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The Identification of Cattle Nematode Parasites Resistant to Multiple Classes of Anthelmintics in a Commercial Cattle Population in the US
Abstract
Resistance to modern anthelmintics by ruminant nematode parasites is an increasing problem throughout the world. To date the problem has largely been reported in parasites of small ruminants, but there are increasing reports of such resistance in nematodes recovered from cattle. Until now there have been no published reports of drug resistant parasites from cattle in North America. In 2002 a producer in the upper Midwest who backgrounds young cattle acquired from the southeastern US experienced lower than expected weight gain as well as apparent parasitic gastroenteritis in his cattle during the fall. Fecal sample results supported the suspicion that decreased productivity and diarrhea were the result of GI nematode parasitism. The operation used intensive grazing management and practiced strategically timed deworming for >17 year. In 2003, all animals were dewormed the first week of May with Ivomec Plus, then with Dectomax Injectable on 4 June and 17 July. On 31 July, 10 randomly taken fecal samples showed EPG values from 0 to 55. To assess whether the apparent decreased drug efficacy was the result of drug resistance in the nematode population, on 18 August approximately 150 heads, previously strategic timed dewormed, of 9-11 month old cattle from one pasture were selected for study. The calves were randomly assigned to 1 of 6 treatment groups: untreated (U), ivermectin injectable (I), moxidectin pour-on (M), doramectin injectable (D), eprinomectin pour-on (E), albendazole oral (A). Cattle were weighed prior to treatment and the drug was dosed according to label directions. Seven days later, 3 calves from each group were slaughtered for worm recovery. Fecal samples taken from the remaining animals at 14 days after treatment showed that the reduction of mean fecal EPG value for each group was: U-46%, I-52%, M-72%, D-61%, E-8%, and A-68%. Worm recovery from the slaughter calves showed that all groups harbored significant numbers of Haemonchus placei and H. contortus. In addition, all avermectin-treated groups contained significant numbers of Cooperia punctata, and smaller numbers of C. oncophora and C. spatulata. These results imply that the pastures studied contain substantial numbers of H. contortus resistant to both avermectins and benzimidazoles, and H. placei and Cooperia sp. resistant to all the commonly used avermectin anthelmintics. This is the first report of anthelmintic resistance in American cattle parasites.
... Worldwide, reports of parasite resistance to anthelmintics, endectocides and acaricides are increasing [79,[87][88][89][90][91][92][93][94][95]. In Europe, the United States of American, Australia, New Zealand, Brazil and elsewhere, helminth resistance to macrocyclic lactone has been widely demonstrated [90,93,[96][97][98][99][100][101][102][103][104]. ...
... In Europe, the United States of American, Australia, New Zealand, Brazil and elsewhere, helminth resistance to macrocyclic lactone has been widely demonstrated [90,93,[96][97][98][99][100][101][102][103][104]. Anthelmintic resistance to benzimidazoles and imidazothiazoles have also been reported in North America, Australia, Brazil and Europe [87,90,93,105,106]. Anthelmintic resistance has even been identified in farms with no or low treatment history and without any epidemiological or trade links [99,103]. ...
... In a survey of cow-calf producers in Western Canada, Wills et al. (2020) found routine dependency on pour-on ML control of external parasites [135]. While not administered for control of internal parasites in this case, the approach exerts substantial pressure to select for anthelmintic resistance (AR) [87,89,98,113]. ...
Simple Summary
Cattle parasites live inside or on the body of beef cattle. The most common beef parasites include intestinal roundworms, flatworms and ticks. The act of parasitizing cattle reduces the health of the animals and reduces the economic value to the farmer through reduced body weight, milk production, coat and hide quality and ability to give birth to healthy calves. As a result, beef cattle producers lose billions of dollars in the value of their herds each year due to parasitism. Preventing and treating parasites is an important step in increasing the farmers’ ability to raise healthy beef cattle, make a profit and meet the world’s need for sustainable protein and other cattle products.
Abstract
Global human population growth requires the consumption of more meat such as beef to meet human needs for protein intake. Cattle parasites are a constant and serious threat to the development of the beef cattle industry. Studies have shown that parasites not only reduce the performance of beef cattle, but also negatively affect the profitability of beef agriculture and have many other impacts, including contributing to the production of greenhouse gases. In addition, some zoonotic parasitic diseases may also threaten human health. Therefore, ongoing cattle parasite research is crucial for continual parasite control and the development of the beef cattle industry. Parasitism challenges profitable beef production by reducing feed efficiency, immune function, reproductive efficiency, liveweight, milk yield, calf yield and carcass weight, and leads to liver condemnations and disease transmission. Globally, beef cattle producers incur billions (US$) in losses due to parasitism annually, with gastrointestinal nematodes (GIN) and cattle ticks causing the greatest economic impact. The enormity of losses justifies parasitic control measures to protect profits and improve animal welfare. Geographical differences in production environment, management practices, climate, cattle age and genotype, parasite epidemiology and susceptibility to chemotherapies necessitate control methods customized for each farm. Appropriate use of anthelmintics, endectocides and acaricides have widely been shown to result in net positive return on investment. Implementing strategic parasite control measures, with thorough knowledge of parasite risk, prevalence, parasiticide resistance profiles and prices can result in positive economic returns for beef cattle farmers in all sectors.
... Anthelmintic drug resistance was first documented in small ruminants in 1964 (Waller, 1994), but recently in 2003, resistance was reported in US beef cattle (Gasbarre et al., 2009). According to the 2008 National Animal Health Monitoring System's survey, Cooperia spp. ...
... The reduced FEC in treated cattle in this experiment is similar to that in previous literature for cattle treated with a macrocyclic lactone or benzimidazole (Gasbarre et al., 2009;Edmonds et al., 2010;Walker et al., 2013;Backes, 2016). Cattle in this experiment were maintained in treatment-specific pastures to prevent crossover effects. ...
... This lower percentage reduction would suggest parasite resistance to extended-release eprinomectin was present at that location (Edmonds et al., 2018), but this was not present in this current experiment. Other previous work has shown signs of resistance to macrocyclic lactones such as ivermectin, eprinomectin, and moxidectin (Gasbarre et al., 2009;Edmonds et al., 2010;Walker et al., 2013). ...
Objective
Our objective was to determine whether parasite resistance to extended-release eprinomectin was present in an operation after 3 yr of eprinomectin use.
Materials and Methods
Fall-born Angus × Simmental heifers (224 ± 22 d of age; 171 ± 17.8 kg initial BW) were stratified by d −2 fecal egg count (FEC) and BW and assigned to 1 of 9 groups (7 heifers per group). Groups were then assigned to 1 of 3 treatments: extended-release eprinomectin (ERE; n = 3), extended-release eprinomectin and oxfendazole (ERE+O; n = 3), or saline control (CON; n = 3). Throughout the experiment, FEC and packed cell volume were evaluated 6 times, and a fecal egg reduction test was conducted on d 28.
Results and Discussion
There was a treatment × time interaction (P < 0.01) for FEC as FEC was not different on d −2 and 28. However, CON had greater FEC than ERE and ERE+O on d 55 and 83. Additionally, at d 55 ERE had greater FEC than ERE+O. On d 112 and 167, FEC was similar among all treatments. Fecal egg reduction for ERE and ERE+O were above the 90% threshold (91 and 98% reduction, respectively). There was no treatment × time interaction or treatment effect (P ≥ 0.14) for packed cell volume.
Implications and Applications
Based on the fecal egg reduction test (>90%), parasite resistance was not present in an operation after 3 yr of use of extended-release eprinomectin.
