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Handbook for Training Field

Extension and Technical Assistance


Personnel

Cooperative Extension Program

Sustainable Non-synthetic
Gastrointestinal Parasites Control in
Small Ruminants

Tuskegee University
Cooperative Extension Program
Editor: Byeng Ryel Min, Ph.D.

July 2017

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Sustainable Non-synthetic Gastrointestinal Parasites
Control in Small Ruminants

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Preface and Acknowledgements

This handbook has been developed to train field level Extension and Technical assistance
personnel, who are involved in educating and helping goat producers. A wide range of topics
relevant to alternative parasites control management, especially focusing on small ruminants, are
included in this handbook.
Development of this handbook became possible from the funding support of Southern
Sustainable Agriculture Research and Education (SSARE) and George Washington Carver
Agricultural Experiment Station (GWCAES), Tuskegee University, AL. Experts from various
institutions (Fort-Valley State University, GA, Louisiana State University, LA, University of
Georgia, GA, and Langston University, OK. I greatly appreciate the contributions of all the authors
and reviewers.

Byeng Ryel Min, Ph.D.


Editor

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TABLE OF CONTENTS

Chapter 1. Understanding of gastrointestinal parasites in small ruminants

Chapter 2. How and why resistance to worm remedies develops

Chapter 3. Conventional method to control internal parasites.


Combination of Dewormers: The Time is Now!

Chapter 4. Potential solutions to highly resistant worms in sheep and goats

Chapter 5. Alternative Methods for Managing Gastrointestinal Parasites and Eimeria spp. in
Small Ruminants

Chapter 6. Non-chemical control of parasites in small ruminants through grazing management


and nutrition

Chapter 7. Overview on Enhancing Immune Responses to Internal Parasites in Small Ruminants

Chapter 8. Decreasing Barber Pole Populations on Grass Pastures: Is Liquid Nitrogen


Fertilizer a Viable Alternative?

Seminar presentation
Chapter 9. An update on anthelmintic resistance on goat farms in the United States

Chapter 10. SERICEA LESPEDEZA for parasite control

Chapter 11. Sustainable Non-synthetic Parasites Control in Our Farm


The way to go?

Chapter 12. Nutrition, Feeding, and Immunity against parasites

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Chapter 1. Understanding of gastrointestinal
parasites in small ruminants
James E. Miller DVM MPVM PhD DipACVM
Department of Pathobiological Sciences
School of Veterinary Medicine, Skip Bertman Dr., Louisiana State University
Baton Rouge, LA 70803
225-578-9652 (Office), 225-578-9701 (Fax), jmille1@ lsu.edu

Gastrointestinal nematodes (worms)

There are a number of worms found in small ruminants. The predominant and most pathogenic
ones are found in the abomasum (stomach) and small intestine. Haemonchus is the most
pathogenic and predominates in warm climates. Teladorsagia is secondary and predominates in
cool climates. Trichostrongylus is can be important in both climates.

General life cycle

It is important to understand some aspects of the life cycle of these worms. Part of their life cycle
is spent inside the animal and part on the pasture (Figure 1).

Worms mate in the host and eggs produces by females pass out in the feces. Eggs hatch and
develop through 2 larval molts to infective larvae while remaining in the feces. The infective larvae
then migrate out of the feces, when a moisture medium (rain, heavy dew, irrigation, etc.) is present,
onto the surrounding forage where they can be consumed during grazing thus completing the cycle.
The prepatent period is the time from ingestion of infective larvae to egg laying adults, and is about
three weeks. Development from egg to infective larvae can be short (7-10 days during warm
summer months), so pasture contamination and reinfection can be quite rapid. Larval development
on pasture is delayed during cooler months and can take a month or two to reach the infective
larvae stage, thus pasture contamination and reinfection is minimized. The infective larvae have a
sheath that protects them from adverse environmental conditions so they can survive for months,

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which extends transmission potential. As long as temperature and moisture conditions are warm
and wet, pasture contamination accumulates, but if the temperature gets too hot/cold and/or the
moisture conditions become dry, larvae are threatened and pasture contamination is less. Worm
transmission can be reduced by implementing control measures to remove worms from the animal
(deworming) and/or using management to reduce reinfection.

Figure 1. Typical worm life cycle

Another way to look at the life cycle is in four phases, the epizootiologic cycle (Figure 2). Phase
1 is the Parasitic Phase (host and the parasite interaction). Phase 2 is the Contamination Phase
(eggs that are passed in the feces). Phase 3 is the Free-Living Phase (larval development and
survival in feces and on pasture). Phase 4 is the Infection Phase (consumption of infective larvae
during grazing). A number of factors affect what happens and influences control strategies during
these phases.

During Phase 1, infective larvae are ingested, lose their protective sheath and invade the mucosa
(lining) of the gastrointestinal tract (abomasum, small intestine or large intestine) depending on
the worm. Larvae develop to the next larval stage and then emerge back surface where they
develop to adult worms. The immune system is the major defense mechanism against worms. A
series of activities act to mobilize various components (antibodies, killer cells, etc.) that then affect
the ability of the worms to survive. The immune system has to mature with age. Young animals
are more susceptible to infection and become more resistant with age. Young animals, therefore,

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harbor the heaviest worm burdens and suffer the most severe consequences. Adult animals have
stronger immunity and harbor lower worm burdens. Infection level is measured by counting the
number of eggs that are passed in the feces. High and low egg counts are usually seen in young
and adult animals, respectively. Signs of infection and clinical disease infection in young animals
can include diarrhea, rough hair coat, anemia, weight loss, bottle jaw, etc. Infection in older
animals usually is subclinical with weight loss and poor condition score. Nutrition and/or stress
can alter a host’s immune competence. Poor nutrition and/or stressful conditions compromises the
immune system which then can’t respond adequately. Therefore, the effects of infection can
become worse no matter what the age of the animal. The prepatent period can be extended for
worms that enter a period of delayed or arrested development in the host called hypobiosis. This
occurs when the environmental conditions are unfavorable for development and survival of larvae
on pasture. This happens during summer in warm/dry climates and during the winter in colder
climates.

During Phase 2, the magnitude of pasture contamination is affected by stocking rate (number of
animals per grazing area), age of the animals, season of the year and hypobiosis. The lower/higher
the stocking rate, the less/more feces are deposited, thus more/fewer eggs on pasture. Young
animals pass more eggs than older animals. Worms have a definite seasonality, so more eggs are
produced and passed during their ‘season’. The phenomena called the peri-parturient rise in fecal
egg output is common in small ruminants. This occurs around parturition and extends through
most of lactation. These two times are stressful and the dam’s immune system is compromised.
Nutrients are used primarily to support fetal development and then lactation and ability to maintain
an effective immune response to worm infection is compromised. This results in female worms
increasing egg production and the number of eggs deposited in the feces. During hypobiosis,
development time to the adult stage is extended which results in fewer worms and fewer eggs
deposited in feces. However, when larvae resume development, massive numbers become adults
over a short period of time. The resultant increase in number of worms results in increased egg
production and deposition in the feces, thus more contamination.

During Phase 3, development and survival of the free-living larvae depends on environmental
(temperature and moisture) and nutritional (oxygen and energy) conditions. The first stage larvae

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develops in the egg. After hatching, development to second-stage and finally third-stage (infective)
larvae occurs in the feces. The unprotected first- and second-stage larvae need oxygen and energy
(feed on nutrients and microorganisms present in the feces) to grow. Because infective larvae are
enclosed in protective sheaths, they do not feed. Normal development and survival occurs between
65-85 degrees F. As the temperature increases or decreases from this range, development and
survival is reduced. Moisture is very crucial for development and survival. Within feces, moisture
is usually adequate to complete development to the infective larvae. However, if temperatures are
high and/or feces are physically disrupted, the first- and second-stage larvae are susceptible to
desiccation and will die. If feces remain intact and conditions remain favorable, infective larvae
can survive for months. A moisture medium (rain, dew, irrigation) is necessary for infective larvae
to migrate out of feces. Once outside the feces and on the forage, they are relatively resistant to
environmental conditions due to their protective sheath. Temperature is usually the determining
factor that adversely affects the survival of infective larvae on pasture. They can survive very low
temperatures, but may die off during hard freezes. Temperatures above 95 degrees F are usually
lethal if exposed for long periods of time. The higher moisture and lower temperature conditions
at ground level under forage cover is usually adequate for infective larvae to survive for extended
periods of time. Their length of survival depends on how fast they use up their energy reserves
because they can’t feed. As temperature increases, the faster they move; therefore, energy stores
are used up quicker and survival is shorter. Infective larvae remain close to the fecal pat (within
12-24 inches) and when there is a moisture medium present (i.e. advancing and receding dew,
rain), they move up and down the blades of grass (2-3 inches). So, as the animals graze closer to
the ground or closer to feces, consumption of infective larvae increases.

During Phase 4, stocking rate again is important. As the stocking rate goes up, there is more
contamination (Phase 2) of the pasture and, consequently, more infective larvae will be available
for consumption, and vice versa. It is well known that animals tend to avoid grazing close to feces
so the further the distance between fecal deposits, exposure is reduced. When feces eventually
disintegrate, grass grows well (fertilization) and animals grazing over that area will be exposed to
more infective larvae. Forage grows well along the edge of natural sources of water (streams,
ponds or lakes). When animals congregate to drink, they consume the attractive forage. Defecation
in these areas also results in increased contamination and eventually infective larvae build up. The

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same can be said for areas where supplements, especially hay, are fed on the ground. Similarly,
trees provide an area for animal congregation and shade. Under all these situations, a high stocking
rate has been artificially created in smaller areas, i.e., hot spots for reinfection.

Figure 2. Epizootiologic cycle of gastrointestinal worms

The Worms

Haemonchus contortus (Barberpole Worm)

Haemonchus contortus is found in the abomasum. They are blood feeding worms that gets the
name from the barberpole appearance of white ovaries twisted around the red blood filled gut
(Figure 3). They feed by disrupting the surface of the abomasum with a lancet which results in
blood flow (Figure 4). They then ingest the blood through the lancet, like a straw. They are rather
large compared to other gastrointestinal worms, measuring up to 3/4 of an inch. If one opens up

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the abomasum, they can be readily seen as thin red hair-like worms on the abomasal surface.
Female worms are prolific egg layers and with a heavy burden, the environment is contaminated
with a very large number of eggs. These worms are found predominantly in tropical and subtropical
regions of the world where they thrive under hot and moist environmental conditions. These
conditions prevail in the southeastern US, but where similar environmental conditions are
encountered during the summer, H. contortus can also be a problem.

Figure 3. Adult female Haemonchus contortus

Figure 4. Head of Haemonchus contortus with lancet

H. contortus transmission and infection is at the lowest level during the winter. As temperatures
get warmer and moisture increases during the spring, transmission and infection increases and
peaks during the summer. As temperature and moisture dissipates during the fall, so does
transmission and infection. Hypobiosis has not been observed to occur to any great extent in the
southeastern US because the life cycle can be maintained year around, but it does occur in more
northern/western temperate (cold/dry) regions of the US.

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The primary sign associated with H. contortus infection is anemia due to blood loss. Mucous
membranes will be pale (most visible be looking at the inside of the lower eyelid) and bottle jaw
(an accumulation of fluid under the chin) may appear. As the worm burden increases, the more
blood is lost and eventually animals may die.

Telodorsagia (Ostertagia) circumcincta (Brown Stomach Worm)

The second abomasal worm of importance, also found in the abomasum, is Telodorsagia
circumcincta which is smaller than H. contortus. It is not as readily visible as H. contortus since it
is about a quarter to half inch long and very thin. These worms feed mostly on nutrients along the
surface and is not a blood feeder. Female worms produce fewer eggs than H. contortus. Infection
causes direct damage to the abomasal surface which interferes with digestion. As a result, infection
is usually considered a production disease because animals do not grow well. That said, when
infection reaches a level that causes clinical disease, the primary symptom is diarrhea and death
can result under very high infection conditions. This worm thrives in cooler wet environmental
conditions such as the more temperate regions of the US outside most of the SE. This worm takes
advantage of hypobiosis when environmental conditions are too cold (winter) or too dry (summer).

Trichostrongylus colubriformis (Bankrupt worm)

Trichostrongylus colubriformis is the most predominant small intestinal worm and is very small
and threadlike. It is present throughout the US, but similar to T. circumcincta, it thrives better when
conditions are more cool and wet. In the southeastern US, T. circumcincta is not very prevalent,
so T. colubriformis is the next most common and important worm after H. contortus. As with T.
circumcincta, this worm feeds on nutrients on the surface of the mucosa and interferes with
digestive function. The most common clinical sign is diarrhea accompanied by weight loss or
reduced weight gain. It is called the bankrupt worm because animals become poor doers leading
to loss of production and income.

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Figure 5. Relative difference between Hamonchus, Teladorsagia and Trichostrongylus

Nematodirus spp. (Long-necked bankrupt worm)

Nematodirus spp. are found in the small intestine and are relatively large worms (easily seen, like
H. contortus). They are found throughout the US, but usually in rather small numbers and thrive
better in cooler climates. Problems are rare in the southeast US, but in cooler areas greater numbers
of worms can accumulate and if this occurs, production and income losses will result (similar to
that of T. colubriformis).

Oesophagostomum spp. (Nodular worm)

Oesophagostomum spp. are found in the large intestine and are relatively large (easily seen, again
like H. contortus). They are found throughout the US, but usually in rather small numbers. The
larvae are found in the mucosa of both the small and large intestine where they form nodules, thus
Nodular worm. After leaving these nodules, the larvae develop to adults in the large intestine where
they feed on blood and can contribute to anemia caused by H. contortus. They also disrupt of
function of the large intestine (water resorption) which contributes to diarrhea.

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Trichuris spp. (Whipworm)

Trichuris spp. are found in the large intestine usually in small numbers. The posterior end of the
worm is rather large and can be readily seen while the anterior end is thread-like, thus Whipworm.
These worms are also blood feeders and, like Oesophagostomum spp., contribute to anemia due to
other worms. In addition, it contributes to disruption of the function, thus diarrhea.

Diagnostic methods (measure how wormy animals are)

The general clinical signs of worm infection include rough hair coat, diarrhea, depression, weight
loss (or reduced weight gain), bottle jaw and anorexia (off feed). Supporting diagnostic findings
from laboratory testing include the fecal egg count (FEC, increases with higher worm burden) and
blood pack cell volume (decreases with higher worm burden). These are tests usually done by a
veterinarian, but can be by others with proper training.

During the FEC exam, the eggs of all the worms mentioned above look similar (called
trichostronglye-type, Figure 6) except for Nematodirus spp. (large football shape, no end plugs,
Figure 7) and Trichuris spp (small football shape with protruding end plugs, Figure 8).

