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Anthelmintics Resistance on
Goat Gastrointestinal
Nematodes (Case Study in Arero District, Southern Ethiopia)
Gerade Abduljami
Gerade Abduljami
Arero District, Southern Ethiopia
1. INTRODUCTION Small ruminant production is important due to the fact that it can easily be managed, requires
small initial investments and its short generation interval (Otte, M.J. and P. Chilonda. 2002). Goats are
widely distributed in all climatic zones but with a high concentration in dry areas. This is because they
are well adapted to hot and dry conditions and mainly to the fact that in dry zones there is less
opportunity for alternative land use (ILCA, 2013). The estimated number of sheep in Ethiopia is about
25.02 million out of which about 73.38 percent are females, and about 26.62 percent males. The
number of goats reported in the country is estimated to be about 22.6 million. Out of these total goats,
about 69.84 percent are females and 30.16 percent are males (Nizam, 2013). A 2013/2014 livestock
Abstract: A study was conducted to assess the development of anthelmintic resistance by gastrointestinal
nematodes from January 2018 to July 2018 in Arero district, Southern Ethiopia. After agreements were made
with the owner of goats in Arero, the fecal samples of traditionally managed and naturally infected of 384 goats
were directly collected from the rectum, the eggs of parasite were counted by using the modified McMaster
technique and the result was recorded using the owner’s name with the animal name which given depend on
body mark, gift and their behavior, for ease of identification. This study was conducted using faecal egg count
reduction test (FECRT). For the study eighty goats of both sexes and aged from six to eighteen months with
faecal egg count (FEC) of more than 150 eggs per gram of faeces were selected for the field experiment. The
animals were grouped in to Albendazole, Tetramisole, Ivermectin and control groups randomly. From a total of
384 goats faecal sample taken during the screening 201(52.3%) of the goats were shedding gastrointestinal
nematodes eggs. Faecal samples were collected on day 0 before treatment, and again on day 12 post treatment.
Efficacy of all the drugs was assessed on day 12 post treatment by faecal egg count reduction test (FECRT).
Multiple anthelmintic resistances in nematodes against Albendazole and Ivermectin were recorded in all age
categories of the goats. However tetramisole showed good efficacy against nematode in this area. However,
large scale studies are needed to assess the current status of anthelmintic resistance against the most commonly
used anthelmintics in different agro ecology, species of animals and management systems in Ethiopia.
Keywords: Anthelmintics resistance, faecal egg count, gastro intestinal nematodes, goats, albendazole
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census puts the goat population in Ethiopia at 22.6 million (CSA, 2013) of which 32% goats were
found in Oromia Regional State. Ethiopia is known to have a high population of sheep and goats.
Majority of Ethiopian goat farmers are subsistence farmer. In southern zone large number of goats and
Small ruminant used for the community as source milk, meat, cash income, skin, manure and
employment for family member (Bedane et al., 2009). Several previous studies conducted in different
parts of Ethiopia indicate that gastrointestinal nematodes in goats are very common and widespread in
all livestock systems in the country (Kumsa and Wossene 2006a; Sissay et al., 2006a; Thomas et al.,
2007).
The most commonly reported adverse effects of gastrointestinal nematodes in goats include: low
productivity, decreased weight gain, unthriftiness, delay in puberty, anorexia, hypoproteinemia, loss of
meat and wool, impaired digestive efficiency, organ condemnation, poor reproductive performance,
and death of severely infected animals (Tembely et al., 2001). Anthelmintic have a pivotal role in
minimizing the negative effects of nematodes worldwide. However, indiscriminate and frequent use of
these drugs has resulted in the emergence of anthelmintic resistance against most of the major classes
of anthelmintics in several countries (Coles et al., 2006; Jabbar et al., 2006, and Saeed et al., 2007).
Anthelmintic resistance in nematodes of small ruminants has been reported from different parts of the
world (Cringoli et al., 2007, and Saeed et al., 2007). In Ethiopia, the use of anthelmintics in helminth
control is known and has been going on for a quite long time, taking a considerable share in drug costs.
Smuggling and improper use of veterinary drugs including anthelmintics is a widespread practice in the
country. Although, anthelmintics are very commonly used in Ethiopia, and despite the great variety of
drugs circulating in the market legally or illegally, almost no efficacy trials are conducted in proper and
regular manner (Sissay et al., 2006b). Despite the great importance and considerable time of use of
anthelmintics in Ethiopia, limited numbers examining the efficacy of these drugs are reported (Asmare
et al., 2005; Kumsa and Wossene 2006b, and Sissay et al. 2006b). This implies that the extent,
prevalence and economic significance of anthelmintic resistance in the country are not known.
Control of gastrointestinal nematode parasites of livestock in smallholder farmer and agro
ecologies is done with limited anthelmintic drug use, or with traditional herbal remedies, and is
performed mainly during the rainy seasons (Miller and Waller, 2004). However, for smallholder
farmers and stock owners in rift valley, drugs are relatively expensive and are often not easily
accessible, while frequent and indiscriminate use of different classes of anthelmintics has been reported
in institutional and large commercial farms in Ethiopia (Sissay et al., 2006a). With the advent of
helminthes parasite populations that have developed resistance to anthelmintics over the last decade.
Especially in small ruminants, livestock productivity has been threatened worldwide (Miller and
Waller, 2004). The Study will be conducted to investigate the status of anthelmintic resistance in goat
flocks maintained as separate operations at pastoral area, located Arero district.
Therefore, the objective of this study was to investigate the existence of GIT resistance for mostly
used Albendazole, Tetramisole and Ivermectin brand, in naturally infected goats under field conditions
in the pastoral area, located Arero district in southern Ethiopia.
