E m e r g i n g D i s e a s e s o f Avi a n

Wildlife
a, b
Susan J. Tyson-Pello, VMD, MS *, Glenn H. Olsen, DVM, MS, PhD

KEYWORDS

Emerging diseases of avian wildlife
Tick-associated diseases
West Nile virus

Lymphoproliferative disease virus
Wellfleet Bay virus
Avian influenza

Salmonella

KEY POINTS

Avian wildlife diseases include Haemaphysalis longicornis, West Nile virus, lymphoprolifer-
ative disease virus, Wellfleet Bay virus, avian influenza, and salmonellosis.

Previously documented avian wildlife diseases have taken a new focus with more affected
species and changes in preventive medicine.

Geographic region and climate change can influence new and existing avian wildlife
diseases.

HAEMAPHYSALIS LONGICORNIS

Neotropical migratory birds have been implicated in the importation of exotic neotrop-
ical ticks to the United States.1The geographic range of ticks such as Ixodes scapularis
has been expanded by migratory birds, with climate change driving the dispersion and
the growth of more suitable climates because of global warming.1 Haemaphysalis
longicornis, the longhorned tick originally native to Asia, was introduced and quickly
established in the eastern United States. The longhorned tick was originally discov-
ered in New Jersey in 2017; however, during importation inspection and quarantine
of horses, the tick was noted in 6 cases over the last 30 years by the US Department
of Agriculture.1 The longhorn tick population in the United States is parthenogenetic,
with the female able to reproduce asexually. Multiple life stages coexist on a wide
range of wild and domestic species (it is also referred to as the 3-host tick) so, along
with the longhorned tick being parthenogenic, controlling the population is difficult.
The longhorn tick has a broad zoophilic host range, including birds, rodents, ungu-
lates, lagomorphs, carnivores, and humans. This broad range of hosts results in rapid
geographic dispersion.2–4 Ticks found in avian wildlife include the longhorn tick, Argas
species, including Argas giganteus; Ixodes scapularis; Ixodes brunneus; Argas

a
Mount Laurel Animal Hospital, 220 Mount Laurel Road, Mount Laurel, NJ 08054, USA; b USGS
Patuxent Wildlife Research Center, 12302 Beech Forest Road, Laurel, MD 20708, USA
* Corresponding author.
E-mail address: [email protected]

Vet Clin Exot Anim 23 (2020) 383–395

https://doi.org/10.1016/j.cvex.2020.01.002 vetexotic.theclinics.com
1094-9194/20/ª 2020 Elsevier Inc. All rights reserved.
384 Tyson-Pello & Olsen

americanum; and Haemaphysalis cordeilis. They are found cofeeding, resulting in co-
infection and pathogen acquisition.1,4
The longhorn tick is the vector for multiple pathogens, including Anaplasma, Coxiella
burnetii, Rickettsia japonica, Theileria mutans, and Theileria orientialis. The most com-
mon tick-associated disease is tick paralysis.5 Ticks can be found primarily on the
feet, legs, keel, and inguinal regions.1 Edema, ecchymoses, and petechiae can be
found at the attachment sites, and infested birds may show sternal recumbency, poly-
neuropathy, distal to proximal ascending paralysis, anemia, dehydration, respiratory
distress, lethargy, ataxia, difficulty swallowing, and death.1,3,6 The longhorned tick
can be found in heavy infestations on multiple hosts and poses agronomic threat for
livestock producers, horses, and humans. With the current state of the environment,
global warming, and the expansion of neotropical species, expansion of this species
and possibly translocation of other species into new geographic locations are
expected.