... In contrast, although the benzimidazoles are highly effective against a large range of internal nematode parasites, their lack of ectoparasite activity and less convenient oral formulation has meant they have been less commonly used in cattle, particularly in North America. Macrocyclic lactone resistance is now common in gastrointestinal nematodes in North American cattle (Gasbarre et al., 2009(Gasbarre et al., , 2015. Anecdotal evidence suggests that more cattle producers are beginning to consider using benzimidazole drugs for gastrointestinal nematode control and this trend is likely to continue as the awareness of ivermectin resistance grows. ...
... Due to the greater risk of clinical disease associated with gastrointestinal nematodes in bison than in cattle, although commercial bison herds still predominantly rely on pour-on macrocyclic lactones for control, there has been somewhat greater use of benzimidazole drugs in this host species (pers comm ref from Dr Roy Lewis, Merck Animal Health). Consistent with the relatively limited use, there has, as yet, only been a few cases of confirmed benzimidazole-resistant parasites in North American cattle (Gasbarre et al., 2009;Chaudhry et al., 2014). However, in countries where the benzimidazoles have been more heavily used in cattle, such as New Zealand, Australia and South America, resistance is becoming widespread in gastrointestinal nematodes of cattle (McKenna, 1991;Waghorn et al., 2006;Cotter et al., 2015;Ramos et al., 2016). ...
... However, benzimidazole efficacy was only tested for five of these herds and there was a >90% reduction of egg counts in each of these cases. Benzimidazole resistance has only been clinically confirmed for H. contortus from parasites infecting cattle from the USA, and so benzimidazole resistance is not considered to be a major issue at present (Gasbarre et al., 2009;Gasbarre, 2014). Nevertheless, the F200Y (TTC > TAC) SNP has been detected at low frequency in H. placei from Georgia, Florida and Arkansas, using a pyrosequence genotyping assay suggesting resistance is at the early stages of emergence in this parasite species (Chaudhry et al., 2014). ...
As genomic research continues to improve our understanding of the genetics of anthelmintic drug resistance, the revolution in DNA sequencing technologies will provide increasing opportunities for large-scale surveillance for the emergence of drug resistance. In most countries, parasite control in cattle and bison has mainly depended on pour-on macrocyclic lactone formulations resulting in widespread ivermectin resistance. Consequently, there is an increased interest in using benzimidazole drugs which have been used comparatively little in cattle and bison in recent years. This situation, together with our understanding of benzimidazole resistance genetics, provides a practical opportunity to use deep-amplicon sequencing to assess the risk of drug resistance emergence. In this paper, we use deep-amplicon sequencing to scan for those mutations in the isotype-1 β-tubulin gene previously associated with benzimidazole resistance in many trichostrongylid nematode species. We found that several of these mutations occur at low frequency in many cattle and bison parasite populations in North America, suggesting increased use of benzimidazole drugs in cattle has the potential to result in widespread emergence of resistance in multiple parasite species. This work illustrates a post-genomic approach to large-scale surveillance of early emergence of anthelmintic resistance in the field.
... Gastrointestinal nematode resistance in stocker cattle was first identified in the United States in 2003 and reported in 2009. 5 Resistance to macrocyclic lactones and benzimidazoles was confirmed the following year by the same research group. 6 Cattle in both of these studies originated in the southeastern United States and were grazed in Wisconsin at the time resistance was detected. ...
... The findings are consistent with other reports that have identified resistance to a wide array of anthelmintic products. [5][6][7] It is important to note that the resistance to a wide array of products found in this study does not necessarily provide evidence of multi-drug resistant parasite populations. Herds in this study only administered a single anthelmintic product so the effects of combination therapy or the presence of multi-drug resistance could not be evaluated. ...
Beef cow-calf producers submitted fecal samples for fecal egg count reduction (FECR) tests. Anthelmintic administration practices were not controlled, and producers were encouraged to follow standard procedures for each herd. Fecal egg counts (FEC) were determined using the Wisconsin method with alimit of detection of 1 egg per gram (EPG). Inclusion criteria included a pretreatment FEC of 25 EPG. A FECR of ≤ 90% was considered indicative of resistance. Seventeen herds submitted a total of 19 sample sets. All major classes of anthelmintics were represented except for levamisole. Injectable, pour-onand oral as well as original label and generic products were represented. Sample sets from 3 herds were excluded from the final analysis based on inadequate pretreatment FEC. Of the 16 sample sets included in the final analysis, 13 exhibited resistance based on the arithmetic mean of individual FECR tests (FECRT). In addition to individual FEC, composite samples for each herd were created using 1 gram of feces from each animal. Four grams of each composite sample were used to determine a composite FEC. Composite samples from 13 herds were included in the final analysis and 11 of 13 exhibited resistance. There was complete agreement between the individual and composite samples for the detection of resistance. Based on the results of this small survey, apparent anthelmintic resistance appears to be widespread in beef cow-calf herds in Oklahoma. Composite sampling appears to be an effectivemethod for detection of herd level resistance.
... In a recent study of the parasite species present in young cattle, Haemonchus contortus was found to be prevalent in pre-weaned calves in regions of the North Island where Haemonchus is common (Waghorn et al., 2019). H. contortus is known to infect cattle overseas (Amarante et al., 1997;Gasbarre et al., 2009;Emery et al., 2016) and in New Zealand (Brunsdon, 1964). However, while H. contortus is regarded as highly pathogenic in sheep (Emery et al., 2016) its role as a parasite of cattle is less clear (Amarante et al., 1997;Santos et al., 2014). ...
... However, collectively the Haemonchus genus of parasites appear to be capable of adapting, by changing their behaviour in response to different environmental conditions and the availability of host species (Santos et al., 2014). For example, Gasbarre et al. (2009) found H. contortus in cattle grazing pastures which had not been grazed by sheep or goats for over 40 years. It might reasonably be hypothesised that in the New Zealand farming systems, where many farms graze both sheep and cattle, that H. contortus remains primarily a parasite of sheep with only limited ability to infect cattle. ...
Haemonchus contortus can frequently be found infecting pre-weaned beef calves on sheep and beef farms around the North Island of New Zealand. The purpose of this study was to consider whether the presence of this parasite alone, or as part of a mixed infection, could be impacting growth rates of young animals, on three commercial farms in the North Island of New Zealand. Trials were conducted on commercial sheep and beef farms in each of the Northland, King Country and Gisborne regions, in late summer/autumn (February to April) of 2016 to measure the effect of treatment with narrow and broad spectrum anthelmintics on liveweight gain of spring-born calves pre-weaning. Each farm was chosen based on the presence of Haemonchus and that it was a beef cow/calf system with the cows and calves grazing the same pastures as sheep at some stage. Three sampling visits were made to each farm with the animals being weighed, faecal sampled and treated with one of two anthelmintics (Closantel alone to remove only Haemonchus or a triple combination containing moxidectin, levamisole and oxfendazole to remove all nematodes) or left untreated, on each of the first two visits. There was no significant difference in liveweight gain between any of the treatment groups, hence there was no evidence for an impact of Haemonchus alone, or a mixed nematode infection, on pre-weaned calf growth rates on these farms. It remains unclear whether there may be a justification to consider treatment of calves should they constitute a significant source of pasture larval infestation with H. contortus, in an integrated cattle-sheep system.
... Denoted the "wonder drug", this chemical class has generated various reviews of efficacy. (Geary, 2005;Gasbarre et al., 2009;Loveridge et al., 2003;Anziani et al., 2004;Loveridge et al., 2003;Fiel et al., 2001;Yazwinski et al., 2009b;Kaplan and Vidyashankar, 2012) Milbemycin is still displaying high levels of efficacy. (Cleale et al., 2004;Yazwinski et al., 2006b;Yazwinski et al., 2013a;Ives et al., 2007) Conflicting reports have been published for imidazothiazoles: Lyndal-Murphy et al. found that the chemical class is still efficacious, but Becerra-Nava et al. reported that it is losing its effectiveness. ...