Figure 6. Typical trichostrongyle-type eggs

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Figure 7. Typical Nematodirus spp. Egg

Figure 8. Typical Trichuris spp. eggs

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Chapter 2. How and why resistance to worm
remedies develops
Ray M. Kaplan, DVM, PhD, DipACVM, DipEVPC

University of Georgia College of Veterinary Medicine, Department of Infectious Diseases, Athens,


Georgia, USA

(Reprinted with permission from Proceedings of "What Works With Worms: 2015 International Congress on Sustainable Parasite Management,
Pretoria, South Africa, May 25-26, 2015).

Introduction

The age of modern chemistry and pharmaceutical solutions to infectious disease ushered in a
renaissance of improved health and productivity of livestock. Starting in the 1960’s, the
availability of highly effective, safe and broad-spectrum worm remedies (anthelmintics) made
parasite control simple and effective. Frequent regularly scheduled treatments with worm remedies
kept animals healthy and productive, and had a great costbenefit return. However, this strategy has
turned out to be shortsighted and unsustainable. This is because gastrointestinal nematodes (GIN;
commonly referred to as roundworms) of sheep and goats have become resistant to multiple
drugs.This problem is extremely common and widespread around the world, and is particularly
serious in Haemonchus contortus (barberpoleworm or wireworm), but also in other species of GIN
(Kaplan and Vidyashankar, 2012). In fact, in many areas of the world, including South Africa,
there is a great risk of having no effective worm remedies to use in the near future. Some farms
are already in such a predicament. This leads to several important questions. First, why does drug
resistance in worms seem to happen so readily and how does this happen? And second, what can
be done to slow down the development of drug resistance?

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What is drug resistance and how does it start?

First we should define resistance to worm remedies. Resistance is defined as a heritable genetic
change (meaning it is passed genetically directly from a worm to its offspring) in a population of
worms that enables some individual worms to survive drug treatments that are generally effective
against the same species or worm and stage of infection at the same drug dose rate. In practical
terms resistance to worm remediesis present in a population of worms when the effectiveness of
the drug falls below that which is historically expected, when other causes of reduced efficacy
have been ruled out. Really, we should not be surprised that worms have become resistant to worm
remedies. Everyone is aware that that bacterial resistance to antibiotic drugs is becoming a major
problem worldwide. Very similar evolutionary processes also occur with worms. In fact, we now
understand quite well that drug resistance is an inevitable consequence of using drugs to kill
bacteria, viruses and parasites. With regard to parasitic worms, these organismshave many biologic
and genetic features that favor the development of drug resistance, such as short life cycles, high
reproductive rates, high genetic mutation rates, and extremely large population sizes. These
biologic characteristics lead to rapid rates of evolution and exceptionally high levels of genetic
diversity. Therefore, even though mutations that cause a worm to become resistant are very rare,
they are constantly occurring due to the enormous sizes of worm populations. For instance, each
female H. contortus worm produces approximately 5,000 eggs per day. If a flock of sheep averages
1,000 worms per animal (a very modest level of infection), then there are 500 females so that a
single sheep will pass 2.5 million eggs per day. In other words, a flock of 100 sheep will shed
almost 2 billion eggs per week. These huge numbers provide the opportunities for rare mutations
that lead to drug resistance to occur. So – what happens to make these very rare mutations increase
in numbers to such a great extent that many or even most worms on a farm have the resistance
trait? As discussed above, initially worms bearing mutations that make them resistant to the drug
are very rare within the midst of a very large genetically diverse population, which may number
in the hundreds of millions or billions. These resistant individuals and their offspring will remain
rare within a worm population, and may even disappear from the population unless they gain a
survival advantage over their parasitic competitors. The way they gain such a competitive
advantage is by treating animals with worm remedies. Treatment per se does nothing positive for
resistant worms, but by killing the drug-sensitive worms, which comprise the vast majority of a
parasite population, resistant individuals are able to reproduce for a given interval in the relative

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absence of competition. As a result, following each and every treatment with a worm remedy, the
numbers of resistant worms increase incrementally. The development of drug resistance to levels
that are clinically important is usually a slow and gradual process, requiring numerous generations
under drug selection (usually taking many years). This can be best understood with a simple
illustration. If say one in one million worms in the population are resistant, and then numbers of
resistant worms double with each treatment we will see the following change in frequency of
resistant worms over 13 treatments: 1/1,000,000; 1/500,000; 1/250,000; 1/125,000; 1/62,500;
1/31,250; 1/16,000; 1/8,000; 1/4,000; 1/2,000; 1/1,000; 1/500; 1/250; 1/125. So – with just 13
treatments we went from 1 in 1,000,000 to 1 in 125. However, even though this signifies an almost
10,000-fold increase, the drugs are still 99% effective and the resistant worms are not noticed. But
then it takes just 6 more treatments to reach complete treatment failure (1/125; 1/62; 1/31, 1/15;
1/8; 1/4, 1/2). In this illustration it took just 19 treatments to change the frequency of resistant
worms from one in one million (0.000001%) one in two (50%). But only in the last 3 treatments
would there be enough resistant worms present to cause a problem. Of course this is just an
illustration, and this process can occur faster or slower depending on numerous factors. Thus from
a practical perspective, drug resistance develops slowly over time, during which time it is
impossible to detect. But then levels of resistance increase very rapidly in the last phase, where it
is then perceived as a clinical event (treatment failure). Alternatively, resistant worms can be
purchased, thus bypassing the many years of worm evolution and drug selection necessary to reach
high levels. Depending upon how many animals are purchased harboring resistant worms,
treatment failures can occur practically instantly or over a relatively short period. This has great
clinical relevance because in either case, resistance can transition from undetectable, to clinically
important levels over a very short period of time. Consequently, unless a surveillance program is
in place that closely monitors the effectiveness of drug treatments over time (see paper on
diagnosis of drug resistance), resistance will not be noticed clinically until levels of resistance are
extremely high. This is a major problem because once resistance reaches detectable levels,
irreversible changes in the genetic structure of the worm population have occurred, ensuring that
“resistance” is fixed in that population forever(Roos et al., 1995). Thus, once resistance is
diagnosed as a clinical problem “reversion” to susceptibility likely will never occur.

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Factors that affect the development of drug resistance

It is easy to understand how resistance may evolve when worm remedies are administered
frequently. But what other factors regulate the rate with which resistance develops? Why does
resistance develop so much quicker in some parasites and in some hosts than in others? We don’t
fully know all the answers to these questions but there is much we do know. Firstly, it is important
to administer quality drugs at the proper dose level, and to deliver the dose using optimal drenching
technique. Under dosing either because of underestimating the animal’s weight or sub-optimal
delivery of the dose can greatly accelerate the rate with which resistance develops. Similarly, the
use of poor quality or degraded drugs (old or stored poorly) can also accelerate resistance because
all of these practices allow partially resistant worms to survive that would otherwise be killed by
the full dose. However, the most important factor affecting the rate of development of resistance
to worm remedies is the proportion of the worm population under drug selection. In other words,
of all the worms on the farm, both in the animals and on the pasture, what percent of these worms
is experiencing the effect of the worm remedy treatment? The more worms that “experience” or
“see” the drug, the more opportunity there is for the resistant worms to gain an advantage. The
fewer the number of worms that “see” the drug, the less advantage the resistant worms gain
because many of the drug-susceptible worms are still around to dilute the resistant ones. We use
the term “Refugia” to describe the portion of a parasite population that is not exposed to a worm
remedy during a treatment event(Van Wyk, 2001). Parasites in refugiaescape selection pressure
from the drug, thus parasites in refugia constitute a reservoir of drugsusceptible parasites that keep
the resistant worms diluted to low levels. Examples of refugia include eggs, infective third-stage
larvae (L3) and pre-infective larvae (L1, L2) in the environment (on the pasture) and parasitic
stages in those individual animals that are not dewormed whenever other herd members are treated.
It is noteworthy that at times of the year when worm transmission is high (rainy season)
thenumbers of parasites on pasture often comprise >99% of the total parasite population on a farm.
In contrast, during hot and dry times of the year few parasitic stages can survive on the pasture,
and therefore most of the worms are inside the animals. To summarize, if we are using worm
remedies to treat and control worm infections in our livestock, we cannot stop drug resistance from
developing. However, there are things we can do to greatly slow down the rate of development of
resistance. Managing refugia is the most important and direct way that we can achieve this. The
more parasites that are in refugia, the slower the development of resistance will be to worm

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remedies. This isbecause the resistant worms that gain advantage every time an animal is treated
are greatly diluted by the untreated refugia. Though managing refugia cannot prevent resistance
from eventually occurring, managing refugia on a farm is critical to delaying the inevitable
development of resistance and improving the sustainability of worm control programs.

Conclusion

Despite the occasional development of new types of worm remedies (anthelmintic classes), history
clearly demonstrates that the development of resistance consistently outpaces the introduction of
new drugs. Clearly then, major changes need to be made in the way that worm control is practiced.
It is no longer acceptable for veterinarians or farmers to view GIN parasite control in terms of a
“deworming program”. Over the past decade a paradigm shift has occurred in how GIN parasite
control must be viewed and practiced. Worm remedies can no longer be viewed as a relatively
inexpensive management tool to be used with little thought to maximize animal productivity.
Rather, they must be viewed as extremely valuable and limited resources. We must balance our
desire for simplicity and ease with the reality that effective long-term control of parasitic worms
will only be possible if worm remedies are used intelligently with prevention of resistance as a
goal, and as part of a sustainable integrated parasite management (sIPM) system.

References

Kaplan, R.M., Vidyashankar, A.N., 2012. An inconvenient truth: Global worming and
anthelmintic resistance. Veterinary Parasitology186, 70-78.

Roos, M.H., Kwa, M.S.G., Grant, W.N., 1995. New Genetic and Practical Implications of
Selection for Anthelmintic Resistance in Parasitic Nematodes. Parasitology Today 11, 148-150.

Van Wyk, J.A., 2001. Refugia - overlooked as perhaps the most potent factor concerning the
development of anthelmintic resistance. Onderstepoort J Vet 68, 55-67.

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Chapter 3. Conventional method to control
internal parasites.
Combination of Dewormers: The Time is Now!
Written By JM Luginbuhl Extension Specialist (Goats & Forage Systems) (919) 515-8743 jean-
[email protected] and Soil Sciences - NC State University

Resistance to dewormers is a fact of life, and the situation has worsened greatly in recent years.
Surveys indicate that most farms have worms resistant to at least two of the three major groups of
dewormers. Many have resistance to all three groups, and some farms now have resistance to all
available dewormers.

There is now very strong evidence that using a combination treatment is the best method for using
dewormers and should be implemented immediately on all farms that have gastrointestinal parasite
resistance problems.

 In New Zealand and Australia, products are sold that contain a combination of dewormers, so only
one product needs to be administered. In contrast, in the USA, no dewormers are yet sold in this
formulation, so the dewormers need to be bought and administered separately. This increases the
cost as compared to the products available in these other countries. In the USA, the different groups
of dewormers available on the market are not chemically compatible, thus they CANNOT be mixed
together in the same syringe. Rather, they need to be administered separately, but can be given one

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immediately after the other. Products that contain a combination of dewormers as those available in
New Zealand and Australia, however, are being considered by the Food and Drug Administration,
 When using dewormers in combination, meat and milk withdrawal times will be equal to the
dewormer used with the longest withdrawal time period.
 All dewormers should be administered at the full recommended dose whether administered singly or
in combination. Check the Parasite Control section of the NCSU Meat Goat Portal for recommended
dewormer dosages and meat and milk withdrawal times.
 If using dewormers in combination, it is critical to maintain refugia; thus, one should be using a
selective treatment approach based on FAMACHA© (see FAMACHA© section of the ACSRPC
website for more information on this method and for further explanations of refugia). The presence
of refugia is essential to realize the full benefits from combinations. In fact, if refugia are not
maintained then you will not get the necessary dilution of the resistant survivors, and this will then
lead to having multiple-resistant worms that can no longer be controlled with the combination
treatment.
 If the efficacy of your dewormers are >80%, it is possible you may not notice any difference in the
clinical response of treatments when applied singly vs. in combination.
 Any safety precautions that exist for a single dewormer will also exist when used in a combination.
Nevertheless, there are no known additional risks with using more than one dewormer at the same
time.

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Chapter 4. Potential solutions to highly
resistant worms in sheep and goats
 By Steve Hart
Goat Extension Specialist
Langston University
 A parasite management program uses the principles of biology of the worm and manages
pastures and animals in such a way to suppress worms. This implies a plan of certain
management actions. This would include such things as rotational grazing with a 40-day
(or more) rest period, not grazing within 4 inches of the ground, and using browse and/or
sericea lespedeza. Higher stocking rates encourage worms.
 Finding an effective way to deworm animals (discussed later) will only provide short-term
relief for the problem and not solve the problem in the long-term. If you have significant
dewormer resistance, you are going to have to develop a parasite management plan if you
want to stay in the sheep/goat business for the long-term.
 Other management practices that can be useful to control worms by reducing the number
of infective larvae on a pasture include baling hay which removes most of the infective
larvae from the pasture (the larvae in the hay bale die within a month). Tillage, such as
used to plant wheat or sorghum-sudan pasture for grazing, is an effective method of
cleaning pasture, since larvae that are tilled an inch under the soil do not survive.
 Grazing with another animal species (horses or cattle; sheep and goats share the same
parasites and will not help one another) is another way to clean larvae off the pasture.
Pasture rest (at least 6 weeks during a hot summer, longer in cooler climates) will also
clean a pasture, especially when the weather is hot. With improved pasture species, the
pasture forage quality will decline with this amount of rest. Solutions include making hay
on the pasture while it is rested, grazing with another animal species, or even mowing to
keep the grass in a vegetative stage.
 There have been several cases where resistant worms have been replaced with susceptible
worms, but this requires superb management and the services of a parasitologist. But,

21
without an effective parasite management program that minimizes the use of dewormers,
this is a solution for only a few years.
 Another way to overcome parasites is to select animals that are more resistant to
parasites. This begins by culling animals. Fifteen percent of the animals in the herd carry
50 percent of the worms,whereas 20 to 30 percent of the animals in the herd carry 70 to 80
percent of the worms. If you get rid of the animals that carry the most worms, then there
are many fewer infective larvae on the pasture to infect the rest of the animals, and you
have prevented these animals from contributing their weak parasite resistance genes to the
herd.
 Everyone knows that some of their animals are always wormy, and those are easy to
identify and cull. There are two ways that wormy animals can be identified. One is by
doing FAMACHA© across the season and the animals that require the most deworming
can be culled. One should categorize animals by litter size (singles, twins and more) and
cull those within each group that require the most deworming. The reason for categorizing
by litter size is that does/ewes that raise more kids will often show more symptoms of
worms.
 Another way to identify the animals with the most worms is to do a fecal egg count on all
animals and cull the ones within each litter size with the highest fecal egg counts. The buck
or ram accounts for 50 percent of the herd genetics. You should take several fecal egg
counts during the summer from your bucks/rams and get rid of those with the highest
fecal
 egg counts. FAMACHA© could also be used, but fecal egg counts are better for the bucks
since fecal egg counts are more accurate and can be justified for the bucks/rams due to their
importance.
 Yearlings will tend to have higher fecal egg counts since their immune systems are not
fully developed. This should be factored into selection. If you identify the most resistant
rams/bucks using this method, they should be bred to the best females (determined by
FAMACHA©) and the resulting offspring saved as replacements.

