eggnogs. Experiments have shown that
salmonella bacteria remains viable in eggs cooked sunny-side up or “over
easy,” as well as in boiled or fried eggs in which the yolk remains liquid.25
Other experiments have shown that “cooking eggs longer than usual—boiling
for seven minutes, poaching for five minutes, and frying on each side for three
minutes—was necessary to destroy salmonella that was artificially inoculated
into yolks.” On the other hand, “no duration of frying ‘sunnyside’ (not turned)
eggs was sufficient to kill all the salmonella.” 26 The temperature of the egg
prior to cooking also makes a difference; eggs taken directly from a refrigerator
require longer cooking to reach a temperature that kills the salmonella.
Outbreaks of salmonellosis caused by chickens or other poultry are less
frequently reported than outbreaks caused by eggs. The main reason for the
discrepancy in reporting probably has to do with how eggs and chicken are
most commonly served. For example, one church social may include with its
dinner offerings five pieces of infected chicken, while another church social
may include five infected eggs. Among the one hundred guests at the former,
five eat the individual chicken pieces and become sick a day or two later, but
people are not likely to connect the illness of these five people to the church
social or to any specific food. At the other church social, however, the infected
eggs are used to make homemade ice cream and forty people become sick.
This outbreak is much more likely to be noticed, reported, and linked to the
infected eggs. Infected chicken meat is most likely to be noted as a cause of
an outbreak of salmonellosis when it is used in a chicken salad and consumed
by many people.
In a study in England of 1,426 food-borne outbreaks of all infectious in-
testinal diseases, 11 percent were caused by salmonella-contaminated poul-
try, approximately three-quarters of which were chickens and the remainder
turkeys and ducks. Among the salmonella serotypes in the poultry outbreaks,
two-thirds were caused by Salmonella enteritidis. As in the case of eggs, under-
cooking the chicken or turkey appeared to be associated with increased expo-
sure to salmonella.27 Undercooking may occur, for example, when poultry is
stuffed and then cooked at a low temperature. Precooked chickens purchased
at stores have also been indicted in some outbreaks.
Salmonellosis may also be caused by the cross-contamination of other
foods by salmonella-infected eggs or poultry, which can occur when kitchen
utensils are not properly washed between the preparation of different foods.
An example was an outbreak of salmonellosis among 102 individuals associ-
ated with a university hospital. The cause of the outbreak was traced to vanilla
pudding that was apparently contaminated when it was made “in direct spa-
tial and temporal association with the preparation of a turkey.” 28
Salmonella can also be transmitted by foods washed with water contami-
nated with these microbes. A recent outbreak of Salmonella Newport infec-
tion resulted in illness in at least seventy-eight individuals in thirteen states;
fifteen were hospitalized, and two died. The outbreak was traced to the eating
of contaminated mangos that came from a farm in Brazil. The source of con-
tamination was water used in a new infusion process carried out at the farm in
an attempt to remove the larvae of the Mediterranean fruit fly before export-
ing the mangos to the United States.29 This is an example of how an attempt
to remove one hazard can lead to new, and unexpected, hazards.
Finally, salmonellosis can be transmitted directly from chickens or other
poultry when humans merely handle live birds. In 1999, outbreaks of salmo-
nellosis occurred among children in two states. Upon investigation, it was
found that the children had handled baby chicks or ducklings, many of which
had been given to them as presents at Easter. The report of the outbreak noted
that “one child kept young birds in his bedroom and another carried chicks
inside his jacket.” 30 In 1991, a similar outbreak of sixteen cases of salmonel-
losis caused by Salmonella hadar occurred among children with pet ducklings
in northeastern states. “In all homes, ducklings were initially kept inside; in
a least three, they were allowed to run free. In one home, a duckling lived in
the bathtub where children bathed.” 31
There are several reasons for the increasing incidence of salmonella in-
fections in the United States, including improved reporting of cases. The in-
creasing practices of buying prepared and precooked foods and of eating out
also account for some of the increase. The largest reason for the increasing
incidence of salmonella infections, however, is the greater mechanization of
the poultry business.
In the United States, poultry production is big business. In 2001, 85.7 bil-
lion eggs and 8.4 billion chickens were sold. On a per capita basis, every man,
woman, and child consumes the equivalent of three hundred eggs and thirty
chickens per year. Approximately two-thirds of the eggs are sold as shell eggs,
and the rest processed as egg products in such foods as pasta, ice cream, cake
mixes, and bakery products.
Large egg producers have highly automated facilities in which up to
eighty thousand hens lay eggs. In the 1970s, in an attempt to increase egg pro-
duction, efforts were undertaken to eradicate two serotypes of salmonella, Sal-
monella gallinarum and Salmonella pullorum, that affect chickens and other
poultry. These serotypes do not affect humans but cause diarrhea and other
illnesses in poultry, leading to decreased egg production. In severe epidemics,
these bacteria have been known to kill entire flocks of chickens.32 Salmonella
enteritidis is closely related to these two serotypes, and in fact, studies suggest
that all three serotypes evolved from a common ancestor.33 As Salmonella gal-
linarum and Salmonella pullorum, which do not cause human disease, were
eradicated from chickens, Salmonella enteritidis, which does cause human
disease, took their place.34 Salmonella enteritidis in very young chicks may
cause symptoms, but in older chickens it is asymptomatic. Thus, an entire

flock of chickens may be infected with this bacteria, with no outward sign to
indicate potential problems for humans.
Chickens infected with Salmonella enteritidis may transmit the infection
to humans through their eggs or their meat. Infection of the eggs may occur
through cracks in the eggs once they have been laid if they come into contact
with chicken feces or other infected material. More ominously, Salmonella en-
teritidis may be passed from the infected chicken to the egg yolk or white even
before the egg is laid.35 Thus, you can have an infected but completely healthy-
looking chicken that lays infected but completely normal-looking eggs.
Eggs may also become cross contaminated during processing if the shell
is cracked. Poor refrigeration allows the bacteria to multiply, making it more
likely that human disease will occur if the egg is eaten raw or undercooked. Al-
though eggs are dated for sale by retailers, the U.S. Department of Agriculture
has reported that “eggs are occasionally removed from retail establishments
when they are within a few days of the expiration or sell-by date stamped on
the carton and returned to the processing plant,” where they are given a new
expiration date.36 Such a practice would give bacteria in the egg additional
time to multiply. A 1998 U.S. Department of Agriculture report, “Salmonella
Enteritidis Risk Assessment,” estimated that approximately 2.3 million eggs
sold that year were infected with salmonella and thus potentially capable of
causing human disease.37 The infection rate would thus be one egg in every
twenty-eight thousand.
Chickens themselves may become infected with salmonella in a variety
of ways. The bacteria may be introduced into the henhouse by mice, which
are common carriers, or by cats used to control the mice.38 Since humans may
be infected with Salmonella enteritidis, they may also carry the bacteria from
henhouse to henhouse.
Cross-contamination from one infected chicken to previously nonin-
fected chickens is thought to occur during the slaughtering process. Poultry-
processing plants have become highly automated, “slaughtering up to 200
birds per minute.” 39 Dead chickens are put together into scalding tanks to
loosen their feathers. The feathers are then plucked by mechanical fingers.
Both the scalding and the plucking processes may transmit salmonella from
one chicken to another. Evisceration is also done mechanically; according to
one study, when one chicken was contaminated, “the next 42 birds were con-
taminated with the tracer bacteria and . . . there was sporadic contamination
up to the 150th bird.” 40
How often are chickens contaminated with salmonella sold in the United
States? A 1998 Consumer Reports study of a number of brands reported a
16 percent average salmonella contamination rate, with variation by brand
from 4 percent (“Foster Farms”) to 53 percent (several “premium” brands).41

Since 8.4 billion chickens were sold in the United States in 2001, a 16 per-
cent contamination rate means that 1.3 billion of them carried salmonella.
A study in England reported “that 30 percent of raw chicken carcasses are
contaminated with salmonella,” with Salmonella enteritidis the most com-
mon serotype.42
Salmonella can reach humans from food sources in addition to eggs and
chicken. The largest salmonella outbreak in the United States occurred in Illi-
nois and Wisconsin in 1984 and affected an estimated two hundred thousand
persons. The source was milk contaminated with Salmonella typhimurium.43
Outbreaks of salmonellosis caused by this serotype have also been reported
as caused by “food samples associated with different types of imported veg-
etables, spices, and seeds, including tahini, fresh and dried spices, banana
leaves, and bean sprouts.” Tahini, which is made from sesame seeds, is used in
hummus. Cases of salmonellosis have also been reported from eating helva, a
sweet made from sesame seed that is popular in the Middle East.44
Outbreaks of salmonellosis have also been caused by eating undercooked
ground beef or beef jerky.45 Especially disturbing for chocolate lovers was the
report of eighty cases of salmonellosis caused by “Christmas-wrapped choco-
late balls” contaminated by Salmonella eastbourne; “bacteriological testing
of samples taken at the plant implicated cocoa beans as the probable source
of the salmonella organisms that, in the low-moisture chocolate, were able
to survive heating during production.” 46 Individuals who use marijuana also
have reason to worry. In 1981, an outbreak of eighty-five cases of salmonellosis
was reported as caused by marijuana contaminated by Salmonella muenchen.
The mechanism of contamination was thought to be “direct mixing of mari-
juana with animal feces, which might occur as a result of fertilization with
untreated animal manure, inadvertent contamination during drying or stor-
age, or simply direct adulteration with dried animal manure to increase the
weight of the product.” 47
Animal Microbes That Cause

Other Food-Borne Illnesses
Although salmonella is thought to be the leading cause of fatalities in the
United States from food-borne illnesses, the CDC has identified five other
microbes that also account for a significant number of deaths.48 These are
the bacteria that cause listeriosis, campylobacteriosis, and colitis due to Esch-
erichia coli; the parasite that causes toxoplasmosis (see chapter 7); and the Nor-
walk viruses that cause diarrhea. The first four of these are usually transmitted
from animals to humans. Norwalk viruses, the most common cause of viral
diarrhea in adults, are thought to be transmitted from person to person. How-
ever, recent studies have identified strains of Norwalk viruses in farm animals,
raising the possibility that these agents may also be transmitted from animals,
or that animals may serve as reservoirs of infection.49
Although not yet a household name, listeriosis is emerging as an impor-
tant food-borne illness because about one-third of human cases are fatal. It
is caused by a remarkably hardy bacterium, Listeria monocytogenes, that can
survive for up to two years in the soil. It has been identified in more than forty
species of domestic mammals and twenty species of birds, including chick-
ens, ducks, and turkeys. In sheep and goats, listeriosis is an important cause of
abortion and other illnesses.
Listeriosis is transmitted from animals to humans mostly through con-
taminated foods. Outbreaks that involve large groups of people have been
attributed to foods as diverse as cheese, pork, turkey, paté, mussels, coleslaw,
and milk.50 Individuals most likely to be infected are pregnant women, the
elderly, and persons with impaired immune systems. Infection in pregnant
women commonly leads to spontaneous abortion, premature birth, or seri-
ous infection of the newborn; surviving infants can have adverse long-term
consequences, especially if the infection involves the brain or central nervous
system. In elderly and immunocompromised individuals, listeriosis begins as
a flulike illness, then may proceed to meningitis, with fever, headache, or dis-
semination of the bacteria throughout the body.
The mortality rate from listeriosis is notably high. An outbreak in north-
eastern states during the summer of 2002 led to seven deaths and three still-
births among forty-six cases.51 The cause of the outbreak was contamination
of turkey deli meat at a poultry-processing plant in Pennsylvania. It led to the
recall of 27.4 million pounds of meat, the nation’s largest meat recall up to
that time, as well as to public accusations that the government was not doing
enough to protect the nation’s food supply.52
Campylobacteriosis is another important but little-known food-borne in-
fection. Recognized only twenty-five years ago, it has since been labeled “the
most common form of acute infective diarrhea identified in most industrial-
ized countries of the world.” 53
Campylobacteriosis is caused by Campylobacter bacteria, which are
closely related to Helicobacter bacteria, the cause of gastric ulcers. It predomi-
nantly affects children and young adults, beginning with flulike symptoms and
a fever and progressing to severe diarrhea with abdominal pain. In most cases,
the illness lasts only two or three days and remits without complications. In
approximately 1 percent of cases, campylobacteriosis is followed by arthritis or
by the Guillain-Barré syndrome, a severe neurological illness. Campylobacter
bacteria have also recently been linked to immunoproliferative small intestine

disease, a type of lymphoma.54
Campylobacter bacteria are widely distributed among birds and among
some domestic animals. Approximately half of all cases of campylobacteriosis
come from chickens, especially those processed by poultry-processing plants,
in which one infected bird may contaminate others. Contaminated chickens
may spread their microbes to other foods as well; as one account notes: “It
does not require much imagination to appreciate the ease with which a few
hundred bacteria can be transferred from, say, a fresh broiler covered in a
million bacteria to a nearby bit of salad or piece of bread.” 55 Undercooked
chicken or other meat, as often occurs in barbecues and fondue cooking, are
especially likely to cause problems.
An unusual outbreak of campylobacteriosis in England was caused by
milk bottles that were capped with only an aluminum foil cover and left on
the doorstep by milk-truck drivers. Magpies and jackdaws, both of which carry
Campylobacter, learned to peck through the caps of the milk bottles to get the
milk, and thereby contaminated the milk with Campylobacter. This problem
was solved by putting more substantial caps on the milk bottles.
The third bacterial disease identified by the CDC as responsible for a sig-
nificant number of food-borne illness-associated deaths in the United States
is diarrheal disease caused by the Escherichia coli and Shigella complex. Al-
though these were originally believed to be separate bacterial families, we
now know that they are part of a single family.56 The most lethal member of
this group is Escherichia coli serotype 0157, which has been responsible for
several outbreaks of severe diarrheal disease.
Escherichia coli in humans may cause mild diarrhea, severe diarrhea with
bloody stools (dysentery), or a hemolytic uremic syndrome (HUS) that is a lead-
ing cause of kidney failure in children. At least 5 percent of children with HUS
die, and a third more have chronic kidney problems such as hypertension.
Escherichia coli bacteria are widely distributed in cattle, most of which
are asymptomatic carriers. Transmission to humans occurs primarily through
undercooked beef, particularly in the form of beefburgers, or through unpas-
teurized milk, but it may occur by any exposure to food or water contami-
nated with cattle feces. In Scotland, for example, a 1996 outbreak caused by
contaminated meat from a local butcher affected more than 400 persons, of
which 151 were admitted to hospitals and 18 died.57 A 1996 outbreak in Japan
affected more than 6,000 schoolchildren, and 102 of them developed kidney
disease with a HUS.58 In the United States, thirty-seven children developed
the hemolytic uremic syndrome after eating beefburgers at a Jack in the Box
restaurant in the Seattle area. Half of the children also had abnormalities in
other organs, including the heart, lung, pancreas, intestinal tract, and central
nervous system, and three of the children died. Further investigation revealed
that this was part of a three-state outbreak comprising 501 cases of disease
resulting in 301 hospitalizations. The main source of illness appeared to be
undercooked beefburgers.59 Similar outbreaks have been reported in other
areas of the country; in some cases, the outbreaks were not recognized as such
until they were investigated by public health officials.60
Escherichia coli may occasionally be transmitted to humans from other
animals, including pigs, goats, and sheep. It may also contaminate a variety
of other foods that may then cause outbreaks of human disease. For example,
in 1997, contaminated alfalfa sprouts were responsible for an outbreak in Vir-
ginia among forty-eight persons, eleven of whom were hospitalized. Similarly,
a 1998 outbreak in North Carolina that affected 142 people was attributed to
contaminated coleslaw in a restaurant, and a 1999 outbreak in Nebraska that
affected 72 people was due to contaminated lettuce in a restaurant.61
The Message from Mad Cows

On December 23, 2003, U.S. secretary of agriculture Ann Veneman called a
news conference to announce the diagnosis of bovine spongiform encepha-
lopathy (BSE), popularly known as mad cow disease, in the first U.S. cow.
Seven months earlier, BSE had been reported in a Canadian cow, so the an-
nouncement should have been expected, especially when it was revealed that
the U.S. cow had come from a Canadian herd. Even so, stocks in beef-related
companies fell sharply, other nations shut their doors to U.S. beef exports, and
thousands of Americans who had possibly eaten beef from the infected cow
worried.
At the news conference, Veneman said: “The risk to human health is
extremely low. . . . I plan to serve beef for my Christmas dinner, and we re-
main confident in the safety of our food supply.” 62 Veneman’s assurances were
reminiscent of those provided in 1989 by John Gummer, the British minister
of agriculture, during an outbreak of BSE in England. At that time, there had
been no proven cases of BSE having been transmitted from cows to humans.
Gummer, accompanied by his four-year-old daughter, appeared on television
to publicly assure people that eating beef was safe, as the two of them were
shown eating large beefburgers.
Such assurances were revealed to have been overly optimistic in 1995,
when a young Royal Air Force cadet became the first known human victim
of BSE. By mid-2004, a total of 146 British citizens and eleven individuals in
other countries had died; all were thought to have gotten BSE by eating con-
taminated beef. In addition, testing of lymphatic tissue randomly taken from
British citizens during routine removal of tonsils and appendices suggested

that as many as 3,800 other individuals are harboring the prions thought to
cause BSE;63 how many of them will eventually develop disease is unknown.
The British epidemic of BSE among cattle was eventually controlled by
slaughtering four million of them. A prominent victim of the BSE epidemic
was the Conservative Party, which went down to resounding defeat, in part
because of its perceived mishandling of the BSE epidemic.
The prions thought to cause BSE are strange and poorly understood mi-
crobes. They are bits of protein that contain no genetic material—neither
DNA nor RNA—and yet are able to reproduce within cells and cause dis-
ease. They are not bacteria, viruses, or protozoa but rather variant proteins
that function as infectious agents by becoming misfolded, thus changing their
structure and clinical properties. Prions attack brain tissue, producing small
holes that give the brain the appearance of a sponge, when examined under a
microscope after death. This gives rise to the official name of prion diseases,
spongiform encephalopathies. Prions are also strange insofar as they may take
years to cause symptoms after they have entered the human body. For many
cases of human BSE, this latent period is thought to be ten years or longer,
and for other human prion diseases, the latent period may be as long as twenty
years.
Symptoms of human prion disease include mental changes, memory
loss, involuntary movements, seizures, and an inevitable progression to de-
mentia and death. There is no known treatment. The best-studied human
prion disease is Creutzfeldt-Jakob disease (CJD), which affects approximately
one person in every million; human BSE is officially referred to as “variant
CJD.” CJD may be transmitted from one infected individual after death to an-
other individual through the transplantation of postmortem brain tissue, such
as dural grafts or pituitary growth hormone, or through corneal transplants.
CJD may also arise spontaneously, and there is thought to be a genetic predis-
position to acquiring it. Researchers have suggested that some “spontaneous”
cases of CJD may in fact be caused by a person’s having eaten beef from cows
infected by BSE; if this is true, then variant CJD obtained from BSE-infected
cows and “spontaneous” CJD may be variants of the same disease.
Another human prion disease is kuru, which was until recently endemic
in the highlands of Papua New Guinea. It was transmitted from person to
person through the eating of brains of dead relatives as a part of local funeral
rituals.
The transmission of BSE between cattle, and from cattle to humans, is
a direct consequence of modern methods of raising and slaughtering cattle.
For thousands of years, cattle were raised on small farms where calves were
nursed by their mothers. Such bucolic scenes have been largely replaced by
giant agribusinesses where “for years calves have been fed cow’s blood instead
of milk, and cattle feed has been allowed to contain composted wastes from
chicken coops, including feathers, spilled feed, and even feces.” 64
Furthermore, for many years, calves and cattle were fed meat- and-bone
meal, which is made from dead cattle. Meat-and-bone meal is a product of
rendering, which is essentially the boiling of animal carcasses to obtain fat
and protein. Although rules now prohibit the feeding of cattle-derived meat-
and-bone meal to other cattle, it still is commonly fed to chickens and pigs.
When the chickens and pigs die, they may, in turn, be rendered, and the prod-
uct fed to cattle. It is a widely used system of high-tech barnyard cannibalism.
Meat-and-bone meal is also a common ingredient in pet foods.
The main danger of meat-and-bone meal is that it may contain tissue
from the central nervous system, including the brain, spinal cord, or nerves,
the main tissues thought to contain prions. Meat-and-bone meal made from
a single animal infected with BSE can theoretically infect hundreds of others
when they ingest the meat-and-bone meal. The BSE epidemic among British
cattle in the 1980s and 1990s was, in fact, caused by an inadvertent change in
the process by which meat-and-bone meal was being made, making it more
likely that prions would be passed on.65
The transmission of BSE from infected cattle to humans is also a con-
sequence of mechanized advanced meat-recovery systems that try to recover
every possible ounce of meat. These systems sometimes also recover tissue
from the brain or spinal cord, or other nerve tissue. Testing by the Depart-
ment of Agriculture in 2002 found that 35 percent of advanced meat-recovery
systems included such tissue.66 This tissue may then become incorporated
into ground beef, sausage, bologna, salami, hot dogs, pizza meat toppings,
taco fillings, and similar foods. If a BSE-infected cow happens to be included,
infective meat may be distributed widely within days of its processing. As a
general rule, eating whole beef, such as steak or roast beef, is safer than eating
ground beef, such as beefburger meat, since the latter is more likely to have
tissue mixed with it that may include prions.
The first reported case of BSE in U.S. cattle stimulated changes in the
beef industry. Until then, less than 1 percent of the thirty-five million cattle
slaughtered each year in the United States was tested for BSE; that percentage
has now increased. Regulations were also tightened regarding the composi-
tion of meat-and-bone meal and the functioning of advanced meat-recovery
systems. Whether these changes will protect the U.S. food chain from the
transmission of animal prion diseases will not be known for a number of years.
Because of the long latent period between humans’ becoming infected with
prions and the onset of symptoms, it is difficult to assess the effectiveness of
such prevention programs.
Other prion diseases of animals include scrapie in sheep and transmis-

sible mink encephalopathy, but these diseases are not known to be transmitted
to humans. Recently, however, a prion disease of deer and elk, chronic wast-
ing disease (CWD), has come under scrutiny. CWD has spread progressively
across western states and caused concern among deer hunters, many of whom
serve venison to their families.67 To date, there has been no proven transmis-
sion of CWD to humans, although there are reports of Creutzfeldt-Jakob dis-
ease in deer hunters who have regularly eaten venison.68
In summary, of all the food-borne diseases transmitted from animals to
humans, BSE is the most publicized and most feared. This is ironic, since
the only person in the United States who has died from BSE became infected
while living in England. The chances of dying from BSE are considerably
lower than the chances of being struck by lightning. Meanwhile, hundreds of
Americans die each year from salmonellosis, listeriosis, campylobacteriosis,
and colitis due to Escherichia coli.
The truly worrisome aspect of prion diseases, including BSE and CWD,
is that so little is known about what prions really do. BSE has been trans-
mitted through contaminated food that contains beef protein to nonhuman
primates.69 BSE has also been transmitted to cats by contaminated pet food.70
In one especially disturbing case, both a cat and its owner simultaneously
developed fatal Creutzfeldt-Jakob disease, although the authors of the report
noted that the cases could have resulted from “horizontal transmission in ei-
ther direction, infection from an unknown common source, or the chance oc-
currence of two sporadic forms.” 71 Mice, hamsters, and raccoons are suscep-
tible to prion disease when artificially injected.72 There are also suggestions
that prion diseases can be passed from infected mothers to their fetuses.73 A
study showed that some animals may be infected with prion disease, have no
symptoms, but still be capable of infecting other animals.74 Especially worri-
some was a study that showed that prions may become more pathogenic when
passed from one animal species to another.75
Given the many unknowns, it would appear prudent to be conservative
in establishing safeguards for our meat supply. The steps taken following the
first U.S. case of BSE in cattle to test more cattle for BSE, keep sick cattle out
of the food chain, and make meat-recovery systems safer are steps in the right
direction. But are they enough?
9=
C H A P T E R
Microbes from the