... This in vivo efficacy evaluation has been used by many researchers in recent years. (Gasbarre, 2009;Jackson et al., 2006;Yazwinski et al., 2009a;Yazwinski et al., 2009b;Barrere et al., 2013;Condi et al.,2009;Rocha et al., 2008) Another, more accurate, in vivo method of efficacy evaluation is the control study. This involves the comparison of treatment groups to a non-treated group, with both groups being sacrificed at the termination of the study and the internal nematode burdens compared. ...
The existence of anthelmintic resistance is not singular in parasite species, host species or geographic region. It has become a problem of worldly stature, especially when considering sheep nematodes. Recommendations have been modified from chemical-based control to multipart, managerial intervention. Compared with nematodes of cattle, the worldwide resistance of sheep nematodes to anthelmintic remedies is much more pronounced and urgent. As the resistance to essentially all anthelmintic classes approaches a cautionary level, the implementation of non-chemical controls has grown increasingly essential. Six-6 to 8 month old Holstein steer calves, six-5 month old Katahdin ram lambs and eight-5 month old Suffolk X Rambouillet lambs were dewormed and inoculated with either cattle-source infective nematode larvae or sheep-source infective nematode larvae. Fecal egg counts (FEC) were followed until necropsy at 39 and 40 days post inoculation. The total mean FEC were highest amongst the hair and wool sheep groups, respectively, which were inoculated with both sheep-source and cattle-source nematodes. The low fecal egg output by treatment group 1 shows that using cattle as models for the sheep-source nematodes can keep the fecundity of the nematodes low; however, caution should be taken before implementation. The host specificity of Haemonchus spp. seems to be a minimal factor in nematode fecundity.
... Many studies are published worldwide on the co-infectionamong theH. placei and H. contortusin small ruminantsand large ruminants (Achi et al., 2003;Amarante et al., 1997;Brasil et al., 2012;Gasbarre et al., 2009b). In contrast the published research works on the interspecies hybridization between the different roundworms are few in numbers (Chaudhry et al., 2015a;Criscione et al., 2007). ...
... H. contortus and H. placei co-infection happens again in many ruminants under characteristic field that could be a possibly critical source. There are very few reports of co-infection of H. placei and H. contortus in cows and not a single reported in the buffalo (Gasbarre et al., 2009a;Gasbarre et al., 2009b). ...
With extensive use of the anthelmintic in many tropical and parasite-endemic countries, the graveness of parasite resistance is exaggerating. The trend in the use of excessive medication in animal is also posing threats to pub-lic health. The governmental bodies are either lacking understanding or underestimating the regime of this emerging issue. This brief overview highlights the need, rationale and urgency of the matter to establish foundations for unified action plans at the national levels as well as international levels in mitigating the development of resistance.
... Cooperia spp. are strongylids most commonly reported to be resistant to anthelmintics (Gasbarre et al., 2009;El-Abdellati et al., 2010;Bartley et al., 2012) and resistance has also been demonstrated in Ostertagia ostertagi (Edmonds et al., 2010;Avramenko et al., 2017). ...
... ML LOE has previously been reported in the US and is considered an increasing problem (Yazwinski and Tucker, 2006;Gasbarre et al., 2009a;Gasbarre et al., 2009b;Edmonds et al., 2010;Gasbarre, 2014;Gasbarre et al., 2015;Edmonds et al., 2018;Kaplan, 2020). One recent review noted the southern US had a high prevalence of ML-resistant Cooperia spp. ...
... and Haemonchus placei [122], which were identified in several reports of AR [67,71,116]. Resistance of the genus Cooperia is also common in countries such as Argentina [73], United Kingdom [123], Mexico [124], Sweden, Belgium, Germany [125], United States [126,127] and Australia [128,129]. Most of these reports are related to resistance to ivermectin. ...
Gastrointestinal nematodes (GIN) significantly, negatively impact livestock worldwide, and their control depends on the use of chemotherapy drugs. However, this approach is unsustainable as anthelmintic resistance (AR) is growing widespread. This article provides a comprehensive overview of the historical and current data published on AR in domestic ruminants in Brazil. Alternative measures of GIN control have been discussed to provide helpful information to prevent the development of AR in the country. This review consisted of a search of technical and scientific publications between January 1960 to January 2023, using online sources such as PubMed, Scielo and Google Scholar. Eighty-three articles published over the last six decades reporting AR in sheep (n = 43), goats (n = 20) and cattle (n = 20) were included. A total of 37.3%, 25.4% and 37.3% evaluated one, two and three or more molecule classes, respectively. Among all studies, 82.1% used fecal egg count reduction test as a method of AR diagnosis. In conclusion, AR is an urgent and emerging issue for ruminant production in Brazil. It is necessary to evaluate on a large scale the distribution and management of anthelmintic drugs and discuss strategies that delay this phenomenon’s development.
... Since drug exposed to sun light may lose their effectiveness due to interaction of active ingredient with UV rays, the claim was realistic. Medicinal products should be handled and transported based on the recommendation and should not be subjected extreme heat and cold (Gasbarre et al., 2009). In Ethiopia misuse and smuggling of anthelmintics in many forms is increased time to time probably due to the absence of a rational policy for anthelmintic use (Hussein et al., 1999). ...
A study was conducted to evaluate the knowledge of farmers on internal parasite prevention and controls, anthelmintic drug utilization and management practices. The study was conducted from September 2014 to 2018 on 393 purposively selected farmers. Farmers were selected from Ada berga (128), Welmera (136) and Grar jarso (129) districts central Oromia, Ethiopia. One-hundred Ninetyfive (49.6%) farmers reported livestock diseases as the major production constraint. Most of the farmers (99.2%) used different drugs for helminthes treatment and control. However, about 76.8% of them were not aware of the existence of drug quality problems. The other problems of currently using anthelminthic drugs as mentioned by the remaining farmers were expired drugs (5.3%), poor efficacy (12.5%), counterfeit (1.3%), and inappropriate usage (1%). Most of the farmers treat their animals by their own (69.2%) and some relied on professionals (9.7%). The most common methods of drug administration were drenching (44.3%), manual (25.2%), and combination methods (21.6%). About 24.7% of the farmers purchased drugs from drug smugglers and more than 80 (19.6%) of them treated their animals with incorrect dosage. The most frequently observed adverse effects following over dose were diarrhea (2.8%), restlessness (1.8%), and death 25 (6.4%). About 42% of farmers didn't know about periodical deworming, whereas 16.3%, 14.8% and 13% of the respondents performed deworming every four, three and six month intervals, respectively. The application of anthelmintic drugs was mainly made by professional advice (95.4%) and about 2.8% and 0.8% were done by guessing and advice of smugglers respectively. Sex, district, sunlight exposure and expiry dates significantly (p<0.05) influenced drug quality.
... Macrocyclic lactone (MLs) resistance was found to have developed in trichostrongyle species of cattle in Europe [47]. The same results also appeared in South and North America [28,48]. Two studies reported multi-drug resistance against ML and BZ [28,49]. ...