WEST NILE VIRUS IN AVIAN WILDLIFE

In a recent retrospective study of raptor mortality in Ontario, Canada, West Nile vi-
rus (WNV) was found to be the most commonly diagnosed infectious disease
among raptor species from 1991 to 2014.7 WNV is an arthropod-borne, single-
stranded RNA virus within the genus Flavivirus, family Flaviviridae, which contains
more than 90 viruses.8,9 The first domestic avian deaths were described in 1997 in
Israel and involved hundreds of young geese (Anser anser).9 In 1999, WNV emerged
on the east coast of the United States, migrated to the west coast by 2003, and is
now considered enzootic.10 Up to 9 distinct lineages of WNV have been found with
molecular phylogenic analysis, with lineages 1 and 2 being grossly distributed
worldwide.9 Lineage 1 viruses are especially virulent to native North American avian
species, causing high mortality in corvids. The route that WNV entered the western
hemisphere is still unknown.11 Lineage 2 viruses were restricted to sub-Saharan Af-
rica and Madagascar but have been isolated in Europe.9,12,13 Lineage 2 spread
resulted in 115 human deaths in 2018 in Europe.9 Despite genomic variability
and the discovery of 9 distinct lineages, only 1 WNV serotype has been described
that would allow the development of vaccines to protect against all WNV
genotypes.9
WNV continues to emerge as vectors move into new geographic regions and un-
documented locations because of climate change.14,15 To date, WNV has been
detected in more than 300 avian species,14 and more than 40 mosquito species are
considered vectors.16
Domestic and wild avian species are the primary amplifying hosts of WNV, and more
than 300 avian species have shown susceptibility.8 WNV also infects more than 30
vertebrate species, including marine mammals, rodents, bats, horses, camelids, ca-
nids, felids, and reptiles.11,12,17 The most common form of transmission is mosquito
borne, Culex spp; however, other vectors have been implicated. Alternate routes of
infection include horizontal transmission among corvids, ingestion of WNV-infected
organs, and blood contamination of wounds. Bird-to-bird transmission has been
confirmed by detection of viremia in magpies.15
Birds are the natural reservoir hosts of WNV; however, species susceptibility,
morbidity, and mortality vary. Species in the order Columbiformes and Galliformes
show low viremia, although other species in the orders Passeriformes, Charadrii-
formes, and Strigiformes show high viremia without clinical disease, making them
more effective competent viral reservoirs for WNV transmission.9,11
 Emerging Diseases of Avian Wildlife 385

Postmortem detection of WNV has been well documented in tissues such as the
central nervous system (CNS), ocular, cardiac, renal, skin, and vascular feather
pulp, as well as blood, oropharyngeal, and cloacal swabs.18,19 Chronic infections
are difficult to diagnose because of clearance of the virus, with the host then suc-
cumbing to chronic inflammatory sequelae of WNV with low amounts of viral antigen
present.20 Immunohistochemistry, viral isolation, and histopathology of organ tissue
can be performed to diagnose WNV. In chronic infections, ocular, CNS, renal, and
feather samples have yielded positive viral/antigen detection results.8,17,21
Clinical signs of WNV in avian species appear 10 to 12 days after infection.22 Neuro-
logic deficits are the most common clinical finding in WNV infection.13 A complete
blood count may reveal a moderate leukocytosis characterized by a heterophilia
and lymphocytosis.13 Other clinical findings include ataxia, head tilt, pinched-off
feathers, myocarditis, myalgias, arthralgias, rashes, pancreatitis, hepatitis, and inflam-
mation of the pecten and choroid.21,23–26 Relapses of neurologic signs can occur for
several years after infection.23
Viremia is often detectable 1 to 8 days after infection.8 Cloacal and oral shedding
during viremia may continue for 14 days or longer. Antibodies are produced 5 to
7 days after infection, so serology and plaque reduction neutralization test (PRNT)
can be used for detection.27,28 PRNT is the is the preferred diagnostic once the virus
has been cleared by the host immune system. WNV affects multiple organ systems
and can be cleared in 1 to 2 weeks; however, WNV has been documented to persist
for longer periods depending on the age and immune status.8 If the period of infection
cannot be determined, running polymerase chain reaction (PCR) and paired PRNT is
recommended.
Sample collection for antemortem WNV detection includes blood and oral/cloacal
swabs, as well as feather, organ, and skin biopsies. Serology is useful when paired
titers are run 2 to 4 weeks apart.8 The high cross reactivity of flavivirus infections com-
plicates the precise serologic diagnosis by immunologic techniques, such as enzyme-
linked immunosorbent assay. Therefore, confirmation with PRNT is the gold
standard.9
The mature WNV virion external protein shell is composed of 180 copies of an N-gly-
cosylated E protein found in most WNV isolates.9 This surface glycoprotein consti-
tutes the major target for neutralizing antibodies, becoming the basis of many
vaccine candidates. Although the lack of glycosylation influences WNV replication in
experimentally infected chickens,9 it does not compromise the induction of anti-
bodies. The E protein carries Flavivirus cross-reactive and WNV-specific epitopes.
This cross reactivity between WNV and related flaviruses results in cross-protection,
which is beneficial but also results in the adverse effect of antibody-dependent
enhancement of the infection.9
Prevention, vaccination, and vector control are important to reduce WNV in avian
wildlife. WNV persists in organs for up to several months, thus playing a role in viral
overwintering and enabling infections to spread through vectors and bird-to-bird
transmission.9
Flaviviruses represent an emerging challenge because of their worldwide spread,
increasing outbreaks of WNV and emergence of Zika virus in 2017.15 Development
of an effective vaccine labeled for birds is essential because of the ability of avian spe-
cies to develop a competent viremia resulting in transmission of WNV to vectors.15
Several commercial equine vaccines are used extralabel in avian species,29 including
a formalin-inactivated whole-WNV killed vaccine (formerly Fort Dodge, now Veteran),
a DNA-based vaccine using the prM and E capsid proteins from Fort Dodge (West Nile
Innovator DNA equine) and Merial Recombitek live canarypox vectored vaccine; the
386 Tyson-Pello & Olsen