Modern Food Chain
Lessons from SARS, Influenza, and Bird Flu
The bottom line is that humans have to think about how they treat their
animals, how they farm them, and how they market them—basically the
whole relationship between the animal kingdom and the human kingdom
is coming under stress.
Peter Cordingly, World Health Organization
T hat animal microbes can be transmitted to humans when humans eat

the meat, milk, or eggs of infected animals is widely known. Less widely
known is that animal microbes can also be transmitted to humans as a conse-
quence of the modern food chain. As our food chain has become more com-
plex and commercialized, opportunities have increased for new microbes to
emerge and old microbes to undergo mutations. Such changes may produce
new and serious threats to human health, as SARS, influenza, and bird flu (a
form of influenza) illustrate.
Wet Markets and SARS

In the spring of 2003, the city of Toronto was virtually shut down. The World
Health Organization and CDC issued travel advisories that warned visitors
not to go there, and hotel operators lost $125 million in revenue. The cause of
the shutdown was an epidemic of SARS (severe acute respiratory syndrome)
that killed 24 individuals in Toronto and 910 worldwide. Some people wore
112 =
M i c r o b e s f r o m t h e M o d e r n Fo o d C h a i n = 113
masks in public, a phenomenon not seen since the 1918 –1919 influenza
pandemic.
The origin of the SARS epidemic was live animal markets, widely re-
ferred to as wet markets, in southern China.1 Permanent large open markets
in cities such as Guangzhou and Shenzhen sell a variety of live animals that
are purchased as food. The animals include chickens, ducks, geese, pigeons,
doves, turtles, dogs, cats, crabs, and other seafood, as well as exotic animals
such as palm civets, raccoon dogs, and ferret badgers. One observer noted
that “everything that’s vaguely edible is for sale.” 2 Such markets often look
as if Noah’s ark had just been offloaded there, with hundreds of metal cages
stacked two and three high packed with animals, vendors sometimes napping
on top of the cages, and masses of people circulating among the cages, look-
ing, coughing, sneezing, drinking, and eating. For animal microbes looking
for new homes, wet markets are paradise.
Following the outbreak of SARS in 2003, the causative agent was rapidly
ascertained to be a coronavirus. Coronaviruses are known to infect dogs, cats,
cows, horses, pigs, chickens, turkeys, mice, and rats, as well as humans. In
humans, one type of coronavirus is a frequent cause of the common cold.
Coronaviruses are also known to selectively cross species barriers, such as a
coronavirus of cows that can also infect chickens but not turkeys. The corona-
virus responsible for the SARS outbreak was a novel type not previously seen,
and molecular studies suggested that it had probably evolved from another
coronavirus shortly before the outbreak.3
The specific animal origin of the SARS coronavirus, at this writing, has
yet to be determined. Palm civets, an animal related to the mongoose, are
commonly sold in the Chinese markets as food, and many of them were found
to be carrying the virus. On the basis of that finding, Chinese authorities or-
dered the killing of approximately ten thousand palm civets being raised on
farms for sale to the markets. However, when a second outbreak of SARS oc-
curred in 2004, one victim had been trapping rats in his apartment, and some
of the rats tested positive for SARS.4 Rats had also been suspected of playing a
role in the original epidemic.5 The question of identifying the definitive res-
ervoir of the SARS virus was further confused when mice, ferrets, cats, foxes,
and monkeys were all shown capable of becoming infected under certain
conditions.
The SARS epidemic demonstrated that the SARS virus has the potential
to spread very rapidly from person to person and to kill approximately 9 per-
cent of those infected. Transmission of the virus may occur through respira-
tory droplets, as when a person coughs or sneezes, or through urine, feces, or
even sweat; thus, it is possible to get SARS merely by touching an infected per-
son.6 With the assistance of air travel, SARS spread to thirty countries on five
continents within a few weeks.7 Especially worrisome was that some infected
individuals, called “super-spreaders,” appear to be highly infectious and capa-
ble of transmitting the virus to large numbers of people, whereas other people
may carry the SARS virus and show few, if any, symptoms.8 Also, between its
appearance in 2003 and its reappearance in smaller outbreaks in 2004, the
SARS virus underwent minor changes, producing a marked increase in its
ability to infect humans.9
Fish Farming and Influenza

Influenza is not usually considered a disease associated with modern food
chains, but in fact, it is. If not for the system of fish farming in southern China,
with its juxtaposition of ducks, fish, pigs, and humans, influenza as a disease
would probably not have emerged to become a major source of epidemics
around the world.
Any understanding of influenza must begin with ducks, which, along
with other aquatic birds, are the natural reservoir for influenza viruses. Her-
ons, gulls, terns, shearwaters, guillemots, and sandpipers are also infected with
influenza viruses, but their role in spreading influenza to other species is not
clear. Ducks are the aquatic species of interest, because ducks, domesticated
approximately four thousand years ago, have had extensive contact with hu-
mans. Twenty-three of the known twenty-four subtypes of influenza A are
found in ducks, with the remaining subtype found in gulls and other shore-
birds. According to influenza expert Robert Webster, there is “a vast reservoir
of influenza A viruses in aquatic birds.” 10
Ducks and other aquatic birds have probably been infected with influ-
enza viruses for millions of years. By contrast, the current strains of influenza
viruses that infect humans emerged only eight thousand years ago.11 Farmers
who raise domestic fowl have long observed the immunity of ducks to the
symptoms of influenza, even when ducks are raised in the same farmyards
with chickens and turkeys that may be experiencing severe symptoms of the
disease.12 Molecular studies of the virus also suggest that the avian influenza
viral proteins are relatively stable as compared to the proteins in human strains
of influenza. If ducks had not been domesticated, we might not even be aware
of the existence of influenza A viruses.
Ducks were probably first domesticated in China and are most numer-
ous there. Rice is also cultivated in China. Ducks are useful in rice growing,
since they feed on the weeds and insects in the rice paddy but leave the rice
alone. Ducks can also be used for their eggs and meat. It has been estimated
that there are more domestic ducks than people in China, especially in the
southern provinces, where rice growing is widespread.
Alongside rice fields and ducks in southern China, fish farming also de-
veloped. The fish are reared in natural or artificial ponds and used for food. As
fish farming developed, it was discovered that fertilizing the ponds with ani-
mal feces produced bigger fish. The feces stimulate the growth of plankton,
which is then eaten by the fish. Pigs, chickens, and ducks have traditionally
been used as sources for excrement to fertilize the fishponds. In some cases,
the feces are collected, dried, and then broadcast widely over the pond. In
other cases, pigs, chickens, or ducks are confined in cages suspended over the
fishpond, so that their feces drop directly into the water. Such systems have
become increasingly elaborate, as is one described in Thailand, where “wide
use is made of pig-hen-fish culture: the hens are in cages above the pigs which
consume hen feces, and the pigs are in pens directly above the fish ponds
into which they defecate.” 13 In recent years, fish farming has become more
widespread throughout Southeast Asia and is often referred to as aquaculture,
or the “Blue Revolution.” In 1970, a World Aquaculture Society was formed;
there is an Asia-Pacific Regional Research and Training Center for Integrated
Fish Farming in China; and manuals such as “Integrated Fish Farming in
China” are available. Fish farming is said to have “grown at over 10 percent
annually during the past decade,” and “within a decade it may overtake world
beef production.” 14
The juxtaposition of fishponds with ducks, pigs, chickens, other animals,
and humans is a unique combination that leads to rapid changes in the influ-
enza virus. Influenza A viruses consist of eight separate genetic units of RNA.
Each of the eight genetic units in turn encodes multiple units of messenger
RNA, and these are constantly changing. Mutations in the RNA genome lead
to alterations in the viral proteins, with resulting changes in the ability of the
virus to replicate, cause disease, and escape detection by the host immune
system. This process produces a slow change called genetic drift. Occasion-
ally, one of the eight genetic units is completely replaced, producing a much
more rapid change called genetic shift. Insofar as the genetic drift or genetic
shift produces changes in the two key molecules—hemagglutinin (H) and
neuraminidase (N)—that lie in the protein coat of the virus, the influenza
virus is no longer as recognizable to cells that previously could produce anti-
bodies against it.
This constant change in the influenza virus is why many individuals must
get a flu shot every year. Last year’s flu shot was made to elicit antibodies
against the specific array of H and N antigens that existed in the virus at that
time. However, during the year, the antigen array often changes, so that last
year’s flu shot may be only partly effective in eliciting antibodies against this
year’s virus. When an entire genetic unit is replaced, as occurs in genetic
shift, last year’s flu shot may elicit almost no antibodies at all. Genetic drift
and genetic shift are mechanisms influenza viruses use to continuously adapt
to new host cells and thereby avoid antibodies left over from past infections
or past vaccines.
It is now thought that genetic shift of influenza viruses occurs when two
or more viruses infect one animal, thereby allowing the genetic components to
recombine and form a new strain. Pigs are unusual insofar as they can become
simultaneously infected with more than one strain of influenza virus. One
study, for example, found that 14 percent of the pigs studied were infected with
two strains of influenza virus.15 This is the main mechanism by which genetic
shift is thought to take place, bringing about the replacement of a hemaggluti-
nin (H) or neuraminidase (N) surface antigen by a new antigen. Pigs are thus
like mixing bowls for influenza viruses, “the leading contender for the role of
intermediate host for reassortment” of the genetic segments.16
Fish farming as practiced in Southeast Asia presents ideal circumstances
for the genetic reassortment of influenza viruses. Ducks, both wild and domes-
tic, regularly swim in the fishponds that have been fertilized with pig feces.
They drink the water and also take in the water through their cloaca. Ducks
also release water and feces into the water, along with whatever influenza vi-
ruses they happen to be carrying. Pigs are given that same water to drink and
thereby ingest the influenza viruses. The pigs may also be fed the carcasses of
dead ducks. No longer confined to ducks, the influenza viruses are provided
with repeated and prolonged access to pigs and other animals that drink the
pond water. When a new strain of virus evolves in its passage between ducks,
pigs, and humans, its widespread distribution is further guaranteed by wild
ducks that land on the fish pond, drink the water, and migrate thousands of
miles to distribute the virus to other bodies of water.
It should be emphasized that it is the juxtaposition of domestic ducks,
which are the reservoir for influenza viruses, to pigs and humans that leads to
the development of new influenza strains. In the absence of ducks, fish farm-
ing would not pose a threat. Similarly, where ducks are abundant but other
animals are largely absent, there is also little threat. For example, many Cana-
dian lakes at which large numbers of wild ducks collect during the summer
months are said to be “a veritable witches’ brew of avian influenza.” 17 But be-
cause no pigs or other domesticated animals drink the water from those lakes,
there is apparently no reassortment of influenza genes and thus no emergence
of new influenza strains.
Given the antiquity of fish farming in China and what is now known
about the origins of human influenza, it is not surprising that epidemics of the
disease have occurred for several centuries. An epidemic in London in 1562

that was probably influenza was described as “a new disease that is common in
this towne . . . which passed also throughe [the queen’s] whole courte, neither
sparinge leaders, ladies nor damoysells. . . . There is no appearance of danger,
nor manie that die of the disease, except some olde folks.” An epidemic in
1781 was especially severe: “In St. Petersburg 30,000 fell ill each day, in Rome
two-thirds of the population were attacked, and in Munich three-quarters. . . .
All reports state that it started in China in the autumn.” 18
Medical historians agree that epidemics of influenza have increased in
the past two centuries, perhaps as a result of more fish farming and improved
transportation of the virus. Pandemics occurred in 1802, 1830, 1847, and
1857. The especially severe pandemic of 1889 began in central Asia and was
thus named the “Asiatic flu”; it affected up to half the population in some
European cities, killing up to 1 percent of those affected. Young adults were
especially affected, a harbinger of what was to come three decades later.
The influenza pandemic of 1918 –1919 demonstrated to the world the
lethal potential of new influenza strains. The pandemic is estimated to have
killed worldwide more than twenty million people and “ranks among the
worst disasters in human history.” 19 According to Alfred Crosby’s definitive
history of the pandemic, “nothing else—no infection, no war, no famine—
has ever killed so many in as short a period.” 20 Approximately 550,000 died in
the United States, more than the number of Americans killed in World War I,
World War II, the Korean War, and the war in Vietnam combined.
The earliest manifestations of the pandemic occurred in Spain in the
spring of 1918. Because it was first reported there, it acquired the name “Span-
ish flu,” but its real origin is unknown. A medical commission concluded that
it had begun in Turkestan, while others asserted that it had been brought to
Europe by Chinese workers hired to dig trenches for the Allied forces. An
analysis of the influenza virus strain responsible for the pandemic has estab-
lished that it first infected humans between 1900 and 1915 and had been
quietly circulating for several years before it developed into an epidemic.21
The pandemic arrived in the United States in August. In Boston, hundreds
of sailors awaiting deployment to Europe developed influenza in the crowded
barracks, and civilians began following suit in early September. Alarmingly,
many of these young and otherwise healthy young men were dying, which
was not supposed to occur with influenza. The deaths caused concern within
the medical community, and the Boston stock market was closed. But it was
difficult to get the public’s attention: In France, 896,000 U.S. troops were
preparing to attack the German lines, and at Fenway Park, Babe Ruth and the
Boston Red Sox were preparing to play the Chicago Cubs in the World Series.
In Boston schools, girls jumped rope to a new song:
I had a little bird

And its name was Enza.
I opened the window
And in-flew-Enza.22
Influenza spread rapidly among the U.S. troops preparing to leave for France.
At many bases in the United States, between 35 and 40 percent of the men
were affected, approximately 3 percent of them fatally. At Fort Devens, Massa-
chusetts, a physician described how the flu developed: “These men start with
what appears to be an ordinary attack of . . . influenza . . . and when brought
to the hospital they very rapidly develop the most viscous type of pneumonia
that has ever been seen. Two hours after admission they have the mahogany
spots over the cheek bones, and a few hours later you can begin to see the
cyanosis extending from their ears and spreading all over the face, until it is
hard to distinguish the colored men from the white. It is only a matter of a
few hours then until death comes, and it is simply a struggle for air until they
suffocate. It is horrible. . . . We have been averaging about 100 deaths per
day.” 23 At Fort Devens, “special trains” were needed to carry away the soldiers
dying from influenza. Approximately four thousand soldiers and sailors died
aboard troopships while being transported to Europe or shortly after landing
there. Influenza’s effects on U.S. troops were devastating. The U.S. Army’s
Eighty-eighth Division suffered 90 men killed, wounded, missing, or captured
in battle, but 444 others died from influenza.24 The high mortality rate in
the 1918 epidemic, especially among young people, has never been fully ex-
plained. It is possible that secondary bacterial infections caused much of it,
in which case antibiotics would have saved many lives. On the other hand,
it may simply have been a very lethal strain of the virus, in which case anti-
biotics would not have helped.
By October 1918, influenza was spreading rapidly through the civilian
population with similarly lethal effects. Philadelphia was especially hard hit,
suffering approximately eleven thousand deaths. At the city morgue, dead
bodies “were piled three and four deep in the corridors and in almost every
room, covered only with dirty and often bloodstained sheets. . . . Six wagons
and a motor truck toured the city and collected . . . corpses.” 25 On October 10
in Philadelphia, 759 people died from influenza. On October 23 in New York
City, 851 died. In Chicago, “trolleys were draped in black and used to collect
the bodies,” and funerals were restricted to a maximum of ten attendees in
addition to the undertaker.26 Washington, D.C., hospitals “stationed under-
takers at their doors to remove each body as soon as death occurred to make
room for another patient.” 27 One anecdotal account of influenza’s lethal ef-
fects told of four women who played bridge together one evening; by the next
morning three were dead. Another told of a man who boarded a streetcar to go
to work but died after it had gone only six blocks. In Washington, D.C., Con-
gressman Jacob Meeker came down with the flu, whereupon he immediately
married his secretary and “died a few hours later.” 28
One of the most visually striking symbols of the 1918 influenza pandemic
in the United States was the use of gauze masks. Although there was no evi-
dence that masks retarded the spread of the influenza viruses, authorities were
desperate to do something, so local ordinances were passed making masks
mandatory in public places and “in any place where two or more persons are
congregated . . . except when partaking of meals.” Surreal photographs show
weddings at which everyone in attendance, including the bride and groom, is
wearing a mask. A picture of a minor league baseball game shows every player
and spectator wearing a mask. Pictures show masked voters casting ballots in
the November 5 national election. And when news of the armistice reached
the United States, there were scenes of “tens of thousands of deliriously happy,
singing, masked celebrants.” 29
Many Americans opposed the wearing of masks. Called “mask slackers,”
they faced fines and in some cities were not allowed to board buses or street-
cars. Since there appeared to be no difference in the influenza rate between
those who wore masks and those who did not, however, the public grew in-
creasingly skeptical of their value. Civil libertarians and Christian Scientists
led the opposition for what came to be called the Anti-Mask League. As 1918
drew to a close, tobacconists complained that cigarette and cigar sales were
down by 50 percent because people could not smoke with their masks on.
Restaurant owners also said that business was down sharply, and shop owners
worried that masks would discourage people from Christmas shopping. And
there were practical problems. In San Francisco, the police complained that
the use of masks had encouraged robberies. In Macon, Georgia, masked army
medics awaited the arrival of fifteen hundred black recruits at the train sta-
tion. When the black recruits descended onto the platform, they fled in terror,
believing that the medics were Ku Klux Klansmen.30
Isolated communities in which people had been less exposed to previous
influenza outbreaks, and thus had fewer antibodies to help ameliorate the new
strain, were especially hard hit. The case mortality among Native Americans
was 9 percent, four times the rate in U.S. cities.31 In Nome, Alaska, 59 per-
cent of the town’s three hundred Eskimos died. In the nearby Eskimo village
of Teller, 53 percent of the inhabitants died. In Teller Mission, six miles away,
“85 percent of the population perished in a single week.” 32
The 1918 –1919 influenza pandemic also affected many U.S. writers.
Mary McCarthy was six years old and living in Seattle when her mother and
father both became ill. Alarmed, the family boarded a train for their grand-
parents’ home in Minneapolis. A conductor tried to force them off the train
“at a small wooden station in the middle of the North Dakota prairie,” but
Mary’s father, brandishing a gun, insisted that they were going to continue
their journey. Five days after they arrived in Minneapolis, her father and
mother were both dead. Mary and her three siblings, along with hundreds of
thousands of other children, were orphans.33
Thomas Wolfe was a student at the University of North Carolina when
he was summoned home by the onset of influenza in his brother Benjamin.
Wolfe later described his brother’s death in a slightly fictionalized passage
in Look Homeward, Angel: “Ben lay upon the bed below them, drenched in
light, like some enormous insect on a naturalist’s table, fighting, while they
looked at him, to save with his poor wasted body the life that no one could save
for him. It was monstrous, brutal.” 34
In Denver, Katherine Anne Porter was a twenty-four-year-old newspaper
reporter and deeply in love with her fiancé, who was going off to war. She
developed influenza so severely that “the newspaper set the type for her obitu-
ary.” 35 She survived, but her fiancé was afflicted by it and died shortly there-
after at his army training camp. Years later, Porter fictionalized those difficult
days in Pale Horse, Pale Rider:
“I wonder,” said Miranda. “How did you manage to get an extension of

leave?”
“They just gave it,” said Adam, “for no reason. The men are dying
like flies out there, anyway. This funny new disease. Simply knocks you
into a cocked hat.”
“It seems to be a plague,” said Miranda, “something out of the Mid-
dle Ages. Did you ever see so many funerals, ever?36
Outbreaks of influenza continued to occur following the 1918 –1919 di-

saster, but no true pandemic was seen again until 1957. Called the “Asian
flu,” this pandemic started in southern China and progressively spread around
the world. In the United States, it was responsible for approximately sixty
thousand deaths, mostly among the elderly. Another influenza pandemic,
the “Hong Kong flu,” swept across much of the world in 1968 and killed ap-
proximately thirty thousand Americans. In 1976, at what appeared to be the
beginning of another influenza epidemic, the “swine flu” scare led to massive
vaccination of the population; the epidemic never appeared, and the vaccina-
tions themselves caused significant illness. It was a political and public health
imbroglio.
The influenza pandemics of 1918, 1957, and 1968 were each the result
of a genetic shift of the virus that created new strains. All three were mixtures
of viruses from ducks and viruses that had adapted to pigs and to humans.
The 1918 strain was described as “a chimera of sorts: One end bore a marked
resemblance to human flu sequences, the middle was strikingly similar to
pig, while the other end again was human.” 37 The strain of influenza virus
that caused the 1957 pandemic had three genetic segments from a duck virus
and five segments from a human virus, while the strain that caused the 1968
pandemic had two of the former and six of the latter.38 Influenza experts are
unanimous in predicting that another pandemic will occur, and most believe
that it will appear soon.
Poultry Farming and Bird Flu