22
How to kill resistant worms

 First, you need to incorporate the support of the animal’s immune system which will
require good nutrition to support an immune response. There are three classes of
dewormers: benzimidazoles (Panacur®, Safeguard®, and Valbazen®), cell-depolarizers
(Prohibit® and Rumatel®) and avermectins and milbermycins (Ivermectin and generics,
Eprinex®, Dectomax® and Cydectin®).
 In general, Valbazen® is the most potent benzimidazole and Cydectin® is the most potent
member of the avermectins and milbermycin group. The use of the more potent members
may prevail over resistant worms. Doubling the dosage will help only little, increasing the
percentage of worms killed often by only 25 percent. Goats should be given twice the sheep
dose of Benzimidazoles and the Avermectin/milbermycin group. They should be given
only one and a half times the dose of Prohibit® due to the narrower margin of safety.
 Animals can be given combinations of dewormers at the same time, one from each of the
different classes of dewormer (usually the most potent members). These can be quite
effective against resistant worms.
 Benzimidazoles can be given every 12 hours for several doses to increase the
effectiveness. The last dose can be given with a dewormer of another class to increase the
effectiveness. Copper oxide wire capsules have been shown to be effective against the
Barberpole worm (Haemonchus contortus).
 The only long term solution to highly-resistant worms is an effective parasite management
program. Combinations of dewormers may work for a while, but will fail without an
effective parasite management program. It is possible to raise sheep/goats without
dewormers (they did exist before dewormers were available and some people manage to
raise them without dewormers), but the weak ones died, they rotated themselves, did not
graze close to the ground, and goats browsed and ate a variety of plants. It is our
management that has caused parasite problems (Adapted by American Consortium for
Small Ruminant Parasite).

23
Chapter 5. Alternative Methods for Managing
Gastrointestinal Parasites and Eimeria spp. in
Small Ruminants
B. R. Min*, N. Gurung, A. Elliott, and S. Solaiman
Department of Agricultural and Environmental Sciences
Tuskegee University, Tuskegee, AL 36088
*[email protected],
334-524-7670

Who cares and why?


Infection with gastrointestinal nematodes (GIN) and coccidia (Eimeria spp.) remains one
of the primary constraints to sustainable production of small ruminants world-wide, and with
resistance to synthetic anthelmintics now reaching epidemic proportions in sheep and goat GIN,
alternative (non-synthetic) control strategies are being explored. Infected animals have lower
growth rates, reduced reproductive performance, and have higher rates of illness and death. In the
past, sheep and goat producers relied heavily on anti-parasitic drugs. Unfortunately, GI parasites
have become increasingly resistant to many of the ruminant anthelmintics. Alternative methods of
GI parasite control for animals raised primarily on forages are vital for the sustainability and
profitability of sheep and goat farms in the southern United States. Consequently, alternative,
sustainable, and affordable methods of parasitic control are required. There is also a need to
examine plant-based alternatives to control coccidiosis in livestock because there are no FDA
approved drugs to treat coccidiosis in small ruminants.

Alternative approaches to control of parasites in goats


If internal parasites are resistant to drenches, grazing management is essential to maintain animal
production as shown follow:
1. Grazing management
2. Safe pasture
3. Selective breeding for host resistance

24
4. Feed additive
- CT-containing diets (Table 1).
- Copper Oxide Wire Particles - fungi

Pasture management
1. Smart grazing management:
Avoid graze below about 5-6 cm (2-3 inches) pasture height.
Over 80% of larvae are within 3 cm of the soil surface.
2. The Gumboot rule;
Avoid pasture height shorter than the toe of your gumboot (Figure 1).

Figure 1. The effect of forage height on fecal egg counts (FEC) in sheep.

Manage pasture quality:


To ensure high quality regrowth for next time it is grazed
1. Goat to cattle system; 5-6 cm deep pasture left behind by the goats, it is acceptable to
production from cattle.
2. Goats + cattle Integrated system: cattle and goats prefer
different species of forage.
- Goats + cattle
(not share the same parasite species)
- Goats + sheep
(share the same parasite species)
- Cattle + Sheep

25
What is safe pasture?
Safe pasture is pasture with few or no parasite larvae
1. New pasture: the time to cultivate new pasture allows larvae to die before being grazed.
2. Forage crops: tannins containing forages.
Sericea lespedeza, Lotus corniculatus
Sainfoin, mimosa
3. Hay and silage regrowth: These paddocks will probably have been closed for 4 to 8
weeks. So most of larvae on the herbage will have been removed or died

Tannin-containing diets
Research has shown that legumes such as Sericea lespedeza (Lespedeza cuneata) contain
condensed tannin (CT) with anti-parasitic properties. The anti-parasitic properties of CT have been
demonstrated to reduce GI parasitic infection in goats in Oklahoma and Georgia and in sheep in
Louisiana and Arkansas. In a series of studies with goats and sheep of differing breeds, life stages
(young, mature), and geographic regions of the southern and eastern U.S., including sericea
lespedeza in the diet as fresh (grazed) or dried (hay, leaf meal, pellets) material has resulted in a
reduction of gastrointestinal parasites eggs and coccidial oocysts in feces (up to 97 percent), lower
numbers of adult parasites in the animals’ stomach and intestines (up to 70 percent), and reduced
development of gastrointestinal parasites eggs to infective larvae in simulated pasture conditions
(Burke et al., 2012 a,b; Min et al., 2004; 2005; Terrill et al., 2009). Researchers at Tuskegee
University found potential benefits of pine bark (PB) supplementation on anti-parasitic effects and
improved feed efficiency. Pine bark is one of the abundant forest byproducts in the southern United
States and contains 11-to-13 percent CT on a dry matter basis. By raising sheep and goats
primarily on forage, farmers can reduce feed costs. Research demonstrates that goats fed on a PB
diet have up to 30 percent fewer worms in a total ration, as well as lower instances of fecal egg
count and fecal coccidian oocyst count. Feeding a pine bark diet reduced both male (64 percent)
and female (59 percent) worm counts compared with the control (without PB) diet. In addition,
mean dry matter intake, feed efficiency, average daily gain, and cold carcass weight were also
greater for goats fed the pine bark diets. On-farm research with local farmers in Alabama also has
shown that goats on a pine bark diet had 74 percent lower fecal egg counts and 5 percent better
animal weight gain compared to control diets during three-month trials. Ground pine bark as a feed

26
ingredient has the potential to improve animal performance while decreasing internal parasites and
coccidian infection. On-going our study indicated that using pine bark in combination with sericea
seems to be even more effective with artificially infected drug-resistant H. contortus (Wright et
al., 2016). The extract from the bark of the pine tree (Pinus radiata), which is rich in condensed
tannins, was reported to inhibit the life cycle of Coccidia as evidenced by decreased sporulation of
the oocysts of E. tenella, E. maxima, and E. acervulina (Molan et al. 2009). Thus, developing
plant-based alternatives such as pine bark and other natural resources for GI parasites control
would be expected to have a greater impact on the goat and sheep industries. This will allow
development of Best Management Practices to prevent or treat coccidiosis and GI parasites in
ruminant livestock.
Ultimately, by raising sheep and goats primarily on forage, farmers can reduce feed costs.

What is the tannins?


Tannins (plant secondary compounds) are plant compounds that bind to proteins and other
molecules. Tannin is related to “tanning”, as in preserving hides, and tannins are found in many
plants. There are two main types of tannins; hydrolyzable (HT), some of which may have toxic
effects on animals, and condensed tannins (CT), which are found in forage legumes (including
sericea lespedeza) and other plants. Effects of tannins vary depending on type of tannin,
concentration, and on the animal consuming the tannins. Ruminants (sheep, goats, cattle, deer etc.)
consume a wide range of plant materials (grasses, legumes, browse shrubs, tree leaves and bark),
and some of the plants contain tannins that have potential effects on animal nutrition, parasites,
and gut microbiome diversity. The CT-containing forage diets typically reduce ruminal protein
digestion, increase rumen bypass protein, and can increase average daily gain and improve health
of sheep, cattle and goats. The potential benefits of tannins-containing diets are not the same for
all the tannins, but rather depend upon the concentration and structure of the tannins.
Negative effects may include reduced intake and reduced digestibility, leading to a decline
in animal productivity (Figure 2). Negative effects are seen more often when CT concentration is
high (above 55 g CT/kg DM in the forage) (Min et al., 2003). Positive effects may include an
increase in by-pass protein (causing the animal to use protein more efficiently), a reduction in
bloating, increased milk production, and a reduction in internal parasite numbers, egg output, and
hatchability.

27
According to Min et al. (2003), low concentrations of CT (20-45 g CT/kg DM) are helpful
to animals, while high forage CT concentrations (>55 g CT/kg DM) may have negative effects.
Results vary according to CT concentration and structure and the animal that is grazing the forage,
however. Researchers have shown that big trefoil, sulla, sanfoin, and sericea lespedeza are useful
in controlling internal parasite infection in sheep and goats. Providing condensed-tannin-
containing forages is one way to boost the health of sheep or goats.

35
response (%) relative to
PEG or pasture group

30
Wool production

25
20
15
10
5 *
0 *
-5 0.7 4 9.9 10 17 18 22 28 34 36 38 50 76 88 88 90
-10
-15
Concentration (g/kgDM) & types of CT

Figure 2. The effect of forage CT concentration on wool production (Min et al., 2003).

Impact Statement (tannin-containing diets)


Goats fed on a PB diet have up to 30 percent fewer worms in a total ration, as well as lower
instances of fecal egg count and fecal coccidian oocyst count.
Goats on a pine bark diet had 74 percent lower fecal egg counts and 5 percent better animal weight
gain compared to control diets during three-month trials. Ground pine bark as a feed ingredient
has the potential to improve animal performance while decreasing internal parasites and coccidian
infection. Thus, developing plant-based alternatives such as pine bark and other natural resources
for GI parasites control would be expected to have a greater impact on the goat and sheep
industries. Development of Best Management Practices to prevent or treat coccidiosis and GI
parasites in ruminant livestock. Raising sheep and goats primarily on forage can reduce farmers
feed costs.

28
Table 1. Condensed tannin (CT; % DM) content in different forage species
____________________________________________________________________
Forage % DM
------------------------------------------------------------------------------------------------------
Perennial ryegrass 0.18
Chicory 0.31
Crabgrass/tall fescue mix 0.32
Alfalfa 0.05
Lotus corniculatus (Birdsfoot trefoil) 4.8
Lotus pedunculatus (Big trefoil) 7.7
Sainfoin 2.9
Sulla 5.1-8.4
Sericea lespedeza 4.6-15.2
___________________________________________________________________
Adapted from Min and Hart, (2003); Min et al., (2005).

Conclusion
This research has enabled goat production to be a more sustainable and low-cost enterprise by
mitigating internal parasites and coccidian infections of grazing animals, thus enhancing overall
meat production, protecting animal and human health, increasing producer profits, and providing
a stable and safe food supply. Producers should not rely on one method e,g, sericea as the sole
method for controlling internal parasites. However, sericea can be useful as one part of a complete
parasite management strategy.

What research is needed?


More research is needed to: study the direct mechanisms of tannins and parasite interactions; look
for ways of validating the anti-parasitic plants of sheep and goats production systems; and to
continue testing the effectiveness of alternative natural dewormers for use in ruminants.

29
References
Burke, J.M., Miller, J.E., Mosjidis, J.A., Terrill, T.H., 2012a. Use of a mixed sericea lespedeza
and grass pasture system for control of gastrointestinal nematodes in lambs and kids. Vet.
Parasitol. 186, 328-336.
Burke, J.M., Miller, J.E., Mosjidis, J.A., Terrill, T.H., 2012b. Grazing sericea lespedeza for control
of gastrointestinal nematodes in lambs. Vet. Parasitol. 186, 507-512.
Min, B.R., and S.P. Hart. 2003. Tannins for suppression of internal parasites. Journal of Animal
Science 81 (E. Suppl. 2):E102–E109.
Min, B. R., T.N. Barry, G.T. Attwood, and W.C. McNabb. 2003. The effect of condensed
tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Animal
Feed Science and Technology 106. p. 3–19.
Min, B.R., Pomroy, W., Hart, S.P. and Sahlu, T. 2004. The effect of short-term consumption of
a forage containing condensed tannins on gastro-intestinal nematode parasite control in
grazing wether goats. Small Ruminant Research 51:279-283.
Min, B.R., Hart, S.P., Tomita, G., Loetz, E. and Sahlu, T. 2005. The effect of condensed tannins
on gastrointestinal parasite control in Angora Does. Veterinary Parasitology 130:105-113.
Molan, A.L., Liu, Z., De, S., 2009. Effect of pine bark (Pinus radiata) extracts on sporulation of
coccidian oocysts. Folia Parasitol. 56, 1-5.
Terrill, T.H., Dykes, G.S., Shaik, S.A., Miller, J.E., Kouakou, B., Kannan, G., Burke, J.M.
Mosjidis, J.A., 2009. Efficacy of sericea lespedeza hay as a natural dewormer in goats: dose
titration study. Vet. Parasitol. 163, 52-56.