last 2 have been discontinued. Experimental vaccines have been assayed, including
ChimeriVax-WN, a chimeric virus vaccine that uses yellow fever 17D vaccine strains
and WNV surface proteins, and a vaccine based on WNV recombinant subviral parti-
cles. Other approaches include DNA plasmid vaccines that express modified WNV E
proteins of lineage 1 and 2.9
Vaccination induces humoral and cellular responses, reducing WNV-related dis-
ease, viral shedding, viremia, and mortality.9 Vaccines may not seroconvert every
bird but may produce tissue-mediated immunity.29 Vaccines have been used in avian
species28–30 and in some cases have shown antibody development. In sandhill cranes
(Grus canadensis), vaccination resulted in reduced viremia and shedding.21,29
Vectored WNV vaccines showed efficacy against WNV infection using a vectored vac-
cine for delivery of WNV genes, which provided protection in a domestic goose
model.31 Further development and research are needed to produce an avian-
labeled WNV vaccine.
WNV is a zoonotic and epizootic infection of great importance in avian wildlife,
which serve as critical vectors because of their high viral load. To prevent exposure,
the US Centers for Disease Control and Prevention recommends reducing mosquito
exposure during times of peak activity, using mosquito nets around outdoor enclo-
sures, and removing standing water to eliminate and reduce mosquito breeding
sites.14 Supportive care and antiinflammatories are the treatment of choice for
WNV-infected avian patients13 because of the severe inflammatory sequelae WNV
causes in the body. However, there is no antiviral treatment available to date. With
the recent loss of marketed vaccines and the degree of infectivity of WNV, it is impor-
tant to continue research to develop a labeled vaccine for avian species.

LYMPHOPROLIFERATIVE DISEASE VIRUS IN WILD TURKEYS

Lymphoproliferative disease virus (LPDV), a C-type retrovirus, is one of 3 oncogenic

avian viruses and is responsible for neoplastic disease in wild and domestic turkeys
(Meleagris gallopavo).32–34 It was first discovered in 1978 in the United Kingdom.
LPDV is characterized by rapid clinical decline with gross intracelomic lesions and
generalized anorexia, lethargy, and ruffled feathers. Clinical signs are not present in
all affected birds and transmission routes are unknown. Recent discovery of LPDV
in wild turkeys in the United States has produced new concern for infection of wild tur-
keys and potential outbreaks in commercial flocks. Before 2009, the virus was consid-
ered rare, with little concern for spread to commercial poultry.32
LPDV targets lymphoid tissue and is the primary site of replication. Age at the time of
infection determines disease manifestation. Experimental infection at 1 day of age
leads to viremia with no other clinical signs, whereas infection at 4 weeks of age results
in neoplastic lesions of multiple organs. Mortality begins at 10 weeks of age and
steadily increases in naturally infected flocks, with mortalities as high as 25%.
Chickens and turkeys are susceptible to LPDV, whereas ducks and geese are not.32
LPDV transmission may occur via horizontal transmission and direct contact during
seasonal flocking. However, vertical transmission and vector-mediated transmission,
both noted in other retroviruses, have not been shown to occur with LPDV.33 There is
potential for bidirectional pathogen spread among wild and domestic turkeys, with
wildfowl, domestic fowl, and other wild avian species possibly acting as disease res-
ervoirs for the others. Shared contaminated environmental substrates in the region of
turkey farms may serve as sources of exposure to wild turkeys and other wildlife.34
LPDV in wild turkeys is spreading from the northeast across the United States, with
recent cases in Ohio and Pennsylvania, but the origin is unknown.34
 Emerging Diseases of Avian Wildlife 387