Influenza A viruses can affect chickens and other poultry, just as they can af-
fect many other animals. Bird flu, as it is now commonly called, was previously
called “fowl plague” and described a century ago; in the intervening years,
outbreaks of bird flu have resulted in deaths among chickens, turkeys, and,
occasionally, domestic ducks. Wild ducks and other aquatic birds, thought
to be the natural reservoir for influenza viruses, are usually not affected by
outbreaks of bird flu among poultry. Until recent years, poultry farming was
usually done on a small scale. Now it is increasingly carried out as part of
larger agribusinesses, and what were once flocks of dozens of poultry are now
flocks of thousands. Thus, when bird flu strikes, it can spread more rapidly
and widely.
Before 1997, there had never been reports of influenza being transmit-
ted directly from birds to humans, since pigs were thought to be necessary as
genetic mixing bowls. In 1997, during an outbreak of bird flu in Hong Kong,
the influenza virus was directly transmitted from infected chickens to eigh-
teen people, six of whom died. These first proven cases of bird flu in humans
were widely considered an ominous development. The strain of influenza
virus that was responsible was H5; until then, all human cases of influenza
had been caused by H1, H2, or H3 strains. The 1997 outbreak suggested that
chickens, like pigs, might serve as mixing vessels for the development of new
influenza strains. And if new strains can occur in chickens, can they also oc-
cur in other animal species known to be infected with influenza, such as
horses, cows, dogs, deer, seals, whales, monkeys, or humans?
Following the 1997 outbreak, the H5 influenza strain continued to circu-
late in ducks in China, but no additional human cases were reported. Then,
in February 2003, two Hong Kong residents returned from a visit to southern
China with bird flu, and one of them died. In December 2003, a severe epi-
demic of H5 (specifically H5N1) bird flu began in Korea. The virus appeared
to be highly pathogenic for chickens, killing them in two or three days, with
100 percent mortality in some flocks. The H5N1 strain of virus is thought to
undergo mutations rapidly and to have “a documented propensity to acquire
genes from viruses infecting other animal species.” 39
The H5N1 epidemic of bird flu spread rapidly across Southeast Asia,
infecting poultry in ten other countries within two months. In an effort to
limit its spread, public health officials ordered the slaughter of all poultry
geographically proximate to infected flocks; by mid 2004, it was estimated that
more than 100 million chickens, turkeys, geese, and ducks had been killed.40
The magnitude of the bird flu outbreak among poultry was termed “histori-
cally unprecedented.” 41
As the bird flu spread more widely, it began to infect other animals. In
Thailand, several housecats became infected and died, as did a leopard in a
zoo. All were thought to have been fed infected dead chickens. Then human
cases were reported. Among the first thirty-seven human cases, all reported
from Vietnam and Thailand, twenty-three individuals died, a mortality rate of
62 percent.42 Almost all the victims had had direct contact with poultry, and it
was assumed that the virus had spread directly from the poultry to them.
Until January 2004, there was no evidence of the spread of bird flu from
person to person. (As noted in chapter 1, many microbes spread from animals
to humans but then spread no further.) For a microbe originally transmitted
from an animal to a human to then spread from human to human usually re-
quires the microbe to undergo some reassortment of genes or mutations. This
is a big step that most microbes, fortunately, do not take. In an editorial in the
New England Journal of Medicine, the difference between animal-to-human
transmission and animal-to-human-to-human transmission was likened to the
words of the first astronaut who landed on the moon. When a microbe crosses
the species barrier from animal to human, it was said to be “one small step
to man.” Developing the ability to spread from human to human, however, is
“one giant leap to mankind.” 43
The development of an ability to be transmitted from human to human
is the major fear surrounding bird flu. In January 2004, four cases of bird flu
occurred in a single family immediately following a wedding. The groom
and both sisters who had nursed him died, while the bride became infected
but survived. Two of the four had had no known contact with poultry, and it
was assumed, although not proven, that this was the first recorded person-to-
person transmission.44
The H5N1 outbreak of bird flu and its spread to humans was not the only
bad news. In 1999, an H9N2 strain of influenza virus was detected in humans,
although it caused no serious illness.45 And in 2003, an H7N7 strain severely
affected poultry in the Netherlands, also infecting eighty-three farm workers
with a mild illness and killing a veterinarian.
As this is written, the 2004 H5N1 bird-flu epidemic has resumed. Given
its documented spread to humans, the possibility of a human epidemic caused
by this avian strain of influenza is a definite possibility. Whatever the out-
come of this epidemic, it is clear that influenza viruses are undergoing rapid
changes, at least partly in response to changing poultry-raising practices. As
noted in an editorial in the Lancet medical journal: “Live-poultry markets in
Asian countries are a breeding ground for avian influenza.” 46 In our efforts to
streamline farming practices to produce more meat for more people, we have
inadvertently created conditions by which a harmless parasite of wild ducks
can be converted into a lethal killer of humans.
Should Americans be concerned about this threat? Bird flu has existed
for many years in the United States and Canada; in fact, at the same time the
H5N1 bird flu epidemic was spreading throughout Southeast Asia, H7 strains
of influenza not thought to be pathogenic for humans were infecting chick-
ens in Delaware, Pennsylvania, Texas, and British Columbia.47 A few poultry
workers were infected with the H7 strains, causing mild avian influenza; of
greater concern was the diagnosis of H7 avian influenza in a man near New
York City who had had no known contact with poultry.48
In addition to bird flu’s presence in the United States, we have created
conditions that may promote the spread of microbes among birds. Poultry
farms house as many as eighty thousand chickens, and live-poultry markets
can be found in all large cities. According to one expert: “In New York the
number of live-poultry markets nearly doubled from 44 in 1994 to over 80 in
2002.” 49
We also import many birds into the United States. By one account: “Peo-
ple who have seen the animal holding facilities at London-Heathrow, New
York-Kennedy, and Amsterdam-Schiphol [airports] describe warehouses in
which every type of bird and other exotic animal are kept cheek by jowl in
conditions resembling those in Guangdong [China] food markets, awaiting
trans-shipment. There, poultry can come into close contact with wild-caught
birds.” 50 For an influenza virus or other microbe that wants to get ahead in life
and expand its territory, such conditions are ideal.
10 =
C H A P T E R
The Coming Plagues

Lessons from AIDS, West Nile Virus,
and Lyme Disease
It is therefore as an animal that we must first consider man in his struggles
with the environment. For man evolved as an animal, even while he was
dreaming of God and the stars.
Rene Dubos, Mirage of Health, 1959
I n 1969, the bar of human hubris was raised significantly when William H.
Stewart, surgeon general of the United States, announced: “The war against
infectious diseases has been won.” 1 Considering that bacteria, viruses, and
protozoa had a more than two-billion-year head start in this war, a victory by
recently arrived Homo sapiens would be remarkable. In fact, the war against
infectious diseases has just begun and is guaranteed to continue for as long as
humans inhabit the planet.
Previews of possible future skirmishes against animal microbes occur
every day in hundreds of places around the world. We remain unaware of
most of these, but a few come to our attention. For example, animal disease
outbreaks that occurred in a random two-month period, May and June 2003,
and that were reported by ProMED-mail, an Internet service that monitors
emerging infectious diseases, included the following:
• A “mystery venereal disease” was affecting baboons in Tanzania,
destroying their reproductive organs and causing them to die “in
excruciating pain.”
• Akabane virus, spread by flying insects, was affecting pregnant cows in
Australia, producing “horribly deformed calves which rarely survive.”
124 =
The Coming Plagues = 125
• Large numbers of monkeys were dying from Kyasanur Forest Disease

virus in India, with the outbreak labeled “the most serious in years.”
• A case of malignant catarrhal fever, caused by a herpesvirus, was
reported among cows, sheep, and pigs in Finland, with an “extremely
high mortality” rate.
• The cause of a “mysterious trout disease” in India, identified as an
iridovirus, was said to be killing “thousands of trout fish” by causing
them to bleed to death.
• An outbreak of gastroenteritis caused by a coronavirus was reported
among young pigs in Cuba, with a 43 percent mortality rate.
• An outbreak of bluetongue virus disease was reported among sheep
and goats in Brazil.
• A previously unknown disease, probably viral in origin, was spreading
among caged parakeets in England and was said to have “a very high
death rate.”
• African swine fever was reported from the Congo Democratic Repub-
lic with “a high mortality rate” among the infected pigs.
• A “highly pathogenic” avian influenza (bird flu) epidemic was being
brought under control in the Netherlands, Belgium, and Germany
by killing 1.5 million chickens, ducks, and other birds in the affected
areas.2
Fortunately, most animal disease outbreaks, like those just cited, are
caused by microbes that are species specific and therefore do not affect hu-
mans. Occasionally, however, when conditions are propitious, animal mi-
crobes do cross from one animal species to another. When the new species
happens to be humans, the result can be disastrous.
The conditions under which animal microbes are most likely to cross to
the human species include changes in human behavior, changes in technol-
ogy, and changes in ecology.
Human Behavior and AIDS

The microbes that cause human AIDS are primate retroviruses that have ex-
isted in African monkeys for millions of years, causing little or no illness in
most of them. HIV-2, which causes the milder form of AIDS, is a slight modi-
fication of a simian immunodeficiency virus (SIV) carried by sooty mangabey
monkeys in West Africa. HIV-1, the more severe form, is a combination of SIV
strains carried by two species of monkeys in central Africa. The two strains
simultaneously infected a chimpanzee species, Pan troglodytes troglodytes and
combined into a new strain of SIV, which was then transmitted to humans.3
Evidence that supports primates as the source of human HIV is strong. At

a molecular level, HIV-1 and HIV-2 are very similar to the viruses carried by
the primates. Furthermore, there is an impressive geographic overlap in Cen-
tral and West Africa where these primates live and where AIDS cases were first
seen. Other retroviruses have also been transmitted from primates to humans.
For example, simian foamy viruses have been transmitted to humans from
chimpanzees, baboons, green monkeys, and macaques.4 The primate T-cell
lymphotropic virus (PTLV-1), another primate retrovirus, was also transmit-
ted from primates to humans; the descendants of these viruses, HTLV-1 and
HTLV-2, are important causes of neurological diseases in modern humans.5
Such cross-species transmission should not surprise us, since primates in gen-
eral, and chimpanzees in particular, are genetically closely related to humans.
As Jared Diamond noted, “the chimpanzees’ closest relative is not the gorilla
but humans.” 6
Humans in Africa have presumably hunted monkeys and chimpanzees as
sources of “bushmeat” for thousands of years. The transmission of SIV from
primates to humans could have taken place by a monkey bite, by the virus
entering an open sore on human hands that were butchering the animals, or
by humans eating undercooked or uncooked primate meat. Such primate-
to-human transmission could have taken place multiple times over the years,
and, in fact, there is evidence that at least eight independent transmissions
did occur.7
If transmission of the primate virus to humans took place multiple times
in the past, why did AIDS become an epidemic only in the latter years of
the twentieth century? The answer to this question is not completely clear
but involves several factors, the most important of which are changes in hu-
man behavior. AIDS is fundamentally a blood-borne and sexually transmitted
disease. Like other sexually transmitted diseases, its pattern of transmission
changes as human sexual practices change.
In the 1960s, colonial rule was ending in Africa and there was an out-
break of civil wars. Increased urbanization was followed by social breakdown
and widespread prostitution. The African social breakdown was mirrored in
developed nations by a sexual revolution in general and a gay revolution in
particular, as well as by increased IV drug use and needle sharing. Indeed, if
one set out to create the social circumstances most favorable for spreading a
sexually transmitted microbe from Africa to the rest of the world, the circum-
stances in the latter years of the twentieth century would provide a perfect
model.
The AIDS epidemic that has resulted from the transmission of primate
viruses to humans has been compared to the Black Plague and other great epi-
demics in history. Since 1980, throughout the world, more than twenty million
people have died. Forty million more are already HIV infected; of these, three
million were predicted to die in 2003 and the remainder within the next de-
cade. According to a 2002 report, “each day, 14,000 people—12,000 adults and
2,000 children—become infected with HIV; . . . there will be 45 million new
HIV infections by 2010.” Sub-Saharan Africa has been most severely affected:
In Botswana, 39 percent of the country’s adults are infected, and in some sub-
Saharan countries, “15 percent or more” of children have been orphaned as
AIDS has killed their parents.8 In the United States, “40,907 new AIDS cases
were diagnosed in 1999 and an estimated 41,113 in 2000”; as of mid-2004, an
estimated 900,000 Americans were infected with HIV.9
The AIDS epidemic, then, illustrates that the transmission of an ani-
mal microbe to humans is merely the first step in an epidemic. Many factors
played a role in the spread of the disease, including intravenous drug use, its
rapid distribution by air travel, and mutations of the virus, but the primary
factors that allowed AIDS to become a worldwide epidemic were changes in
sexual practices, both locally and internationally.
Technological Changes and West Nile Virus

In August 1999, a physician in Queens, New York, reported to health au-
thorities two cases of individuals with unusual encephalitis-like neurologic
symptoms. Within the next week, six more cases had been identified. After
interviews of the affected individuals, “the only thing that linked the patients
in time and place was that they all had spent time outdoors in their backyards
or neighborhoods, especially in the evening hours.” 10 This suggested an infec-
tious disease, probably carried by mosquitoes.
The cause of the encephalitis outbreak was ascertained to be the West
Nile virus, which had never been seen in the United States. This virus had
first been described in Uganda in 1937, near the western branch of the origin
of the Nile River. It had caused human encephalitis in Africa, Asia, the Middle
East, and Europe but not previously in North America. In recent years, it had
caused severe epidemics in Russia, Romania, and Israel. The virus isolated
in New York was, in fact, found to be virtually identical to one that had been
isolated from the epidemic in Israel.11
The West Nile virus is essentially a disease of birds, with mosquitoes used
as vectors, and humans as accidental hosts. In two-thirds of humans, it causes
no symptoms, but in the other third, it causes fever and occasionally inflam-
mation of the brain (encephalitis). Approximately 7 percent of affected in-
dividuals die. Once the virus infects humans, it may also be spread to other
humans by blood transfusions.
Although West Nile virus normally spreads by mosquitoes and migrat-

ing birds, in 1999 it apparently used an airplane. At least a thousand people
travel by air from Israel to New York every day, and it thus seems likely that
the virus was brought on a flight to New York either by an infected person or
by mosquitoes.12
Once in the United States, the virus spread rapidly. In 2001, 66 human
cases were recorded in ten states; by 2002, there were 4,161 cases in thirty-
seven states, including 284 deaths.13 An infected dead crow was even found on
the grounds of the White House, a reminder that nobody is immune.14 How
much of the rapid spread of West Nile virus is attributable to migrating birds
and how much to human-incubating cases carried by airplanes is unclear.
The importance of air travel in disseminating animal microbes is also
illustrated by the spread of SARS. On February 21, 2003, a man with SARS
stayed overnight at a hotel in Hong Kong, infecting at least seventeen other
hotel guests and visitors. Some of the guests, as they were developing SARS,
then flew to Hanoi, Singapore, and Toronto, spreading SARS to individuals
in those three cities. Still others who had been at the hotel developed SARS
and were hospitalized in Hong Kong. A man who visited his sick brother in
the Hong Kong hospital then boarded a flight for Beijing and on the flight
infected twenty-two other individuals, five of whom died. Retrospective analy-
sis of the seating of passengers on the Beijing flight showed that those sitting
immediately in front of, or to the side of, the infected passenger were the most
likely to have become infected, presumably through the dissemination of viral
particles when the man coughed.15
The availability of international air travel has markedly increased the
speed at which microbes can spread. Until the middle of the twentieth cen-
tury, human travel was slower; travelers often developed whatever diseases
they might be carrying before they reached their destinations. By contrast, in
2002, there were 532 million passengers on international flights worldwide,
including many individuals who took multiple flights.16 Increasingly, these
flights include exotic destinations, so that travelers from Chicago or Copenha-
gen often return from their exotic vacations carrying exotic microbes.
In addition to human travel, “increasingly, companion animals are accom-
panying their owners on long-distance travel.” This has been facilitated by the
recent introduction of a “pet passport scheme” and a loosening of pet-quaran-
tine regulations in many countries.17 In England, for example, the number of
dogs and cats entering the country more than tripled between 2000 and 2003,
from 15,871 to 54,572. Not surprisingly, the School of Tropical Medicine in
Liverpool reported that cases of “animal diseases picked up on holiday” dou-
bled between 2002 and 2004.18 Now, not only can humans quickly transport
exotic microbes home, but Fido and Fluffy can do so as well.
Air travel is merely one form of modern technology that promotes the
spread of microbes, including microbes that have been transmitted from ani-
mals to humans. Another technological advance is the widespread availability
of syringes. Glass syringes were invented in 1848 but were little used until
insulin was introduced in the 1930s. With the availability of penicillin and
the invention of inexpensive plastic syringes after World War II, injections
became widely used throughout the world. In developed countries, dispos-
able plastic syringes are normally used once and discarded. In developing
countries, however, it is common practice to use disposable syringes multiple
times without sterilization. Studies have shown that in many countries at least
50 percent of all injections are given with multiple-use, unsterile syringes;
in some countries, the figures is as high as 90 percent.19 It is widely believed
by lay persons that injections are more efficacious than medicine given by
mouth; injections are therefore big business, and in developing nations they
are frequently given by untrained “injection doctors,” “needlemen,” and a
variety of traditional healers.20
The widespread use of injections, which can transmit blood-borne mi-
crobes from person to person, is a new phenomenon. Since hominids evolved
six million years ago, the only routes open for most microbes to breach human
defenses have been through the mouth, intestine, respiratory system, geni-
tal tract, and open wounds. Injecting microbes directly into the muscles and
bloodstream of humans is analogous to opening the gates of a city under siege.
The World Health Organization estimates that, worldwide, twelve billion sy-
ringes are sold each year for injections, sufficient for two injections for every
man, woman, and child if each syringe is used only once. Studies have esti-
mated that in some countries in Southeast Asia and the eastern Mediterranean
regions, where syringes are often used multiple times, each man, woman, and
child receives an average of three unsterile injections each year.21 The use of
unsterile syringes is thought to have played a role in spreading the AIDS virus,
as well as hepatitis B and C, malaria, Ebola virus, and Lassa fever.22
Another technological advance that threatens to increase the transmis-
sion of animal microbes to humans is xenotransplantation, the transplanting
of animal organs into humans. The procedure was first carried out in 1910,
when a monkey kidney was transplanted into a young girl suffering from renal
failure. In 1963, kidneys from chimpanzees were put into six patients with
renal failure, but the longest any patient lived was nine months.23 Since that
time, primates have been largely ruled out as sources for human organs, both
because of ethical concerns and because of the danger of transmitting primate
microbes to humans.24
In recent years, there has been increasing interest in transplanting pig
organs and tissues to humans. Experiments are underway using pig hearts
for patients with heart failure, pig nerve cells for patients with Huntington’s
disease or Parkinson’s disease, and pig pancreatic cells for patients with diabe-
tes. Commercial interest is strong, with projections that xenotransplants could
become a $6 billion market by 2010.25
The need for a supply of human organs is acute. At any given time, more
than fifty thousand individuals are on organ waiting lists, and most will die be-
fore human organs become available. In addition to their limited availability,
transplanted human organs can transmit microbes such as hepatitis C and cyto-
megalovirus. The limited availability and danger of using human organs for
transplantation must be weighed against the dangers of using animals’ organs.
Pigs, like all animals, carry a variety of infectious agents, including a hepatitis
virus, at least three herpesviruses, a paramyxovirus, a torovirus, and a circovi-
rus, although to date the evidence for transmission of these viruses to humans
is scant.26 Of greatest concern is an endogenous retrovirus carried by pigs that
is integrated into the genome and can infect human cells.27 Many of these
viruses cause no problems in pigs but could be pathogenic if transplanted into
humans. If xenotransplantation becomes widespread, therefore, it will provide
a new route for microbes to move from animals to humans.
Bioterrorism will also be affected by technology and thereby increase hu-
man exposure to animal microbes. These include microbes such as small-
pox, anthrax, brucellosis, Q fever, tularemia, and glanders, which have been
known for thousands of years, as well as microbes that have apparently moved
from animals to humans more recently, such as Ebola virus and Lassa virus.28
Technologically sophisticated bioterrorists are likely to discover new methods
for unleashing these microbes. Even more worrisome are potential uses of
the growing field of synthetic biology to modify existing microbes so that,
for example, they could be used to neutralize the human body’s existing de-
fenses or negate the effect of anti-infective medications.29 With bioterrorism
come wars, which promote the spread of microbes through unsanitary living
conditions and malnutrition. As Hans Zinsser noted: “Soldiers have rarely
won wars. They more often mop up after the barrage of epidemics. . . . The
epidemics get the blame for defeat, the generals get the credit for victory. It
ought to be the other way around.” 30
Ecological Changes and Lyme Disease