Helminth parasitic infections are a considerable constraint to the livestock industries worldwide. Nematode parasites cause the major proportion of harm to livestock. The infections caused are accountable for severe economic losses in cattle, goat and sheep farming industries. Morbidity and mortality in livestock due to parasitic diseases are increasing alarmingly. Also, their zoonotic influence on human health is considered significant. Anthelmintic drugs have been developed occasionally to curb this disease and prevent major losses. But the development of resistance against these drugs has put another constraint on this flourishing industry. Helminth parasites have developed resistance against three main classes of anthelmintics: benzimidazoles, macrocyclic lactones and nicotinic agonists. With the intensification of resistance, various screening and confirmatory tests have been developed for the speedy introduction of newer drugs in the livestock industry. At the same time, designing and launching novel anthelmintics is time-consuming and economically restrained. Phytochemicals attract much attention because of their pharmacotherapeutic potential, least toxic profile and low environmental hazards. A lot of work is going on plant-based anthelmintic drugs throughout the world. Plants possessing anthelmintic activity have been found efficacious against gastrointestinal parasites. Nevertheless, these herbal medicines have various drawbacks, which include poor efficacy and the absence of target selectivity. These problems are now being taken care of with the help of nanotechnology. Nanoparticles improve the drug's effectiveness, enhance drug delivery, and target selectivity at specific sites. A comprehensive literature survey was carried out via electronic searches of Google Scholar, PubMed, MEDLINE, Science Direct, Scopus and Cochrane Library databases and based on inclusion and exclusion criteria; articles were selected for this review. The review aims at providing a comprehensive overview of plant-based nanoparticles as therapeutic alternatives over conventional synthetic anthelmintic drugs. It also encompasses the methods of detection of resistance and the ways to overcome this menace. The effectiveness of various organic and inorganic nanoparticles against helminthes is also discussed in this review.
... In many other regions of the world, the two species occur in the same geographic area and co-infection is Table 4 Point mutations E198A, F200Y and E198K in the β-tubulin gene of H. contortus isolates in goats from selected districts of Uganda. common (Achi et al., 2003;Gasbarre et al., 2009). The identification of the H. placei in the current study may be explained by the grazing system along the cattle corridor which involves cattle grazing alongside goats, which may result in cross infestation. ...
Gastrointestinal parasites are among the most economically important pathogens of small ruminants causing serious economic losses and animal welfare problems for the livestock industry worldwide. The emergence of anthelmintic resistant H. contortus in small ruminants is a serious problem because it undermines effective helminth control and results in reduced productivity. Little is known about resistance to benzimidazoles (BZ) in Haemonchus in goats and sheep in Uganda. The objective of this study was to determine the prevalence of gastrointestinal parasites and to identify the presence of benzimidazole resistance associated mutations in the β-tubulin isotype 1 gene of Haemonchus contortus in goats from selected districts of Uganda. A total of 200 goats from 10 districts of Uganda slaughtered at Kalerwe abattoir in Kampala were sampled for H. contortus adult worms. Faecal samples were also collected to detect other intestinal parasites. Faecal microscopy and analysis were performed using flotation and sedimentation techniques. DNA was extracted from adult worms and PCR and sequencing of the ITS-2 region and β-tubulin isotype 1 gene performed to identify H. contortus species and to determine the presence of mutations associated with anthelmintic resistance respectively. Faecal microscopy showed that the most prevalent intestinal parasites were coccidia (98%), strongyles (97.5%), Strongyloides (82%), Paramphistomum (74.5%), Moniezia (46%), Fasciola (1.5%) and Trichuris (1%). Most goats had a high intestinal burden of coccidia (≥ 5000 oocyst per gram) and strongyles (≥ 1000 egg per gram), 65% and 67.5%, respectively. The prevalence of H. contortus adult worms was 63% (126/200). Sequencing of the partial β-tubulin isotype 1 gene of 54 Haemonchus contortus adult male isolates revealed the presence of mutations associated with anthelmintic resistance. The F200Y mutation was the most common mutation (13% of samples with good beta-tubulin sequences) followed by the E198A and E198K mutations, both found in 9% of sequenced samples. Mutation F167Y was not identified in any of the samples and there were no heterozygous individuals for any of the SNPS associated with BZ resistance that were identified in this study. These findings highlight the need for controlled use of anthelmintics especially benzimidazoles, to enable sustainable control of H. contortus in Uganda, and a need for further investigation to understand the resistance of other parasites identified in this study.
... Anthelmintic resistances against different groups have been reported frequently from South America (Waller et al, 1996), South Africa (Mphahlele et al, 2021), Australia (Love and Coles, 2002), UK (Brown et al, 2022), France (Leignela et al, 2010) and China (Hou et al, 2022). Resistance to the gastrointestinal nematodes has been reported in cattle from Brazil (Ramos et al, 2016), New Zealand (Familton et al, 2001), which is also a major problem in Brazil, Argentina (Anziani et al, 2004;Suarez et al, 2007) and USA (Gasbarre et al, 2004). BZ and MLs resistance has also been found in helminths in ruminants from Nordic-Baltic region (e.g. ...
The prevalence of resistance to broad-spectrum anthelmintics among veterinary important helminths has dramatically increased in last three decades in livestock production in many countries. Indiscriminate and improper use of anthemintics without proper diagnosis has led to development of resistance across the globe. A variety of in-vivo, in-vitro and modern molecular techniques have been developed for the detection of helminth population resistant to the particular anthelmintic group. Managemental strategy is one of most powerful, sustainable and eco-friendly technique among the control methods for helminth parasites, by which we can prevent the development of anthelmintic resistance and would get wholesome animal products. Biological control, phytoanthelmintic and potent vaccine candidate against animal parasite could become a strong weapon for a viable alternative sustainable control of parasites of veterinary importance in near future.
... 32 Eprinomectin and moxidectin were further investigated using the FECRT protocol in two separate commercial beef herds owned by the University of Illinois at the Dixon Spring Agricultural Station in Simpson, Illinois to investigate whether the repeated use of eprinomectin or moxidectin would lead to parasite resistance. 16 In the first phase of the first trial, 30 animals in each herd received eprinomectin pour-on according to label directions (0.5mg/kg BW). In the second phase, treated animals from the first trials were ranked based on posttreatment worm egg counts, blocked and randomly assigned to one to two treatment groups. ...
Parasite resistance to the macrocyclic lactones (ivermectin, doramectin, eprinomectin, and moxidectin) is receiving considerable attention in the US cattle industry at a time when the economics of parasitism constitute one of the most important factors involved in beef production. Knowing whether a dewormer is effective is extremely important to an operation. If parasites become resistant to a particular product or product formulation, a serious problem can develop unknowingly unless producers have an easy way to determine product efficacy. The fecal egg count reduction test (FECRT) is a simple test recommended by the American Association of Veterinary Parasitologists (AAVP) as the best way for the practitioner to help producers verify that the dewormer(s) they are using is effective. The FECRT involves conducting a fecal check at the time of treatment and again 14 days following treatment. In the fall of 2007 continuing through the summer of 2008, free lab support was offered to bovine practitioners throughout the US to conduct FECRTs with their clients. This was done according to a standard protocol involving a minimum of 20 samples per treatment group at each collection time. The results are being recorded in a national data base supported by Intervet/Schering-Plough Animal Health and the University of Nevada-Reno. Over 58 veterinary clinics in 19 states have already participated in this program, with over 119 separate tests involving 4,765 samples using a wide range of products and formulations. These data confirm that macrocyclic lactone resistance is widespread and that continued vigilance is required by the veterinary profession, since the problem now appears to be at a critical stage with millions of dollars in production losses at stake.
... Although avermectin resistance was first reported in small ruminants in South Africa, 22 the first report in United States cattle was in 2004 when resistant Cooperia punctata and Haemonchus spp worms were confirmed at necropsy in a grazed stocker operation. 7 Further evidence was confirmed in a controlled efficacy study where necropsy of treated animals demonstrated that avermectin was ineffective in reducing developing or arrested Ostertagia ostertagi and adult Cooperia onchophora. 5 These findings along with the rapid rise in domestic and global publications on anthelmintic resistance in livestock 20 raised the importance of this issue for producers, the veterinary community, and regulatory agencies. ...