2. LITERATURE REVIEW
2.1 Anthelmintic drug
Anthelmintics are drugs that are used to treat infections with parasitic worms. This includes
both flat worms, flukes and tapeworms and round worms, i.e. gastrointestinal nematodes are one of the
most important causes of losses in productivity of goats in Ethiopia. Economic losses incurred by
nematodes include reduction in weight gain, low fertility, reduced performance, condemnation of
organs, cost of treatment and mortality in severely infected cases. Several previous coprological and
abattoir studies conducted in different parts of Ethiopia indicate high prevalence and wide distribution
of gastro intestinal nematodes in goat (Kumsa and Wossene, 2006a). Owing to lack of sound
management strategies against helminthes of livestock in any of the agroecologies in Ethiopia, control
of adverse effects of nematodes on grazing ruminants relies almost exclusively on the use of
anthelmintic. Despite the prevalence of parasitic worms, anthelmintic drug discovery is the poor
relation of the pharmaceutical industry. The simple reason is that the nations which suffer most from
these tropical diseases have little money to invest in drug discovery or therapy. It comes as no surprise
therefore that the drugs available for human treatment were first developed as veterinary medicines. In
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some respects, this situation has been exacerbated by the remarkable success of Ivermectin over the last
twenty years, which has decreased motivation for anthelmintic drug discovery programmes (Harder,
2002). This prompts concern, as anthelmintic resistance has been widely reported in livestock and it
may also only be a matter of time before this phenomenon occurs in parasites of humans. There is
large range of formulation and substances from which to choose (Boden, 2005). Many highly effective
and selective antis parasitic are available to obtain a favorable clinical response, accomplish good
control, and minimize selection for anthelmintic resistance (Harder, 2002).
The ideal Anthelmintic should have broad spectrum activity against mature and immature
parasite (including hypo biotic larvae), be easy to administer, inhibit reinfection for extended period of
time, have a wide margined of safety and be compatible with other compounds, not require long with
holding period and cost effective (Radostits et al., 2007). Antiparasitic must be selective toxic to the
parasites. This is usually achieved either by inhibiting metabolic process that is vital to the parasite but
not to host or by inherent pharmacokinetic properties of the compounds that cause the parasite to be
exposed to higher concentration of the antiparasitic than are the host cells. The pharmacological basis
of treatment for helminthes generally involves protective mechanism against host and immunity, which
lead to starvation, paralysis expulsion of the parasites by two major mechanisms: 1.They interfere with
energy generating metabolism causing death by starvation and 2. Interfere with neuromuscular
transmission in nematodes causing paralysis (Kahn and line, 2005). Antiparasites are administered to
animals by variety of methods and formulations, the three common route of administration are oral,
injection and topical (Harder, 2002).
2.1.1. Pharmacokinetics
After administration ant parasites are usually absorbed into the blood stream and transported to
different parts of the body including liver where they may be metabolized and eventually excreted in
feace and urine. Intestinal parasite comes in contact not only with the unabsorbed drug passing the
gastrointestinal tract but also any that is recycled into the gut (Kahn and line, 2005).
2.1.2 Major Anthelmintics drugs
Many broad spectrum anthelmintics are now available that combine high efficacy against larval
and adult worms with low toxicity in sheep, goats, and cattle. Most however belong to just three major
chemical groups namely: benzimidazoles, imidazathiazoles and macrocyclic lactones (Urquhart et al.,
1996, 2006, Radostits et al., 2007).
2.1.2. a. Benzimidazole
Benzimidazoles are group of broad spectrum anthelmintic drugs with high degree of efficacy
and good margin of safety and similar mode of action. The disrupt energy metabolism of parasites by
binding to tubules, a protein required for uptake of nutrient in the parasites (Kahn and line, 2005).
Benzimidazoles are large chemical family used to treat nematodes and trematodes infection in domestic
animals. However, with the wide spread development of resistance and availability of more efficiently
and easier to administer compounds, their use is rapidly decreasing. Benzimidazoles of interested are:
Albendazole, Fenbendazole, Thiabendazoles, Triclabendazole, Mebendazole, Oxfendazole,
Oxibendazole and Febantel (Radostits et al., 2007). Because of most benzimidazoles are sparingly
soluble in water they are given oral as suspension, paste and bolus. Difference in the rate and extent of
absorption from gastrointestinal tract is depending on such factor as species, formulation and
solubility. The most effective of the group are those with the longest half-life such as Oxfendazole,
Fenbendazole, and their pro drug, because the nature of their antiparasitic action depends of
prolongation of contact time (Albnico, 2003, Kahn and Line, 2005, Entrocasso et al., 2008). In
ruminant oral treatment with the benzimidazoles removes most major adult gastrointestinal parasites
and many of larval stages. The relative rate of oxidation in the liver and reduction in the gastrointestinal
tract vary between cattle and sheep, with the metabolism and excretion of benzimidazoles compound
being more extensive in cattle are often higher than those in sheep (Radostits et al., 2007, Entrocasso et
al., 2008).
Albendazole is a broad spectrum anthelmintic for the treatment of intestinal helminth infections.
It also hydatid activity and is recognized to have important application in treatment of human cystic
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and alveolar echinococcosis. Kahn and Line (2005) reported that albendazole is a potent member of
benzimedazole (BZS) group of anthelmintics, with a wide range of activity against GIT round worms
including inhibited larval stages, tapeworms, liver fluke and lung worms in many species. It blocks
glucose uptake in the larval and adult stages of susceptible parasite, there by depleting the energy stores
and decreasing formation of ATP leading to immobilization and death of the parasite (Harder, 2002).