In October 1999, the Institute of Medicine held a workshop on emerging in-
fectious diseases. Ecological changes, including urbanization, global warm-
ing, and changes in forestation, were among the more prominent factors cited
as contributing to the spread of microbes.31
It is not generally appreciated that big cities are a relatively recent phe-
nomenon. For the first eight thousand years after humans settled into villages,
the population of the largest settlements rarely exceeded 20,000 inhabitants.
By 1000 b.c.e., only four cities in the world had populations of 50,000 or
more. In the fourteenth century, Paris, with 100,000 people, was the largest
city in Europe, and as late as 1840, New York was the largest city in the United
States, with 250,000 inhabitants.
Megacities, with populations of ten million or more, are new. New York in
1950 was the first to surpass that mark, but by 2000, fourteen other cities in the
world had joined it. In 2015, there are projected to be twenty-one megacities,
five of which (Bombay, Delhi, Dhaka, Tokyo, and Sao Paulo) are expected to
have populations of more than twenty million.32 Such population concentra-
tions are likely to create novel patterns of infectious disease transmission and
also lead to the emergence of new microbes that require huge populations for
their natural reservoirs. Urbanization also promotes the spread of microbes
through contaminated water supplies, poor sewage systems, trash heaps that
attract rodents, and crowded living conditions. As noted in 1998 by one expert
on emerging infections: “The mega cities of the tropics, with their lack of
sanitary systems, serve as incubators for emerging zoonoses—they represent
the most difficult zoonotic diseases risks of the next century.” 33
Global warming has been widely discussed as a phenomenon likely to in-
crease the distribution of infectious diseases. It is projected, for example, that
global warming could lead to the reemergence in such cities as New York,
Rome, and Tokyo of the protozoa and viruses that cause malaria, yellow fever,
and dengue.34 Other infectious diseases whose spread would be favored by a rise
in temperature include viral encephalitis, schistosomiasis, and leishmaniasis.35
Deforestation, reforestation, irrigation, dam building, and alterations in
agriculture can also bring about ecological change. All have been known to
produce changes in the transmission of microbes. Argentine hemorrhagic fe-
ver, for example, increased sharply among humans in South America follow-
ing the conversion of grasslands to maize cultivation, a change that favored
the rodent, the natural reservoir for the virus that causes this disease.36
The best example in the United States of a rise in a human disease
brought about by ecological change that affects an animal microbe is Lyme
disease. The disease is caused by a spirochetal bacteria, Borrelia burgdoferi,
that is transmitted to humans by ticks. Ticks have a complex life cycle, taking
two years to mature and then attaching themselves to mammals such as deer,
which have become the main natural reservoir for Lyme disease.
Deer were plentiful in the eastern United States when Europeans first
colonized it. As forests were turned into fields and deer were killed for their
meat, deer became rare. In 1854, for example, when Henry David Thoreau
wrote Walden, he said that deer had not been seen in his part of Massachusetts
for eighty years.37
After the Civil War, many New Englanders moved westward to more fer-
tile land, allowing their fields to return to woodland. By 1980, northeastern
states had four times more forested area than they had in 1860, and this trend
has continued as more farms have been abandoned. In contrast to the forests
of the early nineteenth century, however, the reforested areas have almost no
cougars, wolves, bears, or other predators that previously kept the deer popula-
tion in check.
In the early twentieth century, deer returned to the reforested areas, now
devoid of natural predators. They multiplied steadily until, in the last two
decades, their population exploded. There are now thought to be at least
as many deer in the United States as there were when the colonists arrived,
but the deer are concentrated in smaller, often suburban, areas. As one study
concluded, deer “are now as commonly noted as squirrels in some suburban
communities.” 38
One measure of deer population is how often they are hit by vehicles.
According to a recent U.S. survey, deer “are struck by cars, trucks, and motor-
cycles more than a million times a year, with the accidents killing more than
100 people annually. . . . The human toll makes deer deadlier than sharks,
alligators, bears, and rattlesnakes combined.” In Connecticut, between 1995
and 2000, “the number of drivers who reported hitting a deer rose 297 per-
cent.” In addition, according to the Federal Aviation Administration, at air-
ports “deer have been struck by more than 500 aircraft over the last decade,
including fighter jets and Boeing 737’s.” 39
While deer were moving into suburban woodlands, people were moving
out of cities and building houses next to the woodlands. The homeowners
proceeded to plant their lawns with flowers, vegetables, and shrubs that deer
like to eat. The suburbanites brought along their dogs and cats, which can also
be affected by Lyme disease and can bring ticks from the adjoining woods into
the house, thus making it easier for them to infect humans.
The current epidemic of Lyme disease in the United States is a natural
and predictable consequence of the exploding deer population. Since the
initial 1977 outbreak in Lyme, Connecticut, the incidence of the disease has
risen sharply. In the decade between 1991 and 2000, the number of newly af-
fected individuals doubled to almost eighteen thousand per year, even as cases
continued to be underreported.40 In 2002, reported cases of Lyme disease
increased to 23,763 and are apparently continuing to increase. Children are
most commonly affected, but individuals of all ages are vulnerable. The initial
signs, flulike symptoms and a rash, if untreated, may be followed by arthritis
and complications of the central nervous system or heart, including meningi-
tis, encephalitis, paralysis of the facial nerves, psychiatric symptoms, or heart-
rhythm abnormalities.41 Untreated, Lyme disease may become a chronic and

disabling illness that continues for many years.
The Great Unknown

The greatest danger in the transmission of microbes from animals to humans is
not what we know but what we don’t know. As noted in chapter 1, researchers
compiled a list of 1,415 microbes known to cause diseases in humans.42 One
can compare that number to the estimated three hundred thousand to one
million different species of bacteria and the five thousand species of viruses
thought to exist, the vast majority of which have not yet been identified.
We should also remember that humans are merely one of 4,500 species
of mammals and that almost all research on microbes has been done on those
that are presently thought to affect humans. Except for laboratory rodents,
which have been studied for research purposes, we know almost nothing
about microbes that infect other mammals, to say nothing of microbes that
infect birds, reptiles, amphibians, fish, or simpler forms of life. In short, we are
aware of only a tiny fraction of microbes that may cause disease in humans; we
should therefore be very modest about our ability to predict the microbial ef-
fects of any changes in the relationship between humans and other animals.
As molecular studies proceed, it is inevitable that additional human dis-
eases will be identified as caused by animal microbes. Of particular interest
is the role of microbes in chronic human diseases, since the identification of
these relationships requires the application of sophisticated molecular tech-
niques that are just starting to be applied to the study of chronic diseases.
What, for example, is the relationship between Chlamydia pneumonia and
human coronary disease? This microbe has been found in coronary artery
plaques in many people with this disease.43 The human strain of Chlamydia
pneumonia appears to be closely related to the strain found in horses, which
could conceivably have been the origin of this pathogen before it became
adapted to human-to-human transmission.44
The possible relationship of human cancers to animal cancers is another
area that is mostly unknown. Cancer is a leading cause of death in dogs; can-
cer of the breast, testes, and bone are especially common.45 Cats are especially
affected by leukemias and lymphomas. Experimental work has shown that
some human microbes may cause cancer when injected into animals.46 And
some human cancers, such as cancer of the stomach, liver, and cervix, have
been linked to microbes such as Helicobacter pylori, hepatitis B virus, and hu-
man papilloma viruses, respectively. Whether or not any human cancers will
ultimately be associated with exposure to animals remains to be determined,
but anecdotal accounts of humans and their pets being diagnosed with similar
cancers are intriguing.47
What Can Be Done?

Viewed in historical perspective, human health has improved significantly in
recent centuries. The world’s population has increased from 2 billion in 1875
to 6.3 billion today. Those with access to modern medicine and antibiotics
have a quality of life much better than that of their forebears.
At the same time, as noted by infectious disease specialists, the “emergence
of new zoonotic pathogens seems to be increasing.” 48 The recent emergence
of AIDS, SARS, monkeypox, West Nile virus, bird flu, and other infections, all
caused by microbes transmitted from animals to humans, should be regarded
as a wake-up call. In 2003, the Institute of Medicine published a report from
its Committee on Emerging Microbial Threats to Health in the Twenty-first
Century. The tone of the report was sober and subdued: “As the work of this
Committee draws to an end, none of its members are sanguine about what
the future may hold with respect to microbial threats to health. . . . Today’s
outlook with regard to microbial threats is bleak on a number of fronts. . . .
Microbial threats present us with new surprises every year.49
The most urgent task, according to the report, is “to strengthen global
infectious disease surveillance . . . to recognize previously unknown illnesses
or unusual outbreaks of disease that may have global significance.” 50 Cur-
rently, one effective network set up to accomplish this task is the Program for
Monitoring Emerging Diseases, or ProMED, an Internet reporting system
administered by the International Society for Infectious Diseases using foun-
dation funding. Similarly, the World Health Organization (WHO) launched
the Global Outbreak Alert and Response Network in 2000 but, like many
WHO endeavors, it has been slow to reach its potential because of the politics
of that organization.
A fundamental problem at both international and national levels is a lack
of coordination between agencies that have responsibility for animal health
and agencies that have responsibility for human health. Internationally, the
World Organization for Animal Health (Office International des Epizooties,
OIE), based in Paris, has responsibility for animal diseases, whereas the World
Health Organization, based in Geneva, has responsibility for human diseases.
Coordination between these two separate agencies has traditionally been very
poor. Influenza for example, is a disease of great importance for both poultry
and humans. According to the 2003 Institute of Medicine report, OIE is in-
terested in “only certain influenza virus types that are highly pathogenic for
poultry, . . . those viruses that are found to be rather nonpathogenic in poultry,

but for which a potential threat to humans exists, are ignored.” 51
At the national level, cooperation between agencies responsible for ani-
mal and human health has been equally deficient. In the United States, for
example, the Department of Defense (DOD) operates infectious disease
research laboratories in five countries (Egypt, Indonesia, Kenya, Peru, and
Thailand). DOD also collects infectious disease information at the Armed
Forces Intelligence Center and through an Electronic Surveillance System
for Early Notification of Community-Based Epidemics (ESSENCE) at mili-
tary facilities worldwide. The Centers for Disease Control and Prevention
(CDC) collects data from states on notifiable infectious diseases and pub-
lishes them weekly in Morbidity and Mortality Weekly Reports. These data
include, however, only selected and recognized diseases. In response to the
threats of bioterrorism, CDC recently also launched a National Electronic
Disease Surveillance System (NEDSS) and a Web-based communications
network for public health officials (Epi-X).
Yet information on animal diseases in the United States is not the re-
sponsibility of either DOD or CDC, but of the Animal and Plant Health In-
spection Service (APHIS) of the Department of Agriculture. APHIS employs
more than three hundred U.S. and host-country nationals in twenty-seven
countries, with the primary mission of protecting U.S. animal and plant re-
sources from agricultural pests and diseases, such as foot-and-mouth disease;
thus, its focus is on protecting animals and plants, not people. APHIS also
operates a laboratory at Plum Island, off the coast of Long Island, which is the
major U.S. facility for research on animal microbes from foreign countries.
These various government agencies are poorly coordinated, despite some
of them, like CDC, individually doing excellent work. In 1992, the Institute of
Medicine, in its report Emerging Infections, noted that “there is little coordi-
nation among these [federal] agencies and organizations regarding infectious
diseases surveillance.” 52 Ten years later, another Institute of Medicine report
described “evidence of new turf tensions” between the federal agencies: “The
risk that this will get worse affects zoonotic disease episodes in particular,
where laboratory and field activities resemble research projects and many dif-
ferent specialists must be involved. In several recent zoonotic episodes, how-
ever, scientists became competitive and insular, seeming to worry more about
their publications than about the public’s health.” 53
Federal agencies with responsibility for different aspects of West Nile vi-
rus, for example, are these:
• Centers for Disease Control and Prevention (CDC): Reporting and

investigation of human cases
• Food and Drug Administration (FDA): Protection of blood supply

against contamination by the virus
• National Institutes of Health (NIH): Research on the virus
• Department of Defense (DOD): Research on the virus
• Department of Agriculture: Surveillance and reporting of the effect
of the virus on poultry and livestock
• Department of the Interior: Assistance to states with diagnosis of the
virus among birds and other wildlife
• Department of Commerce: Research on mosquito populations; plans
for controlling mosquitoes
• Environmental Protection Agency: Research on pesticides used in
prevention efforts54
The lack of federal agency coordination is especially evident for microbes

that are transmitted from animals to humans, such as West Nile virus, SARS,
BSE, and monkeypox. In mid-2004, several members of Congress publicly
urged Tommy Thompson, secretary of the Department of Health and Hu-
man Services, to create a task force to coordinate research on diseases such as
BSE.55 Until this lack is remedied, Americans will remain unnecessarily vul-
nerable to animal-transmitted diseases. One of the major recommendations of
the 2003 Institute of Medicine report, in fact, was that “the overseas diseases
surveillance activities of the relevant U.S. agencies . . . should be coordinated
by a single federal agency, such as CDC.” 56
A basic cause of this lack of coordination of disease information is a gulf
that has long existed between veterinarians, the specialists in animal diseases,
and infectious disease physicians, the specialists in human diseases. The two
groups have trained in different schools and have worked in different profes-
sional worlds for more than a century. Although it has become increasingly
clear that most emerging human infectious diseases originate in animals, little
effort has been made to bridge this gulf. The lack of coordination between
animal- and human-disease specialists was highlighted again during the re-
cent bird-flu epidemic. “Medical and veterinary schools need to cooperate
more,” noted Frederick Murphy, an expert on zoonoses.57 A model for such
coordination exists in Denmark, which has developed “a zoonosis center as
an element of its national public health institution, . . . uniting veterinary and
human health professionals.” 58
Another aspect of disease surveillance that needs improvement is the au-
topsy rate. In 1964, 41 percent of all persons who died in U.S. hospitals un-
derwent autopsy, which is useful to pinpoint the cause of death and to detect
new diseases as they emerge. Since 1964, the autopsy rate in U.S. hospitals
has fallen progressively; it is now only 5 percent.59 By not doing more autop-
sies, especially ones that use sophisticated molecular techniques to identify
microbes, we are missing one of our best opportunities to detect emerging

microbes and diseases that may be transmitted from animals to humans.
Coordinating veterinary and medical personnel in a single center would
also be very useful for advancing research on microbes being transmitted from
animals to humans. The CDC, the Department of Defense, and the National
Institute of Allergy and Infectious Disease (NIAID) under NIH are all carry-
ing out important research on infectious diseases, but research on animal
diseases is the responsibility of the Department of Agriculture. Given what is
now known about the importance of zoonoses, it is illogical to have research
on bird flu in poultry carried out by one government agency and research on
bird flu in humans carried out by another.
For reducing exposure to animal microbes at an individual level, each
of us must decide how much and what kind of contact we want to have with
pet animals, and parents must make this decision for their children. It is pos-
sible to keep a pet and minimize exposure to animal-transmitted microbes by
choosing a nonexotic pet and by following commonsense principles, the most
important of which are related to hand washing after pet contact, observing
other aspects of personal hygiene, and ensuring that pet immunizations are
up to date. Individuals may wish to keep exotic animals as pets, but this falls
into the category of high-risk behavior, along with motorcycle riding and sky-
diving, and the risk to other family members must also be taken into consider-
ation. Another important principle for minimizing one’s exposure to animal
microbes is to cook eggs, meat, and other food to recommended temperatures
to reduce transmission opportunities for food-borne microbes.
It is clear, however, that regulations need to be revisited for the importa-
tion of exotic animals. Currently, dogs imported into the United States must
have been vaccinated against rabies at least thirty days before importation,
and dogs and cats must undergo quarantine in some states. For exotic ani-
mals, however, there are few restrictions. The Department of Agriculture
Web site states explicitly: “We do not have any regulations or restrictions on
the importation of fish, reptiles, lions, tigers, bears, foxes, monkeys, endan-
gered species, guinea pigs, hamsters, gerbils, mice, rats, chinchillas, squirrels,
mongoose, chipmunks, ferrets, or other rodents provided they have not been
inoculated with any pathogens for scientific purposes.” 60 It is not just a ques-
tion of whether these animals have been inoculated with pathogens; it is also
a question of what pathogens they are already carrying.
Perhaps the most important activity for minimizing the transmission of
microbes from animals to humans is education. Most people are unaware of
the potential of animals to cause human disease. In one study, for example,
only two out of thirty-two dog owners “expressed awareness that diseases other
than rabies could be transmitted from pet dogs to human beings.” 61 Another
survey regarding “pet-associated health risks” reported that “pediatricians’

knowledge was incomplete, parents’ knowledge even more so, and anticipa-
tory guidance about pets notably lacking.” Still another survey found that
“most physicians felt uncomfortable advising patients about the health risks of
animal contact and indicated that veterinarians should play a greater role.” 62
Owners of pet stores also have a responsibility to educate customers. One
study examined the role of pet-store managers in advising individuals who buy
animals regarding their possible disease transmission to humans. It was found
that “only 23 percent of owners/managers of pet shops advised customers of
the potential zoonotic risks from puppies.” Giving medicine to puppies to kill
the dog’s intestinal worms is widely recommended as standard procedure, but
in this survey, “four petshops advised customers to worm themselves and/or
their children as preventive measures for parasitic infection of their dogs.” 63
In summary, the relationship between humans and other animals is marked

by contradictions. Domesticated animals have provided us with food, cloth-
ing, and other essentials, making our civilization possible. At the same time,
animals have transmitted to humans microbes that have caused, and are caus-
ing, many of our worst diseases. At a personal level, we regard ourselves as
far superior to other members of Phylum Craniata, Subphyulum Vertebrata,
Class Mammalia—the beasts of the earth—and yet we treat these other ani-
mals, when they are our pets, as if they are one of us.
It seems certain that we will experience additional epidemics of human
diseases that will be transmitted to us from animals. Popular representations
of such epidemics depict them as arising in the jungles of Africa or the rain-
forests of South America. Ebola, Lassa, Marburg, Machupo—these are the
dreaded and deadly “andromeda strains” that Hollywood portrays and about
which we worry. In fact, the coming human plagues are equally likely to come
from an exotic pet kinkajou in New York, a pet prairie dog in Chicago, or even
a child’s kitten in Los Angeles. It is not a question of whether we will experi-
ence such plagues, but rather a question of when and how often.
11 =
C H A P T E R
A Four-Footed View of History

That men do not learn very much from the lessons of history is the most
important of all the lessons that history has to teach.
Aldous Huxley
H omo sapiens has had a peculiar history. For almost a million years, we
wandered the world as hunters, living in small groups but creating no
permanent civilizations. Then, approximately ten thousand years ago, we do-
mesticated plants and animals; in the following eight thousand years, we cre-
ated city-states, monuments, centralized governments, art, architecture, litera-
ture, and philosophy. Thus, during less than 1 percent of our time as a species,
we went from being peripatetic nomads to the likes of Aristotle and Cicero.
The remains of these early civilizations—the pyramids of Egypt, sculp-
tures of Greece, and temples of Rome—are indeed impressive. The Harrapan
cities in the Indus Valley five thousand years ago had elaborate sewage systems
that one can still see in ruins such as Mohenjo Daro. Roman cities more than
two thousand years ago had aqueducts to bring water, public baths that ac-
commodated hundreds of people, and public lavatories “fitted with marble
urinals, . . . a small charge being made for admission.” The first public lava-
tories in London did not open until 1851. It has been said that “in its cleanli-
ness, sanitation and water supply, Rome was much more akin to twentieth-
century London and New York than to medieval Paris or eighteenth-century
Vienna.” 1
Domesticated animals played a large role in these evolving civilizations.
For example, at Tell Leilan, which increased in size sixfold between 2600 and
2400 b.c.e. as a political center for northern Mesopotamia, the inhabitants
kept pigs, sheep, goats, and cattle, and used horses and mules for transporta-
tion.2 The shards, paintings, friezes, and other relics of these early civilizations
clearly illustrate the importance of domesticated animals—Sumerian sheep
and pigs, Persian horses and water buffalo, Chinese ducks and geese, Egyptian
cattle and cats, Minoan bulls and goats, Roman hunting dogs and chickens.
= 139
It seems reasonable to conclude that without domesticated animals to provide