Anthelmintic resistance in the United States has recently gained the attention of the veterinary and livestock communities. The rapid rise in resistance to 2 new drug classes shortly after approval outside the United States calls for new strategies and recommendations for maintaining an effective anthelmintic program even as new drugs become available. The development of resistance is product-dependent, with observable differences between classes. Methods used to test anthelmintic efficacy allow the veterinary practitioner to make informed treatment decisions; however, the results should be interpreted carefully due to the limitations for the fecal egg count procedure.
... (3) moderate (3-9 eggs or larvae/field); (4) numerous/heavy/ many (10+ eggs or larvae/field). Then, a fecal egg count reduction test (FECRT) was conducted according to Gasbarre et al. (2009) using a modified Wisconsin Sugar Floatation Technique in order to determine the number of eggs per gram of feces. A subsample of 10 heifers/treatment was collected at processing and snap-frozen in liquid nitrogen for subsequent analysis. ...
A total of 80 crossbred, high-risk heifers (initially 250 ± 4.2 kg BW), were transported from an Oklahoma City, Oklahoma sale barn to the Kansas State University Beef Cattle Research Center. Cattle were unloaded and randomly placed into one of four receiving pens and provided ad libitum hay and water. Each pen was randomly assigned to one of four rest-times before processing: 1) immediately upon arrival (0); 2) after a 6-h rest period (6); 3) after a 24-h rest period (24); and 4) after a 48-h rest period (48). After all cattle were processed, heifers were allotted into individual pens with ad libitum access to a receiving ration and water. Heifers were weighed individually on d 0, 7, 14, 21, 28 and 35 to calculate average daily gain (ADG). Feed added and refusals were measured daily to determine dry matter intake (DMI). A fecal egg count reduction test and analysis of blood serum metabolites were also conducted. All data were analyzed using the GLIMMIX procedure of SAS (v. 9.4, Cary, NC) with individual animal as the experimental unit. Processing time did not impact (P > 0.05) heifer BW or ADG. From d 0 to 35, DMI decreased linearly (P = 0.027) as rest time increased. The number of days for heifers to reach a DMI of 2.5% BW was linearly increased (P = 0.023) as rest time increased. There was no evidence of differences (P ≥ 0.703) among rest times for feed efficiency. While morbidity did not differ between treatments (P > 0.10), mortality increased linearly (P = 0.026) as the time of rest increased. A significant processing time × day interaction (P < 0.0001) was observed for the prevalence of fecal parasites, where the percentage of positive samples was significantly lower 14-d after anthelmintic treatment, regardless of the processing time. Serum IBR titer for heifers processed at either 0 or 6-h upon arrival was significantly higher (P < 0.01) on d 35 compared to d 0. Heifers processed after a 48-h rest period had significantly higher glucose values (P < 0.01) on d 0 compared to heifers processed at 0, 6, or 24-h. In summary, rest time prior to processing did not impact receiving calf growth performance. A 6-h rest period upon arrival appeared to be most beneficial to DMI. Anthelmintic treatment at processing reduced the parasitic load in heifers processed at all times. Vaccine titer did not increase after initial processing in heifers processed 24- or 48-h after arrival, indicating the seroconversion of IBR antibodies during the longer rest period.
... Cooperia punctata is also one GIN species that most commonly develop resistance to macrocyclic lactones, with several USA cattle reports [30,31]. Ivermectin is currently the most widely used macrocyclic lactone in western Canadian beef operations [19]. ...
Background
The species composition of cattle gastrointestinal nematode (GIN) communities can vary greatly between regions. Despite this, there is remarkably little large-scale surveillance data for cattle GIN species which is due, at least in part, to a lack of scalable diagnostic tools. This lack of regional GIN species-level data represents a major knowledge gap for evidence-based parasite management and assessing the status and impact of factors such as climate change and anthelmintic drug resistance.
Methods
This paper presents a large-scale survey of GIN in beef herds across western Canada using ITS-2 rDNA nemabiome metabarcoding. Individual fecal samples were collected from 6 to 20 randomly selected heifers (n = 1665) from each of 85 herds between September 2016 and February 2017 and 10–25 first season calves (n = 824) from each of 42 herds between November 2016 and February 2017.
Results
Gastrointestinal nematode communities in heifers and calves were similar in Alberta and Saskatchewan, with Ostertagia ostertagi and Cooperia oncophora being the predominant GIN species in all herds consistent with previous studies. However, in Manitoba, Cooperia punctata was the predominant species overall and the most abundant GIN species in calves from 4/8 beef herds.
Conclusions
This study revealed a marked regional heterogeneity of GIN species in grazing beef herds in western Canada. The predominance of C. punctata in Manitoba is unexpected, as although this parasite is often the predominant cattle GIN species in more southerly latitudes, it is generally only a minor component of cattle GIN communities in northern temperate regions. We hypothesize that the unexpected predominance of C. punctata at such a northerly latitude represents a range expansion, likely associated with changes in climate, anthelmintic use, management, and/or animal movement. Whatever the cause, these results are of practical concern since C. punctata is more pathogenic than C. oncophora, the Cooperia species that typically predominates in cooler temperate regions. Finally, this study illustrates the value of ITS-2 rDNA nemabiome metabarcoding as a surveillance tool for ruminant GIN parasites.
Graphical Abstract
... This findings of albendazole efficacy is similar with the studies done by [7] in Germany on monitoring the efficacy of ivermectin and albendazole against gastro intestinal nematodes of cattle. There are anthelmintic resistance in gastrointestinal nematodes of cattle according to the study done by [8] in US on the identification of cattle nematode parasites resistant to multiple classes of anthelmintics in a commercial cattle herd. In general the result showed that the mean FECR value of Albendazole and tetraclozan were 95.6 and 97.1 percent respectively. ...
Gastrointestinal parasites are economically important in the dairy industry. A study was carried out to evaluate the therapeutic efficacy of anthelmintic drugs (Tetraclozan 3400 mg and Albendazole 2500mg) for the treatment of GIT worms in cross-bred cows at Holeta research center. A total of sixty crossbred cows were purposively screened and divided into three groups for the current study. The first groups served as untreated control, the second and third groups were treated with Albendazole and Tetraclozan drugs respectively. Moreover, fecal samples were collected before and after treatment to count the eggs per gram (EPG) of feces and to evaluate drug efficacy percentage. Efficacy for each anthelmintic was determined by the Fecal Egg Count Reduction Test (FECRT). The mean EPG count before and after treatment with Tetraclozan drug on 0. 14 th and 21 st days was 520±102.1, 100±54.6 and 15±6.7 respectively whereas the mean EPG count on 0, 14 th and 21 st days before and after treatment with Albendazole drug was 450±127.2, 150±46.2 and 20±6.8 respectively. The overall percentage efficacy of Tetraclozan and Albendazole drugs were 97.11 and 95.5 percent respectively. The study indicated that the two anthelmintic drugs were efficacious against worm infection and thus, leads to reduction in EPG count. It is important to explore the detailed pharmacokinetic and toxic effects of these drugs for wide therapeutic uses in animals. It is also recommended that the clinical responses of GIT helminthes to prophylactic and therapeutic drugs need to be periodically monitored in the farms and further introduced to smallholder farmers.
... Likewise, anthelmintic resistance is becoming an increasing global problem resulting from the misuse of these drugs. Resistance to anthelmintic by ruminant nematode parasites is a growing problem throughout the world [6]. Food animals and foods of animal origin are traded worldwide; thus, drug resistance affecting the food supply of one country becomes a potential problem for other countries [2]. ...