30
Chapter 6. Non-chemical control of parasites in
small ruminants through grazing management
and nutrition
Steve Hart

Langston University, OK

Introduction

It is well established that worms are the leading cause of morbidity, mortality and loss of profit in
small ruminants in regions where there is sufficient rainfall. Worms or roundworms refers to
gastrointestinal nematodes of the Trichostrongylus superfamily. Although there are more than 30
species of worms that parasitize small ruminants, three species cause most of the infections and
death here in the Southeastern US. They are the barberpole worm (Haemonchus contortus; a
tropical roundworm), the brown stomach worm (Teleddorsagia circumcincta or Ostertagia
ostertagia, a temperate species roundworm) and the black scour worm (Trichostrongylus
colubriformis, a temperate species roundworm). The same grazing management practices and
nutritional strategies used against these three major roundworms will usually discourage infection
by the other thirty species. The barberpole worm will tend to dominate in warmer regions such at
the Southeastern US. Even in cold Canada, the barberpole worm is a problem, but only for 6 to 8
weeks. The brown stomach worm and black scour worm, being temperate species worms are
greater problems in the spring and fall. Before the advent of dewormers, sheep and goat producers
used management to prevent worms. Animals with poor resistance to worms usually died. A
producer who did a poor job of managing against worms was not a producer very long.

Worms are normal, we cannot, nor should we try to eradicate worms. They have a useful role in
animals in the wild, preventing a population from overrunning an area when conditions for forage
growth are good (high rainfall and warm weather) and killing the more susceptible animals when
growing conditions are bad (drought forcing animals to graze close to the ground), ensuring that
the strong survive. We want animals to have a few worms to keep the immune system functioning

31
against worms, but not so many as to impair animal production. An excessive number of worms
causes pathology, such as anemia, poor appetite, diarrhea, edema and death. Our goal should be to
manage animals to keep worm numbers from becoming excessive. It is possible to raise small
ruminants using good grazing management, appropriate nutrition and good animal genetics
without having to deworm them. This is particularly important for organic producers where
dewormers are prohibited, but it is becoming very critically important for all small ruminant
producers as worms become more resistant to our dewormers.

Rotational grazing

Rotational grazing can be used to prevent animals from picking up infective larvae in the
pasture if the grazing period (time animals are grazing a specific area) is short enough so that
infective larvae do not develop and the rest period (time between successive grazings of the same
area) is sufficiently long so that few larvae survive on the pasture. So the first question we must
answer is how long does it take for worm eggs to develop into infective larvae available for small
ruminants to consume them. This depends on temperature and moisture. Eggs are in the fecal
pellets of small ruminants, being laid by adult worms in the digestive tract and then end up in the
fecal pellet or pat. Generally about 50oF is the minimum temperature for hatching eggs. Eggs
hatch slowly at this temperature. The optimal temperature for hatching eggs is about 86oF and
eggs will hatch in 4-24 hours at this temperature. This is why when it is colder than 50oF, worms
are much less of a problem. Higher temperatures can reduce hatch rate slightly. Once the egg is
hatched, it has to be developed to an infective third stage larva and then migrate from the fecal
pellet or pat onto the grass. The hatched egg is referred to as a first stage larva which wanders
through the fecal pellet eating bacteria such as E. coli and growing. It then molts (sheds skin like

32
a snake) to a second stage larva which does the same thing, wondering through the fecal pellet
eating bacteria and growing until becoming a third stage larva. Larva are very small, being about
as long as the period at the end of this sentence and finer than a spiderweb. The first and second
stage larvae are subject to being killed by drying out. Hot, dry weather at this time can kill
developing larvae. When the second stage larva molts to a third stage larva (infective stage larva),
it is an incomplete molt. That is, the skin of the second stage larva slips up, but does not come off.
Because the larva has an extra layer of skin, it is more resistant being dried out by the heat.
However, when the skin slipped up, it now covers his mouth preventing him from eating. Now as
a third stage infective larva, it must be released from the fecal pellet or pat and float on a layer of
moisture from dew or rain onto the grass to be picked up by sheep or goats. The main trigger for
release is rainfall, requiring two inches of rain in a month’s time based on studies in Australia.
Several days of heavy dew can also release some larva, but rain is the major factor for release.
This is why worms are much less of a problem in areas with less than 25” of rainfall.

It takes a minimum of 4 days for an egg to develop into an infective larvae at optimal
temperatures if there is sufficient humidity (O’Conner et al., 2006). It may take as long as 14 days
at 50oF. Actual field studies determined 4 days as being the minimum and 5-6 days under practical
conditions. So, then the amount of time for the grazing period should be limited to 3 or 4 days,
assuming there has been sufficient rain to release infective larvae from the feces, and then animals
are moved to prevent consumption of infective larvae. Animals can remain on pasture until there
is sufficient rain to release larvae from the fecal pellet. If the fecal pellet is exposed to the summer
sun for a significant period of time, the temperature in the pellet may rise to 150oF, killing the eggs
and larvae in the pellet.

33
The next question that needs to be answered is how long dolarvae survive on the pasture
so that the time to rest a pasture can be determined. Basically, infective larvae die when they run
out of body reserves since they cannot eat, although heat and low humidity can enhance mortality.
Since infective larvae are cold-blooded, their metabolism reflects ambient temperature. Hot
temperatures speed up metabolism and loss of body stores and therefor cause death of the larvae.
In the review by O’Conner et al. (2006) survival times ranged from 30 days in the tropics to 10
weeks in more temperate areas. One study has noted that as little as 2 weeks of hot, dry weather
could reduce infection rate (H. Jordan, personal communication).

Barger et al. (1994) grazed sheep in a tropical environment (Fiji islands) with a 3.5 day
graze period and 31.5 day rest period and were successful at avoiding worms. Pomroy et al.
(2002) grazed goats on a pasture for 5 days and rested pastures for 65 days. This reduced fecal
egg counts from 309 to 121 epg and eliminated the need for deworming. Pasture contamination
was greatly reduced 630 vs 40 worms/animal for tracer animals demonstrating that rotational
grazing can successfully control worms in the Southeast US. In the French West Indies, a
compilation of data from several grazing studies showed that infective larvae numbers started to
increase after a week on pasture and were reduced to 10% of peak infective larval numbers after
35 days of rest (Mahieu et al., 2008). Colven et al. (2008) was successful at controlling worms in
grazing sheep with a 5 day grazing period and 100 days of rest period. But a problem with such
long rest periods, is that forage quality declines to the point that animal production is markedly
reduced.

Stocking rate

Stocking rate is an important consideration in worm control because increased animals


density results in an increased number of infective larvae on the pasture and there are more animals
picking up infective larvae. With a stocking rates below two ewes or does and their lambs or kids
per acre, stocking rate is not a significant factor, but as it increases, so do parasitism problems.
Unfrotunately, stocking rates must be higher than two animals per acre in many cases if the small
ruminant enterprise is to be profitable. The producer should be aware that as stocking rates
increases, so will parasite problems. Furthermore, the benefit of some technologies used to

34
increase stocking rate such as high levels of fertilization and irrigation may be somewhat offset by
increased parasite problems.

Trees, barns and water sources can act to increase stocking rates in localized areas,
exacerbating parasite problems. Water sources generally increase humidity and often increase soil
moisture, improving conditions for egg hatch and development to infective larvae. If animals are
being rotationally grazed, but use a common lane and water source, the area may accumulate high
levels of infective larvae contamination, causing severe parasite problems despite having a rotation
grazing system that should suppress infective larvae. Trees can be big offenders in this regard as
they shade infective larvae from the sun, increase humidity, encourage animals to congregate
which increases concentration of infective larvae, and encourages close grazing (picking up
infective larvae) around the trees they rest under. The great effect of trees promoting worms was
previously identified by Pomroy et al. (2002), and it was noted that rotation grazing reduced the
effect of trees, but did not eliminate it.

The residual height or height of forage when animals are removed is an important factor in
that the infective larvae are concentrated in the lower 2-3 inches of forage. Therefore, removing
animals before they graze pastures down to 4 inches will reduce the consumption of infective
larvae. Irrigation and periods of high rainfall may move infective larvae to higher levels
necessitating higher pasture residual levels. Irrigation also creates a humid environment that
increases the success of egg hatch and larval development. Sod forming grasses such as
bermudagrass create a humid microenvironment protected from the sun that promotes the
development of infective larvae as compared to a bunchgrass which allows some sun to penetrate
and allows the ambient air to blow humidity from plant transpiration away. When small ruminants
are consuming browse, they consume very few infective larvae and seldom need to be dewormed.

Pasture contamination may be reduced by resting the pasture or by grazing with another
species such as cattle or horses which consume the infective larvae and then the larvae die in the
digestive tract. Even grazing small ruminants with cattle or horses has been demonstrated to
effectively reduce worm problems (Jordan et al., 1988). Making hay on pastures will clean many
of the larvae off in the hay where they die in about a month. Those left on the field are killed by
direct sunlight and low humidity. Cornell University recommends that in areas where hay cannot
be made, the pasture can be mowed short at the end of the graze period to help infective larvae to

35
die. If the ground can be clean tilled and the larvae buried by an inch, they die. Kentucky State
University recommends planting sorghum X sudan or millet for goats to graze. This takes
advantage of tillage to bury the infective larvae at the beginning of the season and with these
grasses the animals graze high away from the ground and avoid picking up infective larvae.
Animals that are born early in the spring have fewer parasite problems than animals born later that
must contend with a greater level of pasture infection due to warmer weather.

Nutrition

Nutrition helps to control parasites by providing nutrients for a strong immune system. The
immune system is the body’s first line of defense against worms. The immune system requires
nutrition (protein, energy, minerals and vitamins) for effective functioning, but genetics and stress
are also factors in the strength of immune response against worms. The immune response of very
young animals is reduced, whereas immunity wanes in elderly animals. Without appropriate
nutrition, the immune response is compromised. The effect of nutrition on parasite infection has
been extensively studied in Australia and New Zealand.

It appears from a number of studies that growth, pregnancy and lactation have a priority in
terms of nutrient partitioning and with functioning of the immune system impaired if nutrient
intake is insufficient for these functions (Coop and Kyriazakis, 1999). Therefore, nutrition of the
animal is very important for the immune system to suppress worms. High producing dairy goats
have been shown to be more susceptible to worms than low producers. Generally, an increased
energy supply improves immune response little except for the effect that it may have on microbial
protein synthesis (Houdijk et al., 2012), even though a fever response greatly increases energy
requirement. Rumen undegradable protein supplementation from animal origin supplements
appears to be superior to microbial protein for promoting immune response due to amino acid
balance. There are many studies that demonstrate a reduction in fecal egg count with protein
supplementation, especially with rumen undegradable protein.

Supplementation with protein has also been shown to reduce fecal egg counts of high
producing dairy does. It has been demonstrated that animals infected with worms have greater
protein secretion into the gut. This loss of protein is exacerbated by the reduction in appetite

36
associated with a worm infection. Protein supplementation not only stimulates the immune system,
but often increases the level of animal production.

It is well known that during lactation, the immune response to worms is depressed
(periparturient relaxation of immunity). Houdijk et al. (2000) demonstrated that increased intake
of protein could overcome much of this phenomena, significantly reducing fecal egg counts. Fecal
egg counts were substantially reduced in suckling lambs as compared to weaned lambs (Iposu et
al., 2010) and worms had reduced fecundity (likely due to enhanced immune response of the
animal). It appears that suckling (provision of milk protein) enhanced the immune response of
lambs early in life. Although protein supplementation has been very well demonstrated to reduce
worm problems in small ruminants, it is seldom utilized due to the cost of the supplement and
feeding on a daily basis.

Several minerals are known to be important for a healthy immune system and deficiencies
of these minerals will reduce immune system functioning. However, there has been little research
addressing direct effects of minerals on worms or fecal egg counts. Hence, it is assumed that
mineral supplementation improves immune response, it should improve suppression of worms. In
general, when various minerals are deficient, supplementation will improve immune system
functioning. There is little confirmation of supplementation of a mineral at supranutritional levels
(levels which are substantially above requirements) is useful for immune system functioning.
However, the requirements of various minerals for goats have not been adequately determined. In
addition, the biological responses used to determine the adequacy of minerals are parameters such
as growth and not immune functioning.

37
Copper, zinc, iron, selenium, cobalt, magnesium, manganese and possibly chromium
(ultra-trace mineral) are all important for immune system functioning (Carroll and Forsberg,
2007). Excess iron, above 400 ppm, can be antagonistic to other minerals, so more is not
necessarily better. Excess zinc may also be antagonistic to immune responses. Selenium works in
conjunction with vitamin E as an antioxidant and is well-recognized as an immunostimulant in
animals. Mineral contents of forages and feeds from nutrition tables cannot be relied upon to be
accurate for a specific location. Forages and other feedstuffs need to be analyzed for mineral
content. Liver is a very good tissue to analyze for determining mineral status of an animal,
although blood may be necessary for a few minerals (Kincaid, 1999). Mineral supplements should
be formulated to meet the deficits in a given area. They need to be monitored to insure adequate
consumption.

Vitamins E, A, B6, B12, folic acid, carotenoids and C are well known for their support of
the immune system (Carroll and Forsberg, 2007). Vitamin E of course works in conjunction with
selenium and its functions in the immune system have been well documented. Vitamin A has been
shown to improve immune functioning in deficient animals. Carotenoids have been shown to
benefit immunity aside from being precoursers of vitamin A. Vitamin C, apart from its function as
an antioxidant, has been shown to stimulate immunity in several species. Although only vitamins
E and A are required by the ruminant, we should make sure they are provided in adequate
quantities, whether through green grass or as mineral/vitamin supplements.

References

Barger, I. A., K. Siale, K. J. D. Banks and L. F. Le Jambre. 1994. Rotational grazing for control
of gastrointestinal nematodes of goats in a wet tropical environment. Vet. Parasitol. 53:109-116.

Carrol, J. A. and N. E. Forsberg. 2007. Veterinary Clinics of North America. Food Animal Practice
10:105-149.

Coop, R. L., and I. Kyriazakis. 1999. Nutrition-parasite interaction. Vet. Parasitol. 84:187-204.

Houdijk, J.M. 2012. Differential effects of protein and energy scarcity on resistance to nematode
parsites. Small Rumin. Res. 103-41-49.

38
Iposu, S.O., A.W. Greer, R.W. McAnulty, M. Stankiewicz and A.R. Sykes. 2010. Does milk
supply have long-term benefits for resistance and resilience to nematode parasites in sheep? Small
Rumin. Res. 94:142-149.

Jordan, H. E., W. A. Phillips, R. D. Morrison, J.J. Doyle and K. McKenzie. 1988. A 3-year study
of continuous mixed grazing of cattle and sheep: parasitism of offspring. Int. J. for Parasitol.
18:779-784.

Kincaid, R. L. 1999. Assessment of trrace mineral status of ruminants: A review. Proceedings of


American Society of Animal Science 77(1) http://www.asas.org/jas/symposia/proceedings/
0930.pdf. Viewed 3/17/08/

Mahieu, M., T. Archimede, J. Fleury, N. Mandonnet, and G. Alexandre. 2008. Intensive grazing
system for small ruminants in the tropics: The French West Indies experience and perspectives.
Small Rumin. Res. 77:195-207.