meat, clothing, and transportation and to guard the sheep and grain, these
early civilizations would not have evolved.
Equally as impressive as the rise of these civilizations was their fall. In
Mesopotamia in approximately 2200 b.c.e., there occurred a “sudden col-
lapse of the Akkadian empire.” Excavations at Tell Leilan have shown that it
was “suddenly abandoned” and that “similar abandonments are evident at al-
most all excavated sites of this period across the Habur and Assyrian Plains.” 3
Most of the ancient civilizations did not decline as precipitously as the Ak-
kadian Empire did, but a pattern of decline can be traced in all of them:
Civilizations grew and flourished for hundreds of years, then withered for a
period and eventually died.
Historians have speculated exhaustively on reasons why ancient civiliza-
tions fell. Drought and other climatic changes are certainly part of the answer.
This has been cited as the main reason for the sudden demise of the Akkadian
Empire,4 and similar climatic changes affected Egypt, the Indus River Valley,
and the Aegean area at this time. Civil unrest and wars, famine, and natural
disasters such as floods, earthquakes, volcanic eruptions, and infestations of
locusts also played a role and often occurred in combination.
Perhaps the most important reason for the decline of ancient civiliza-
tions, however, was the spread of infectious diseases, most of which were
caused by microbes that had spread to humans from domesticated animals.
Measles, smallpox, tuberculosis, bubonic plague, typhus, dysentery, dengue,
diphtheria, influenza, yellow fever, malaria, pertussis, polio, cholera, schis-
tosomiasis, and leprosy probably all existed as human diseases by the sixth
century c.e., when the last of the ancient civilizations, the Roman Empire,
finally expired.
Fragmentary evidence supports the important role played by infectious
diseases. For example, in 480 b.c.e., when Xerxes attempted to expand his
Persian Empire by invading Greece, dysentery struck his army, reducing it
by more than a third. As R. S. Bray notes in Armies of Pestilence, dysentery
was “the final nail in the coffin of the Persian pretensions in Greece and the
Mediterranean world. . . . It might be claimed with justification that Greek
and European culture owe their continued existence to Greek arms and dys-
entery.” The defeat threw the Persian Empire “into a state of languid torpor,
from which it could not rise again.” 5
Fifty years later, in 430 b.c.e., Athenian civilization was at its zenith and
also at war with Sparta. A severe disease, never definitively identified, struck
Athens and its fleet, killing at least one-third of the population, including
Pericles and many other political and military leaders. As described by Thucy-
dides, those afflicted suffered from coughing, vomiting, diarrhea, and terrible
A Fo u r - Fo o t e d Vi e w o f H i s t o r y = 141
skin sores. “Unable to bear the touch of clothes or bedding, they staggered
naked through the streets. . . . They died in streets, in temples, in wells into
which they had fallen.” Thucydides, who himself was afflicted, noted: “Words
indeed fail when one tries to give a general picture of this disease; and as for
the suffering of individuals, they seemed almost beyond the capacity of hu-
man nature to endure.” 6
The Athenian epidemic was followed by widespread tuberculosis, de-
scribed by Hippocrates in 400 b.c.e. The diseases led to the eventual defeat
of Athens and its demise as a major power. According to Arno Karlen’s Man
and Microbes, “Athens would never fully regain its political and cultural glory.
More than 2,000 years later the West’s finest minds would still dream of recre-
ating the golden age that the plague had helped destroy.” 7
Egypt also suffered from epidemic diseases that contributed to its down-
fall. Evidence from Egyptian mummies suggest that smallpox, tuberculosis,
malaria, schistosomiasis, and polio all occurred.8 Old Testament stories de-
scribe a “very severe plague” of Egyptian cattle and another epidemic that was
characterized by “boils breaking out in sores on man and beast.” 9 Still another
disease, according to Exodus, killed “all the first-born in the land of Egypt . . .
and all the first-born of the cattle.” 10 However apocryphal, such stories suggest
that epidemic diseases were important events in ancient Egypt.
In the East, the Harrapan civilization flourished in the Indus River Valley
from approximately 3000 to 1800 b.c.e. but then rapidly declined. Although
warfare and drought played a role, Paul Ewald has proposed that the spread
of cholera was also an important factor.11 In China, “mention of unusual out-
breaks of disease abound in the Han dynastic history, . . . including some that
acted in epidemic fashion from time to time.” 12 Measles and smallpox are
both thought to have existed, and “from 200 b.c. to a.d. 200 [China’s] popu-
lation declined severely because of new epidemics.” 13 In 310 –312 c.e., an
epidemic disease, “preceded by locusts and famine, left only one or two out of
a hundred persons alive in the northwestern provinces of China; and this was
followed ten years later, in 322, by another epidemic in which two or three out
of ten died over a wider region of the country.” 14 The effect of such epidemic
was to bring to a close the Han Empire, which then “fell like a rotten tree
before a gale.” 15
It is the Roman Empire, however, for which the most definitive records
link infectious diseases to its decline. The historian Livy “records at least
eleven cases of pestilential disaster in republican times, the earliest dated 387
b.c.” 16 One of the most severe of these was the “plague on Antoninus,” which
raged from 165 to 180 c.e. It was brought to Rome by soldiers returning from
Syria and is estimated to have killed one-quarter to one-third of the Roman
population, including Emperor Marcus Aurelius. Some historians have desig-
nated this epidemic “the turning point of the Roman Empire,” the beginning
of its decline.17
Even more severe was the plague of Cyprian, which lasted from 250 to
265 c.e. Edward Gibbon claimed that it “raged without interruption in every
province, every city, and almost every family of the Roman empire. During
some time, five thousand persons died daily in Rome, and many towns . . .
were entirely depopulated.” 18 The epidemic not only affected the Roman
Empire but spread throughout Europe and is said to have killed over half its
population: “More died than survived, and not sufficient people were left to
bury the dead.” 19 According to one source, the plague of Cyprian “indisput-
ably changed the course of history in western Europe.” 20
The precise microbial causes of these Roman epidemics have never been
ascertained, although smallpox and measles have been suggested as candi-
dates. However, the cause of the final epidemic to devastate the Roman Em-
pire, the plague of Justinian, has been clearly identified as Yersina pestis, the
bacteria that causes bubonic plague. As described in chapter 6, this epidemic
raged for more than fifty years in the sixth century c.e., initially devastating
the eastern Mediterranean and then spreading to Italy, where, according to
Gibbon, “the harvest and the vintage withered on the ground.” 21 From Italy,
it spread from city to city along the Mediterranean coast, carried by infected
rats on ships, eventually reaching England. Estimates of the total dead from
this plague are as high as 100 million, but the true number is unknown.22
The plague devastated trade and the economy of the Mediterranean region
and altered the course of history. As a consequence of the Justinian plague,
it has been speculated that “the relatively plague-free nomads and barbarians
moved in to settle or graze the land,” “enormous areas . . . became Islami-
cised,” “letters and art in Europe entered the Dark Ages,” and “monastic life
took a stranglehold on the intellectual mainstream of the Christian world.” 23
According to Hans Zinsser’s Rats, Lice and History, the Justinian plague
was “the coupe de grâce to the ancient empire.” Zinsser suggests that “the
calamitous epidemics which—sweeping the Roman world again and again
during its most turbulent political periods—must have exerted a material, if
not decisive, influence upon the final outcome.” 24
We are not arguing that infectious diseases alone caused the decline of
ancient civilizations. Natural disasters, famine, and warfare often work in uni-
son with microbes to bring about the final result. Warfare and natural disas-
ters, for example, often destroy farm animals and crops, whose scarcity leads
to famines; these in turn weaken people’s immune systems, making them
more susceptible to infectious diseases. Conversely, infectious diseases, es-
pecially in epidemic waves, have secondary consequences: They demoralize
populations and undermine human authority. Lawlessness was a common
A Fo u r - Fo o t e d Vi e w o f H i s t o r y = 143
denominator during many of the world’s great epidemics. As Zinsser notes:

“The effects of a succession of epidemics upon a state are not measurable
in mortalities alone. Whenever pestilences have attained particularly terrify-
ing proportions, their secondary consequences have been much more far-
reaching and disorganizing than anything that could have resulted from the
mere numerical reduction of the population.” 25
Some historians have also suggested that ancient disease epidemics con-
tributed to the rise of Christianity and other world religions. Since the micro-
bial origins of epidemics were unknown, their cause was usually attributed to
divine acts. As William McNeil noted in Plagues and People, Christianity had
an advantage over paganism insofar as “faith made life meaningful even amid
sudden and surprising death.” 26 The promise of physical resurrection after
death and of life everlasting offered great solace during periods when large
numbers of people were dying.
Conversions to Christianity were more common during epidemics and
natural disasters. This is illustrated impressively by the Roman “plague of
Cyprian,” which took its name from St. Cyprian, the bishop of Carthage. At
its height, Cyprian and his fellow priests “baptized as many as two or three
hundred persons a day.” 27 He wrote a tract extolling the epidemic:
Many of us are dying in this mortality, that is many of us are being freed
from the world. This mortality is a bane to the Jews and pagans and en-
emies of Christ; to the servants of God it is a salutary departure. As to the
fact that without any discrimination in the human race the just are dying
with the unjust, it is not for you to think that the destruction is a common
one for both the evil and the good. The just are called to refreshment,
the unjust are carried off to torture; protection is more quickly given to
the faithful; punishment to the faithless. . . . How suitable, how necessary
it is that this plague and pestilence, which seems horrible and deadly,
searches out the justice of each and every one and examines the minds
of the human race.28
Cartwright and Biddiss in Disease and History suggest that “Christianity

would hardly have succeeded in establishing itself as a world force . . . if the
Roman Empire had not been ravaged by incurable disease during the years
which followed the life of Christ.” Zinsser similarly noted that “Christianity
owes a formidable debt to bubonic plague and to smallpox, no less than to
earthquake and volcanic eruptions.” 29
In proposing this four-footed view of history, we have necessarily focused
on the epidemic diseases, such as smallpox, measles, and bubonic plague,
which were so momentous that they were recorded as written history. No
less devastating, perhaps, were endemic human diseases also originating in
animals. Thus, tuberculosis, dysentery, pertussis, and other diseases almost
certainly occurred in small outbreaks, killing farmers who supplied food to

the cities along with government leaders, military commanders, artisans, and
philosophers. This ongoing loss of population was an important contributor
to the decline of ancient civilizations, although it is much less visible because
it was not usually passed down in recorded history.
In conclusion, the great civilizations of the ancient world came into ex-
istence in the centuries following the domestication of plants and animals.
Sheep, goats, pigs, cattle, horses, and other domesticated animals played a
major role in making such civilizations possible. At the same time, domes-
ticated animals brought with them their microbes, many of which adapted
to humans, causing infectious diseases. As people in ancient civilizations
became urbanized and transportation improved, infectious diseases spread
more easily, some in epidemic fashion. These diseases played a major role
in the decline of these civilizations. The role of animals, therefore, was to be
both a cause and a curse, contributing to the creation and then the dissolution
of civilizations that, even today, we regard as extraordinary.
Notes
CHAPTER 1. The Smallest Passengers on Noah’s Ark
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3. Stephen Jay Gould, Foreword, in Margulis and Schwartz, Five Kingdoms.
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8. Tony McMichael, Human Frontiers, Environments, and Disease (Cambridge: Cam-
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15. Hans Zinsser, Rats, Lice, and History (1934; repr. Boston: Little, Brown, 1963), 57.
= 145
146 = No t e s t o Pa g e s 5 – 1 2
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19. Richard Fiennes, Man, Nature, and Disease (New York: Signet, 1964), 91.
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23. Fiennes, Man, Nature and Disease, 88.
24. W. Plowright, “The Effects of Rinderpest and Rinderpest Control on Wildlife in Af-
rica,” Symposia of the Zoological Society of London 50 (1982): 1–28.
25. A. Dobson and J. Foufopoulos, “Emerging Infectious Pathogens of Wildlife,” Phil-
osophical Transactions of the Royal Society of London, Series B, 356 (2001): 1001–
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26. C. D. Harvell, K. Kim, J. M. Burkholder et al., “Emerging Marine Diseases: Climate
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28. M. A. Miller, I. A. Gardner, C. Kreuder et al., “Coastal Freshwater Runoff Is a Risk
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CHAPTER 2. Heirloom Infections:

Microbes before the Advent of Humans
1. Ronald Hare, Pomp and Pestilence: Infectious Disease, Its Origins and Conquest (Lon-
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CHAPTER 3. Humans as Hunters: Animal Origins of Bioterrorism

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3. McMichael, Human Frontiers, 47.
4. Ibid., 44, 47– 48.
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CHAPTER 4. Humans as Farmers: Microbes Move into the Home

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CHAPTER 5. Humans as Villagers: Microbes in the Promised Land

1. Karlen, Man and Microbes, 25.
2. Cole, The Neolithic Revolution, 55–56 (see chap. 4, n. 6).
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32. Ibid., 104.
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CHAPTER 6. Humans as Traders: Microbes Get Passports

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3. Martin, “Earth History” (see chap. 1, n. 14).
5. 2 Sam. 24:15
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CHAPTER 7. Humans as Pet Keepers: Microbes Move into the Bedroom

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CHAPTER 8. Humans as Diners: Mad Cows and Sane Chickens

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CHAPTER 9. Microbes from the Modern Food Chain:

Lessons from SARS, Influenza, and Bird Flu
The epigraph quote is from Peter Cordingly, speaking for the World Health Organization
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29. Ibid., 102, 105.
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49. Webster, “Wet Markets.”
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CHAPTER 10. The Coming Plagues: Lessons from AIDS,

West Nile Virus, and Lyme Disease
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12. Dobson and Foufopoulos, “Emerging Infectious Pathogens of Wildlife” (see chap. 1,
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14. D. Brown, “West Nile Virus Kills Four, Sickens 88 in Three States,” Washington Post,
August 3, 2002.
168 = No t e s t o Pa g e s 1 2 8 – 1 3 3
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21. Y.J.F. Hutin, A. M. Hauri, and G. L. Armstrong, “Use of Injections in Healthcare Set-
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23. R. S. Boneva, T. M. Folks, and L. E. Chapman, “Infectious Disease Issues in Xeno-
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24. J. S. Allan, “The Risk of Using Baboons as Transplant Donors: Exogenous and Endog-
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25. D. Butler, “Last Chance to Stop and Think on Risks of Xenotransplants,” Nature 391
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26. D. Yoo and A. Giulivi, “Xenotransplantation and the Potential Risk of Xenogeneic
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27. R. A. Weiss, S. Magre, and Y. Takeuchi, “Infection Hazards of Xenotransplantation,”
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28. Rosenbloom et al., “Biological and Chemical Agents” (see chap. 3, n. 23).
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30. Zinsser quoted in Karlen, Man and Microbes, 25 (see chap. 1, n. 17).
31. Jonathan R. Davis and Joshua Lederberg, eds., Emerging Infectious Disease from the
Global to the Local Perspective: Workshop Summary (Washington, D.C.: National
Academy Press, 2001).
32. E. Zwingle, “Cities,” National Geographic, November 2002, 70 –99.
33. Murphy, “Emerging Zoonoses” (see chap. 1, n. 35).
34. Garrett, The Coming Plague, 567 (see chap. 1, n. 4)
36. S. S. Morse, “Factors in the Emergence of Infectious Diseases,” Emerging Infectious
Diseases 1 (1995): 7–15.
37. Arno Karlen, Biography of a Germ (New York: Knopf, 2001), 138.
38. A. G. Barbour and D. Fish, “The Biological and Social Phenomenon of Lyme Dis-
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39. A. C. Revkin, “Out of Control, Deer Send Ecosystem into Chaos,” New York Times,
November 12, 2002.
40. “Lyme Disease: United States, 2000,” Morbidity and Mortality Weekly Report 51
(2002): 29–31.
41. A. C. Steere, “Lyme Disease,” New England Journal of Medicine 345 (2001): 115–125.
42. Taylor et al., “Risk Factors” (see chap. 1, n. 29)
43. P. Saikku, M. Leinonen, K. Mattila et al., “Serological Evidence of an Association of a
Novel Chlamydia, TWAR, with Chronic Coronary Heart Disease and Acute Myocar-
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44. C. Storey, M. Lusher, P. Yates et al., “Evidence for Chlamydia pneumoniae of Non-hu-
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Genus Chlamydia Based on 16S Ribosomal DNA Analysis,” Journal of Bacteriology
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45. D. M. Vail and E. G. MacEwen, “Spontaneously Occurring Tumors of Companion
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46. H. zur Hausen, “Proliferation-Inducing Viruses in Non-permissive Systems as Pos-
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Knight, and M. C. Lancaster, “Lymphomas Associated with a Tolerant Lymphocytic
Choriomeningitis Virus Infection in Mice,” Laboratory Animals 14 (1980): 117–121.
47. M. V. Viola, “Hematological Malignancies in Patients and Their Pets,” Journal of the
American Medical Association 205 (1968): 95–96.
48. Murphy, “Emerging Zoonoses.”
49. Mark S. Smolinski, Margaret A. Hamburg, and Joshua Lederberg, eds., Microbial
Threats to Health: Emergence, Detection, and Response (Washington, D.C.: National
Academy Press, 2003), 245.
50. Smolinski et al., Microbial Threats to Health, 165.
51. Ibid., 170.
52. Lederberg et al., Emerging Infections, 131 (see chap. 1, n. 36).
53. Tom Burroughs, Stacey Knobler, and Joshua Lederberg, eds., The Emergence of Zoo-
notic Diseases (Washington, D.C.: National Academy Press, 2002), 7.
54. This list is adapted from information in Animal-Borne Epidemics Out of Control:
Threatening the Nation’s Health (Trust for America’s Health, 2003), www.healthy
americans.org.
55. John Files, “Effort to Coordinate Some Disease Research,” New York Times, June 3,
2004.
57. L. K. Altman, “As Bird Flu Spreads, Global Health Weaknesses Are Exposed,” New
York Times, February 3, 2004.
59. E. Williamson, “Mad-Cow Fear Raises Concerns in Md. Death,” Washington Post,
January 11, 2004.
60. http://www.aphis.usda.gov/vs/ncie/pet-info.html, accessed July 15, 2003.
61. P. M. Schantz, D. Meyer, and L. T. Glickman, “Clinical, Serologic, and Epidemio-
logic Characteristics of Ocular Toxocariasis,” American Journal of Tropical Medicine
and Hygiene 28 (1979): 24 –28.
62. Morrison, “Zoonotic Infections from Pets” (see chap. 7, n. 119).
63. D. Robertson, P. J. Irwin, A. J. Lymbery et al., “The Role of Companion Animals in
the Emergence of Parasitic Zoonoses,” International Journal of Parasitology 30 (2000):
1369–1377.
CHAPTER 11. A Four-Footed View of History

1. Cartwright and Biddiss, Disease and History, 8.
2. H. Weiss, M.-A. Courty, W. Wetterstrom et al., “The Genesis and Collapse of Third
Millennium North Mesopotamian Civilization,” Science 261 (1993): 995–1004.
170 = No t e s t o Pa g e s 1 4 0 – 1 4 3
3. Ibid.
4. Ibid.
6. Encyclopaedia Britannica (1954), s.v. Xerxes.
8. Eva Panagiotakopulu, “Pharaonic Egypt and the Origins of Plague,” Journal of Bio-
geography 31 (2004): 269–275.
9. Exod. 9:3, 9.9 (RSV).
10. Exodus 12:29–30.
11. Ewald, “Evolution and Ancient Diseases,” 117–124.
15. H. G. Wells, The Outline of History: Being a Plain History of Life and Mankind (New
York: Macmillan, 1925), 553.
18. Edward Gibbon, The History of the Decline and Fall of the Roman Empire, chap.10,
sec. 3, “Famine and Pestilence,” http://www.ccel.org/g/gibbon/decline/volume1/chap10
.htm, accessed May 17, 2004.
19. Zinsser, Rats, Lice and History, 139.
21. Gibbon, History of the Decline and Fall, chap. 43, sec. 3, “Plague,” http://www.ccel
.org/g/gibbon/decline/volume2/chap43.htm#plague, accessed May 17, 2004.
22. Chase, The Barbary Plague, 33.
24. Zinsser, Rats, Lice and History, 133, 131.
25. Ibid., 128.
28. McNeil, Plagues and People, 136 –137.
29. Cartwright and Biddiss, Disease and History, 15. Zinsser, Rats, Lice and History, 139.
Glossary of Definitions
Related to Microbes
animals One of three phyla of complex forms of life, the other two being
plants and fungi. There are approximately thirty million animal
species, of which mammals constitute less than 0.1 percent.
bacteria Single cells without a nucleus but able to reproduce themselves,
probably the oldest form of life on earth.
commensal A microbe that lives with an animal but does not cause any disease.
DNA Deoxyribonucleic acid, a large molecule composed of a string of
nucleotides and sugars connected by phosphate bonds shaped in
the form of a double helix. DNA contains all of our genetic informa-
tion. DNA encodes RNA, which then encodes proteins, the build-
ing blocks of all of our body structures and functions.
endemic Prevalent in a particular animal or region.
epidemic Highly prevalent, widespread, and rapidly increasing.
fungi A large group of organisms related to plants but without green color.
The group includes some members that occasionally cause human
diseases such as histoplasmosis.
gene Long strands of DNA, situated on chromosomes in cells, that de-
termine what proteins a cell will express at any given time. Some
viruses use RNA instead of DNA as their genes.
host The animal that is infected.
humans A species of hominid primate, officially called Homo sapiens. As
primates, humans are classified as mammals and thus as animals.
microorganism Literally, a small organism, usually implying bacteria, viruses, and
protozoa. Often shortened to microbe and in common parlance re-
ferred to as “a germ.”
mutation A rare change in the DNA nucleotide pattern, sometimes produc-
ing a change in proteins expressed by the cell. Some mutations re-
sult in diseases in individuals who have them.
pathogen A microbe capable of causing disease.
= 171
172 = Glossary
polymorphism A variation in the DNA nucleotide pattern that occurs commonly

in the human population. Some are associated with individual dif-
ferences in the ability to fight infections.
protozoa Single cells with nucleus and mitochondria, thus more complex
than bacteria. Types include amoeba, flagellates, ciliates, sporozoa,
coccidia, and microsporidia.
reservoir An animal in which large numbers of microbes may be found, often
the source of a microbe’s spread to other animals.
RNA Ribonucleic acid, a large molecule encoded by DNA and similar
in structure to DNA but different in some of the building blocks.
Encodes proteins and has other regulatory functions.
vector An organism, usually an insect or arthropod, that carries a microbe
from one animal to another, such as fleas, flies, ticks, and mosqui-
toes, e.g., ticks carry the bacteria that causes Lyme disease from deer
to humans.
virulence The relative strength of a particular microbe. Many viruses, bac-
teria, and protozoa have different strains, some of which are more
virulent than others.
viruses DNA or RNA surrounded by a protein or lipoprotein coat. Viruses
are unable to reproduce themselves unless they get into living cells.
zoonosis A disease caused by microbes that spreads naturally from other ani-
mals to humans.
Appendix
Timeline
2 billion years ago Bacteria, viruses, and protozoa evolve
1 billion years ago The first animals evolve
155 million years ago Mammals evolve
60 million years ago Primates evolve
6 million years ago Hominids separate from primates
1.7 million years ago Hominids migrate out of Africa for the first time
1.0 million years ago Hominids become meat-eating hunters
130,000 years ago anatomically modern Homo sapiens evolves
100,000 years ago Homo sapiens migrate out of Africa
30,000 years ago Paleolithic people make drawings of animals in caves