Following oral administration, Albendazole is rapidly absorbed and cannot be detected in
plasma, because the drug is quickly metabolized in liver mainly to albendazole sulfoxide and a lesser
extent, to other metabolites (Marriner et al., 2001) About 3 hours after oral administration, the
sulfoxide attains its maximum plasma concentration. The metabolites are mainly excreted in the urine
and only a small amount is excreted in the feaces. Albendazole is absorbed to a much great degree than
the other BZS because 47% of the administered dose is recovered in urin over a 9-day period (Marriner
et al., 2001).
2.1.2 .a. Imidazothiazoles
Imidazothiazoles are groups of anthelmintics drugs effective against round worm the group acts
by interfering with parasitic nerve transmission causing muscular paralysis effective against adult and
larval gastrointestinal round worm and lung worm infectious including Protostrongylus infections.
Most worms are expelled within 24 hrs of administration of the drugs (Harder, 2002, Radostits et al.,
2007). The commonly used drugs belonging to this family are tetramisole and levamisole. These drugs
act on round worms, nerves system as cholinergic agonist thereby causing paralysis and expulsion of
the parasites (Radostits et al., 2007). It is commonly used in cattle, sheep, pigs, goats and poultry to
treat nematode infections. It is normally administered oral and sc. Efficacy is generally considered
equivalent with either route (Urquhart et al., 2003 Upadhayay, 2005). In ruminant, levamisole or
tetramisole is highly effective against the common adult GIT nematodes and lung worm (Upadhayay,
2005).
2.1.2. c. Macrocyclic lactones
Macrocyclic lactones are compounds derived from fermentation products of soil dwelling
bacteria of genes streptomycin. The product is active against both GI round worms and ectoparasites of
animals when used at lower concentration (Kahn and Line, 2005). The macrocyclic lactones are well
absorbed when administered oral, Parenteral or as pour on formulation. Regardless of the route of
administration macrocyclic lactones are extensively distributed throughout the body and concentrate
particularly in adipose tissue. Effective levels are reached in the GI system, lung and skin regardless of
route of administration (Kahn and Line, 2005). The macrocyclic lactones in commercial use are
ivermectin, abamectin, doramectin, eprinomectin and selamectin. They are active against many mature
and immature nematodes, and arthropods. The macrocyclic lactones have a very high efficacy against
all stages including in active forms of the common cattle, sheep, and goats nematodes. The least
susceptible nematodes are cooperies and Nematodirus species (Radostits et al., 2007). The macrocyclic
lactones bind to glutamate-gated chloride ion channels in invertebrate nerve and muscle cells. The cell
membranes then develop an increased permeability to chloride ions causing hyperpolarization of
affected cells and subsequent paralysis and death of the parasite. Medications in this class also interact
with other ligand gated chloride channels, including ones gated by gamma aminobutyric acid (GABA).
Because mammals do not have glutamate-gated chloride channels and macrocyclic lactones have a low
affinity for other mammalian ligand-gated chloride channels, mammals have low susceptibility to the
effects of macrocyclic lactones. Also, these medications are slow to penetrate the blood brain barrier
(BBB), protecting the GABA gated channels in mammalian central nervous systems (Kahn and Line,
2005).
Ivermectin activate the chloride channel, causing an inhibitory effect, which when excessive
results in paralysis and death of the parasite. The rout of administration for ivermectin is Subcutaneous.
Minor differences in vehicle may alter the bioavailability of subcutaneously administered ivermectin.
One study showed significant variations in absorption, peak plasma concentration, and mean residence
time among generic ivermectin injection productions (Radostits et al., 2007).
The predominant route of elimination for the macrocyclic lactones is by excretion through bile
into the feces (50 to 96% of the dose), primarily as unmetabolized drug. Small amounts are eliminated
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in the urine (Mealey et al., 2001). Macrocyclic lactones have been marked as broad spectrum
anthelmintics with most of them having effect against nematodes, insects, mites and ticks. Therefore,
they classified as anthelmintic, insecticides and acaricides (Kahn and Line, 2005).
2.2 Anthelmintics Resistance
Anthelmintic resistance is defined as a decrease in the efficacy of an anthelmintic against a
population of parasites that is generally susceptible to that drug the extensive use of anthelmintic for
control of helminthes infection on grazing livestock has resulted in the development of resistance that
has become a major practical problem in many countries resistance in the field is usually suspected
when there is an apparent poor clinical response to anthelmintic treatment (Taylor et al, 2002).
This decrease in susceptibility is caused by an increase in the frequencies of „„resistance‟‟ gene
alleles that result by selection through repeated use of an anthelmintic. Gastrointestinal nematodes of
small ruminants have a number of genetic characteristics that promote the development of anthelmintic
resistance. Among the most important of these features are: (1) rapid rates of nucleotide sequence
evolution and extremely large populations resulting from the high fecundity of each individual
nematode, providing an exceptionally high level of genetic diversity (Leathwick, 2012) and (2) a
population structure consistent with high levels of gene flow (dissemination), suggesting that host
movement is an important determinant of nematode population genetic structure. As a result, these
helminths have the genetic potential to respond rapidly and successfully to chemical attack and the
means to ensure dissemination of their resistant genes by host movement from farm to farm (Taylor et
al, 2002).