O’Conner, L.J., S. W. Walkden-Brown and L.P. Kahn. 2006. Ecology of the free-living stages of
major trichostrongylid parasites of sheep. Vet. Parasitol. 142:1-15.

Pomroy, W. E., S. P. Hart and B. R. Min. 2002. Rotational grazing as a parasite management tool
for goats. J. Anim. Sci. Vol. 80 (Suppl 1):193

39
Chapter 7. Overview on Enhancing Immune
Responses to Internal Parasites in Small
Ruminants
Zaisen Wang

The American Institute for Goat Research, Langston University, Langston, OK

Internal parasitism poses a major problem in the small ruminant industry. The USDA
National Animal Health Monitoring System reported that 74% of sheep in the U.S. encountered
gastrointestinal nematode parasitism (USDA, 2003). The level in goats may be more severe since
goats may be more susceptible to nematode parasites than sheep (Lightbody et al., 2001). In
clinical cases during 1993 to 2000 at the Auburn University Veterinary Medical Teaching
Hospital, 91% of goats examined and treated related to internal parasite diseases (Pugh and
Navarre, 2000). Parasitism significantly reduces performance of animals, including decreased
body weight, fertility (older age at first kidding and longer intervals of kidding cycles), birth
weights and growth rates, and markedly increased mortality of kids (Gatongi et al., 1997). Clinical
signs may not develop until just prior to death. Sudden onset of weakness or death is a common
finding in gastrointestinal parasitism cases (Valentine et al., 2007). The current management of
internal parasitism mainly relies on uses of anthelmintics. This practice is challenged by
widespread of anthelmintic resistance in the US and other parts of the world (Zajac and Gipson,
2000; Terrill et al., 2001; Kaplan, 2004). Mortenson et al. (2003) described resistance to two
classes of drugs on 14 of 15 goat farms and resistance to 3 classes of anthelmintics on 5 of 15 goat
farms. Kaplan et al. (2005) reported a total anthelmintic failure on a meat goat farm in Arkansas.
Furthermore, the anthelmintic resistance in goats seems to be more prevalent than in other species
of animals. Cabaret (2000) searched the literature and found that 30% of the anthelmintic articles
on goats concerned anthelmintic resistance as compared to 22% for sheep, 18% for horses, and
6% for cattle. From these facts, it is not surprised that alternative approaches have attracted much
attention. These approaches include enhancing resistance by nutritional manipulation, genetically
selection, and vaccination; feeding or browsing forages with helmintic-suppressing properties; and
avoiding contaminated pastures by grazing management.

40
Overview of immune responses to nematode parasites
Immunity to internal parasites in small ruminants has been evidenced by the existence of
genetically resistant animals (Miller et al., 1998; Pena et al., 2006) though the mechanism of such
resistance is not clearly demonstrated. Infections of nematode parasites result in mastocytosis,
eosinophilia, and raised levels of serum immunoglobulins (Huntley et al., 1992, 1995; Lacroux et
al., 2006). Immune responses to pathogens are mediated by cytokines. The most studied cytokines
include interferon (IFN)-γ, interleukine (IL)-2, IL-12, and tumor necrosis factor (TNF)-α for Th1
type, and IL-4, IL-5, IL-10, IL-11, and IL-13 for Th2 type immunity. Nematode parasites (such
as Haemonchus contortus) infection induces a decline in IFN-γ, increases in IL-4, IL-5 and IL-13
expression (Gill et al., 2000; Lacroux et al., 2006). These changes in cytokines may lead to
recruitment of mast cells, eosinophils, macrophages, and lymphocytes at the infected site (Huntley
et al., 1995; Balic et al., 2002; Perez et al., 2003). Mast cells may mediate expulsion of some
worms from the host gut. A study found that mast cells induced intestinal paracellular permeability
during helminth infection and the increased permeability was necessary for expulsion of worms
from the intestine in mouse (McDermott et al., 2003). Eosinophils kill certain types of parasites
by adhering to the worms or larvae and releasing their granule proteins and (or) superoxide radicals
that are toxic to the tegumental membrane of parasites (Caulfield, 1980). Despite the fact that H.
contortus infection induces eosinophilia and mastocytosis in goats and sheep, the eosinophil and
mast cell counts in animals infected with H. contortus are not consistently related to worm
resistance (Huntley et al., 1995; Chiejina et al., 2002; Muturi et al., 2005). In addition to these
cells, immunoglobulin A (IgA), IgE, and IgG4 increase when animals are infected with H.
contortus (Gill et al., 1994; Strain and Stear, 2001). These manifestations indicate a strong Th2
biased immune response. However, the long time survival and active fecundity of parasites in host
animals, even in genetically parasite-resistant animals (Gill et al., 1994; Strain and Stear, 2001;
Pena et al., 2006) suggest that the outcome of immunity is not sufficiently protective to the host.
The situation is further complicated by possible regulation by parasites. Emerging evidence
indicates that some nematode parasites are able to regulate their host’s immunity to create a
favorable environment for themselves (Maizels et al., 2004). The alteration of immune responses
by nematode infection has been evidenced in patients infected with other pathogens. The infection
of human T cell lymphotropic virus type 1 activates T cells, triggers an uncontrolled proliferation

41
of lymphocytes and a Th1 response characterized by a high level of IFN-γ and low levels of IL-5
and IL-10 expression (Porto et al., 2005). The expressions of these cytokines are reversed when
patients are coinfected with helminthic parasites (Porto et al., 2005). If the ineffective immune
response in ruminants is resultant of parasitic regulation, it becomes possible that a protective
immunity may be achieved by enhancing expression of certain cytokines of the hosts to overcome
the parasitic regulation.

Nutritional manipulation
Protein and amino acids. Protein intake affects resistance to internal parasites in both
ruminants and non-ruminants (Ing et al., 2000; Ford et al., 2001; Sykes and Coop, 2001).
Compared with those fed a straw-based diet (low in protein), sheep fed a lucerne-based diet (high
in protein) harbored less nematodes at 56 days after infection (Bawden, 1969). Supplementation
of a hay-based diet with fish meal (van Houtert et al., 1995) or soybean meal (Strain and Stear,
2001) substantially reduced worm burden in sheep infected with nematodes Trichostrongylus
colubriformis and H. contortus. In spite of the fact that goats are more susceptible to
gastrointestinal nematode infections than sheep (Pomroy et al., 1986; Lightbody et al., 2001), goats
respond to protein supplementation similarly. One investigation (Singh et al., 1995) showed that
worm burden was lower in goats fed supplemental protein (cottonseed meal) than in control
animals. The increased resistance to parasite infection by protein supplementation has been
attributed to improved immunity. This is because protein supplementation increases availability
of amino acids (Ipharraguerre et al., 2005) for immune cell proliferation and synthesis of
immunoglobulins. On the other hand, many of the amino acids, including arginine, cysteine and
glutamine, have been demonstrated to be involved in regulation of immune responses.
The regulating effect of glutamine on immunity in ruminants is evidenced by selectively
promoting certain subset of lymphocytes. Postruminal glutamine supplementation in dairy cows
consuming a corn silage and hay based diet increased the relative abundance of CD4+ cells
(Doepel et al., 2006). CD4+ cells are shown to be responsible for resistance to parasites in
genetically resistant sheep (Gill et al., 1993; Pena et al., 2006). Glutamine is used at a high rate
by lymphocytes and even higher if the lymphocytes are activated by mitogens (Brand et al., 1989;
Calder, 1995). The concentration of plasma glutamine decreased after extensive exercise and
athletic training in humans (Hack et al., 1997), which are associated with an increased

42
susceptibility to infections suggestively due to decline in glutamine supply to lymphocytes
(Newsholme and Calder, 1997). Indeed, increasing availability of glutamine enhances the
production of cytokines, such as IL-2, IL-10, and interferon-γ, by cultured lymphocytes (Rohde et
al., 1996; Yaqoob and Calder, 1998).
Cysteine may affect immunity through glutathione (GSH). The availability of cysteine is
a limiting factor for synthesis of GSH in animals. Supplementation with cysteine or its precursor,
methionine, to low protein diets increases tissue GSH concentrations (Alhamdan and Grimble,
2003). Glutathione plays a vital role not only in detoxification of free radicals and other oxidants
(Deneke, 2000; Lu, 2000) but also in modulation of immunological functions in humans and
animals (Droge et al., 1994). Clinical studies in humans indicate that HIV patients are more
susceptible to other infections and GSH deficiency is a key determinant of survival in HIV disease
(Herzenberg et al., 1997). Intracellular availability of GSH is critical to activity of many types of
cells including immune cells. Rats fed a lipid peroxide diet showed a marked depression of
intestinal mucosal proliferation and the depression was reversed by GSH supplementation
(Tsunada et al., 2003). Lymphocytes cannot proliferate when GSH is depleted (Hamilos et al.,
1989; Kavanagh et al., 1990). Intracellular concentration of GSH even determines the immune
responsive types. Antigen-presenting cells direct T-cell responses toward a Th1 or Th2 type
response, depending on the level of intracellular GSH. Th2 responses occur when GSH levels are
low (Peterson et al., 1998). This may be because the antigen-presenting cells cannot process the
antigen when their cellular concentration of GSH is low (Short et al., 1996). In addition, parasites
may alter the concentration of GSH in the locale where they are dwelling. An in vitro study with
nematode Ascaris suum indicated that the parasites could utilize exogenous GSH to replenish their
GSH level (Hussein and Walter, 1996). If this finding is plausible to other nematodes, the internal
parasites in animals will induce a GSH deficiency in their micro-environment. The low
concentration of GSH may lead to a lack of immune response in the animal.
Arginine as an immune regulator plays a critical role in the development of immunity.
Arginine supplementation in humans is associated with increased lymphocyte and monocyte
proliferation and Th cell formation (Barbul, 1990; Cerra, 1991), activation of macrophage
cytotoxicity, and increased cytokine production (Kirk and Barbul, 1990). Arginine deficiency
depresses early B cell maturation (de Jonge et al., 2002). This may explain why arginine
supplementation increases antibody production and enhances humoral immune response (Shang

43
et al., 2003; Moriguti et al., 2005). Furthermore, arginine may affect immunity by regulating
lymphocyte migration between blood stream and other tissues. Sufficient supply of arginine is
essential for mononuclear cell migrating through the layer of endothelial cells prestimulated with
cytokines (Isenberg, 2003).
Doubtlessly the amino acids play a crucial role in immune regulation and it is very likely
that they act orchestraly upon immune responses. More work focusing on the exact mechanisms
by which the amino acids finely tune the immunity will be necessary for efficiently using amino
acids in the strategy of parasite control in goats. In addition to elevating availability of amino
acids, protein supplementation increases production of ruminal volatile fatty acids (VFA)
(Ipharraguerre et al., 2005). The VFA are not only a major energy source for ruminants but also
involved in immune regulation.
Volatile fatty acids. The three major ruminal VFA, acetic, propionic and butyric acids, can
influence different arms of the immunity. Butyrate depresses production of IL-12 and IFN-γ, and
increase expression of IL-4 and IL-10 in monocytes (Saemann et al., 2000). Since the IL-4 and
IL-10 are important cytokines for Th2 immunity which is responsible for expulsion of some
nematode parasites (Finkelman et al., 1997; Miller and Horohov, 2006), butyrate may be a potent
player in the immune response to internal parasites in ruminants. Acetate and propionate are able
to activate G protein-coupled receptors GPR41 and GPR43 in adipocytes and monocytes (Brown
et al., 2003) and mast cells (Karaki et al., 2006). The activated GPR41 and GPR43 stimulate leptin
production (Xiong et al., 2004; Covington et al., 2006). It has been reported that leptin tends to
skew the immune response to a Th1 immunity (Lord, 2002), which may result from the negative
regulation of regulatory T cells by leptin (De Rosa et al., 2007). From these findings it becomes
possible that an enhanced immunity to internal parasites may be achieved by manipulating ruminal
VFA ratio. Indeed the ratios of ruminal VFA can be altered by dietary protein sources (Litherland
et al., 2000), and the proportion of butyric acid increases when animals are fed a diet high in protein
(Ipharraguerre et al., 2005). Given the immune regulating nature, more work is needed to define
the importance of VFA in immunity to internal parasites.
Minerals. The effects of minerals on immunity to internal parasitism have been reviewed
recently in detail (McClure, 2008). Here we briefly review the application of copper oxide wire
particles (COWP) in treatment of parasitism. The COWP, a supplementary form for copper
deficiency in small ruminants, has been found to be effective in treatment of internal parasites in

44
sheep (Bang et al., 1990; Knox, 2002; Burke et al., 2004, 2006, 2007). The research in goats has
produced mixed results. Glennon et al. (2004) observed a 32% to 41% reduction in fecal egg
counts (FEC) in yearling goats receiving 5 g of COWP and a 57% reduction with a 10 g dose. In
their subsequent study (Lugginbuhl et al., 2006) COWP did not seem to have any effect on FEC
in weanling goats receiving 2.5 g COWP. However, Burke et al. (2007) found that COWP capsules
were effective as an anthelmintic for up to 21 days after dosing and a dose as little as 0.5 g was
effective for weanlings and 5 g for mature goats. Furthermore, COWP is more effective against
H. contortus (Burke et al., 2007) and less effective to Teledorsagia, Trichostrongylus or Trichuris
genus (Pomroy and Adlington, 2006). Nevertheless, more studies are needed in the area to use
COWP capsules as an alternative anthelmintic.