in France and Spain
14,000 years ago Domestication of dogs
11,000 years ago Domestication of sheep
10,000 years ago Domestication of goats
8 –10,000 years ago Domestication of pigs and cattle; settlement of the

earliest towns
5,000 years ago Domestication of horses; development of earliest

centers of civilization
= 173
Index
The notation 6f refers to Figure 1-1 on page 6; 17–18t refers to Table 2.1 on pages 17–18
abortions, spontaneous (miscarriages): alligators as exotic pets, 92, 93

in animals, 28, 78, 83, 89, 106; in amphibians, 15, 90, 133
humans, 85, 90, 106 Animal and Plant Health Inspection Ser-
advanced meat recovery systems, 110, 111 vice (APHIS), 135
African pouch rats, 92, 95–96 animal bites: as an example of direct trans-
agribusiness, 97–98, 103–107, 109–110, mission of infection, 6f, 7; cats, 77–78,
112, 121, 123. See also advanced meat 82; dogs, 7, 39, 77–78, 80; monkeys, 16,
recovery systems; fish: fish farming and 126; rabies, 6f, 80, 94
influenza animal domestication. See domestication
agriculture: development of, 33–34, 48, of animals
139, 144; effects of changing practices, animal feed, contaminated wastes in, 110.
131. See also agribusiness; grains, See also fish: fish farming and influenza
grasses, cereals; plants animal-human relationship, 25–27, 33,
AIDS/HIV infection: as a blood-borne 38 –39, 52, 78. See also bestiality;
illness, 126 –127, 129; as a retrovirus, domestication of animals; pet keeping:
21–22, 125–126; concurrent with other increasing owner-pet intimacy
illnesses, 17–18t, 18, 47, 78, 79, 85– 86; animals: as transportation, 57, 139–140;
effects on the immune system, 9, 15, bones as tools, 25, 36; importance in
22, 47, 85; epidemic nature, 126 –127; trade, 56 –57; in ancient art, 26 –27, 38,
infection rates, 1, 127; lethal potential, 39, 52, 58, 139; in creation myths, 25;
5–7; molecular studies, 126; mortality number of species, 2; surveillance of
rates, 80, 85, 126 –127; pet ownership diseases affecting, 134, 135; work done
in patients, 75; psychiatric symptoms by, 35, 37, 38, 68, 75, 140. See also
in patients with toxoplasmosis, 86; animal-human relationship; clothing,
recent emergence, 11, 22, 126, 134; animal sources of; domestication of
relationship to simian viruses, 125–126; animals; meat; milk; specific animals
transmission, 1, 6f, 7, 11, 125–127, 129; anthrax, 6f, 27, 28, 30, 63, 130
viral mutations, 6f, 127 antibiotics, 134; against plague, 65, 66, 83;
air travel and infection transmission, against other microbes, 47, 78, 80, 82,
113–114, 127, 128 –129 85, 89, 118; effects on host’s immune
airborne transmission of infection, 6f, 39, system, 15; in animal feed, 100; resis-
49, 129; anthrax, 28, 30; Chlamydia tance to, 10, 47, 66, 100
psittaci, 88; glanders, 30; hantavirus, antibodies, 9, 81, 82, 84, 89, 115–116, 119
7, 67; lymphocytic choriomeningitis, APHIS (Animal and Plant Inspection
89; plague, 65; Q fever, 30; SARS, 113, Service), 135
128; Toxoplasma gondii, 83; tularemia, aquaculture. See fish: fish farming and
30 influenza
Akabane virus, 124 aquatic birds. See ducks
allergies and exposure to animals: benefits, archeological findings, 24, 58, 139, 140.
77; risks, 77, 88, 89 See also art: ancient art; cave art
= 175
176 = Index
arenaviruses, 89 11; migration, 128; sold as food at wet
Argentine hemorrhagic fever, 131 markets, 113; infectious diseases/mi-
Armed Forces Intelligence Center, 135 crobes: ancient viral infections, 14, 22;
art, animals depicted in: ancient art, 38, campylobacteriosis/Campylobacter,
39, 52, 58, 139; paintings, 72. See also 107; giardiasis/Giardia lamblia, 88; he-
cave art padnaviruses, 19; herpesviruses, 15–16,
arthritis, 78, 87, 89, 100, 106, 132. See also 17–18t; influenza, 88, 114, 121; liste-
osteoarthritis; rheumatoid arthritis riosis/Listeria, 106; malaria, 19; New
asthma, 77, 88 Castle disease, 88; paramyoxovirus, 88;
aurochs. See cattle possible implication in rheumatoid
Australopithecus afarensis, 23 arthritis, 87; psittacosis/Chlamydia psit-
autism, 76 taci, 88 – 89; salmonellosis/Salmonella,
autopsies, 45, 64, 136 –137 88, 99; typhoid fever/Salmonella typhi,
avian influenza. See bird flu 7, 99; West Nile virus, 1, 6f, 7, 127–128;
Yersinia pseudotuberculosis, 59. See also
baboons, 17–18t, 23, 124, 126 bird flu; chickens and other poultry;
bacteria: as ancient microbes, 2–3, 4, ducks; fish: fish farming and influenza;
14 –15, 39, 124; as fermenting agents, parakeets
34; as microparasites, 2; beneficial bison, 25–26, 38. See also buffalo; water
bacteria, 15; hardiness, 2; integration buffalo
into the human genome, 3; nucleic bites. See animal bites
acid sequencing, 12–13; number of Black Death/Black Plague. See plague:
species, 2, 3, 133; percentage of zoono- epidemics/pandemics
ses caused by, 12; rate of reproduction, blindness. See eyes, damage to
13; relationship to protozoa and viruses, blood-borne infections, 19, 126 –127, 129
3– 4; self-preservation, 5; transmission, blood transfusions and infection transmis-
8, 49, 57; virulence, 9. See also specific sion, 6f, 19, 127
bacteria “Blue Revolution.” See fish: fish farming
“Baghdad Boil,” 79 and influenza
bats, 11, 41, 80, 94 bluetongue virus disease, 125
bears, 25, 27, 92, 132, 137 boars. See pigs
beaver, 25, 94 Bond, Colin, 87
beef and foodborne illnesses, 6f, 7, 27, bone disease, 94, 100, 133
84, 105, 107–108, 110. See also bone meal, 110
bovine spongiform encephalopathy; bones, animal, 14, 24, 25, 28, 36
Creutzfeld-Jakob disease bordetellosis/Bordetella, 41, 78
Belyaev, D.K., 35 bovine spongiform encephalopathy (BSE),
bestiality, 39 1, 6f, 7, 108 –111, 136
Biddiss, Michael, 143 bovine tuberculosis, 42– 43
bioterrorism/ biowarfare: surveillance ef- brain, evolution of, 25, 33
forts, 30, 135; possible agents: anthrax, brain infections, causes of: bovine spongi-
28, 30, 130; brucellosis, 28, 30, 130; form encephalopathy, 109; cat scratch
Ebola virus, 130; glanders, 30 –32, 130; disease, 82; Chlamydia psittaci, 88;
Lassa fever virus, 130; plague, 65, 66; cysticercosis, 27; dog and cat bites, 78;
Q fever, 28, 30, 130; smallpox, 41, 42, E. coli, 107–108; herpesviruses, 16,
130; tularemia, 29, 30, 130 17–18t; ingestion of brain tissue, 109;
bipolar disorder and Toxoplasma gondii listeriosis, 106; Lyme disease, 132;
infection, 86 lymphocytic choriomeningitis virus,
bird flu, 12, 112, 121–123, 125, 134, 136, 89; measles virus, 51; nipah virus, 41;
137 prions, 109; Toxoplasma gondii, 85, 86;
birds: aquatic birds, 114, 121; as pets, 72, Trichinella spiralis, 27; West Nile virus,
87, 88; eggs as food, 23; evolution, 127. See also encephalitis; meningitis
15; infection transmission to humans, brain tissue, ingestion of, 109, 110
Index = 177
brain tumors, 86 flu, 122; bordetellosis/Bordetella, 41,
Bray, R.S., 140 78, 82; bovine spongiform encepha-
breeding, selective, 38, 70 lopathy, 111; campylobacteriosis/Cam-
brucellosis, 27, 28, 30, 78, 97, 130 pylobacter, 78, 82; cat scratch disease,
BSE. See bovine spongiform encephalopa- 6f, 7, 82; coronaviruses, 113; cowpox
thy virus, 42; Creutzfeld-Jakob disease,
bubonic plague. See plague 111; cryptosporidiosis/Cryptosporidium
Budiansky, Stephen, 36 parvum, 78, 82; feline herpesvirus, 16,
buffalo, 10, 43, 92. See also bison; water 17–18t; feline panleukopenia virus,
buffalo 11; giardiasis/Giardia lamblia, 79, 82;
buffalopox virus, 42 Helicobacter pylori, 40; leukemias and
Burkitt’s lymphoma, 17–18t lymphomas, 133; Lyme disease, 80, 82,
bushpigs, 10, 23 132; multiple sclerosis, 81; Mycobacte-
butchering, risk of infection during, 27, 28, rium bovis, 42; nipah virus, 41; plague/
29, 40, 104, 109–110, 126 Yersinia pestis, 82, 83; rabies, 11, 80,
82, 94, 95; retroviruses, 22; rheumatoid
camels, 57 arthritis, 86 – 87; roundworms, 80;
campylobacteriosis/Campylobacter, 78, 92, salmonellosis/Salmonella, 104; SARS,
99, 105–107, 111 113; toxocariasis/Toxocari, 80, 82;
cancer: relationship of human cancers to toxoplasmosis/Toxoplasma gondii, 82,
animal cancers, 133; causes: Campylo- 83– 86
bacter, 107; Helicobacter pylori, 8, 133; cattle (general): as a source of clothing, 25,
hepatitis B, 18 –19, 133; herpesviruses, 37, 38; as a valuable commodity, 37–
16, 17–18t, 18, 22; HTLV viruses, 21; 38, 39, 57, 144; as farm animals, 37, 97;
human papilloma viruses, 133; lym- as objects of worship, 37, 69; breeding,
phocytic choriomeningitis, 90; types: 38; contaminated feed for, 110; cow’s
carcinomas, 17–18t; cervical cancer, milk, 37, 39, 52, 77; diet of, 35, 36 –37,
133; Kaposi’s sarcoma, 17–18t, 18, 22; 110; domestication, 37–39, 42, 50, 52;
leukemias, 21, 133; liver cancer, 19, effects of agribusiness, 97–98, 109–110;
133; lymphomas, 17–18t, 90, 107, 133; in ancient art, 26, 38, 52, 139; infection
stomach cancer, 8, 133 transmission to humans, 11
Cantor, Norman, 63 cattle (infectious diseases/microbes), 87;
carnivores, 10, 11. See also humans: as Akabane virus, 124; anthrax, 28; bovine
hunters tuberculosis, 42– 43; brucellosis, 28,
Cartwright, Frederick F., 143 78; buffalopox virus, 42; coronaviruses,
cats (general): associations with witchcraft / 113; cowpox virus, 42; Creutzfeld-Jakob
evil, 70 –71, 72; benefits of cat owner- disease, 109; E. coli, 6f, 7, 91, 107–108;
ship/exposure to cats, 74, 76 –77; bites Helicobacter pylori, 40; herpesviruses,
from, 77–78, 82; cat ownership and 17–18t, 125; influenza, 121; malignant
psychiatric illness, 86; contaminated catarrhal fever, 125; measles, 6f, 7, 11,
food for, 111; domestication, 35, 38; 50 –52; Mycobacterium bovis, 42– 43;
feral cats, 90; history of cats as pets, 38, Q fever, 28; rhinoviruses, 50; rinder-
69–72, 82; in advertising, 71–72; in art, pest virus, 9–10, 51–52; Taenia, 27;
72, 139; in literature, 71–72; in pres- toxoplasmosis/Toxoplasma gondii, 85;
ent-day China, 73; increasing intimacy tuberculosis, 42– 43. See also bovine
with owners, 73; infection transmission spongiform encephalopathy
to humans, 11; infections transmitted cave art, 26 –27, 38
from humans, 10; quarantine restric- Centers for Disease Control and Preven-
tions, 137; risks of exposure to, 77– 87; tion (CDC): surveillance of: emerging
for rodent control, 38, 70; sold as food infectious diseases, 12, 112; foodborne
at wet markets, 113; statistics on cat illnesses, 98 –99, 105, 107; infectious
ownership, 72–73 diseases in general, 135–136, 137;
cats (infectious diseases/microbes): bird threats of bioterrorism, 135
178 = Index
cereals/grasses/grains, 34, 48 cockroaches, 84
cerebral palsy, 85 coevolution, 16
cheese. See milk Cold War bioterrorism, 32
chickenpox, 17–18t, 52 colitis, 105, 111
chickens and other poultry: as animal feed, commensals, 15, 66
110; as farm animals, 97; contaminated common cold, 50, 113
feed for, 110; domestication, 38; ef- companion animals, 74 –77, 128
fects of agribusiness, 97–98, 103–105, congenital infections. See fetuses, infec-
109–110, 121, 123; feces of, as fertil- tions in
izer, 115; in ancient art, 139; sold at consumption. See tuberculosis
wet markets, 113; infectious diseases/ contaminated food, 97–98; bovine spongi-
microbes: bird flu, 121–123, 125, 137; form encephalopathy, 108 –111; brucel-
campylobacteriosis/Campylobacter, losis, 28; Creutzfeld-Jakob disease, 109;
107; coronaviruses, 113; influenza, 114, E. coli, 6f, 7, 107–108; glanders, 29;
115, 134 –135; listeriosis/Listeria, 106; hepatitis, 18; kuru, 109; Listeria, 106;
retroviruses, 22; salmonellosis/Salmo- Salmonella, 99–105; Taenia, 27; trichi-
nella, 99, 102–105. See also ducks; eggs nosis, 27; tularemia, 29; typhoid fever,
childbirth and infection transmission, 19 99. See also fecal contamination
children: benefits and risks of exposure to contaminated water: as a result of urbaniza-
animals, 76 –77; infections at risk for: tion, 131; contaminated wells, 49;
campylobacteriosis, 106; cat scratch dis- contamination with infected urine,
ease, 82; hemolytic uremic syndrome, 79– 80; fecal contamination, 39, 78, 79,
107; Lyme disease, 132; malaria, 19; 97, 107; infectious agents: Cryptospo-
measles, 51; salmonella, 93; toxoca- ridium parvum, 78; E. coli, 6f, 7, 107;
riasis, 80; toxoplasmosis, 83. See also echinococcus, 79; Giardia lamblia, 79;
petting zoos glanders, 31; Helicobacter pylori, 40;
chimpanzees: as early organ donors in xe- hepatitis A, 18; leptospirosis, 79– 80;
notransplants, 129; as exotic pets, 92; as Salmonella Newport, 102–103; Salmo-
food, 126; diet of, 23; evolution, 25, 59, nella typhi, 99; Toxoplasma gondii, 10,
126; infectious diseases/microbes: AIDS/ 83– 84. See also fish: fish farming and
HIV, 11; endogenous retroviruses, 21, influenza
126; hepatitis, 18, 19; malaria, 19; sim- coprolites, 28
ian viruses, 125–126 corneal transplants, 109
chipmunks, 65, 137 coronary disease. See heart infections/dis-
Chlamydia pneumonia, 88, 133 ease
chocolate as a source of Salmonella, 105 coronaviruses, 113, 125
cholera, 4, 64, 140 cowpox virus, 42
Christianity, effects of epidemics on, 53, cows. See cattle
63, 143 coyotes, 94
chronic wasting disease (CWD), 111 Creutzfeld-Jakob disease (CJD), 109, 111
circovirus, 130 Crosby, Alfred, 117
cities. See urbanization and infection cross-species transmission of infection:
transmission factors influencing, 8, 39, 125; transmit-
Civil War, U.S., 29–30, 55 ted infections: AIDS/HIV, 126; bird
civilizations, growth and decline of, 19, 53, flu, 122; coronaviruses, 113; feline
139–144 panleukopenia virus, 11; herpesvirus,
CJD (Creutzfeld-Jakob disease), 109, 111 16; prions, 111; rinderpest virus, 10. See
Cleland, Leslie, 87 also fish: fish farming and influenza
climatic changes and infection transmis- crowded living conditions: as a result of
sion, 24, 25, 33–34, 67, 140 urbanization, 44, 131; in the ancient
clothing, animal sources of, 25, 36, 37, 38, world, 49, 50, 57; transmitted infections/
61, 68, 140 microbes: Helicobacter pylori, 40; influ-
Clutton-Brock, Juliet, 36 enza, 117; Mycobacteria, 43; plague,
Index = 179
44; psittacosis, 88; tuberculosis, 45. See requirements, 137; in ancient art, 139;
also population: density/size require- in literature, 36, 70; in present-day
ments for microbe transmission China, 73; increasing intimacy with
crows, 128 owners, 73–75; infection transmission
cryptosporidiosis/Cryptosporidium parvum, to humans, 11; infections transmitted
78, 92, 99 from humans, 10; migration, 35; risks of
cutaneous larva migrans, 78 –79 exposure to, 77– 82, 87; sold as food at
CWD (chronic wasting disease), 111 wet markets, 113; statistics on, 72
Cyclospora, 99 dogs (infectious diseases/microbes): borde-
cysticercosis, 27 tellosis/Bordetella, 41, 78; brucellosis,
cysts: as a means of infection transmission, 78; campylobacteriosis/Campylobacter,
27, 83– 84, 86; as a symptom of infec- 78; cancer, 133; canine distemper virus,
tion, 27, 79, 85 10, 51, 81– 82; canine herpesvirus, 16,
cytomegalovirus, 16, 17–18t, 130 17–18t; canine parvovirus, 11; corona-
viruses, 113; cryptosporidiosis/Crypto-
dairy products: in the human diet, 36, 37; sporidium parvum, 78; cutaneous larva
as a source of foodborne illness, 28, 106 migrans, 78 –79; dirofilariasis/Dirofi-
deafness, 51, 85 laria immitis (canine heart worm), 79;
death rates. See mortality rates echinococcus, 79; giardiasis/Giardia
deer: as a source of clothing, 25; as food, lamblia, 79; heart worm, 79; Heli-
111; changing population, 131–132; cobacter pylori, 40 – 41; hookworm,
in cave art, 26; infectious diseases/ 78 –79; influenza, 121; leishmaniasis, 8,
microbes: chronic wasting disease, 79; leptospirosis, 79– 80; Lyme disease,
111; Creutzfeld-Jakob disease, 111; 80, 132; multiple sclerosis, 80 – 82;
influenza, 121; Lyme disease, 1, 7, 80, nipah virus, 41; rabies, 6f, 7, 11, 80, 94,
131–132 137; rheumatoid arthritis, 87; round-
deer mice, 67 worms, 80; tapeworm, 79; toxocariasis/
dementia, 109 Toxocari, 80
dengue, 131, 140 dolphins, 51
departments, U.S. See federal agencies domestication of animals, 33, 35–39,
dealing with infectious diseases; Federal 48, 140, 144. See also animal-human
Aviation Administration; Transportation relationship; specific animals
Department drug use and infection transmission, 19,
Diamond, Jared, 5, 126 79, 126, 127, 129
diarrheal disease, 78, 89, 91, 106, 107 ducks: as human food, 38, 113, 114; as
Dilger, Anthony “Tony,” 31 pets, 103; carcasses of, as animal feed,
dinosaurs, 2, 6f, 14 116; domestication, 38, 114 –115; feces
diphtheria, 140 of, as animal food, 116; feces of, as fer-
dirofilariasis/Dirofilaria immitis (canine tilizer, 115–116; fish farming, 114 –116;
heart worm), 79 in ancient art, 139; infection transmis-
disease surveillance. See under animals; sion, 87; migration, 116; sold at wet
bioterrorism/ biowarfare; emerging markets, 113; wild ducks, 116, 121, 123;
infectious diseases; epidemics/pan- infectious diseases/microbes: bird flu,
demics; plants; SARS; West Nile virus; 121–123, 125; influenza, 6f, 114 –116,
zoonoses 120 –121; listeriosis/Listeria, 106;
distemper virus in dolphins and seals, 51 salmonellosis/Salmonella, 102, 103. See
DNA (deoxyribonucleic acid), 3, 37, 59, also chickens and other poultry
109 dural grafts, 109
dogs (general): as companion/service dysentery, 53, 107, 140, 143–144
animals, 74 –77; bites from, 7, 39,
77–78, 80; breeding, 38, 70; domes- E. coli, 6f, 7, 91, 99, 105–106, 107–108,
tication, 35–36, 37, 78; history of, as 111. See also hemolytic uremic syn-
pets, 69–72; immunization/quarantine drome
180 = Index
Ebola virus, 129, 130, 138 exotic animals: as food, 113, 123; as pets,
echinococcus, 79 90 –96, 123, 137, 138
ecological changes and infection transmis- eyes, damage to, 27, 51, 80, 82, 85
sion, 67, 125, 130 –132
eggs: in the human diet, 68, 114; as a farcy, 29
source of infection, 99–105; dangers of farm animals, benefits of early exposure
undercooking, 101–102, 137 to, 77
elderly, the: companion animals for, farming. See agriculture
75–76; risk of infection in, 100, 106 fecal contamination, 97; of cattle feed,
Electronic Surveillance System for Early 110; transmission of shed viruses,
Notification of Community-Based 66 – 67, 89; infectious diseases/microbes:
Epidemics (ESSENCE), 135 Chlamydia psittaci, 88; Cryptospo-
elk and chronic wasting disease, 111 ridium parvum, 78; cutaneous larva
emerging infectious diseases: defined, 12; migrans, 78; E. coli, 7, 107; echinococ-
global increase, 12; proportion trans- cus, 79; hantaviruses, 7, 66; hepatitis
mitted from animals, 12; recent out- A, 98; hookworm, 78 –79; lymphocytic
breaks, 124 –125; surveillance efforts, choriomeningitis (LCM), 89; Salmo-
11–13, 98 –99, 104 –105, 130, 134 –137; nella, 104, 105; SARS, 113; Toxocari,
specific diseases: bird flu, 12, 125, 134, 80; Toxoplasma gondii, 10, 83– 84. See
136; bovine spongiform encephalopa- also fish: fish farming and influenza
thy, 136; leishmaniasis, 79; listeriosis, feces: as fuel/fertilizer, 36, 37, 39,
106; monkeypox, 134, 136; SARS, 12, 115–116; fossilized, 28. See also fecal
134, 136; West Nile virus, 1, 134, 136. contamination
See also foodborne illnesses federal agencies dealing with infectious
encephalitis: favorable conditions for, diseases: Agriculture, 104, 108, 110,
131; causes: herpes B virus, 16; Lyme 136, 137; Commerce, 136; Defense,
disease, 132; lymphocytic choriomenin- 135, 136, 137; Health and Human
gitis, 89; measles, 51; nipah virus, Services, 136; Interior, 136. See also
41; Toxoplasma gondii, 85; West Nile Centers for Disease Control and
virus, 127; types: Eastern equine Prevention; Environmental Protection
encephalitis, 1 Agency; Food and Drug Administra-
endocarditis, 78, 100 tion; National Institute of Allergy and
endogenous retroviruses, 4, 21–22, 81, 130. Infectious Diseases; National Institutes
See also AIDS/HIV infection of Health
Environmental Protection Agency, 136 Federal Aviation Administration, 132
Eperythrozoon coccoides, 9 feral animals, 90
epidemics/pandemics: ancient, 57–58, ferret badgers as food, 113
141; effects on history, 139–144; future ferrets, 92, 113, 137
possibilities, 138; resulting from bioter- fetuses, infections in, 17–18t, 83, 84 – 85,
rorism, 130; resulting from human 111. See also abortions, spontaneous
migration, 57–58; surveillance efforts, (miscarriages); newborns; pregnancy,
135. See also specific diseases risk of infection in
epilepsy, 27, 80, 86. See also seizures Fiennes, Richard, 19
Epstein-Barr virus, 16, 17–18t fire, domestication of, 24
Escherichia coli. See E. coli fish: as food, 115; as a cause of foodborne
Eskimos, 53–54, 119 illness, 98; as pets, 72, 87, 137; fish
espundia, 79 farming and influenza, 114 –116, 117;
ESSENCE (Electronic Surveillance other infectious diseases/microbes:
System for Early Notification of Com- herpesviruses, 15; iridovirus, 125; trout
munity-Based Epidemics), 135 disease, 125
Ewald, Paul, 5, 141 fleas: as vectors, 7, 39; transmitted infec-
excrement. See feces tions: cat scratch disease, 82; plague, 7,
Index = 181
59, 61– 63, 65, 82, 83; trypanosomiasis, global warming and infection transmission,
8 130, 131
flies: as vectors, 7, 39, 49; transmitted goats: as a valuable commodity, 36 –39,
infections/microbes: Helicobacter pylori, 144; diet of, 35, 36 –37; domestica-
40; leishmaniasis, 79; salmonella, 103; tion, 36 –39, 43, 144; in ancient art,
Toxoplasma gondii, 84; trypanosomiasis, 139; infection transmission, 11, 39, 87;
8; tularemia, 29 infectious diseases/microbes: anthrax, 28;
Food and Drug Administration, 136 bluetongue virus disease, 125; brucel-
food poisoning. See foodborne illnesses; losis, 28; E. coli, 108; listeriosis/Listeria,
specific illnesses 106; Mycobacterium bovis, 42– 43;
food processing. See advanced meat pest-des-petits virus, 51; Q fever, 28 –29;
recovery systems; agribusiness; fish: fish rabies, 95; tuberculosis, 42– 43
farming and influenza gorillas, 21
foodborne illnesses, 97–111. See also Gottlieb, Norman, 87
agribusiness; contaminated water; fecal grains/grasses/cereals, 34, 48
contamination; raw and undercooked Great Pestilence. See plague: epidemics/
food, dangers of; specific illnesses pandemics
forestation changes and infection transmis- Guillain-Barré syndrome, 86, 106
sion, 34, 130 –132 guinea pigs, 87, 89, 137
fowl plague. See bird flu
foxes, 25, 35, 79, 92, 94, 113, 137 hair, as a source of infection, 28
fruits and vegetables: in the human and hamsters, 89–90, 96, 111, 137
animal diet, 23–24, 34; as a source of hantavirus infections, 1, 7, 66 – 67, 89
foodborne illness, 84, 97–98, 103, 105, hay fever, 77
108, 113 heart infections/disease: absence of, in
fungi, 2, 12 early humans, 24 –25; benefits of pet
ownership, 76; treatment of, through
Gambian pouch rats, 92, 95–96 xenotransplant, 129–130; causes: cat
gastric ulcers, 8, 106 scratch disease, 82; Chlamydia pneumo-
gastroenteritis, 125 nia, 133; Chlamydia psittaci, 88; dog
geese. See chickens and other poultry and cat bites, 78; E. coli, 107; Lyme
genes: genetic mapping, 11; genetic pre- disease, 132–133; Q fever, 28 –29;
disposition, 8 –9, 40, 86, 109; genetic salmonella, 100; Toxoplasma gondii, 85;
protection, 8 –9, 21–22; malaria, 8; Trichinella spiralis, 27
peptic ulcers, 40; phylogenetic trees, heart worm (Dirofilaria immitis), 79
13; rheumatoid arthritis, 86. See also heirloom infections: commensals, 15, 66;
genome, human/nonhuman; muta- defined, 6f, 7, 11, 14 –15; endogenous
tions, genetic retroviruses, 21–22; Helicobacter pylori,
genetic drift /shift, 115–116, 120 –121 40; salmonella, 14; yellow fever, 14, 20,
genital infections, 16, 17–18t 22, 57. See also hepatitis; herpesviruses;
genome, human/nonhuman, 3– 4, 21–22, malaria
39, 115, 130 Helicobacter pylori, 8, 40 – 41, 106, 133
geographic distribution of infection, 81, 84 helminths, 2, 12
Gerberding, Julie, 12 hemolytic uremic syndrome, 91, 99, 107
gerbils, 59, 89, 96, 137 hepadnaviruses, 19
germ warfare. See bioterrorism/ biowarfare hepatitis: from acquired toxoplasmosis, 85;
German measles (rubella), 52, 81 as an heirloom infection, 6f, 14, 18,
giardiasis/Giardia lamblia, 79, 88 22, 57; effects of human migration, 57;
Gibbon, Edward, 142 hepatitis A, 6f, 18, 22, 98; hepatitis B,
glanders, 27, 29, 30 –32, 58, 97, 130 6f, 9, 14, 18 –19, 22, 129, 133; hepatitis
Global Outbreak Alert and Response C, 18, 129, 130; hepatitis D, 9
Network, 134 herpesviruses: animals infected with,
182 = Index
15–16, 17–18t, 130; as heirloom infec- human genome. See genome, human/non-
tions, 6f, 14, 15–16, 18, 22; as latent human
infections, 16; common characteristics, human papilloma viruses, 133
16; evolution of, 15–16, 18; herpes humans: as farmers, 33–39, 139; as hunt-
families, 15–16, 17–18t; illnesses ers, 23–27, 48, 139; as migrants, 33,
caused by, 14, 16 –18, 17–18t, 81, 125; 48, 56 –57, 59, 64, 66, 81; in cave art,
in immunocompromised individuals, 26 –27; Neolithic population, 33; as
17–18t, 18, 22; proposed relationship to carriers of infection, 98, 104. See also
multiple sclerosis, 81; risks of xenotrans- transmission of infection (types of ):
plants, 130; symptoms, 14, 16, 17–18t; human-to-animal, human-to-human
transmission, 6f, 16, 18; specific viruses, hydrocephaly, 85
16, 17–18t, 22, 130
Herv-K, Herv-W, 21. See also endogenous iguanas and salmonella infection, 93–94
retroviruses immigration restrictions, 64 – 65
hides, animal. See skins, animal immune system and infectious disease:
Hippocrates, 28, 141 immune system abnormalities, 86;
history, effects of infectious disease on, 20, population density, 50; specific diseases:
29, 140 –144. See also under malaria; AIDS/HIV, 9, 15, 47, 85; measles, 51,
measles; plague; smallpox; tuberculosis 53, 55; plague, 44; yellow fever, 20
HIV infection. See AIDS/HIV infection; immunizations. See vaccinations
endogenous retroviruses immunocompromised individuals:
hominids: contact with animals, 23–24, infections at risk for: bordetellosis, 78;
25, 38; diet, 23–24; evolution, 3, cryptosporidiosis, 78; cytomegalovirus,
14 –15, 22, 24 –25, 129; infection trans- 17–18t; Kaposi’s sarcoma, 17–18t, 18,
mission, 6f, 7, 11, 14 –15, 22, 50, 129; 22; leishmaniasis, 79; listeriosis, 106;
infectious diseases, 19–20, 40; migra- salmonella, 93–94; toxoplasmosis, 85;
tion, 33, 56; population growth, 33 weakening agents: AIDS/HIV, 9, 15, 18,
Homo sapiens: brain development, 25; diet, 22, 47, 78, 79, 85; concurrent illnesses,
24; evolution and infectious diseases, 51, 52, 54; famine, 142; plague, 44
3, 7– 8, 14, 18, 19, 124; migration, 33. immunoproliferative small intestine
See also humans: as farmers; humans: disease, 107