The problem of anthelmintic resistance in gastrointestinal nematodes of small ruminants is
worldwide. In the past25 years, no new classes of anthelmintics have been developed for use in
animals, and given the limited economic potential of small ruminant production; there is little interest
in pursuing licensing of anthelmintics for this group of animals. Currently, there are 3 classes of
anthelmintics commonly used in small ruminants: benzimidazoles (including albendazole,
fenbendazole), cholinergic agonists (including levamisole/morantel), and the macrocyclic lactones or
ivermectins and milbemycins. The earliest documentation of anthelmintic resistance was to
phenothiazine in 1957 followed by thiabendazole in 1964 (Sykes and Coop, 2001).
There is no anthelmintic use policy in the country as a result misuse and smuggling of
anthelmintics in many forms like illegal trading in open market and irrational administration is a
widespread practice. As severity of anthelmintics resistance increase in nematodes of small ruminant it
is evident that no single approach remains to control the steady. Efficacy of anthelmintics is
continuously constrained by many factors like under dosage, exclusive use of drugs of the same mode
of action, substandard drugs and inappropriate use of anthelmintics. Demise of the available
anthelmintics. Anthelmintics resistance is an important consideration influencing the choice and
intensity of control measures (Kahn and Line, 2005; Radostits et al., 2007).
2.3 Development of Anthelmintics Resistance
It is accepted that during anthelmintic treatments, a small number of worms survive; these being
the most resistance proportion of population and these worms contaminate the pasture with majority of
resistance larvae for subsequent generation, leading gradually to the selection pressure of anthelmintic
resistance. This selection rate depends on the percentage contribution to the next generation between
nematodes surviving after treatment and other one not exposed to it (Papadopoulos, 2008)
Parasite resistance against all important anthelmintics is a significant problem in some animals
host condition such as return to infected pasture the proportion of a parasite population that is not
exposed to anthelmintics during any one treatment e.g. nematode larval stages on pasture, thus escaping
selection for resistance and potentially able to propagate its genes to the next generation, emergency of
hypobiotic larvae, mass medication in appropriate therapy resulting in drug resistance most of the
reports of anthelmintic resistance are from large scale commercial or institutional farms. Under these
conditions, the selection pressure for anthelmintic resistance is often intense with, for example,
frequent anthelmintic treatment of the whole herd. This in itself exposes a greater proportion of the
nematode population to anthelmintics and leaves fewer worms in refugia than would be the case, for
example, if only those individual animals showing signs of helminthosis were drenched (Van Wyk J A,
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2001). The frequent use of anthelmintics increases the frequency with which individual nematodes and
their offspring are exposed to anthelmintics as well as the probability that a nematode will be exposed
to an anthelmintic within a certain period of time. Large herd size has been reported as a risk factor for
the presence of resistance. Farmers with large flocks are more likely to be able to buy anthelmintics.
Conversely, farmers with smaller flocks often cannot afford to buy anthelmintics and this may serve to
slow down the onset of resistance (Kahn and Line, 2005, Entrocasso et al, 2008).
Various authors speculate that the occurrence of anthelmintic resistance in a flock/herd resulted
from the introduction of resistant worms from other flocks/ herds. This may have been through the sale
or distribution of stock (together with their resistant worms) from larger commercial or government
owned farms to smaller farms), through the introduction of stock from other farms (where no mention
of size of farm is made), through the appropriation of farms from commercial farmers and addition to
existing communal pastures; and through communal grazing (Vatta et al; 2001). Over use chemical as
deworming agent in the past lead to the development of anthelmintics resistance of gastrointestinal
nematodes (Burke and Miller, 2008).
2.3.1 Generally factor lead to anthelmintics resistance
2.3.1.1. Treatment frequency
It has been observed that frequent usage of the same group of anthelmintic may result in the
development of AR (Silvestre and Humbert, 2002). There is evidence that resistance develops more
rapidly in regions where animals are dewormed regularly. Anthelmintic resistance in H. contortus has
been reported in some humid tropical areas where 10 to 15 treatments per year were used to control this
parasite in small ruminants. Drug resistance, however, can also be selected at lower treatment
frequencies, especially when the same drug is used over many years and also reported the development
of AR even when only two or three treatments were given annually (Silvestre and Humbert, 2002).
2.3.1.1. Under dosing
Under dosing is generally considered an important factor in the development of AR because sub
therapeutic doses might allow the survival of heterozygous resistant worms (Kahn and Line, 2005).
Several laboratory experiments have shown that under dosing contributes to the selection of resistant or
tolerant strains. Moreover, variation in bioavailability in different host species also is crucial for
making a decision about correct dose. Some indirect field evidence further supports this conclusion.
For an example, the bioavailability of benzimidazole and levamisole is much lower in goats than in
sheep, resultantly those goats should be treated with dosages 1.5 to 2 times higher (the single dose is
much less inferior than “sub-optimal”, it is rather near half the dose necessary for goats) than those
given to sheep (Hennessy, 1994). For many years, however, sheep and goats were given the same
anthelmintic doses. The fact that AR is very frequent and widespread in goats may be a direct
consequence of difference in metabolism of drugs (Silvestre and Humbert, 2002).
To reduce the costs of anthelmintic treatment in developing countries, the use of lower dosages
than the recommended therapeutic ones has been advocated. Such practices should clearly be avoided.
Most of the currently applied anthelmintics are in fact sub curative in at least part of the population.
Additionally, there are a number of species of nematodes which are present as mixed infection in
animals‟ throughout the world which responds to different groups of anthelmintics differently due to
the irregular susceptibility of these species to a given anthelmintic. This is considered acceptable for
morbidity control, but in the long run such strategies may contribute to the development of AR as well
(Silvestre and Humbert, 2002).