Cutaneous tumors are noted on the head, neck, and feet of wild turkeys, and do not
present in domestic turkeys. Tumor formation leads to direct mortality caused by
blindness and lack of mobility resulting in starvation. It is conjectured that this tumor
formation is caused by a secondary infection or novel pathogenesis.32,33 It is rare for
LPDV to cause large-scale die-offs in wild birds. Many wild turkeys test positive for
LPDV without showing internal or external gross lesions, making it difficult to deter-
mine the level of effect that subclinical infection has on the wild bird population.33
Diagnosis of LPDV is difficult because of inconsistent clinical signs. PCR of whole
blood, bone marrow, or buffy coat is a viable option for testing live birds.32
Recent discovery of LPDV in wild turkeys leaves concern for infection to spread from
these wild turkeys to commercial flocks, causing potential outbreaks. Further moni-
toring and research are needed to protect domestic and commercial flocks from LPDV.

WELLFLEET BAY VIRUS

Wellfleet Bay virus (WFBV) is a recently identified orthomyxovirus associated with

mortality in wild avian species. The mortality events of consequence started in 1998
 
in and around Cape Cod, Massachusetts (41 540 1500 N, 70 20 3300 W),35,36 although
there were smaller, unrecognized mortality events starting as early as 1956. The virus
that causes WFBV has been classified in the genus Quaranjavirus and may be an
arbovirus.35
Mortality events have largely been confined to common eider (Somateria mollissima
dresseri). Common eider are large (w2 kg) sea ducks that breed from Massachusetts
(Boston Harbor) north to Labrador and winter from Newfoundland to the Chesapeake
Bay on the eastern coast of North America. The largest concentration of wintering
common eider are in the Cape Cod area, including Cape Cod Bay, Wellfleet Bay,
and Nantucket Sound, where rafts of more than 100,000 birds may be found.37 The
mortality events occur in the fall, winter, and early spring, and sometimes primarily
involve only 1 sex. Mortality in other subspecies of common eider found in the Hudson
Bay area of Canada and along the Pacific and Arctic coasts of North America have not
been reported. Other common eider subspecies occur in Europe and Asia, and no dis-
ease outbreaks have been reported from these areas.
The first documented mortality event may have occurred from September 1956 to
March 1957 in the Cape Cod area.38 Two further events occurred in the 1980s and
early 1990s in midwinter and late spring associated with acanthocephaliasis.39 The
first large-scale mortality event of the current epizootic occurred in 1998, with events
now occurring once or sometimes twice a year.40
Most common eider are found dead, with those still alive having nonspecific clinical
signs of incoordination, lethargy, respiratory distress,40anemia, and emaciation.35
Necropsy findings include acute hepatic necrosis with variable amounts of pancreatic
necrosis, splenic necrosis, or intestinal necrosis.40 In a study40 to test Koch’s hypoth-
esis, 6-week-old common eider ducklings were inoculated with WFBV. Clinical signs
developed in 25% of the inoculated ducklings, and weight loss alone occurred in
another 18.75% compared with control ducklings. WFBV was isolated from 37.5%
of the infected ducklings, and serum antibody titers were detected 5 days after inoc-
ulation in surviving ducklings.40
Little is known about routes of transmission, host range, and origin of WFBV.
Studies in common eider subspecies, S m dresseri and Somateria mollissima borea-
lis,41 showed significantly higher numbers of eider with titers in Massachusetts and
Rhode Island (16.3%, n 5 387), compared with Maine (3%, n 5 346), Nova Scotia
(3%, n 5 180), Quebec (1%, n 5 501), Nunavut (0%, n 5 530), or Iceland (0%, n 5 52).
388 Tyson-Pello & Olsen