The rational use of drugs in veterinary medicine has various significances, such as reducing the risk of drug resistance, increasing efficacy, reducing drug residue, and decreasing adverse drug reactions. A retrospective study was conducted to assess veterinary drug prescribing practices at Batu and Arsi-Negelle district veterinary clinics in the rift valley areas of Ethiopia. A total of 2,464 cases were recorded from the case registration books at both the clinics for diseases treated between September 2012 and February 2015. The study results showed that for a total of 2,464 cases diagnosed at both clinics, 3,811 different drugs were prescribed, with an average per encounter of 1.6. Among the total drugs, oxytetracycline, ivermectin, penstrep, sulfa drugs, and albendazole were the most leading prescribed drugs with a frequency of 43.0%, 17.6%, 10.2%, 6.5%, and 1.3%, respectively. All drugs were prescribed by the generic name without any laboratory support of the disease. About 68.3% of the cases were diagnosed by unspecified professionals, whereas 21.7% and 10.1% were done by animal health assistants and veterinarians, respectively. The prescribing practices showed 61.0% of antibiotics and 29.7% of anthelmintics where 45.3% and 54.7% of antibiotics and 17.8% and 82.2% of anthelmintics were given at Batu and Arsi-Negelle veterinary clinics, respectively. Of the prescribed drugs, 4.6% oxytetracycline and 2.6% penstrep were prescribed irrationally to treat diseases that were tentatively diagnosed as parasitic cases. Similarly, 40.5% ivermectin and 17.7% albendazole were prescribed for bacterial infections. In conclusion, this study revealed problems in antibiotics and anthelmintics use, description of routes of administration and length of treatment, and shortage of laboratory diagnostic facilities. Therefore, veterinary drugs, particularly antibiotics and anthelmintics, should be used appropriately to safeguard the public from residual drug impacts and resistance development.
1. Introduction
The rational use of drugs is the use of the right medicines, correct dosage, and correct cost, which is well reflected in the World Health Organization (WHO) definition: “Rational use of drugs requires that patients receive medications appropriate to their clinical needs, in doses that meet their requirements for an adequate period, at the lowest cost” [1]. However, the irrational use of medicines is when one or more of these conditions are not met, for example, too many medicines are prescribed per patient, injections are used where oral formulations would be more appropriate, antimicrobial agents are prescribed in inadequate doses or duration, or antibiotics prescribed for nonbacterial infections, thereby contributing to the growing problem of antimicrobial resistance and prescriptions do not follow clinical guidelines [2].
Problems like lack of information, poor communication between health professionals and animal owners, lack of diagnostic facilities, demand from the owners, and high burden of diseases with overlapping clinical symptoms (e.g., pain, fever, and depression are common symptoms for different conditions which require different drugs) [3] lead to the irrational use of drugs causing ineffective and unsafe treatment, exacerbation or prolongation of illness, distress and harm to the patient, and increase the cost of treatment [4, 5].
Antibiotics are widely used in healthy food-producing animals to promote growth and prevent diseases. This practice favors the emergence and spread of resistant bacteria in both animal and human populations. The routine use of antimicrobials in vast numbers of healthy animals is likely to result in the emergence and spread of antimicrobial-resistant bacteria and cause resistant infections in animals and humans. Likewise, anthelmintic resistance is becoming an increasing global problem resulting from the misuse of these drugs. Resistance to anthelmintic by ruminant nematode parasites is a growing problem throughout the world [6]. Food animals and foods of animal origin are traded worldwide; thus, drug resistance affecting the food supply of one country becomes a potential problem for other countries [2].
There are essential measures to be taken to improve rational drug prescribing. These are critical assessment and evaluation of benefits and risk of drug used; safety and cost of the drug with the existing drug for some indication; identification of the patient’s problem based on symptoms and recognizing the need for action; diagnosis of the disease, identifying underlying cause, and motivating factors that may be specific as in infectious disease or nonspecific; use of possible intervention or treatment which may be nondrug treatment or drug treatment by choosing from different alternatives based on efficacy, convenience, and safety of drugs including drug interactions and high-risk group of patients; start the treatment by writing an accurate and complete prescription, for example, the name of drugs with dosage forms and schedule and total duration of the treatment [7–10].
Currently, in the clinical practice of human and veterinary medicine throughout the world, large amounts of antibiotics are used. Equally, many scientists intensively work on the discovery and synthesizing of new drugs with a broader antimicrobial spectrum, stronger action, and a more satisfactory safety profile. Most failures during antimicrobial therapy may occur when the pathogenic microorganism is unknown and a combination of two or more drugs administered empirically. To avoid these mistakes, clinically confirmed, effective antimicrobial combinations should be used [11]. Globally, more than half of all medicines are prescribed, dispensed, or sold improperly, and 50% of the human patients fail to take them correctly. This is more wasteful, expensive, and dangerous, both to the health of the individual animal patient and to the public as a whole that magnifies the problem of misuse of antimicrobial agents [2].
In humans, assessments of drug use patterns with the WHO drug use indicators are becoming increasingly necessary to promote rational drug use. They are now widely accepted as a global standard for problem identification and used in developing countries [12, 13]. In Ethiopia, a survey conducted on human subjects at hospitals located in different regions of the country revealed irrational drug use [14, 15]. However, in veterinary practice, a few published reports on the rational use of veterinary drugs in the country in general, although different studies were conducted by Beyene et al., revealed irrational use of drugs in veterinary clinics [16].
Hence, the present study was designed to evaluate the rational use of veterinary drugs and to compare magnitudes of different drugs commonly used for the treatment of food animal diseases in the Batu and Arsi-Negelle district veterinary clinics in general and to describe current treatment practices and to evaluate the adherence of the prescriber to the national veterinary treatment guidelines.
2. Materials and Methods
2.1. Study Area and Period
The study was conducted from November 2014 to March 2015 at Batu veterinary clinic, located in the East Shoa zone of the Oromia regional state, and Arsi-Negelle veterinary clinic, located in the Western Arsi zone of the Oromia regional state. Batu has a latitude of 7°56′N and a longitude of 38°43′E with an elevation of 1,643 meters above sea level. The average annual temperature in Batu is 19.3°C and 837 mm of precipitation falls annually. Arsi-Negelle is found in the Western Arsi zone of Oromia having a latitude and a longitude of 7°21′N and 38°42′E, respectively, with an altitude of 2,043 meters above sea level and annual rainfall and temperature of 1,300 mm and 21.5°C, respectively [17].
2.2. Study Design
A retrospective and cross-sectional study was designed to assess rational drug use and to compare commonly used drugs for the treatment of animal diseases at Batu and Arsi-Negelle district veterinary clinics based on WHO drug use indicators as described in [1]. The sample was selected using a systematic random sampling method, and the sampling unit was an animal patient encountered at both veterinary clinics for the treatment of acute and/or chronic illness. Secondary data are the source of information. Accordingly, data were collected from the case book records from the office of both clinics by using systematic random sampling in which every third case and tenth case were recorded at Batu and Arsi-Negelle veterinary clinics, respectively.
2.3. Study Population
The study was conducted between November 2014 and March 2015 on food animal patients (cattle, sheep, goats, and chicken of all ages and sex groups) that were admitted to Batu and Arsi-Negelle district open-air veterinary clinics and treated with drugs. All other nonfood animals (e.g., pets and equines) were excluded from the study. A total of 2,464 case data were collected to evaluate the rational use of veterinary drugs both at Batu and Arsi-Negelle veterinary clinics.