2.3.1. c. Mass treatment
Prophylactic mass treatments of domestic animals have contributed to the widespread
development of AR in helminths. Computer models indicate that the development of resistance is
delayed when 20% of the flock is left untreated (Van wyk, 2001) but it needs confirmation through
experimentation. This approach would ensure that the progeny of the worms surviving treatment will
not consist only of resistant worms. Leaving a part of the group untreated; especially the members
carrying the lowest worm burdens should not necessarily reduce the overall impact of the treatment. In
worm control in livestock, regular moving of the flocks to clean pastures after mass treatment and/or
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planning to administer treatment in the dry seasons is a common practice to reduce rapid reinfection.
However, these actions result in the next helminths generation that consists almost completely of
worms that survived therapy and, therefore, might contribute to the development of AR (Van wyk,
2001).
2.3.1. d. Single drug regimens
Frequent and continuous use of a single drug leads to the development of resistance. For
example, a single drug, which is usually very effective in the first years, is continuously used until it no
longer works. In a survey of sheep farmers in Tennessee found that one out of every two flocks was
dosed with a single anthelmintic until it failed. Long term use of levamisole in cattle also led to the
development of resistance, although the annual treatment frequency was low and cattle helminthes
seemed to develop resistance less easily than do worms in small ruminants. Frequent use of ivermectin
without alternation with other drugs has also been reported as the reason for the fast development of
resistance in H. contortus in South Africa and New Zealand. Development of resistance depend upon
whether resistance worms are as fit, by means of life cycle completion, egg production pasture survival
and infectivity or less fit than susceptible ones (Coles et al., 2006: Van Wyk et al, 2006; and
Papadopoulos, 2008).
2.4. Detection of Resistance
Two tests are available to veterinarians for determining the presence of anthelmintic resistance
in small ruminants. One is a simple test that can be performed locally, and the other requires a
laboratory that specializes in this type of testing. Larval identification can be used to determine which
species of parasites are resistant (Maingi et al., 1998).
2.4.1. Fecal Egg Count Reduction Tests
The test most commonly used to detect anthelmintics resistance remain the faecal egg count
reduction test (FECRT), It is suggested that guidelines published by the World Association for the
Advancement of Veterinary Parasitology (WAAVP) be used to perform and evaluate data from a fecal
egg count reduction test, applying practical modifications to fit the situation on the farm. Which is
suitable for all anthelmintics, including ones undergoing metabolism within the host and can be easily
applied in goats (Coles, 2005). This test considered to be reliable if more than 25% of the worms are
resistance. generally it compares the egg count before and after treatment with anthelmintics,
obviously an untreated (control) group of animals should be included, in order to any natural change
to egg counts, Which may occur during the test period Once resistant helminths are documented, the
species should be determined through larval identification (Papadopoulos, 2008).
2.4.2. Egg Hatch Assays / Larval Development Tests
Eggs from feces are incubated with concentrations of the anthelmintic to be tested and the eggs
are allowed to hatch. A dose response curve is generated. The advantage of this test is that a single
fecal sample can be tested simultaneously for all available classes of anthelmintics.
2.4.3. Other Tests
Larval development tests, adult development tests, and DNA probes have been described in
research settings, but are not commercially available at this time.
2.5. Control of Anthelmintics Resistance
2.5.1. Adoption of strict quarantine measures
Effective management strategies to prevent development of anthelmintic resistance are
worthless if producers purchase resistant worms residing in breeding stock. Therefore, strict quarantine
procedures should be instituted for all new additions. This practice is more important than ever, as in
recent years several farms with high quality breeding stock dispersed herds where H. contortus and T.
colubriformis were resistant to benzimidazoles (Utzinger and Keiser, 2004).
There is no faster way to spread resistance than to bring gastrointestinal nematodes to a farm.
The current recommendation is to quarantine (on dry lot where feces can be removed) every new
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addition, dose with triple class anthelmintic therapy, and perform fecal egg count reduction tests. Feed
should be withheld for 24 hours before treatment, then levamisole, and albendazole should be
administered consecutively (do not mix drugs together) at the appropriate dose for sheep or goats.
Fourteen days later, treated animals should be evaluated by fecal egg count and fecal flotation
techniques. The fecal egg count should be zero, and flotation should yield very few or no eggs.
Furthermore, after receiving this treatment, animals should be placed on a contaminated pasture. Never
should an animal be placed onto a clean pasture after a triple anthelmintic class treatment regimen is
administered, because any surviving worms will be triple resistant and there will be no refugia on
pasture to dilute the future transmission of any eggs that are shed (Fleming et al.,2006)
2.5.2. A combination drug strategy
Treating simultaneously with 2 drugs from different anthelmintic classes is one method of
preventing the development of anthelmintic resistance (Fleming et al, 2006). A computer based model
has documented that if this strategy is used when the drugs are first introduced, before there is any
selection for resistance to either drug, appreciable resistance will not develop for over 20 years.
However, once resistance alleles accumulate in worm populations, this strategy will probably not be
successful. Compared with individual drug effects, anthelmintics of different chemical classes
administered together induce a synergistic effect, resulting in clinically relevant increases in the
efficacy of treatment. This synergistic effect is most pronounced when the level of resistance is low.
Once high level resistance to both drugs is present, the synergistic effect is unlikely to produce
acceptable levels of efficacy. In contrast, the same model indicated that rotating drugs with each
treatment, using annual rotation or a 5 or 10 year rotation resulted in high level resistance within 15 to
20 years (Van wyk, 2001).