Mortality events only occur in the Cape Cod area, which may indicate exposure to a
carrier, an arthropod vector, or environmental factors that favor the virus.41 Herring
gulls (Larus argentatus) from Massachusetts and New Jersey have tested positive
for WFBV,42 as have ring-billed gulls (Larus delawarensis) from Massachusetts, a sin-
gle white-winged scoter (Melanitta fusca) from Massachusetts, and black scoters
(Melanitta americana) also from Massachusetts.42 Several of these positive birds
were collected either from the Boston Harbor nesting islands of common eider or
from Cape Cod. Herring gulls and common eider overlap in most of their range, so
it is unlikely that herring gulls are the reservoir host or exposure to the disease in com-
mon eider would not just be confined to Massachusetts. However, ring-billed gulls are
winter-only residents of Massachusetts, nesting at inland areas across North Amer-
ica.43 White-winged and black scoters are also both winter-only residents of coastal
Massachusetts, breeding in the far north.43 Furthermore, they dive to feed on mol-
lusks, as do eider.
The characterization and cause of WFBV have progressed since our last review,44
but there are still some unknown factors. The virus has now been found in several
other avian species but not in high incidence and not shown to cause any disease.42
The highest incidence of disease prevalence is known to be in the Massachusetts
and Rhode Island area41,42 and centered on common eider that nest in the spring
and summer on Calf Island in Boston Harbor. However, the mortality events occur
during the fall, winter, and early spring in the waters surrounding Cape Cod, and
can involve common eider from other nesting areas along eastern North America.
The method of transmission has not been discovered. The arboviruses are normally
associated with tick transmission, but, to date, no ticks have been found on the birds
or in the nesting material. However, the authors have found lice on many of the com-
mon eider brought in for veterinary examination, and these lice have been submitted
for analysis.
WFBV is still a mystery. The route of infection in the wild is unknown. In the duckling
study,40 inoculation was done using a standard World Organization of Animal Health
procedure for determining pathogenicity of avian influenza in poultry by inoculating
via 3 routes simultaneously (intravenous, intratracheal, and oral), and infection
resulted. In this study,40 there was a single contact control eider housed with the inoc-
ulated eiders. This control eider gained weight, showed no signs of illness, and did not
develop detectable antibody titer, indicating lack of transmission of the virus from the
inoculated eider ducklings to this control duckling.40 There are several other Quaran-
javirus species that affect avian wildlife, such as the Cygnet River virus from Kangaroo
Island, South Australia,45 that may have caused mortality in Muscovy ducks (Cairina
moschata), and Quaranfil, Johnston Atoll, and Lake Chad viruses, which are all asso-
ciated with colonial nesting avian species and ticks.46 Quaranfil has also been isolated
from 2 young children that had a mild febrile illness47; therefore, there are zoonotic im-
plications with this group of viruses. Continued research is needed to learn more about
WFBV and its implications for common eider, other avian wildlife, and people.

AVIAN INFLUENZA

The emergence and spread of H5N1, H5N8, and other highly pathogenic forms of
avian influenza virus across Eurasia, Africa, and (for H5N8) North America has meant
an increased interest in tracking and following this disease. Waterfowl (Anseriformes),
along with shorebirds and gulls (Charadriiformes), are the primary reservoir hosts of
the various forms of avian influenza, and these forms are normally considered of
low pathogenicity.48
 Emerging Diseases of Avian Wildlife 389