2.4. Data Collection
Data were collected in data collection format retrospectively using case registration books at both the clinics, namely, Batu and Arsi-Negelle veterinary clinics. The specific types of data necessary to measure the prescribing indicators were recorded for each animal patient encounter and entered directly into an ordinary prescribing indicator form. For this particular study, 2464 prescriptions that contain the animal’s characteristics (age, sex, breed, body condition, clinical signs, and symptoms observed); disease diagnosis (name, empiric or physical clinical examination, and confirmatory laboratory tests used); prescribed drugs (type, naming (generic or brand), number of drugs prescribed, route of administration, duration of treatment); and prescriber’s signature, level of education, and years of experiences were collected retrospectively from about 16500 prescriptions written for two and half years period from September 2012 to February 2015. Accordingly, the evaluation of the rational use of veterinary drugs was made based on generic prescription and antimicrobials and anthelmintics prescribed for tentatively diagnosed clinical cases.
2.5. Data Analysis
All data in the ordinary prescribed indicator recording form were entered into a Microsoft Excel spreadsheet (version 2010) and imported and analyzed using SPSS (Version 20). Descriptive statistics such as frequencies, percentages, and cross-tabulation were used to describe the characteristics of the drugs. The Chi-square test was used to compare categorical variables where appropriate. All statistical tests were two-sided, and was considered significant.
2.6. Prescribing Indicators
There was no available guideline for prescribing indicators used in veterinary medicine. As a result, the PRESCRIBING indicators were used in this study [18]. The indicators were pretested and slightly modified to match with clinical practice in veterinary medicine so that they could be used easily to provide accurate data. The final versions of the pretested indicators are as follows:(1)The average number of drugs prescribed per encounter was calculated by dividing the total number of different drug products prescribed with the number of encounters surveyed to measure the degree of polypharmacy.(2)The percentage of drugs prescribed by the generic name was calculated by dividing the number of drugs prescribed by the generic name with the total number of drugs prescribed, multiplied by 100 to measure the tendency of prescribing by generic name.(3)The percentage of encounters in which antimicrobials, anthelmintics, and other drugs prescribed were calculated by dividing the number of patient encounters in which the drug was prescribed with the total number of drugs prescribed and multiplied by 100 to measure the overall use of commonly overused (irrationally prescribed) and costly forms of drug therapy.(4)The percentage of drugs prescribed for each disease encountered was calculated by dividing the number of drugs prescribed for each disease for the total number of encounters and multiplied by 100.
3. Results
A total of 2,464 presented cases to clinics were assessed from Batu (1163) and Arsi-Negelle (1301) district veterinary clinics. A retrospective study has shown that 3,811 drugs were prescribed, and the average number of drugs per encounter was 1.6 with a maximum of 3 and a minimum of 1. Among 3,811 prescribed drugs, 1,637 (43.0%) Oxytetracycline, 671 (17.6%) Ivermectin, and 389 (10.2%) Penstrep were most commonly used. Of these drugs, 45.0% and 55.0% of Oxytetracycline, 16.5% and 83.5% of Ivermectin, and 48.1% and 52.9% of Penstrep were prescribed in Batu and Arsi-Negelle, respectively (Table 1).
Commonly prescribed drugs
Total N (%)
Name of clinics
Batu N (%)
Arsi-Negelle N (%)
Total drugs
3811
1199 (31.5%)
2612 (68.5%)
Oxytetracycline
1637 (43.0%)
736 (45.0%)
901 (55.0%)
Ivermectin
671 (17.6%)
111 (16.5%)
560 (83.5%)
Penstrep
389 (10.2%)
187 (48.1%)
202 (52.9%)
Sulfa drug
247 (6.5%)
100 (40.5%)
147 (59.51%)
Albendazole
51 (1.3%)
6 (11.8%)
45 (88.2%)
Others
816 (21.4%)
59 (7.2%)
757 (92.8%)
N = frequency; others = penicillin, tricalbendazole, multivitamin, tetraconazole, copper sulfate, anesthetic agents, diminazene aceturate, intramammary infusion, digestion powder, vitamin K, and calcium borogluconate.
... Intensive administration of anthelminthic agents is not only accompanied with some adverse biochemical consequences for a patient (negative adverse effects) but also leads to appearance and establishment of the biocide-resistant forms in helminth population. This fact was noted by P. Erlich as early as in the beginning of the 20 th century, and resistance to frequently used anthelminthic substances is now registered universally [52][53][54][55][56][57][58][59][60][61][62][63]. ...
... Gastrointestinal parasites (GIP) remain a significant problem in livestock production due their ability to decrease production and productivity by depleting animals from nutrients, red blood cells or full blood [1]. These parasites also cause problem due their capacity to re-infect the host and to resist medication [2,3]. In Cameroon, bovine production is subjected to gastro-intestinal parasitism [4,5]; consequently cattle raised in the country also suffer from the harmful effect of parasitism as well. ...
PurposeThe main objective of this study was to assess the gastrointestinal parasitism in relation with the worm control practices (WCP) in dairy cattle in areas of major importance for dairy/milk production of Cameroon.Methods
Fresh fecal samples were randomly collected from 402 cattle from August to October 2016 in North West Cameroon, and analyze using the McMaster technique. Data on WCP were collected using a questionnaire.ResultsA total of 11 parasites species were identified: Trichostrongylus sp. (5.97%); Oesophagostomum sp. (5.47%); Haemonchus sp. (2.48%); Bonostomum sp. (1.74); Cooperia sp. (1.49%). Toxocara sp (0.24%); Ostertagia sp. (0.50%); Nematodirus sp. (0.74%); Trichuris sp. (0.50%); Moniezia sp. (0.50%); Eimeria sp. (0.50%). The mean individual parasite load for helminthes and protozoa ranged from 100 to 400 eggs per gram of feces (epg) and 333–400 oocysts per gram of feces (opg), respectively. Most farmers (95.12%) used conventional drugs (Albendazole, Doramectin, Fenbendazole, Ivermectin.) to deworm animals as compared with traditional phytotherapy (e.g., Carica papaya leaves) (4.88%). The mean epg/opg in animals treated with conventional drugs was significantly higher (p < 0.05) than in those receiving traditional treatment. Animals treated less than four times a year with conventional drugs had the highest (p < 0.05) mean epg/opg compared with animals treated four to six times a year.Conclusion
This study suggests that treating at least four times a year with conventional drugs, and at least two times a year with traditional approaches could help reducing GIP burden in dairy cattle in North West Cameroon. Since the majority of farmers use conventional drugs, it is imperative for them to appropriately use these conventional drugs for a better control of GIP on their farms.
... In the absence of effective vaccines and optimal pasture management systems, parasite control relies exclusively on anthelmintic treatment. To date, this approach has remained viable for remediating infections of O. ostertagi; however, resistance of O. ostertagi to macrocyclic lactones is on the rise in the United States (8)(9)(10) and in other cattle-producing nations worldwide (11)(12)(13)(14). Further, strong resistance in the small-ruminant parasite Teladorsagia circumcincta (15), a close relative of O. ostertagi, foretells future resistance in Ostertagia and justifies the need for alternative control strategies. ...