Thus, the common recommendation of annual rotation must be challenged. Rotation of drugs
was originally suggested on the basis of the hypothesis that reversion to susceptibility (or at least
substantial decrease in resistance gene allele frequency) might occur if resistant worms were less fit
than were susceptible worms, and counter selection was applied via treatment with a drug from a
distinct chemical class. However, evidence that resistant worms are any less fit or that true reversion
occurs in the field is scant. Despite this, the concept of rotation is often viewed as a bona fide resistance
prevention scheme, which it is not. Therefore, some leading small ruminant parasitologists are now
calling for an end to the practice of rotation (Van wyk, 2001).
It is suggested that a drug should be used until it is no longer effective, then a different drug should be
used. For veterinary parasites, a combination of mebendazole and levamisole has been shown to be
synergistic against H. contortus in sheep (Radostits et al., 2007).
Generally the development of anthelmintic resistance can be discouraged by changing the class
of anthelmintic used for each years; dosing program (Boden, 2005). Do not under dose, use an effective
drug in most efficient manner and make sure that the farmer is aware of the problem and consequence
of anthelmintic resistance; education is the principal requirement for assisting resource poor farmers to
improve the health, productivity and welfare of their animals. Without knowledge, the resource poor
farmer cannot improve herd management and prophylaxis of disease by means of vaccination.
Knowledge is required to be able to recognize the importance of specific disease conditions and
circumstances favoring their development, for instance a greater awareness of the presence and
pathogenic effects of nematodes, the epidemiological conditions that are optimal for their survival, and
how to manage the infections for the long term. (Radostits et al., 2007).
3. MATERIALS AND METHODS
3.1 Study Area
The study was conducted from January 2018 to July 2018, on goats originated from Arero
district of Borana zone. Arero is one of the woredas in the oromia regional of Ethiopia .part of the
borena zone, arero is bordered on the southwest by Dire, on the west by yabelo, on the north by Hagere
Mariam, on the northeast by the Guji zone, on the east by the Somali region, and on the south by
Moyale; the only river in this woreda, separates arero from odo shakiso and Liben. The altitude of this
woreda ranges from 750 to 1700 above sea level. Its population are urban dwellers, which is greater
than the Zone Average of 11.6%.With an estimated area of 10,841.88 square kilometers, Arero has an
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estimated population density of 4.1 people per square kilometer, which is less than the Zone average of
21.1 (CSA 2005).
A survey of the land in this woreda shows that 20% is arable (1.7 % was under cultivation),
40.3% pasture, 1.6% forest, the remaining 38.1% is considered swamp, mountainous or otherwise
unusable (SPDZ 2006). Arero has 260 kilometers of dry weather roads, for an average road density of
24 kilometers per 1000 square kilometers. About 33.8% of the urban and 12.5% of the rural population
has access to drinking water (SPDZ 2006). The 2007 national census reported a total population for this
Woreda of 48,126, of whom 24,281were men and 23,845 were women; 3,004 or 6.24% of its
population were urban dwellers. The majority of the inhabitants said they practiced traditional beliefs,
with 67.73% of the population reporting they observed these beliefs, while 22.67% of the population
were Muslim, 6.82% were Protestant and 2.62% practiced Ethiopian Orthodox Christianity (CSA
2005).
Figure 1: Administrative map of Ethiopia and Borana zone study areas.
Source: Google map
Its pattern is of a bimodal type with 60% occurring in the long rainy season (Gana) extending
from mid-March to May and the small rainy season (hagaya) from mid-September to mid-November.
The other two seasons are the cool dry season (adolessa) extending from June to August and the major
dry season (bona) from December to February (BZDPED,1998). The districts were selected primarily
because the zone is important as a source of animals for domestic consumption and export (Coppock,
1994) and also the districts are the most affected by drought. Animal husbandry in the area is
characterized by extensive pastoral productions system and seasonal mobility. Surface water is a
serious problem in the area. Traditional deep wells “ellas”, ponds, perennial spring, permanent river
(Dawa) and seasonal sources (streams, ephemeral ponds and shallow wells) are water sources for both
human and live stocks. Deep wells and large ponds (Machine excavated) are used in dry season while
seasonal streams, ephemera ponds and shallow wells are used in wet seasons (Helland, 1982).
3.2. Study of Animal population
The livestock population of the district was estimated Cattle 175000, Goats 110585, Sheeps
49691 (Arero district pastoral Development bureau, 2008).
3.3. Study design and study animals
The screening examination was done from the goats‟ population in Arero district that kept in
traditional backyard management system with an age range of 6–18 months, and then suitable
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arrangements and agreements was made with those farmers who were willing to have their animals
used in a faecal egg count reduction test (FECRT). After agreements were made the fecal samples
from 384 goats were directly collected from the rectum, the eggs of parasite were counted by using the
modified McMaster technique and the result was recorded using the owner‟s name with the animal
name which given depend on body mark, gift and their behavior, for ease of identification. Goats with
more than 150 eggs per gram (EPG) of faces were eligible for inclusion in the field experiment on
Anthelmintic resistance; following guidelines by Coles et al. (1992).
Simple random sampling design was employed for this field experimental study (Gomez and
Gomez, 1984). For fecal egg count of these 80 goats with fecal egg counts greater than 150 were
selected for Anthelmintic resistance study (Coles et al., 1992) the selected goats were randomly as-
signed in to four groups, each group contain 20 goats: the first group for albendazole, the second group
for tetramisole, the third group for ivermectin treatment and the fourth group for control. The faecal
sample of each goat under experiment was taken again 11-12 days after treatment, the eggs count was
done as previously done pre-treatment in order to compute the variation of eggs number before
treatment and after treatment.