Influenza viruses are found in the Orthomyxoviridae family. The influenza viruses are
described as enveloped, segmented, negative-stranded RNA viruses with 2 surface
glycoproteins.49 The influenza viruses are divided into types A, B, and C based on
M and nucleocapsid proteins.50 Types B and C are primarily found in humans,
whereas the influenza A virus is the only form found in avian species, but it can infect
humans too. Dogs and cats can be infected with influenza A virus both naturally and
experimentally, but no cases of transmission to humans have occurred.49 Influenza A
is further classified by differences in the surface glycoproteins hemagglutinin (H) and
neuraminidase (N). Sixteen H glycoproteins and 9 N glycoproteins are known50 for a
total of 144 subtype combinations, such as N1H1, N5H1, and N5H8. Through muta-
tions during virus replications, new combinations with varying virulence are constantly
being created. The virulence or pathogenicity is further described as being either low
pathogenic avian influenza (LPAI) or highly pathogenic avian influenza (HPAI), with the
pathogenicity referring to the disease as seen in chickens.
A form of avian influenza that is highly pathogenic in chickens may produce little to
no clinical illness in another species, especially in the reservoir host species, such as
waterfowl. Birds are capable of shedding high concentrations of influenza virus in their
feces, with feces/oral transmission being the primary route of transmission in wild
birds.51 Birds carrying influenza virus may also shed virus in saliva and nasal secre-
tions. Poultry become infected through direct contact with other birds or indirectly
through contact with contaminated food, water, or inanimate objects such as equip-
ment or even the clothing of humans. The virus can persist for 1 to 2 days on the sur-
face of inanimate objects.49 Some highly pathogenic H5N1 have evolved to be able to
be transmitted by aerosol.52 HPAI has a 1-day to 5-day incubation and typically man-
ifests as lethargy; facial edema; discoloration or swelling of eyelids, comb, or wattle;
swollen hocks; diarrhea; soft-shelled or misshapen eggs; decreased egg production;
incoordination; and death.49 LPAI has few clinical signs, but these include mild respi-
ratory symptoms, such as nasal discharge, coughing, or sneezing; inappetence; and
decreased egg production.49
The influenza viruses are always changing, using mutation, reassortment, insertion,
deletion, and recombination to evolve into new viral forms.53 Reassortment has been
detected in wild waterfowl.54 More avian influenza viral isolations have been found in
mallards (Anas platyrhynchos) than in any other bird species.49 Peak viral load timing
and thus the spread of the influenza viruses differ among avian species.53 In waterfowl,
primarily ducks, in North America, the peak is just before fall migration during a period
called staging, when there are many naive juveniles in the population. For shorebirds,
the peak is during the spring migration.53 During spring migration, shorebirds congre-
gate along stretches of shoreline rich in seasonal food resources, such as the shores
of Delaware Bay, where horseshoe crabs (Limulus polyphemus) come ashore to depo-
sit eggs that literally cover the beaches. Ruddy turnstones (Arenaria interpres) are
considered a key agent in spreading the virus.53 It is possible that the influenza virus
may overwinter in the frozen earth of the high Arctic in North America and Eurasia.55,56
When the authors last reported about avian influenza in Veterinary Clinics of North
America: Exotic Animal Practice,44 H5N1 had emerged as a pathogen in wild water-
fowl, specifically bar-headed geese (Anser indicus) in China.56 Avian influenza H5N1
spread across Eurasia and into Africa but was never found in the Americas. However,
in the 7 years since this previous publication, new forms of avian influenza have
emerged and spread around the world. In January 2014, an H5N8 HPAI emerged
on a duck farm in South Korea.57 In further studies in South Korea, H5N8 was found
in 167 out of 771 dead wild birds of 8 different species.57 Baikal teal (Anas formosa),
bean geese (Anser fabalis), and whooper swans (Cygnus cygnus) were among the
390 Tyson-Pello & Olsen

most common wild birds to die of H5N8.57 Histopathologic findings were those asso-
ciated with renal failure and gout.57 H5N8 spread rapidly to China and Japan, then to
Germany, the Netherlands, and the United Kingdom by November 2014.58 Also, in
November 2014, H5N2 influenza virus, which was a novel reassortment of the
Eurasian clade of H5, appeared on a poultry farm in British Columbia, Canada, and
adjacent Washington state. H5N2 was found by PCR in dead northern pintail (Anas
acuta), several mallards, and an American widgeon (Anas americana) on a nearby
lake 32 km from the original Washington state outbreak.58 Four captive gyrfalcons
(Falco rusticolus) and gyrfalcon crosses fed a dead American widgeon also died of
avian influenza, H5N8. In another study, mortality caused by HPAI H5N8 was detected
in 6 species of raptors from Midwestern and western US states in association with
areas where HPAI outbreaks occurred in poultry.59
In 2017, ring-billed gulls (L delawarensis) in Minnesota were tested for avian influ-
enza, with positive results in various age classes, including 57.8% of juveniles testing
positive.60 In January 2019, HPAI H5N8 was found to be the cause of mortality in
several hundred African penguins (Spheniscus demersus) in Namibia, Africa.61 Novel
reassortment again led to outbreaks of H5N8 in Korea and Japan in 2016 to 2017, and
later in China and Vietnam.62 The recent and rapid spread of these avian influenza vi-
ruses globally through wild birds and with some mortality occurring in the wild bird
populations is of some concern.48
The emergence with novel reassortment and movement among wild bird popula-
tions poses health risks to wild bird populations, to domestic poultry, and possibly
to human health, although H5N8 has not been linked to disease in humans, unlike
the H5N1 epizootic. There is need for continued determination to maintain HPAI-
free domestic poultry flocks through testing, eradication programs, prevention and
control methods, appropriate use of vaccinations, and postvaccination monitoring.62
Wild bird monitoring programs that were established during the H5N1, but are not
currently in place in North America, should be reestablished. The recent increase in
backyard or hobby poultry in the United States poses a challenge for continued
HPAI surveillance and control programs.