Selection of resistant animals


The capability of resistance to internal parasites may be achieved through genetic selection.
The genetic trait is measured generally by FEC. It has been noticed that some breeds of goats are
more resistant to internal parasites than others. For example, the Small East African goats have
lower FEC and higher PCV as compared to the Galla goats throughout the year and the difference
is even greater during lactation (Baker et al., 1998). Similarly, Kiko or Spanish breeds seem to be
more resistant than Boer goats (Browning et al., 2007). Pralomkarn et al. (1997) also observed
that Thai native goats had much lower FEC than crosses of 50 and 75% Anglo Nubian. Only 8%
of a trickle infection became established in the Thai native goats as compared to 17% for the Anglo
Nubian crosses. Even in the same breed, FEC of individual animals are not normally distributed,
but are rather over dispersed with a positive skewness (Hoste et al., 2001). A few individual
animals of the population have most of the worms (Costa et al., 2000). Typically 20-30% of the
goats in a herd have 70-80% of the worms and the FEC are relatively repeatable (Hoste et al.,
2001). Vlassoff et al. (1999) observed a considerable individual variability in FEC of Angora
goats following either a natural or experimental challenge infection. Repeatabilities of 0.22 to
0.41 are similar to those observed in sheep. This indicates that they are heritable since the
repeatability is the upper limit for heritability. Though the heritability estimates for FEC are
moderately low in goats (average 0.29; range 0.19 to 0.37) (Mandonnet et al., 2001; Olayemi et
al., 2002), establishing a resistant sub-breed is possible. Ruvuna et al. (1984) was able to select
divergent groups of animals. The selected group of animals which comprised 11% of the initial

45
population had a FEC of only 15% of the remainder of the population. Rohrer et al. (1991) reported
a heritability of FEC in this population to be 0.4. The does of cashmere goats that were selected
for seven generations for parasite resistance in Scotland had 35% lower fecal egg counts than their
unselected counterparts (Jackson, 2002).
The mechanism for heritability is not well established. The genes for the major
histocompatability complex of the immune system in sheep have been identified as candidates
(Benavides et al., 2002). The genetic trait measured (FEC) may be affected directly by genetic
effects on immune system (Fakae et al., 1999), or indirectly through improved diet selection for
improved nutrition, or grazing habits which reduce exposure to infective helminth larvae
(Hutchings et al., 2007). There may also be other factors involved as Hutchings et al. (2007)
identified that animals with lower FEC picked up fewer larvae due to their grazing habit.
Nevertheless, there is a great need for the establishment of a breeding program utilizing the major
goat breeds available in the US. Genetically selected lines of goats that are resistant to H. contortus
could be distributed to aid in developing genetic resistance in goat herds. In addition, this research
would increase our understanding of mechanisms of inheritance as well as biology of the host-
parasite interaction. If such program is initiated by a national breed registry, the production losses,
cost of treatment, morbidity and mortality in the goat industry could be greatly reduced. Producers
could also use FAMACHA scores and/or the number of times that a goat required deworming as
the basis for culling and gradually eliminate those animals (and their genes) from the flock. This
would be very easy to implement. The meat goat industry could do well to follow the program
initiated by the Katahdin sheep breeders to measure resistance under field conditions by taking
fecal samples according to a standardized protocol and then calculating expected progeny
differences for parasite resistance. Such information can be used for genetic selection of animals
for resistance to internal parasites.

Vaccination
Early research showed that sheep could be vaccinated with X-irradiated H. contortus larvae
and develop immunity to the worm (Jarrett et al., 1959). In subsequent research immunoprotection
against H. contortus was conferred after immunization with cysteine protease enriched protein
fraction (Ruiz et al., 2004). A degree of immunity in goats can be developed by natural parasite
infection (Pomroy et al., 1989). There has been a tremendous effort in Australia and New Zealand

46
to develop a vaccine for control of helminth. Although most vaccines would be specific for only
one species of helminth, this would still be effective since usually only one species predominates
in a given season.

Summary and future research


Internal parasitism significantly reduces performance of goats and increases costs of
production. In the face of anthelmintic resistance, alternative approaches have been explored
extensively. Nutritional, especially protein, supplementation plays an important role in immune
response. Amino acids do not only serve as substrates for immunoglobulin synthesis but also act
as regulators of cytokine expression. The same importance is for VFA that exert regulatory roles
in immunity. This area warrants more work to clarify how these molecules mediate the immune
responses. The results of using COWP to treat internal parasites in goats are not consistent and
more studies are needed to substantiate the effectiveness and define the dosage. Genetically
selection for resistant populations is a promising approach and there is a great need for the
establishment of a breeding program utilizing the major goat breeds available in the US. The
tannin-containing plants and nematophagus fungi possess a potential anthelmintic activity. More
research is needed to finalize the dosages and a strategy to apply them in the practical goat
production. Most importantly, the mechanisms of immune responses to internal parasites are not
understood fully. Much work is needed to demonstrate how the host to react to the infection of
parasites and whether the parasites manipulate the immune outcome of the host. Only if the
specific pathways of immune responses are clearly elucidated, a precise manipulation on immunity
becomes possible.

Reference

Alhamdan, A. A., and R. F. Grimble. 2003. The effect of graded levels of dietary casein, with or
without methionine supplementation, on glutathione concentration in unstressed and
endotoxin-treated rats. Int. J. Vitam. Nutr. Res. 73:468-477.
Baker, R. L., D. M. Mwamachi, J. O. Audho, E. O. Aduda and W. Thorpe. 1998. Reisstance of
Galla and Small East African goats in the sub-humid tropics to gastrointestinal nematode
infections and the peri-parturient rise in fecal egg counts. Vet. Parasitol. 79: 53-64.

Balic, A., V. W. Bowles, and E. N. T. Meewsen. 2002. Mechanisms of immunity to Haemochus


contortus populations in sheep. Parasite Immunol. 24:39-46.

47
Bang, K.S., A. S. Familton, A. R. Sykes. 1990. The effect of copper oxide wire particle treatment
on establishment of major gastrointestinal namatodes in lambs. Res. Vet. Sci. 49:132-137.

Barbul, A. 1990. Arginine and immune function. Nutrition 6:53-58.


Bawden, R. J. 1969. The establishment and survival of Oesophagostomum columbianum in male
and female sheep given high and low protein diets. Aust. J. Agric. Res. 20:1151-1159.
Benavides, M. V., T. A. Weimer, M. F. S. Borba, M. E. A. Berne, and A. M. S. Sacco. 2002.
Association between microsatellite markers of sheep chromosome 5 and faecal egg counts.
Small Rum. Res. 46:97-105.

Brand, K., W. Fekl, J. von Hintzenstern, K. Langer, P. Luppa, and C. Schoerneret. 1989.
Metabolism of glutamine in lymphocytes. Metabolism 38(Suppl. 1):29-33.
Brown, A. J., S. M. Goldsworthy, A. A. Barnes, M. M. Eilert, L. Tcheang, D. Daniels, A. I. Muir,
M. J. Wigglesworth, I. Kinghorn, N. J. Fraser, N. B. Pike, J. C. Strum, K. M. Steplewski, P. R.
Murdock, J. C. Holder, F. H. Marshall, P. G. Szekeres, S. Wilson, D. M. Ignar, S. M. Foord,
A. Wise, and S. J. Dowell. 2003. The orphan G protein-coupled receptors GPR41 and GPR43
are activated by propionate and other short chain carboxylic acids. J. Biol. Chem. 278:11312–
11319.

Burke, J. M., and J. E. Miller. 2006. Evaluation of multiple low doses of copper oxide wire
particles compared with levamisole for control of Haemonchus contortus in lambs. Vet.
Parasitol. 139:145-149.

Burk, J. M., J. E. Miller, D. D. Olcott, B. M. Olcott, and T. H. Terrill. 2004. Effect of copper oxide
wire particles dosage and feed supplement level on Haemonchus contortus infection in lambs.
Vet. Parasiuitol. 123:235-243.

Burke, J. M. D. Morrical, and J. E. Miller. 2007. Control of gastrointestinal nematodes with copper
oxide wire particles in a flock of lactating Polypay ewes and offspring in Iowa, USA. Vet.
Parasitol. 146:372-375.

Burke, J. M., T. H. Terrill, R. R. Kallu, J. E. Miller, and J. Mosjidis. 2007. Use of copper oxide
wire particles to control gastrointestinal nematodes in goats. J. Anim. Sci. 85:2753-2761.

Cabaret, J. 2000. Anthelmintic resistance in goats: from fiction to facts. Pages 793-794 in:
Proceeding of the 7th international conference on goats. Tours-Poitiers, France.
Calder, P. C. 1995. Fuel utilization by cells of the immune system. Proc. Nutr. Soc. 54:65-82.
Caulfield, J. P. 1980. The adherence of human neutrophils and eosinophile to schistosomula:
evidence for membrane fusion between cells and parasites. J. Cell Biol. 86:46-63.
Cerra, F. B. 1991. Nutrition modulation of inflammatory and immune function. Am. J. Surg.
161:230-234.

48
Chiejina, S. N., B. B. Fakae, J. M. Behnke, P. A. Nnadi, G. A. Musongong, and D. Wakelin. 2002.
Expression of acquired immunity to a local isolate of Haemonchus contortus by the Nigerian
West African Dwarf goat. Vet. Parasitol. 104:229-242.
Costa, C. A. F., L. Da S. Vieira, M. E. A. Bverne, M. U. E. D. Silva, A. L. Guidoni and E. A. P.
Figueiredo. 2000. Variability of resistance in goats infected with Haemonchus contortus in
Brazil. Vet. Parasitol. 88:153-158.

Covington, D. K., C. A. Briscoe, A. J. Brown, and C. K. Jayawickreme. 2006. The G-protein-


coupled receptor 40 family (GPR40–GPR43) and its role in nutrient sensing. Biochem. Soc.
Transact. 34:770-773.

De Jonge, W. J., K. L. Kwikkers, A. A. te Velde, et al. 2002. Arginine deficiency affects early B
cell maturation and lymphoid organ development in transgenic mice. J. Clin. Invest. 110:1539-
1548.
Deneke, S. M. 2000. Thiol-based antioxidants. Curr. Top. Cell. Regul. 36:151-180.
De Rosa, V., C. Procaccini, G. Calı, G. Pirozzi, S. Fontana, S. Zappacosta, A. La Cava, and G.
Matarese. 2007. A key role of leptin in the control of regulatory T cell proliferation. Immunity
26:241–255.

Doepel, L., M. Lessard, N. Gagnon, G. E. Lobley, J. F. Bernier, P. Dubreuil, and H. Lapierre.


2006. Effect of Postruminal Glutamine Supplementation on Immune Response and Milk
Production in Dairy Cows. J. Dairy Sci. 89:3107–3121.

Droge, W., K. Schulze-Osthoff, S. Mihm, D. Galter, H. Schenk, H. Eck, S. Roth, and H. Gmunder.
1994. Functions of glutathione and glutathione disulfide in immunology and
immunopathology. FASEB J. 8:1131-1138.
Finkelman, F. D., T. Shea-Donohue, J. Goldhill, C. A. Sullivan, S. C. Morris, K. B. Madden, W.
C. Gause, and J. F. Urban, Jr. 1997. Cytokine regulation of host defense against parasitic
gastrointestinal nematodes: Lessons from studies with rodent models. Annu. Rev. Immunol.
15:505-533.

Ford, J. T., C. W. Wong, and I. G. Colditz. 2001. Effects of dietary protein types on immune
responses and levels of infection with Eimeria vermiformis in mice. Immunol. Cell Biol.
79:23-28.
Gatongi, P. M., M. E. Scott, S. Ranjan, J. M. Gathuma, W. K. Munyua, H. Cheruiyot, and R. K.
Prichard. 1997. Effects of three nematode anthelmintic treatment regimes on flock
performance of sheep and goats under extensive management in semi-arid Kenya. Vet.
Parasitol. 68:323–336.

Gill, H. S., A. J. Husband, D. L. Watson, and G. D. Gray. 1994. Antibody-containing cells in the
abomasal mucosa of sheep with genetic resistance to H. contortus. Res. Vet. Sci. 56:41-47.

49
Gill, H. S., D. L. Watson, and M. R. Brandon. 1993. Monoclonal antibody to CD4+ T cells
abrogates genetic resistance to Haemonchus contortus in sheep. Immunology 78:43-49.

Glennon, H. M., J-M. Luginbuhl, J. P. Mueller, A. M. Zajac, K. L. Anderson, J. W. Spears, T. T.


Brown, and C. Brownie. 2004. Effect of copper oxide needles on gastrointestinal parasites in
grazing meat goats. J. Anim. Sci. 82(Suppl. 2):29.

Hack, V., C. Weiss, B. Friedmann, S. Suttner, M. Schykowski, N. Erbe, A. Benner, P. Bartsch,


and W. Drogeet. 1997. Decreased plasma glutamine level and CD4+ T cell number in response
to endotoxin shock in the rat. Am. J. Physiol. Endocrinol. Metab. 272:E788-E795.
Hamilos, D. L., P. Zelarney, and J. J. Mascali. 1989. Lymphocyte proliferation in glutathione-
depleted lymphocytes: direct relationship between glutathione availability and the proliferative
response. Immunopharmacology 18: 223-235.
Herzenberg, L. A., S. C. De Rosa, J. G. Dubs, M. Roederer, M. T. Anderson, S. W. Ela, S. C.
Deresinski, and L. A. Herzenberg. 1997. Glutathione deficiency is associated with impaired
survival in HIV disease. Proc. Natl. Acad. Sci. USA 94:1967-1972.
Hoste, H., Y. H. L. Frileux, and A. Pommaret. 2001. Distribution and repeatability of faecal egg
counts and blood parameters in dairy goats naturally infected with gastrointestinal nematodes.
Res. Vet. Sci. 70:57-60.

Hoste, H., F. Jackson, S. Athanasiadou, S. Thamsborg, and S.O. Hoskin. 2006. Anthelmintic
effects of tanniferous plants on nematodes in ruminants. Trends parasitol. 22:253-261.

Huntley, J. F., M. Patterson, A. Mackellar, F. Jackson, L. M. Stevenson, and R. L. Coop. 1995. A


comparison of the mast cell and eosinophil responses of sheep and goats to gastrointestinal
nematode infections. Res. Vet. Sci. 58:5-10.
Hussein, A. S. and R. D. Walter. 1996. Inhibition of glutathione synthesis of Ascaris suum by
buthionine sulfoximine. Parasitol. Res. 82:372-374.
Hutchings, M. R., K. J. K. Knowler, R. McAmnulty, and J. C. McEwan. 2007. Genetically resistant
sheep avoid parasites to a greater extent than do susceptible sheep. Proc. Biol. Sci 274:1839-
1844.

Ing, R., Z. Su, M. E. Scott, and K. G. Koski. 2000. Suppressed T helper 2 immunity and prolonged
survival of a nematode parasite in protein-malnourished mice. Proc. Natl. Acad. Sci. USA
97:7078-7083.
Ipharraguerre, I. R., J. H. Clark, and D. E. Freeman. 2005. Varying Protein and Starch in the Diet
of Dairy Cows. I. Effects on Ruminal Fermentation and Intestinal Supply of Nutrients. J. Dairy
Sci. 88:2537–2555.

Isenberg J. S. 2003. Modulating effects of l-arginine on cytokine-stimulated lymphocyte migration


in vitro. Microsurgery 23:262-267.

50
Jackson, F., D. McBean, E. Jackson, D. Bartley, M. Merchant, and S. Bishop. 2002. The
responsiveness against gastrointestinal nematodes of a selected line of Scottish cashmere goats.
In 3rd International conferences: Novel approaches-A workshop meeting on helminth control
in livestock in the New Millennium.