The Anthelmintic resistance assessment was conducted from January 2018 to July 2018, on 80
goat‟s located Arero district. All goats under experiment treated with different Anthelmintic according
to the manufacturer‟s recommended dose rate except control group. Fecal samples were directly
collected from rectum again 11 to 12 days post-treatment from all goats under study, the nematode
faecal egg counts were made by using the modified McMaster technique (Coles et al., 1992).
Table 1: Table of drug used and their route of administration
Trade name Generic
name Manufacturer
Dose/kg body
weight
Mode of
administration
Albenda
albendazole
Chengdu qiankun
veterinary pharmaceuticals
Co.Ltd., China
7.5mg/kg Oral
Ashitetra
Tetramisole
ashish life science
pvt.Ltd.,india 15mg/kg Oral
Noromectin Ivermectin
Chengdu qiankun
veterinary pharmaceuticals
Co.Ltd.,china
0.2 mg/kg SC injection
The Anthelmintic resistance was evaluated on the basis of the reduction in faecal egg count.
Calculation of the Anthelmintic mean, percentage reduction and 95% upper and lower confidence
limits was according to Coles et al. (1992). Resistance is declared if the percentage reduction was less
than 95% and the 95% lower confidence limit is less than 90%.Hence the interpretation of result was
given based on this guides.
4. RESEARCH RESULT
The faecal samples collected from 384 goats during the screening indicated that 201(52.3%) of
the studied goats were shedding gastrointestinal nematodes eggs in their faeces (Table 2). The mean
egg count per gram of faeces was 684.55 ± 119.7.
Table 2: Prevalence of goats‟ gastrointestinal nematodes in Arero district
Factor Category
No of
animals
examined
Prevalence 95% CI
Sex Male 169 89(52.7%) 45.1-62
Female 215 112(52.1%) 45.4-58.6
Age Young 214 119(55.6%) 49-62.2
Adult 170 82(48.2%) 40.7-55.7
Overall 384 201(52.3%) 47.3-57.3
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Table 3: Summary of mean gastrointestinal egg count per gram of faeces
Species Category No of animals examined Mean EPF ± Std.
Error 95% CI
Sex Male 169 311.79 ± 29.96 258.99 378.08
Female 215 372.76 ± 31.25 310.83 434.70
Age Young 214 331.09 ± 29.58 272.50 389.67
Adult 170 374.39 ± 32.32 310.06 438.71
Overall 384 684.55 ± 61.9
The mean pre and post treatment faecal egg counts (EPG) and the percentage of faecal egg
count reduction (FECR) and the lower and upper 95% confidence limit for each groups of anthelmintic
drugs tested was summarized in Table 4. The percentage reduction of faecal egg count, (95%
confidence intervals) for albendazole, ivermectin and tetramisole were 87.2% (470.30 to 703.69),
81.06% (431.10 to 598.89) and 96.15% (506.47 to 658.52) respectively. Among the three drugs,
tetramisole are a faecal egg count reduction percentage above 95%, and other is less than 95%
percentage. Hence result indicated that albendazole and ivermectin were suspected for development of
resistance against gastrointestinal nematodes, while tetramisole was found to be effective.
Table 4: Table to show the results of pre-treatment and post-treatment faecal egg count and reduction
percentage in goats at Arero
Treatment
Group
EPG
Reduction
%
95% CL Pre-treatment Post-treatment
Albendazole 695 ± 49.504 108 ± 16.56 87.2% (470.30 - 703.69),
Ivermectin 675 ± 42.68 160 ± 21.94 81.06% (431.10 - 598.89)
Tetramisol 615 ± 33.26 32.5± 6.56 96.15% (506.47 - 658.52 )
Control 682.5 ± 40.761 845 ± 65.68 - -
5. DISCUSSION
The coprological examination performed for this study using direct faecal floatation method
revealed the existence of gastrointestinal nematodes with an overall prevalence rate of 52.3% in the
goat examined. The current prevalence was slightly lower when compared to various research outputs
in Ethiopia by, Tefera et al. (2011) in and around Bedelle, Moti (2008): In and around Welinchity,
Tesfaheywet (2012) in and around haramaya and who reported 93.29%,76.3% and 61.4%,
respectively. The higher prevalence observed in different parts of Ethiopia could be ascribed to over
stocking, poor nutrition (starvation), poor management practice of the animals (lack of sanitation) and
frequent exposure to the communal grazing lands that have been contaminated. However, the finding is
higher than previous studies reported 40.6% by Biqila et al. (2013) from Gechi District, Southwest
Ethiopia.
From a total 384 goats examine during the screening 201(52.3%) of the goats were found
infected with gastrointestinal nematodes in Arero district. There was no significant variation in the
infection of age and sex groups (χ2 = 2.064, P = 0.91; and χ2 = 0.012 and P = 0.497, respectively). The
anthelmintics resistance was evaluated depend on arithmetic mean ,percentage reduction and 95%
upper and lower confidence limit were computed using the guide and formula described by Coles et al
(1992).
Depend on this formula the FECR% of ivermectin group, albendazole group and tetramisole
group were 81.06%, 87.2% and 96.15% respectively. Based on this criterion, the FECR percentage and
the lower confidence limit obtained from Arero district smallholder goats production system revealed
the presence of a significant level of gastrointestinal resistance to albendazole and ivermectin. This
finding is disagree with other studies conducted in various parts of Ethiopia, on the efficacy of the
most commonly used anthelmintics in small ruminants (Asmare et al., 2005; Kumsa and Abebe, 2008;
Kumsa and Nurfeta, 2008; Kumsa and Wossene, 2006; Sheferaw and Asha, 2010; Tadesse et al., 2009;
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Sheferaw et al., 2013). However it agrees with albendazole resistance with Sheferaw et al., 2013;
Bersisa and Girma, (2009) reported except on tetramisole and absence of resistance of tetramisole with
this study. Furthermore this finding was total disagree with Asmare et al. (2005) who reported
ivermectin and albendazole susceptibility and resistance for tetramisole.