SALMONELLOSIS

The genus Salmonella is one of the most common causes of gastroenteritis and infec-
tious diarrhea. One author estimates that less than 1% of cases are reported correctly.
Salmonella is a genus of gram-negative, facultative, anaerobic, rod-shaped bacteria
with more than 2300 serotypes or serovars associated with the genus, with Salmonella
enteritidis and Salmonella typhimurium being the most common.63 Pullorum disease
(S pullorum) and fowl typhoid (Salmonella galinarum) are avian forms of salmonellosis
that cause disease in poultry. Wild birds can become infected with either of these bac-
teria, but wild birds are more commonly infected with S typhimurium.64 Outbreaks in
birds are most common in colonial nesting species or concentrated around food sup-
plies.65 Songbirds in winter congregating at bird feeders can lead to higher transmis-
sion rates and high mortality.66
In birds, clinical signs can include ruffled feathers or fluffed feathers, shivering, deep
or rapid respiration, weakness, diarrhea, plaques on the oral mucous membranes and
crop, lethargy, and death. Enteritis is usually seen as diarrhea, although, given the na-
ture of avian droppings in general, this is more difficult to determine than in mammals.
Diarrhea can lead to soiled feathers around the vent, or the vent can be pasted with
fluid feces or urates. Sometimes S typhimurium becomes isolated in other organs,
such as joints.67 Exposure to Salmonella spp may produce disease, either acute or
 Emerging Diseases of Avian Wildlife 391

chronic, but may also produce an asymptomatic carrier stage in the intestinal tract of
the bird. Necropsy findings include emaciation, hepatic necrosis and inflammation,
hemorrhagic or necrotizing enteritis or enterocolitis,63 and arthritis.63,67 Birds dying
acutely have few gross lesions.68 Nonspecific lesions may be seen, such as con-
gested lungs and kidneys, and swollen, congested, mottled livers and spleen with
or without small hemorrhagic or necrotic foci.68 In more chronic disease situations,
tan to white foci or nodules form in the liver, spleen, pectoral muscles, subcutaneous
tissue, brain, and other locations.68 Infection that is passed through egg transmission
presents as a creamy or caseous yolk sac that is not absorbed into the celomic cavity
at hatching.68
S typhimurium has either evolved or become more prevalent in songbirds that are
frequent visitors at bird feeders.68 Population density of the songbirds and seasonal-
ity/winter when more bird feeders are available have been factors in the spread of this
form of salmonellosis. The use of bird feeders as a recreational pursuit in developed
countries has led to the emergence of several diseases in songbirds, not just salmo-
nellosis. Escherichia coli septicemia69 and mycoplasma infections70 are both
emerging diseases also associated with songbirds and bird feeders.
Less common, Salmonella enterica subspecies enterica serovar Hessarek has been
isolated from some passerines. This disease was first identified in common raven
(Corvus corax) from Hessarek, Iran, and has caused epizootics killing 10 to more
than 1000 passerines in Europe, and was recently identified in Piciformes, the great
spotted woodpecker (Dendrocopus major), in the United Kingdom.71 The reservoir
host for this form of salmonellosis is unknown and there is no seasonal association
or connection with human-supplied food sources such as bird feeders with S typhimu-
rium.71 Woodpeckers have a primarily insectivorous diet and, therefore, there is less
possibility of a fecal-oral transmission cycle as seen with S typhimurium.
Salmonella was among the organisms that were developed and used in biowarfare
from 1932 to 1945 during World War II.66,72 S typhimurium was used by bioterrorists in
Oregon in 1984 to contaminate salad bars in 10 restaurants as part of a trial for a larger
attack. This bioterrorist attack sickened 750 people and hospitalized 45.66,73 Attempts
to contaminate a city water supply with Salmonella by the same bioterrorist group was
not successful.66,74 This incident highlights the danger that Salmonella spp pose to
public health if used in a sophisticated bioterrorist attack. The wildlife form, S typhimu-
rium is especially dangerous because of its capability to infect multiple domestic spe-
cies and humans.66 Salmonella spp are still listed as category B (second highest
priority) critical biological agents that could be used in a bioterrorism attack.66

DISCLOSURE

The authors have nothing to disclose.

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