Jarrett, W. F. H., F. W. Jennings, W. I. M McIntyre, W. Mulligan and N. C. C. Sharp. 1959. Studies


on immunity to Haemonchus contortus infection-Vaccination of sheep using a single dose of
X-irradiated larvae. Am. J. Vet. Res. 20:527-536.

Kaplan, R. M. 2004. Drug resistance in nematodes of veterinary importance: a status report. Trends
Parasitol. 20:477-81.

Kaplan, R. M., J. M. Burke and T. H. Terrill. 2005. Total anthelmintic failure on a meat goat farm
in Arkansas. Proc. Am. Assoc. Vet. Parasitol.

Karaki, S. I., R. Mitsui, H. Hayashi, I. Kato, H. Sugiya, T. Iwanaga, J. Furness, and A. Kuwahara.
2006. Short-chain fatty acid receptor, GPR43, is expressed by enteroendocrine cells and
mucosal mast cells in rat intestine. Cell Tissue Res. 324:353–360.

Kavanagh, T. J., A. Grossmann, E. P. Jaecks, J. C. Jinneman, D. L. Eaton, G. M. Martin, and P. S.


Rabinovitch. 1990. Proliferative capacity of human peripheral blood lymphocytes sorted on
the basis of glutathione content. J. Cell. Physiol. 145: 472-480.

Kirk, S. J. and A. Barbul. 1990. Role of arginine in trauma, sepsis, and immunity. J. Paren. Ent.
Nutr. 14:226S-229S.

Knox, M. R. 2002. Effectiveness of copper oxide wire particles for Haemonchus contortus control
in sheep. Aust. Vet. J. 80:224-227.

Lacroux, C., T. Nguyen, O. Andreoletti, F. Prevot, C. Grisez, J. Bergeaud, L. Gruner, J. Brunel,


D. Francois, P. Dorchies, and P. Jacquiet. 2006. Haemonchus contortus (Nematoda:
Trichostrongylidae) infection in lambs elicits an unequivocal Th2 immune response. Vet. Res.
37:607-622.
Lightbody, J. H., L. M. Stevenson, F. Jackson, K. Donaldson, and D. G. Jones. 2001. Comparative
aspects of plasma antioxidant status in sheep and goats, and the influence of experimental
abomasal nematode infection. J. Comp. Pathol. 124:192-199.

Litherland, A. J., T. Sahlu, C. A. Toerien, R. Puchala, K. Tesfai, A. L. Goetsch. 2000. Effects of


dietary protein sources on mohair growth and body weight of yearling Angora doelings. Small
Rumin. Res. 38:29-35.

Lord, G. 2002. Role of leptin in immunology. Nutr. Rev. 60:S35-S38.

Lu, S. C. 2000. Regulation of glutathione synthesis. Curr. Top. Cell. Regul. 36:95-116.

51
Luginbuhl, J-M., H. M. Glennon and J. P. Mueller. 2006. Effect of copper-oxide needles on
gastrointestinal parasites in weanling meat goats control-grazed on bermudagrass pastures. J.
Anim. Sci. 84(Supp. 2):21.

Maizels, R. M., A. Balic, N. Gomez-Escobar, M. Nair, M. D. Taylor and J. E. Allen. 2004.


Helminth parasites – masters of regulation. Immunol. Rev. 201:89-116.

Mandonnet, N., G. Aumont, J. Fleury, R. Arquet, H. Varo, L. Gruner, J. Bouix and J. V. T. Kahang.
2001. Assessment of genetic variability of resistance to gastrointestinal nematode parasites in
Creole goats in the humid tropics. J. Anim. Sci 79:1706-1712.

McDermott, J. R., R. E. Bartram, P. A. Knight, H. R. Miller, D. R. Garrd, and R. K. Grencis.


2003. Mast cells disrupt epithelial barrier function during enteric nematode infection. Proc.
Natl. Acad. Ssc. USA 100:7761-7766.
Miller, J. E., M. Bahirathan, S. L. Lemarie, F. G. Hembry, M. T. Kearney, and S. R. Barras. 1998.
Epidemiology of gastrointestinal nematode parasitism in Suffolk and Gulf Coast Native sheep
with special emphasis on relative susceptibility to Haemonchus contortus infection. Vet.
Parasitol. 74:55–74.

Miller, J. E., and D. W. Horohov. 2006. Immunological aspects of nematode parasite control in
sheep. J. Anim. Sci. 84(E. Suppl.):E124-E132.

Moriguti, J. C., E. Ferriolli, E. A. Donadi and J. S. Marchini. 2005. Effects of arginine


supplementation on the humoral and innate immune response of older people. Eur. J. Clin.
Nutr. 59:1362–1366.

Mortenson, L. L., L. H. Williamson, T. H. Terrill., R. Kircher, M. Larsen, & R. M. Kaplan. 2003.


Evaluation of prevalence and clinical implications of anthelmintic resistance in gastrointestinal
nematodes of goats. J. Am. Vet. Med. Assoc. 223:495-500.

Muturi, K. N., J. R. Scaife, M. A. Lomax, F. Jackson, J. Huntley, and R. L. Coop. 2005. The effect
of dietary polyunsaturated fatty acids (PUFA) on infection with nematodes Ostertagia ostertagi
and Cooperia oncophora in calves. Vet. Parasitol. 129:273-283.

Newsholme, E.A., and P. C. Calder. 1997. The proposed role of glutamine in some cells of the
immune system and speculative consequences for the whole animal. Nutrition 13:728-730.

Olayemi, M. E., S. W. Walkden-Brown, J. H. J. van der Werf and L. F. Le Jambre. 2002. Genetic
variability of resistance indicators for gastrointestinal nematode infection in Angora and
Cashmere goats. 7th World Congress on Genetics Applied to livestock Production.
Montpellier, France.

52
Pena, M. T., J. E. Miller, and D. W. Horohov. 2006. Effect of CD4+ T lymphocyte depletion on
resistance of Gulf Coast Native lambs to Haemonchus contortus infection. Vet. Parasitol.
138:240–246.

Pena, M. T., J. E. Miller, M. E. Fontenot, A. Gillespie, and M. Larsen.2002. Evaluatation of


Duddingtonia flagrans in reducing infective larvae of Haemonchus contortus in feces of sheep.
Vet. Parastitol. 103:259-265

Perez, J., P. M. Garcia, E. M. Hernandez, S. Camara, A. Martinez-Moreno. 2003. Experimental


haemonchosis in goat: effects of single and multiple infections in the host response. Vet.
Parasitol. 111:333-342.
Peterson, J. D., L. A. Herzenberg, K. Vasquez, and C. Waltenbaugh. 1998. Glutathione levels in
antigen-presenting cells modulate Th1 versus Th2 response patterns. Proc. Natl. Acad. Sci.
USA. 95: 3071-3076.
Pomroy, W. E., and B. Adlington. 2006. Efficacy of Sulla (Hadysarium coronarium) and copper
oxide wire particles against a mixed natural infections of gastrointestinal nematodes in goats.
Vet. Parasitol. 136:363.

Pomroy, W. E., and W. A. G. Chaarleston. 1989. Development of resistance to Trichostrongylus


colubriformis in goats. Vet. Parasit. 33:283-288.

Pomroy, W. E., S. P. Hart, and B. R. Min. 2002. Rotational grazing as a parasite management tool
for goats. J. Anim. Sci. 80 (Suppl. 2):193.

Pomroy, W. E, W. G. Lambert, and K. Betteridge. 1986. Comparison of faecal strongylate egg


counts of goats and sheep on the same pasture. N. Z. Vet. J. 34:36-37.
Porto, A. F., S. B. Santos, A. L. Muniz, V. Basílio, W. Rodrigues, Jr., F. A. Neva, W. O. Dutra, K.
J. Gollob, S. Jacobson, and E. M. Carvalho. 2005. Helminthic Infection Down-Regulates Type
1 Immune Responses in Human T Cell Lymphotropic Virus Type 1 (HTLV-1) Carriers and Is
More Prevalent in HTLV-1 Carriers than in Patients with HTLV-1 Associated
Myelopathy/Tropical Spastic Paraparesis. J. Infect. Dis. 191:612-618.
Pugh, D. G. and C. B. Navarre. 2001. Internal parasite control strategies. The veterinary Clinics
of North America: Food Animal Practice 17:231-244.

Rohde, T., D. A. MacLean, and B. K. Pederson. 1996. Glutamine, lymphocyte proliferation and
cytokine production. Scand. J. Immunol. 44:648-650.
Rohrer, G. A. S., J. F. Taylor, S. K. Davis, R. M. Waruiru, F. Ruvuna and B. A. J. Mwandotto.
1991. The use of randomly amplified polymorphic DNA marker (RAPD) in an analysis of
susceptibility to Haemonchus and coccidia infestations in goats. J. Anim. Sci. 69(Suppl2):2.

53
Ruiz, A., J. M. Molina, J. F. Gonzalez, M. M. Conde, S. Martin and Y. I. Hernandez. 2004.
Immunoprotection in goats against Haemonchus contortus after immunization with cysteine
protease enriched protein fractions. Vet. Res. 35:565-572.

Ruvuna, F., R. M. Waruiru, J. F. Taylor, S. K. Davis, B. A. J. Mwandotto, F. R. Rurangirwa and


T. C. McGuire. 2003. Production parameters and resistance to gastrointestinal helminths of the
Kenya dual purpose goats. Pages 652-657 in Recent Advances in Goat Production. C. Gall, ed.

Saemann, M. D., G. A. Böhmig, C. H. Osterreicher, H. Burtscher, O. Parolini, C. Diakos, J. Stockl,


W. H. Horl, G. J. Zlabinger. 2000. Anti-inflammatory effects of sodium butyrate on human
monocytes: potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J.
14:2380-2382.

Shang, H., H. Tsai, W. Chiu, and S. Yeh. 2003. Effects of dietary arginine supplementation on
antibody production and antioxidant enzyme activity in burned mice. Burns 29:43–48.

Short, S., B. I. Merkel, R. Caffrey, and K. L. McCoy. 1996. Defective antigen processing correlates
with a low level of intracellular glutathione. Eur. J. Immunol. 26: 3015-3020.
Singh, R., M. R. Knox, R. A. Leng and J. V. Nolan. 1995. Aspects of parasite management in
goats. Page 54 in: Novel Approches to the Control of Helminth Parasites of Livestock, H. S.
Hill, ed., University of New England, Armidale, NSW, Australia.
Strain, S. A., and M. J. Stear. 2001. The influence of protein supplementation on the immune
response to Haemonchus contortus. Parasite Immunol. 23:527-531.
Sykes, A. R., and R. L. Coop. 2001. Interaction between nutrition and gastrointestinal parasitism
in sheep. New Zeal. Vet. J. 49:222-226.
Terrill, T. H., R. M. Kaplan, M. Larsen, O.M. Samples, J. E. Miller and S. Gelaye. 2001.
Anthelmintic resistance on goat farms in Georgia: efficacy of anthelmintics against
gastrointestinal nematodes in two selected goat herds. Vet. Parasitol. 97:261-268.

Thamsborg, S. M., R. J. Jorgensen, P. J. Waller and P. Nansen. 1996. The influence of stocking
rate on gastrointestinal nematode infections of sheep over a 2-year grazing period. Vet.
Parasitol. 67:207-224.

Tsunada, S., R. Iwakiri, T. Noda, K. Fujimoto, J. Fuseler, C. A. Rhoads, and T. Y. Aw. 2003.
Chronic exposure to subtoxic levels of peroxidized lipids suppresses mucosal cell turnover in
rat small intestine and reversal by glutathione. Dig. Dis. Sci. 48:210-222.
USDA-APHIS-VS. 2003. Part II. Reference of Sheep Health in the United States, 2001.
USDA:APHIS:VS, CEAH, Natl. Anim. Health Monitoring System, Fort Collins, CO.

Valentine, B. A., C. K. Cebra, and G. H. Taylor. 2007. Fatal gastrointestinal parasitism in goats:
31 cases (2001-2006). J. Am. Vet. Med. Assoc. 231:1098-1103.

54
Van Houtert, M. F. J., I. A. Barger, J. W. Steel, R. G. Windon, and D. L. Emery. 1995. Effects of
dietary protein intake on responses of young sheep to infection with Trichostrongylus
colubriformis. Vet. Parasitol. 56:163-180.
Vlassoff, A., S. A. Bisset, and L. W. McMurtry. 1999. Faecal egg counts in Angora goats following
natural or experimental challenge with nematode parsites: within-flock variability and
repeatabilities. Vet. Parasitol. 84:113-123.

Xiong, Y., N. Miyamoto, K. Shibata, M. A. Valasek, T. Motoike, R. M. Kedzierski, and M.


Yanagisawa. 2004. Short-chain fatty acids stimulate leptin production in adipocytes through
the G protein-coupled receptor GPR41. Proc. Natl. Acad. Sci. USA 101: 1045-1050.

Yaqoob, P., and P. C. Calder. 1998. Cytokine production by human peripheral blood mononeuclear
cells: Differential sensitivity to glutamine availability. Cytokine 10:790-794.
Zajac, A. M. and T. A. Gipson. 2000. Multiple anthelmintic resistance in a goat herd. Vet.
Parasitol. 87:163-172.

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Chapter 8. Decreasing Barber Pole
Populations on Grass Pastures: Is Liquid
Nitrogen Fertilizer a Viable Alternative?
Dr. JM Luginbuhl, Extension Specialist (Goats & Forage Systems)(919) 515-8743 jean-
[email protected] and Soil Sciences - NC State University

As it is well known, barber pole larvae show increased


resistance to commercial anthelmintics drenched to small ruminant livestock, and
producers are looking for other alternatives. What about bypassing the livestock entirely
and applying a larvicidal product directly on the pasture itself?
Studies we conducted at North Carolina State University showed that 96.6% L3 barber
pole larvae were not moving or dead when immersed in solutions of liquid nitrogen
fertilizer (containing 32.7% urea and 42.2% ammonium nitrate [21.1% ammonium and
21.1% nitrate), corresponding to field applications of 30 lb of nitrogen per acre. Another
laboratory study showed that a 10% solution of household bleach (5.25% sodium
hypochlorite) resulted in 99.1% of L3 larvae not moving or dead. Higher solutions of
household bleach caused lysis (disintegration) of the larvae.
The larvicidal action of liquid nitrogen fertilizer has been attributed to the toxic qualities
of ammonia and nitrate, as well as to the increased osmotic pressure created with an

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accompanying water loss when in direct contact with L3 larvae. Do you remember as a
child how water leaked out of slugs when dribbling table salt on them?