Mostly believed that benzimidazoles are the most widely used anthelmintic family followed by
the macrocyclic lactone in the study area. It also indicated that the imidazothiazoles family is used only
by institutional farms who keep animals under intensive management system. It also revealed that
farmers in the study area perform several practices that may be responsible in lowering the efficacy of
anthelmintics that agrees with many earlier studies conducted elsewhere in the world (Arece et al.,
2004; Chandrawathani et al., 2004).Studies on efficacy of anthelmintic drugs are useful to establish and
maintain effective and sustainable control strategic against helminthes of livestock, especially for small
ruminants.
Efficacy evaluations of the anthelmintics carried out and interpreted as per the WAAVP
recommendations provided evidence of susceptibility of nematodes to tetramisol families. This finding
agree with previous studies conducted on small ruminants maintained under extensive type of
production by resource poor smallholders in some parts of Ethiopia (Kumsa and Wossene, 2006b;
Sissay et al., 2006a,b) and with other studies in different parts of the world (Arece et al., 2004; Saddiqi
et al., 2006).
The lower efficacy of ivermectin and albendazole against nematodes of goats in this study area
might be caused several factors like poor quality drugs of low price, continuous under dosages
treatments at the drug dose rate by pastoralists due to low bioavailability in goats, misuse smuggle drug
and inappropriate treatment by owners. Similar factors have already been reported to contribute to
lower efficacy (Chandrawethani et al., 2004; Saddiqi et al., 2006; Saeed et al., 2007).
6. CONCLUSION From this study, we can conclude that albendazole and ivermectin is not effective in the area
against gastrointestinal parasites. Gastrointestinal nematodes in Arero, were suspected for development
of resistance against albendazole and ivermectin, while tetramisole was found to be effective. On the
other hand, both albendazole and ivermectin showed lower efficacy, especially against nematodes in
goats of the study area. However, many factors like use of drugs from black market, under dosage,
misuse and inappropriate treatments may all hasten failure in efficacy of currently efficacious
anthelmintics.
Depending on the above fact the following recommendations were forwarded
As a result to maintain and prolong, the lifespan of the efficacy of available drugs pastoralist
should be educated by proper veterinary extension about the importance of correct use of
anthelmintics, annual rotations anthelmintic group and avoiding all factors that favor reduction
in efficacy leading to anthelmintic resistance.
Further studies should be conducted based on a comparative efficacy of drugs from reliable
source and drugs used by the owners from unreliable sources such as imported drugs or
smuggle drugs.
Furthermore to prevent development of anthelmintic resistance in this area, the following
practices will be helpful: avoid frequent and unnecessary treatments with anthelmintics and
avoid under dosing of animals.
7. ACKNOWLEDGEMENTS
All the praises and thanks be to Allah for his favour to me in completing my work and without
whom I would have not been successful.
Next, I would like to express my grateful thanks to my advisor Dr. Fatu Mudasir and my co
advisor Dr. Gobu Boru for their intellectual guidance, helpful input, valuable comment and devotion of
time in preparing this research. Furthermore I would like to thank my family, all teachers/instructors
who provide their input to reach here specially Dr Belay Abebe, my classmates and other students who
give constructive idea. I wish to extend my heartfelt thanks to staff of Adami Tulu Agricultural Animal
Health Laboratory, for support of laboratory materials, reagents and for their assistance and
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encouragement. Besides I would like to thank animal health laboratory team for their material support
and moral encouragement during the period of my research work.
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8. ANNEXES
Annex. 1. Description of dentition with corresponding age estimates protocol
Characteristics Age (in months) Young with fully grown milk teeth 9
The milk teeth started to wear down, or are fully spread out 12
With erupted & growing 1st
pair of permanent teeth 14 – 17
With erupted & growing 2nd
pair of permanent teeth 18 – 23
With erupted & growing 3rd
pair of permanent teeth 24 – 36
With erupted & growing 4rth
pair of permanent teeth 3 – 5
The four pair of permanent incisors have started to Wear down 4 years
The permanent incisors have worn down & have started to spread out >5 years
Source: (Yami and Merkel, 2009)
Annex. 2. Sample collection format
ID Spp Sex Age Origin
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Annex.3. McMaster Egg count
McMaster Egg count is quantitative method for determining the number of nematode eggs per gram of
feces in order to estimate the worm burden in an animal. The advantage of this method is it is quick as
the eggs are floated free of debris before counting, the disadvantage is you must use a special counting
chamber.
1. 4 grams of feces was taken and grinded.
2. The mixture of feces and floatation solution was passed through sieves. Lift the sieve and hold
over the dish. Push out any remaining solution from the feces.
3. While mixing vigorously (you may want to put the solution into a flask to prevent spillage) take
a sample of the mixture with a pipette and transfer it to one of the chambers of the McMaster
slide. Repeat the procedure and fill the other chamber.
4. Wait 30 sec then count the total number of eggs under both of the etched areas on the slide.
Focus first on the etched lines of the grid, then go down a tiny bit, the eggs will be floating just
below the top of the chamber. Multiply the total number of eggs in the 2 chambers by 50; this is
the eggs per gram (EPG).
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