as hunters imports: exotic pets, 93, 95–96, 123;
hookworm, 78 –79 foodstuffs, 98, 105. See also trade and
horses: as food, 25–26, 37; as transporta- infection transmission
tion, 29, 37, 57, 139; domestication, Indians: Latin American, 41, 53; North
37–38, 57, 144; in ancient art, 26, 139; American, 25, 41, 53–54, 92, 119
in warfare, 57; infection transmission to industrial revolution, 45
humans, 11, 87; infections transmitted infection rates. See specific diseases
from humans, 10; infectious diseases/ infection transmission. See transmission of
microbes: bordetellosis/Bordetella, 41; infection
Chlamydia pneumonia, 133; corona- infections, latent. See latent infections
viruses, 113; Eastern equine encepha- influenza: as a deadly disease, 9, 53–54,
litis, 1; farcy, 29; glanders, 29, 30 –32; 59, 117–120, 140; as an ancient disease
Helicobacter pylori, 40; herpesviruses, in aquatic birds, 114; as a relatively
17–18t; influenza, 121; nipah virus, 41; recent disease in humans, 114; carri-
rhinoviruses, 50; trichinosis/Trichinella ers, 88, 92, 114 –117; concurrent with
spiralis, 27; trypanosomiasis, 8 measles, 53–54; epidemics/pandemics,
household crowding. See crowded living 58, 113, 114, 116 –121; evolution, 41,
conditions 114 –117; in literature, 120; masks as
HTLV viruses, 21–22, 126. See also endog- prophylactics, 112–113, 119; molecular
enous retroviruses studies, 114; mutations, 115–116; pro-
human-animal relationship. See animal- posed relationship to multiple sclerosis,
human relationship 81; transmission, 6f, 7, 10. See also bird
Index = 183
flu; fish: fish farming and influenza; live animal markets, 113, 123
genetic drift /shift liver disease, 18 –19, 79, 80, 82, 85, 88
inhalation. See airborne transmission of “Lucy,” 23
infection lung disease, 67, 79, 80, 82, 107. See also
insects: as food, 23; as vectors, 6f, 7, 84, pneumonia; tuberculosis
124. See also cockroaches; fleas; flies; lupus, 22
mosquitoes; ticks Lyme disease: infection rates, 1, 132;
Institute of Medicine, 12, 79, 130, 134, symptoms, 132; transmission, 1, 6f, 7,
135, 136 80, 82, 131–133
International Society for Infectious Dis- lymph nodes, enlarged, 29, 44, 60, 63
ease, 134 lymphocytic choriomeningitis (LCM),
intestinal disorders, 89, 98, 107. See also 89–90
foodborne illnesses lymphoma, 17–18t, 90, 107, 133
intestinal microbes, 3, 4, 15
intestinal worms. See parasites macroparasites, 2, 27–28, 97
iridovirus, 125 mad cow disease. See bovine spongiform
Islamic medicine, 52 encephalopathy
malaria: affected animals, 19–20; as a
Johnson-Reed Act, 65 contemporary zoonosis, 20; as an
joint disease, 88, 89. See also arthritis; heirloom infection, 6f, 14, 19–20, 22,
osteoarthritis; rheumatoid arthritis 57; concurrent with other diseases, 20;
effects of global warming, 131; effects
Kaposi’s sarcoma, 17–18t, 18, 22. See also of human migration, 57; effects on
AIDS/HIV infection history, 19, 20, 140, 141; evolution,
Karlen, Arno, 5, 48, 49, 53, 141 19–20; genetic protection against, 8;
Kete, Kathleen, 71 mortality rates, 19; mosquito control,
kidney disease, 20, 88, 100, 129. See also he- 20; Plasmodium protozoa, 8, 19–20;
molytic uremic syndrome; Weil’s disease similarity to other diseases, 79; species,
Klein, Richard, 25 19–20; symptoms, 19; transmission, 6f,
Korean hemorrhagic fever, 66 10, 19–20, 129
Krause, Richard, 13 malignant catarrhal fever, 125
kuru, 109 Mallon, Mary (“Typhoid Mary”), 99
Kyasanur Forest Disease, 125 malnutrition and infectious disease, 51, 52,
54, 130
laryngotracheitis virus, 17–18t mammals: evolution, 2, 14, 15–16;
Lassa fever virus, 89, 129, 130, 138 herpesviruses, 15–16; listeriosis, 106;
latent infections: bovine spongiform en- number of species, 2, 133; transmission
cephalopathy, 109, 110; herpesviruses, of infections, 10
16; measles encephalitis, 51; multiple Marek’s disease virus, 17–18t
sclerosis, 81, 82; prions, 109, 110; psit- marijuana as a source of Salmonella, 105
tacosis, 88; toxoplasmosis, 85 marmots and plague, 59, 64
LCM (lymphocytic choriomeningitis), masks as prophylactics, 112–113, 119
89–90 McGeoch, Duncan J., 17–18t
leishmaniasis, 8, 79, 131 McMichael, Tony, 24
leprosy, 140 McNeil, William, 53, 77, 143
leptospirosis, 79– 80, 92 measles: as a benign infection, 51; as a
leukemia, 21, 133 cause of brain damage/infection, 51; as
listeriosis/Listeria, 92, 99, 105–106, 111 a childhood disease, 51, 55; as a deadly
literature: biblical plagues, 58; cats, 71–72; disease, 29, 51, 52–55; cattle-to-human
cholera, 4; dogs, 36, 70; influenza, 120; transmission, 6f, 7, 11, 50 –52; concur-
plague, 4, 58, 62, 63– 64, 65; rats, 60 – rent with other illnesses, 51, 52–54, 55;
61; sheep, 41; tuberculosis/consump- during the Civil War, 29, 55; effects
tion, 4, 44, 45– 47; typhoid fever, 4 of human migration, 57; effects on
184 = Index
history, 53, 140, 141–143; effects on E. coli, 107; Helicobacter pylori, 40;
the immune system, 51, 52, 53, 55; Listeria, 106; Mycobacteria, 43; Salmo-
epidemics, 53–55, 58, 141, 142, 143; nella, 105; Toxoplasma gondii, 84; other
evolution, 51–52; human-to-human microbes, 39, 97
transmission, 6f, 7, 51, 55; human-to- minks, 11, 111
primate transmission, 10; in the ancient miscarriages. See abortions, spontaneous
world, 52; infection rates, 51; measles (miscarriages)
encephalitis as a latent infection, 51; molecular clocks, 13
minimum population requirement for molecular studies: employed in autopsies,
transmission, 51, 52; molecular studies, 136 –137; future studies, 133; infectious
51; proposed relationship to multiple diseases/microbes: AIDS/HIV, 126; bird
sclerosis, 81– 82; relationship to rinder- flu/influenza, 114; measles, 51; Myco-
pest virus, 51–52; similarity to other bacteria, 42– 43; plague/Yersinia pestis,
diseases, 52; vaccine, 51 59; rabies, 95; SARS, 113; smallpox, 42
meat: in the human diet, 23–27; in the monkeypox virus, 1, 42, 95–96, 134, 136
primate diet, 23; as cattle feed, 110; monkeys: as early xenotransplant donors,
as a source of infection, 6f, 28, 39, 43, 129; as meat, 23, 126; as pets, 38, 137;
97–98, 106. See also advanced meat evolution, 21; monkey bites, 16, 126;
recovery systems; agribusiness; beef and infectious diseases/microbes: AIDS/HIV,
foodborne illnesses; bovine spongiform 125–126; endogenous retroviruses,
encephalopathy; contaminated food; 21–22; hepatitis B, 19; herpesviruses,
raw and undercooked food, dangers of; 16, 17–18t; influenza, 121; intestinal
specific animals protozoa, 15; Kyasanur Forest Dis-
mechanization of the food industry. See ad- ease, 125; SARS, 113; simian viruses,
vanced meat recovery systems; agribusi- 125–126; Trichomonas vaginalis, 15;
ness; fish: fish farming and influenza tuberculosis, 43; yellow fever, 20
Mediterranean fever, 28 mononucleosis, 16, 17–18t
Mediterranean fruit fly, 103 Morbidity and Mortality Weekly Reports,
meningiomas, 86 135
meningitis, 10, 78, 89, 106, 132 morbillivirus, 51
mental retardation, 51, 85, 86 mortality rates: effects of malnutrition, 51,
mice: as carriers of disease, 49; as pets, 87, 52, 54; effects of poverty, 54. See also
89, 137; evolution, 58 –59; migration, specific diseases
66; infectious diseases/microbes: corona- mosquitoes: as vectors, 6f, 7, 39, 49;
viruses, 113; cytomegalovirus, 17–18t; research on and control of, 20, 136;
hantavirus, 1, 7, 66 – 67, 89; hepatitis, transmitted infections/microbes: Eastern
9; herpesvirus, 17–18t; lymphocytic equine encephalitis, 1; heart worm (Di-
choriomeningitis, 89; prion diseases, rofilaria immitis), 79; malaria, 14, 19,
111; retroviruses, 22; salmonellosis/ 20; West Nile virus, 1, 6f, 7, 127–128;
Salmonella, 104; SARS, 113; toxoplas- yellow fever, 14, 20
mosis/Toxoplasma gondii, 85– 86. See mules. See horses
also rodents multiple sclerosis, 22, 80 – 82
microcephaly, 85 mummies, 43, 50
microorganisms (defined), 2 Murphy, Frederick, 136
migration: human, 33, 48, 56 –57, 59, Muslim medicine, 52
64, 66, 81; nonhuman, 10, 35, 48, 50, mutations, genetic: brain development,
56 –57 (see also under birds; ducks; 25; defined, 3– 4, 7; effects of agribusi-
mice; rats) ness, 112; mutation rate of RNA viruses,
milk: animal sources, 36, 37, 39, 40, 43, 12; selective breeding, 70; specific
52; beneficial effects against childhood infections: AIDS/HIV, 6f, 127; bird flu,
allergies, 77; human-animal intimacy, 122, 123; feline panleukopenia virus to
37, 39, 52; microbes carried by milk: parvovirus, 11; influenza, 115; malaria,
brucellosis, 28; Campylobacter, 107; 20; measles, 6f; plague/Yersinia pestis,
Index = 185
59, 66; rhinoviruses, 50; SARS, 114; parainfluenza, 81
typhoid fever, 6f; yellow fever, 20. See parakeets, 87, 88, 125
also genetic drift /shift paramyxovirus, 88, 130
mycarditis, 85 parasites, 4, 98, 138. See also macropara-
Mycobacteria, 8, 42– 43, 47, 87 sites; malaria: species
parrot fever (psittacosis/Chlamydia psit-
National Electronic Disease Surveillance taci), 88 – 89
System (NEDSS), 135 peptic ulcers, 40
National Institute of Allergy and Infectious peritonitis, 40
Diseases (NIAID), 13, 137 pertussis (whooping cough), 41, 78, 140,
National Institutes of Health (NIH), 136, 143
137 pest-des-petits virus, 51
Native Americans. See Indians; Indians: pestilence. See plague
North American pet keeping: among royalty/aristocracy, 69–
natural disasters, effects of, 140, 142, 143 70; benefits, 74, 75–77; cancer in pets
Neanderthals, 24 and owners, 133; companion animals
needles. See syringes, unsterile and air travel, 74, 128; contaminated
Neolithic revolution: climate, 33–34; pet food, 110, 111; history of pet keep-
development of agriculture, 33–34, ing, 68 –72; increasing owner-pet inti-
48; dissemination of microbes, 39; macy, 73–75, 76, 77, 88; increasing pet
domestication of animals, 33, 35–39, ownership, 72–73; legislation regard-
48; human migration, 33; urbanization, ing, 74 –75; pet specialty items, 73–74,
48 – 49, 56, 66 92; pet stores, 138; pet travel, 73–74;
neurological symptoms/disorders, 21, 81, relationship to rheumatoid arthritis, 87;
85– 86, 89, 106, 127 relative risks of infection, 87–90, 137;
newborns: bacteria in, 3; infections statistics on current practices, 72–74;
at risk for: congenital toxoplasmosis, veterinary expenses, 74. See also exotic
85; hepatitis B, 19; herpesviruses, animals; specific animals
17–18t; listeriosis, 106; lymphocytic petting zoos, 90 –91
choriomeningitis, 90; salmonella, phocine distemper virus, 10, 51
93, 100 phylogenetic trees, 13
Newcastle disease, 88 pigs: as a valuable commodity, 37–38,
nipah virus, 41 39, 144; as animal feed, 110; as organ
Norwalk viruses, 98, 105–106 donors, 129–130; contaminated feed
nutrition. See malnutrition and infectious for, 110, 116; diet of, 35, 37; domestica-
disease tion, 37–38, 39, 52; feces of, as animal
nuts, 23 food, 116; feces of, as fertilizer, 115,
116; feral pigs, 90; fish farming, 114,
ocular larva migrans, 80 115–116; in ancient art, 139; infec-
Office International des Epizooties (OIE), tion transmission to humans, 11, 87;
134 religious dietary taboos against, 37;
Olson, Steve, 34 infectious diseases/microbes: African
organ/tissue transplants, 74, 91, 109. See swine fever, 125; bordetellosis/Borde-
also xenotransplants tella, 41; circovirus, 130; coronaviruses,
orthopoxvirus, 42, 95 113, 125; E. coli, 108; endogenous
osteoarthritis, 87 retroviruses, 130; gastroenteritis, 125;
osteomyelitis, 94, 100 Helicobacter pylori, 40; hepatitis, 130;
otters, 10 herpesviruses, 125, 130; influenza, 41,
114 –116, 120 –121; malignant catarrhal
Paleolithic period, 24 –28, 29, 38, 48, fever, 125; Mycobacterium bovis, 42;
68 – 69, 97 nipah virus, 41; paramyxovirus, 130;
palm civets, 1, 8, 113 Taenia, 27; torovirus, 130; toxoplasmo-
pandemics. See epidemics/pandemics sis/Toxoplasma gondii, 85; trichino-
186 = Index
sis/Trichinella spiralis, 27; whooping retroviruses, 21–22, 125; Helicobacter
cough (pertussis), 41. See also pork pylori, 40; hepadnaviruses, 19; hepatitis,
pituitary growth hormone, 109 18, 19; malaria, 19–20. See also specific
plague (Yersinia pestis): as a cause of primates
anti-immigrant sentiment, 62, 64 – 65; prion disease, 2, 7, 109–111
carriers/vectors, 7, 58 – 66, 82– 83, 89, ProMED (Program for Monitoring Emerg-
142; concurrent with other diseases, ing Diseases), 134
44, 63; control through antibiotics, 65, protein, dietary, 24, 37, 68, 110, 111
66; control through rat catchers, 61; proteins, prions as variant, 109
earliest cases, 60; effects on history, 63, proteins, viral, 3, 21, 114, 115
141–142, 143; effects on the immune protozoa: as ancient microbes, 4, 14 –15,
system, 44; epidemics/pandemics, 39, 124; as microparasites, 2, 4; concur-
58, 59, 60 – 65; evolution, 59; future rent infections, 9; nucleic acid sequenc-
concerns, 65– 66, 99; in literature, 4, ing, 12–13; percentage of zoonoses
58, 62, 63– 64, 65; in the U.S., 64 – 66, caused by, 12; rate of reproduction, 13;
82– 83; infection rates, 65, 83; molecu- relationship to bacteria and viruses, 4;
lar studies, 59; mortality rates, 60 – 64, self-preservation, 5; specific protozoa, 8,
83, 141–142; prophylactic measures, 10, 19–20, 78, 79, 83; transmission, 8,
64; quarantines, 63; symptoms, 60, 63 49, 57; virulence, 9
plants: as food, 23, 24, 34, 36 –37; evolu- psittacosis/Chlamydia psittaci (parrot
tion, 2; in the Fertile Crescent, 34; fever), 88 – 89
surveillance of diseases affecting, psychiatric symptoms: companion animals
135; viruses derived from, 3. See also for patients with, 75, 76 –77; in Lyme
agriculture: development of; grains/ disease, 132; in rabies, 94; in toxoplas-
grasses/cereals mosis, 85, 86
Plasmodium protozoa. See under malaria public health, development of, 63
pneumonia, 10, 29, 51, 55, 85, 88, 89, 100
polio, 10, 140, 141 Q fever, 27, 28 –29, 30, 130
population: density/size requirements for quarantines, 63, 128, 137
microbe transmission, 43, 50 –52, 131;
effects of disease on isolated popula- rabbits, 29, 41, 42, 87– 88, 96
tions, 15, 51–55, 119; statistics on rabies, 6f, 7, 11, 80, 92, 94 –95, 137
population growth/decline, 33, 44, raccoon dogs as food, 113
48 – 49, 53, 131, 134 raccoons, 11, 80, 93, 94 –95, 111
pork, 27, 37, 106. See also pigs rats: as a source of clothing, 61; as pets,
poultry. See chickens and other poultry 89, 137; evolution, 58 –59; hardiness,
poverty and infectious disease, 54 60, 65; in ancient art, 58; in literature,
prairie dogs, 1, 42, 65, 66, 93, 95–96, 138 60 – 61; migration, 59– 61; rat catchers,
pregnancy, risk of infection in, 22, 83, 61; reproduction, 60; infectious dis-
84 – 85, 90, 106, 124. See also abortions, eases/microbes: bordetellosis/Bordetella,
spontaneous (miscarriages); fetuses, 41; coronaviruses, 113; hantavirus, 66,
infections in; newborns 89; leptospirosis, 79; monkeypox virus,
prepared foods and foodborne illnesses, 96; plague/Yersinia pestis, 7, 58 – 66, 89,
98, 102, 103. See also restaurants and 142; retroviruses, 22; SARS, 113; toxo-
foodborne illnesses plasmosis/Toxoplasma gondii, 85– 86;
primates: as early organ donors in trypanosomiasis, 8. See also Gambian
xenotransplants, 129; evolution, 2–3, pouch rats; rodents
14 –15, 19, 21–22, 126; transmission raw and undercooked food, dangers of:
of infections to and from humans, 6f, eggs, 101–102, 137; fish, 98; pork, 27;
10, 11, 18; infectious diseases/microbes: poultry, 102, 107; primate meat as
AIDS/HIV, 1, 7, 125–126; bordetello- human food, 126; red meat, 27, 83– 84,
sis/Bordetella, 41; bovine spongiform 105, 107–108, 137
encephalopathy, 111; endogenous religious dietary taboos, 37, 97
Index = 187
reptiles: as pets, 72, 93–94, 137; evolution, seafood, 98, 106, 113
2, 14; infections, 14, 19, 22, 93–94, seals, 10, 51, 121
99, 133 seeds: in the human and animal diet, 23; as
restaurants and foodborne illnesses, 98, a source of Salmonella, 105
101, 102, 103 seizures, 27, 51, 85, 109. See also epilepsy
retroviruses. See endogenous retroviruses Serpell, James, 38, 69
rheumatoid arthritis, 86 – 87 severe acute respiratory syndrome. See
rhinoviruses, 50 SARS
rickettsial bacteria, 29 sexual practices, effects of changes in, 18,
rinderpest virus, 9–10, 51–52 126 –127
RNA (ribonucleic acid), 109 sexually transmitted diseases: AIDS/HIV,
RNA viruses, 3– 4, 12, 115 126 –127; as protection against plague,
rodents: as pests, 38, 68, 70; as pets, 87, 89; 64; hepatitis B, 19; herpesviruses, 16,
evolution, 58; in the laboratory, 133; 17–18t, 18; syphilis, 5; venereal diseases
transmission of infection by, 11, 131; in animals, 8, 124
infectious diseases/microbes: Argentine sheep: as a source of clothing, 25; as a
hemorrhagic fever, 131; hantavirus, 1, valuable commodity, 37–38, 39, 144;
66 – 67, 89; lymphocytic choriomenin- breeding, 38; diet of, 36 –37; domesti-
gitis (LCM), 89; malaria, 19; monkey- cation, 36 –38, 41, 144; in ancient art,
pox virus, 42, 95–96; plague/Yersinia 139; infection transmission, 11, 39, 87;
pestis, 59, 65– 66, 82– 83, 89; toxoplas- infectious diseases/microbes: anthrax,
mosis/Toxoplasma gondii, 84; typhus, 28; bluetongue virus disease, 125; bor-
89; Yersinia pseudotuberculosis, 59. See detellosis/Bordetella, 41; E. coli, 108;
also specific rodents Helicobacter pylori, 40 – 41; listeriosis/
roundworms, 80. See also trichinosis/Trich- Listeria, 106; malignant catarrhal fever,
inella spiralis 125; Mycobacterium bovis, 42; pest-des-
rubella (German measles), 52, 81 petits virus, 51; Q fever, 28, 30; scrapie,
111; toxoplasmosis/Toxoplasma gondii,
saliva, transmission of infection through, 83, 85; whooping cough (pertussis), 41
66, 94. See also animal bites shellfish. See seafood
salmonellosis/Salmonella, 14, 88, 92, Shigella, 99, 107
93–94, 99–105, 111 shingles, 17–18t
sandboxes/sandpits, 80, 83 ships and infection transmission, 57,
sandflies and leishmaniasis, 79 59– 64, 66, 142
sanitation, lack of, and infection transmis- sickle-cell disease, 8
sion, 18, 98, 102, 130, 131 simian immunodeficiency virus, 125–126
SARS: as an emerging infectious disease, Sin Nombre virus, 67
12, 134; control through slaughter, 113; skin ulcers, 28, 29
coronaviruses, 113; infection rates, 1; skins, animal, 25, 28, 37, 61
molecular studies, 113; mortality rates, sleeping sickness, 8
80, 112, 113; mutations, 114; origins, smallpox: as a microbe for bioterrorism, 41,
113; palm civets, 1, 8, 113; rats, 113; 42, 130; concurrent with measles, 53;
surveillance efforts, 134, 136; transmis- effects of human migration, 57; effects
sion, 1, 6f, 7, 8, 113–114, 128 on history, 41, 53, 141–143; in the
scarlet fever, 52 ancient world, 52, 58; origins, 41– 42;
schistosomiasis, 131, 140, 141 similarity to other diseases, 52, 95;
schizophrenia: benefits of pet ownership in transmission, 50
childhood schizophrenia, 76 –77; rela- socioeconomic status and infectious
tionship to endogenous retroviruses, 22; disease, 54
relationship to Toxoplasma gondii, 86 spices and foodborne illnesses, 105
scrapie, 111 spongiform encephalopathies, 109
scrofula, 44, 45 spores. See anthrax
sea otters, 10 squirrels, 19, 29, 65, 66, 96, 137
188 = Index
staphylococcus, 10, 14 transport): blood exchange during
Stewart, William H., 124 childbirth, 19; close contact, 29, 39,
stillbirths, 85, 106 43; contaminated bodily fluids, 39, 66,
streptomycin, 47 79, 89, 94, 113; oral contact, 16, 129;
surveillance of emerging infectious dis- organ/tissue transplants, 109; sexual
eases. See emerging infectious diseases: contact, 129; touch, 114. See also
surveillance efforts airborne transmission of infection;
sushi/sashimi, 98 animal bites; blood transfusions;
Swabe, Joanna, 39, 69, 70 contaminated food; contaminated
sweat, transmission of infection through, water; fecal contamination; fleas; flies;
113 mosquitoes; sexually transmitted dis-
syphilis, 5 eases; syringes, unsterile; ticks; vectors;
syringes, unsterile, 19, 126, 127, 129 xenotransplants
transmission of infection (types of ), 6f,
T-cell lymphotropic virus (PTLV-1), 126 7, 27; animal-to-animal, 11, 16, 90,
Taenia, 27, 97 109–110, 111, 116; animal-to-human,
tapeworm, 2, 79. See also Taenia 11–12; human-to-animal, 10, 18, 19,
technological changes and infection trans- 43, 104; human-to-human: AIDS/
mission, 127–130 HIV, 6f, 7; bird flu, 122; Chlamydia
Thomas, Keith, 39, 52 pneumonia, 133; Chlamydia psittaci,
Thomas, Lewis, 3– 4 88; Creutzfeld-Jakob disease, 109;
ticks: as vectors, 7, 39; transmitted infec- Helicobacter pylori, 40; hepatitis A, 6f,
tions: Lyme disease, 1, 7, 78, 80, 82, 18; hepatitis B, 6f, 19; herpesviruses, 6f;
131–132; tularemia, 29 human rhinoviruses, 50; influenza, 6f,
tissue/organ transplants, 74, 91, 109. See 7; kuru, 109; leishmaniasis, 79; malaria,
also xenotransplants 6f; measles, 6f, 7, 50 –51, 55; Norwalk
tools: from animal bones, 25, 36; from viruses, 106; prions, 109; SARS, 6f, 7,
stone/metal, 24, 34 8, 113, 128; tuberculosis, 42; typhoid
torovirus, 130 fever, 6f, 7, 99; urban yellow fever,
toxocariasis/Toxocari, 80 20; West Nile virus, 127–128. See also
toxoplasmosis/Toxoplasma gondii, 10, cross-species transmission of infection;
83– 86, 105 mutations, genetic
trade and infection transmission, 56 –57, transmission of infection (vulnerable
59– 61, 142 populations): the elderly, 100, 106;
transmission of infection (factors influenc- fetuses, 17–18t, 83, 84 – 85, 111. See
ing): air travel, 113–114, 127, 128 –129; also children; immunocompromised
changes in forestation, 130 –132; individuals; newborns
changing dietary patterns, 98; closeness transplants, organ/tissue, 74, 91, 109. See
of animal species/order, 10; global also xenotransplants
warming, 130, 131; increasing intimacy transportation, 37, 38, 57, 68, 140, 144.
between animals and humans, 77; See also migration; ships and infection
lack of sunlight, 49; malnutrition, 51, transmission
52, 54, 130; poor air circulation, 49; Transportation Department, 74
poor refrigeration, 104; population trichinosis/Trichinella spiralis, 27, 97
size, 50 –52; trade, 56 –57, 59– 61, 142; Trichomonas vaginalis, 15
unsanitary conditions, 18, 98, 102, 130, trypanosomiasis, 8
131. See also agribusiness; bioterror- tuberculosis: among royalty, 44; among
ism/ biowarfare; crowded living condi- writers and artists, 45– 47; causes,
tions; fish: fish farming and influenza; 42– 43; concurrent with other illnesses,
migration; mutations, genetic; sexual 47, 51; drug-resistant strains, 47; dur-
practices, effects of changes in; urban- ing the Civil War, 29; early cases, 43;
ization and infection transmission effects of human migration, 57; effects
transmission of infection (modes of on history, 44, 141, 143–144; efforts
Index = 189
to eradicate, 47; genetic predisposi- 3– 4, 12; SARS, 112. See also endog-
tion, 8; in animals, 43, 92; in literature enous retroviruses; specific viruses
(consumption), 4, 44, 45– 47; infection visceral larva migrans, 80
rates, 8, 44, 45, 47; mortality rates, 42, voles, 66
44 – 45; Mycobacteria, 42– 43; roman-
ticization of, 45– 46; scrofula, 44, 45; warfare and infection transmission, 56 –57,
symptoms, 44; transmission, 10, 42– 43, 126, 140, 141, 142–143. See also bioter-
44, 45, 50, 57 rorism/ biowarfare; Civil War, U.S.;
tularemia, 27, 29, 30, 87– 88, 95, 97, 130 Cold War bioterrorism; World War I
tumors. See cancer water, contaminated. See contaminated
turkeys. See chickens and other poultry water
typhoid fever, 4, 6f, 7, 29, 51, 58, 59, 99 water buffalo, 38, 42, 139
typhus, 58, 63, 89, 140 Webster, Joanne, 86
Webster, Robert, 114
ulcers. See farcy; gastric ulcers; peptic Weil’s disease, 80
ulcers; skin ulcers West Nile virus: as an emerging infectious
undercooked food. See raw and under- disease, 1, 134; effects of air travel, 128;
cooked food, dangers of infection rates, 128; mortality rates,
undulant fever. See brucellosis 127, 128; origins, 127; surveillance
University of Edinburgh study, 11–12 efforts, 135–136; symptoms, 127; trans-
urban yellow fever, 20 mission, 1, 6f, 7, 127–128
urbanization and infection transmission, wet markets and infection transmission,
45, 49–50, 52, 56, 126, 130 –131, 144 113, 123. See also specific animals sold
urine, transmission of infection through, whooping cough (pertussis), 41, 78, 140,
66, 79, 89, 113 143
wolves, 35–36, 70, 79, 132
vaccinations, 13, 41, 42, 51, 80, 115–116, woodchucks, 19, 94
120, 137 World Aquaculture Society, 115
vaccinia virus, 42 World Health Organization (WHO), 112,
varicella-zoster virus, 16, 17–18t 129, 134
vectors, 6f, 7, 49. See also fleas; flies; mos- World Organization for Animal Health, 134
quitoes; ticks World War I, 30 –31, 117–118
vegetables. See fruits and vegetables worms, 98. See also hookworm; parasites;
venereal diseases. See sexually transmitted roundworms; tapeworm
diseases
venison, 111 xenotransplants, 129–130
vertebrate evolution, 16
Vibrio, 99 yellow fever, 14, 20, 22, 57, 131, 140
viral hemorrhagic fevers, 89 Yersin, Alexandre, 64
virulence, 8, 9, 53 Yersinia pestis. See plague
viruses: as ancient microbes, 4, 14 –16, 39, Yersinia pseudotuberculosis, 59
124; as microparasites, 2; defined, 3;
integration into the human genome, Zeuner, Frederick, 37
3– 4; nucleic acid sequencing, 12–13; Zinsser, Hans, 5, 59, 130, 142, 143
number of species, 3, 133; percentage zoonoses: defined, 1; effects of urbaniza-
of zoonoses caused by, 12; rate of repro- tion, 131; heirloom infections as
duction, 13; recent outbreaks, 124 –125; contemporary zoonoses, 20; increasing
relationship to bacteria and protozoa, incidence, 1–2; pets that are relatively
3– 4; self-preservation, 5; transmission, zoonosis-free, 87– 88; significance of
8, 49, 57; virulence, 9; viral mutations: zoonoses in human infections, 11–12;
AIDS, 127; bird flu, 112, 122; feline surveillance of emerging zoonoses,
panleukopenia virus, 11; influenza, 12–13. See also emerging infectious
112, 115–116; rhinoviruses, 50; RNA, diseases: surveillance efforts
About the Authors
E. Fuller Torrey, M.D., is a psychiatrist in Bethesda, Maryland. He is as-
sociate director for Laboratory Research at the Stanley Medical Research In-
stitute, professor of psychiatry at the Uniformed Services University of the
Health Sciences, and president of the Treatment Advocacy Center. His re-
search focuses on infectious agents as possible causes of schizophrenia and
bipolar disorder. He is the author of eighteen books, including The Roots of
Treason, which was nominated by the National Book Critics Circle as one of
1983’s five best biographies.
Robert H. Yolken, M.D., is a pediatrician and a specialist in infectious dis-