One agricultural practice recommended


by the N.C. Cooperative Extension Service is to apply 50 lb of nitrogen fertilizer per acre
to cool-season grasses such as fescue and orchardgrass both in early spring and late
summer, and one or several applications during summer for warm-season grasses such as
bermudagrass, millet and sorghum. So, could we pop two balloons with one dart by
fertilizing pastures with liquid nitrogen fertilizer to promote forage growth and at the same
time reducing pasture nematode larvae population, their subsequent ingestion by grazing
animals and ultimately reducing gastrointestinal parasite loads?

Experimentation

We conducted 3 experiments to test this


hypothesis on predominantly tall fescue pastures, one in spring and two in fall. In each of
these experiments, a field was grazed by does heavily infected with gastrointestinal
parasites for 21 to 26 days until the ground was well covered by fecal pellets. The goats
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were then removed from the field, which was immediately flail-chopped (forage was cut
and moved off-site) to a height of 5 inches. Then, according to experimental principles that
took into account differences in slope, soil, etc., the fields were divided into several sub-
pastures so that each experimental treatment was replicated 3 or 4 times. Sub-pastures
within each replication were then randomly assigned to be either treated with liquid
nitrogen fertilizer or untreated (control). Granular urea was applied to the untreated
(control) sub-pastures to ensure that forage would grow at an equal rate in all sub-pastures
and because granular urea has a very limited negative effect of L3 larvae survival. As
infective L3 larvae migrate up the blades of forage crops during mornings and evenings
with the dew, we sprayed pastures with liquid nitrogen fertilizer starting at 6:30 AM or
after 4PM depending on weather conditions. Large amounts of liquid nitrogen can be lost
from evaporation to the atmosphere if applied under full sun, and may also burn the tip of
leaves.
A 4th experiment was conducted on bermudagrass during the summer. The differences in
preparing the field compared to the previous 3 experiments were the following: the field
was only contaminated for 11 days, forage was flail-chopped 3 days later, and liquid
nitrogen fertilizer was only applied 11 days later.
Five days after applying liquid nitrogen or urea, ‘clean’ goats were randomly assigned to
each plot and control-grazed. Why the 5-day delay? Because we were concerned with
nitrate poisoning if goats had been turned immediately into the sub-pastures that had been
sprayed with liquid nitrogen.

Fecal egg counts were performed on all goats as they were entering the sub-pastures to get
a baseline count. We also took blood samples to determine packed cell volume, and

58
FAMACHA-scored the lower eyelids of each goat. All sampling and scoring took place on
a weekly basis.
The Bottom Line
Nothing is simple when dealing with biology and dynamic environmental conditions one
cannot control.

1. Results from experiments conducted in the laboratory do not necessarily translate into
the same outcome in field situations. The field experiments described above
necessitated a large amount of coordination, resources and labor, the results were
disappointing with the exception of Expt. 1 conducted under ideal environmental
conditions (rainfall and temperature), and many questions still remain unanswered.

2. The main limitation of liquid nitrogen is that it kills or incapacitates larvae on contact
and that its effectiveness is very short-lived, such that on a heavily contaminated field
another crop of larvae may hatch and molt as soon as the effect of liquid nitrogen has
disappeared (Expt. 4). In addition, as larvae can bury in the forage mat or the soil, or
stay at the base of forage plants for protection from desiccation, it is important to spray
liquid nitrogen very early in the morning when the dew is still present, or late in the
day under cloudy skies, on forage that is not more than 5 inches in height. Therefore,
another limitation is owning or having access to a flail-chopper, a tractor and a boom-
sprayer. Finally, not everybody has easy access to a source of liquid nitrogen fertilizer.

3. Adequate temperature and moisture are necessary for larvae to hatch, molt and migrate
onto the leaves of forage crops. In the absence of rainfall during the contamination
period (Expt. 2), only a minimum number of larvae will hatch and molt, whereas the
majority will stay protected in the fecal pellets and wait for outside conditions that
will favor their survival.

4. Spraying liquid nitrogen on pastures during dry conditions (Expt. 2) will be less
effective or not effective at all due to the combination of the short effectiveness of
liquid nitrogen and the low number of larvae that hatched, molted and migrated to
grass blades. In addition, liquid nitrogen will have no effect on eggs still in the fecal
pellets. If adequate amounts of rain falls following a drought, fecal egg counts will
shoot up within the next 2 to 3 weeks (Expt. 2), even on the plots previously sprayed
with liquid nitrogen.

5. Too much rain on a field having a certain slope may mean that most of the feces and
larvae could be washed away from the experimental plots, resulting in low fecal egg
counts for more than a month (Expt. 3) due to a hurricane passing through the day
after nitrogen was applied. Nonetheless, larvae and feces may accumulate on a field

59
located downslope that may belong to you or your neighbor, and it could become
heavily contaminated without goats having grazed it.

6. Should we have used another approach, such as waiting for a longer period of time
between contamination and spaying to give the majority of fecal eggs the opportunity
to hatch and molt to achieve a better ‘kill’? Or, should we have used split applications
to also achieve a better kill? Possibly! In the case of split applications, fast forage
growth may decrease the direct contact of liquid nitrogen fertilizer with L3 larvae. Or
should we have used applications of liquid nitrogen fertilizer and in addition several
separate applications of household bleach solutions?

7. The objectives of the experiments described herein were never to pretend that liquid
nitrogen be used as the sole source of a gastrointestinal parasite control program, but
that hopefully it could be included as part of an integrated program. Environmental
conditions and their interaction with forage growth and the dynamic life cycle of
gastrointestinal nematodes represent a complex challenge that may greatly affect
outcomes.

60
Seminar presentation

Chapter 9. An update on anthelmintic resistance on


goat farms in the United States
Sue B. Howell, Bob E. Store, and Ray M. Kaplan

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62
63
64
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Chapter 10. SERICEA LESPEDEZA for parasite
control
Thomas H. Terrill, Ph.D.
Fort Valley State University, Georgia

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70
71
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Chapter 11. Sustainable Non-synthetic
Parasites Control in Our Farm
The way to go?

Byeng R. Min, Ph.D.


Tuskegee University, AL
[email protected]

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Chapter 12. Nutrition, Feeding, and
Immunity against parasites
N. Gurung, Ph.D.
Tuskegee University

Nutrition, Feeding, and


Immunity Against Parasites

Nar Gurung, PhD, PAS

CAENS/TUCEP, Tuskegee University, Tuskegee AL 36088

July 29, 2017

Goat Industry Challenges


 Internal parasites (production disease)
 Fencing costs
 Predators
 Lack of knowledge

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Bipedal Stance
Diet Preference Differences
(% of diet)
Animals Grass Weeds Browse

Horse 90 4 6

Cattle 70 20 10

Sheep 60 30 10

Goats 20 20 60

Source: An Peischel, 1999

Browsing Plants
Nutrition and Feeding…
• Ideal mix should be both browse and
pasture unlike sheep

• A good mix is about two acres of


browse for every one acre of open
grassland

• Problem is growing browse back after


grazing goats for more than two
seasons

Browsing/Parasites Barber Pole Worm


• Browsing goats have less parasites • The Barber-pole worm has become resistant
problem due to higher grazing heights and to most of the available dewormers:
due to tannin-containing browse species  Frequent and indiscriminate uses
 Use of many under doses

• Goats grazing grass on high stocking rates


• Goats graze to the ground level:
are become susceptible to parasites
 Ideally should not be grazed below 6 inches
from the ground

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Nutritional Management: Nutritional Management: Integrated
Integrated Approach Approach…
• Animals need energy, protein, fats, fat soluble
• Many approaches vitamins, water soluble vitamins (B-vitamins and
• Nutritional management is one of the vitamin C), macro minerals, and trace minerals
integrated approaches for parasite control
• Well-fed animals are able to defend • Lack of any of these results into reduced animal
themselves better productivity as well as impaired immune system

What is immunity? Immunity…


• Means that an animal is protected from catching
• Active or passive
a certain disease or infection
• Immune System: • Active –animal is more or less
permanently immune
 Protects body from infectious agents and
toxins • Passive – animal is only temporarily
 Enables the body to repair damaged cells immune

Immunity… Nutrition and Immune System…


• Animals prioritize immune system for
• Animals are born with some nutrients over growth
immunity • Nutrients not available for growth, thus,
• Colostrums is rich in antibodies: immune system depresses growth and feed
efficiency
 Serve the new animal until its own
• Sick or infected animals reduce feed intake
immune system can take over which further depresses immune system

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Vicious Cycle
poor nutrition – worms - anorexia

Animals may be deficient at levels that affect immunity without displaying clinical signs of deficiency

Nutrition and Immune System… Nutrition and Immune System…


• When antigens (infectious agents) act on the • Young animals are relatively susceptible
lining of the stomach. to infection and become more resistant
with age.
• Damage to host tissues caused by excessive
• Immunity also wanes around the time of
activity of the immune system
(immunopathology)
kidding/lambing

Host immunity
Goats tend to be more susceptible to parasites than sheep, especially hair sheep.

Periparturient females Weanlings


• Ewes and does suffer a temporary loss of
immunity around the time of parturition.
• Have no natural immunity
to parasites.
Nutrition for Optimum
• The length and intensity of the
periparturient egg rise varies by species,
• Will develop immunity to
parasites over time; by 4-9
Immune System?
breed, individual, and season of kidding. months of age, but varies
by species, breed, and
• Management of periparturient egg rise
individual.
– Deworm females during late gestation
– Increase protein content of late gestation ration. • Development of immunity
– Alter dates of kidding and lambing
requires continued
– Keep herd in dry lot during PPP.
exposure to parasites.

Source: Susan Schoenian, 2015)

87
Energy Sources Energy Sources
• Gold standard:
– EFA rich (linoleic ) • Most important but it’s not
– Antioxidants labelled in a feed bag
– 95% digestible
• By-product feeds such as • Flushing: 10% increase in drop
soybean hulls, corn gluten
feed, beet pulp, and rate
brewers’ grains, etc.

Effect of Protein Levels on Worm Burdens


Protein in Lambs
• Low protein; low concentrations of
antibodies
• Body proteins are broken down to provide
energy and amino acids for the immune
system
• Low levels of antibodies weaken animals’
ability to fight off diseases and parasites

Effect of Protein on FEC


Minerals
• Magnesium and phosphorus
• Trace minerals such as copper, zinc,
iron, manganese

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Copper and Immunity Copper and Immunity…
• Proper copper nutrition is essential for a healthy
• Forage surveys conducted across the United
immune system in goats.
States are marginally to severely deficient in
copper. • Copper for proper development of antibodies
and white blood cells in addition to antioxidant
• Also higher levels of antagonistic minerals
enzyme production.
(sulfur, molybdenum and iron) bind with
copper making it unavailable for use by the • Copper deficient goats are more susceptible to
goats. infections and do not respond as well to
vaccinations.

Effect of copper oxide wire Wholesale Costs for Supplying 100% of


particles (COWP; n = 8/dose) on fecal egg counts (FEC; Mineral Needs of a 150 lb Goat for Various
A) and blood packed cell volume (PCV; B) from d 0
through 21 after administration of COWP in weaned kids
Minerals in 1 Year
on pasture (Burke et al., 2007) Minerals Costs ($)
Calcium 1.15
Phosphorus 4.50
Salt 0.40
Magnesium 1.11
Potassium 1.50
Trace minerals 0.45
Other minerals 0.65
TOTAL 9.70
Source: Steve Hart, 2005

Dietary requirements set by the


National Research Council (NRC)
Vitamins • Optimal
immunocompetence may
• Vitamin A and D play important roles in occur at nutrient levels that
regulating immunity: are: higher than the NRC
o Reduced resistance to all types of diseases requirement (panel A); equal
including parasites to the NRC requirement
• Vitamin D is required to activate the killer cells (panel B); or less than the
NRC requirement (panel C).
of the immune system (e.g., T-cells)
• Vitamin E is the most important antioxidant

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Supplementation of Vit E (1500 IU) and Se (0.3ppm)
Vitamin E Levels in Milk and Plasma in increases plasma concentration of vitamin E and
Healthy and Mastic Cows reduce incidence of mastitis (Smith,1986)
Plasma concentration alpha tocopherol
Milk Plasma

Source: Aroshi et al., 1986

Role of Trace Minerals on Immune


Effects of Supplemental Dietary Vitamin E on Systems
Morbidity and Performance of Transport- • Their roles goes beyond stimulating the
Stressed Calves activity of immune cells, it includes protecting
the host from toxic substances formed by
Item Control Vitamin E*
macrophages
Daily gain, kg 0.8 0.9
Dry matter intake, kg 7.5 7.5 • Macrophages use superoxide to destroy
Feed to gain ratio 12.4 9.0 pathogens and other foreign substances
Morbidity 55 48
*Vitamin E levels were 400 to 1,000 IU/head/day
Source: Secrist et al. (1997); Means of 5 trials

Role of Trace Minerals on Immune Role of Trace Minerals on Immune


Systems… Systems…
• Superoxide, however, is also toxic to host cells • Superoxide, however, is also toxic to host cells
and therefore, needs to be converted to and therefore, needs to be converted to
compounds that are less toxic compounds that are less toxic
• The crucial step in this scavenging of • The crucial step in this scavenging of
superoxide requires superoxide dismutase, an superoxide requires superoxide dismutase, an
enzyme in which zinc, manganese, and copper enzyme in which zinc, manganese, and copper
are essential co-factors. are essential co-factors.

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Two Sample Creep Feeds for Goat Kids
Practical Dietary Recommendations Ingredient Sample 1 Sample 2
Items % Protein % TDN Cracked corn 50% 50%

Growing kids (0.3 lb/day) 12 - 13 58 - 63


Soybean hulls 30% ----
Dry does and bucks 9 - 10 54 – 58 Oats ---- 30%

Lactating goats 12 - 13 62 - 68 Soybean meal 15% 15%

Molasses 5% 5%

Source: Pinkerton and Pinkerton, 2000 Source: Rankins, 2004

Two Sample Diets for Growing


Young Kids
Summary and Conclusion
Ingredient Sample 1 Sample 2
Ground hay 25% ---- • Inadequately fed goats cause reduced
Cottonseed hulls ---- 25% goat performance:
Cracked corn 44% 41%  Reduced feed intake
Soybean hulls 15% 15%
Soybean meal 10% 13%  Reduced feed efficiency
Molasses 5% 5%  Protein leakage, gut damage
Trace mineral salt 0.5% 0.5%
Dicalcium phosphate 0.5% 0.5%  Nutrients are diverted away from
production
Source: Rankins, 2004

Summary and Conclusion… Thank You!


• Adequately fed animals can tolerate
increasing levels of parasites

• Interrelationship which exists between


nutrition and immunity must be taken
into consideration

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