eases in Baltimore, Maryland. He is the director of the Stanley Laboratory of
Developmental Neurovirology and the Ted and Vada Stanley Distinguished
Professor of Pediatrics at the Johns Hopkins University Medical Center. He
has authored over three hundred professional papers and book chapters, is an
editor of the Manual of Clinical Microbiology, and has received numerous
awards for his research on infectious diseases. He owns two cats.
= 191

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= Beasts OF THE Earth

ALSO BY E. FULLER TORREY

Surviving Manic-Depression (2002, senior author)

Animals, Humans, and Disease

E. Fuller Torrey, M.D.

Rutgers University Press

Torrey, E. Fuller (Edwin Fuller), 1937–

Copyright © 2005 by E. Fuller Torrey, M.D., and Robert H. Yolken, M.D.

All rights reserved

Design by John Romer

Manufactured in the United States of America

the relationship between animals and humans is changing in important ways.

The Smallest Passengers

Jonathan Swift, 1733

increasing incidence of animal-associated human diseases? As we shall see,

Where Do Microbes Come From?

appeared 60 million years ago; when hominids separated from primates

How Microbes Get Ahead in Life

Figure 1-1: Types of Animal-to-Human Transmission of Microbes

Many of the genes that predispose or protect an individual in encounters

How Many Human Infections

researchers to create phylogenetic trees for microbes, arranging the microbes’

Rene Dubos, Mirage of Health

Herpes and Hepatitis Viruses

in turn further divided, so that, for example, approximately 8 million years

Table 2.1. Herpesviruses of Humans and Other Animals

Table 2.1. (continued)

Malaria and Yellow Fever

Juliet Clutton-Brock, Domestic Animals from Early Times

By the late Paleolithic period, humans had become highly dependent

the plains, became the Paleolithic equivalent of a McDonald’s golden arch.

Taenia and Trichinosis

Numerous other macroparasites are known, but most are of little or

Anthrax, Brucellosis, and Q Fever

Tularemia and Glanders

Paleolithic Microbes in the Modern Age

The use of glanders in germ warfare was probably tested in extensive

Arno Karlen, Man and Microbes

culture as the glaciers started to recede approximately ﬁfteen thousand years

to this scenario, wolves began hanging around human campsites to scavenge

referred to as the “Big Five” 24—was an enormous advantage for Neolithic

Enter the Microbes

Following domestication, therefore, animals not only entered the home

Ulcers, Whooping Cough, and Smallpox

it is a member of the orthopoxvirus family. This family includes the monkey-

The King’s Evil

One manifestation of tuberculosis is enlargement of lymph glands in the

Strangely visited people,

resistance to infections. It was a chaotic century, both socially and politically,

“Blood Was Its Avatar”

One year later, Keats died at the age of twenty-ﬁve.

Lewis Thomas, The Lives of a Cell

P aleolithic hunters were remarkably isolated. For hundreds of thousands

from animals to humans but is instead transmitted exclusively from humans

after the domestication of cattle. Rinderpest is endemic in cattle and, when