Ostertagia ostertagi is an abomasal parasite with significant economic impact on the cattle industry. Early host immune responses are poorly understood. Herein, we examined time course expression of Toll like receptors (TLRs) in peripheral blood mononuclear cells (PBMC) during infection where PBMC macrophages (MΦ) generated both pro- and anti-inflammatory responses when incubated with excretory secretory products (ESP) from fourth stage larvae (OoESP-L4) or adult worms (OoESP-Ad). First, changes in cell morphology clearly showed that both OoESP-L4 and OoESP-Ad activated PBMC-MΦ in vitro resulting in suppressed CD40 and increased CD80 expression. Expression of mRNAs for TLRs 1, 4, 5 and 7 peaked 7 days post infection (dpi) (early L4), decreased by 19 dpi (post emergent L4 and adult), then increased at 27 dpi (late adults). The pro-inflammatory cytokine TNF-α (transcript and protein) increased in the presence of OoESP-Ad, and the anti-inflammatory cytokine IL-10 (protein) decreased in the presence of OoESP-L4 or OoESP-Ad; however, IL-10 mRNA was up-regulated, and IL-6 (protein) was down-regulated by OoESP-L4. When PBMC-MΦ were treated with ligands for TLR4 or TLR5 in combination with OoESP-Ad, the transcripts for TNF-α, IL-1, IL-6 and IL-10 were significantly down-regulated relative to treatment with TLR4 and TLR5 ligands only. However, the effects of TLR2 ligand and OoESP-Ad were additive but only at the lower concentration. We propose that O. ostertagi L4 and adult worms utilize competing strategies via TLRs and MΦ to confuse the immune system which allows the worm to evade the host innate responses.
... Cases of resistance in cattle parasites have been reported in South and North America (Mejía et al., 2003;Anziani et al., 2004;Suarez and Cristel, 2007;Edmonds et al., 2010;Ramos et al., 2016;Avramenko et al., 2020), Europe (Demeler et al., 2009;Bartley et al., 2012) and Oceania (Loveridge et al., 2003;Waghorn et al., 2006;Lyndal-Murphy et al., 2010). Commonly the first reports of resistance have involved the macrocyclic lactone (ML) class of anthelmintic, generally in Cooperia species although reports of resistance in other genera have occurred (McKenna, 1991;Soutello et al., 2007;Gasbarre et al., 2009;Alonso-Díaz et al., 2015). Recently, reports of ML-resistant Ostertagia ostertagi, have been made in the US (Edmonds et al., 2010), New Zealand (Waghorn et al., 2016) and Argentina (Meija et al., 2003) but reports of benzimidazole (BZ) resistance are less common (Rendell., 2010;Cotter et al., 2015;Kelleher et al., 2020). ...
The prevalence of anthelmintic resistance in the bovine nematode Cooperia oncophora has been well documented globally but lack of efficacy against the more pathogenic nematode species Ostertagia ostertagi is less common. The sensitivity of an O. ostertagi isolate to the benzimidazole class of anthelmintic was investigated using classical parasitological techniques following apparent clinical failure of controlled release fenbendazole capsule administration in first season grazers at pasture. A controlled efficacy test (CET) was conducted in conjunction with sequencing of the β-tubulin isotype 1 gene of larvae pre- and post-fenbendazole administration. Twelve helminth-naïve calves were infected experimentally with 20,000 third stage larvae; six received oral fenbendazole (7.5 mg/kg bodyweight) 28 days post infection. Total abomasal nematode burdens were compared between treatment and control groups to determine efficacy. Fenbendazole resistance in O. ostertagi was confirmed with a total treatment failure in reducing worm burden: efficacy of 0%. Sequence analysis of the β-tubulin isotype-1 gene from forty-five infective larvae from both control and treated groups was performed. The three commonest single nucleotide polymorphisms (SNPs) associated with benzimidazole resistance, namely F167Y, E198A and F200Y, were examined. The predominant resistance-associated SNPs were F200Y (78 % control and 79 % treated groups) and F167Y (remaining genotypes) and emphasises the importance of these SNPs in clinical disease in this isolate. The development of diagnostic molecular tools based on a characterised field-derived isolate of benzimidazole-resistant Ostertagia will enable future prevalence surveys to be undertaken to assess the possible risk posed by resistance in this economically important species.
... This is partially due to the widespread use of veterinary drugs, macrocyclic lactones what resulted in reduced drug effectiveness (Stromberg et al. 2012). The trichostrongylid roundworms including Cooperia spp., have acquired a multi-species anthelmintic resistance what was, for instance, experimentally demonstrated on cattle in the western parts of the United States (Gasbarre et al. 2009;Edmonds et al. 2010). Nematodes of the genus Cooperia are monoxenous parasites with a direct life cycle where pre-parasitic larval phase is completely free-living. ...
This review updates the current knowledge on the taxonomy of intestinal nematodes of the genus Cooperia parasitizing in wild and domestic ruminants. The emphasis is put on revision of 19 valid species belonging to the genus. This analysis focuses on main features of the genus Cooperia, including its geographic occurrence and the life cycle details. The most widespread congeners are Cooperia curticei, C. oncophora, C. pectinata, and C. punctata, having nearly worldwide distribution. The fifth species, referred by electronic databases from the European territory as Cooperia asamati Spiridonov, 1985, is unveiled here originally as nomen nudum.
... A study conducted on 16 farms in Brazil established that the prevalence of sheep nematodes resistant to oxfendazole, levamisole and ivermectin was 88%, 41% and 59%, respectively [7]. Similarly, widespread resistance has been reported in Africa [8], Europe [9], US [10] and Asia [11]. These challenges have led to development of new drugs with different modes of action. ...
The objective of this study was to evaluate in vitro ovicidal, larvicidal and adult mortality activity of bromelain encapsulated in chitosan nanocarriers against H. contortus. Bromelain was isolated from peels of ripe pineapple from Kiambu County, Kenya. Isolation of bromelain was conducted with several stages of fractionations with ammonia sulphate salt and dialysis. Encapsulation of bromelain was done by use of methyl cellulose-chitosan in order to control release and activity. The encapsulated chitosan nanocarriers were then subjected to in vitro ovicidal, larvicidal and adult mortality activity according to standard procedures. The results of the assays showed that encapsulated bromelain had an IC50 of 0.249 mg/ml, 0.251 mg/ml and 0.140 mg/ml on the egg hatch, larval and adult worm mortality assays, respectively. All these values showed better activity than bromelain although there was no significant difference (p˃0.05) between activities of encapsulated bromelain and bromelain. There was also a significant difference (p<0.05), between Albendazole and the rest of the test drugs. In conclusion, this study has shown that encapsulated bromelain has anthelmintic activity on different developmental stages of H. contortus parasite and that it should be further investigated and developed as a novel anthelmintic drug for control of H. contortus and hence improve production of small ruminants.
... Extrinsic factors include weather condition, amount of forage present, quality of forage, host density and development of (AR), which is one of the major causes of failure of worm control program (Body et al., 2011). Intrinsic factors include, gender, age, physiological condition, nutritional status, genetic differences as well as immune status of the animal (Waghorn et al., 2006;Marquez et al., 2008;Gasbarre et al., 2009). Extensive use of same dewormer in field or at farm level results in failure of anthelmintics and development of resilient/resistant parasites as the frequency of these dewormers is 6-9 times/year practiced in the field (Webb and Ottaway, 1986;Love et al., 1992;Bygarski et al., 2014). ...
Anthelmintic resistance (AR) is the major constraint towards controlling parasitism of livestock. This study was executed to evaluate relative efficacy of oral formulation consisting of ivermectin (IVM) and levamisole (LEV) towards Haemonchus contortus under in-vitro condition. The worms were isolated from abomasa (n=384), collected from nearby slaughter house. The egg hatch test (EHT), adult motility test (AMT), and larval development test (LDT) were performed for estimation of lethal concentration (Lc) 90. A typical sigmoid dose response was converted to linear function by using Probit transformations. Different concentrations of LEV (0.172, 0.086, 0.043, 0.021, 0.010, 0.005 μl/mL), and IVM (0.002, 0.001, 0.0005, 0.00025, 0.000125, 0.0000625 μl/mL) were incubated with 100 eggs / concentration. The LC 90 values of LEV and IVM were found higher than values suggested by World Association for the Advancement of Veterinary Parasitology (WAAVP), which is (0.1µg/ml). The dose-dependency stipulates development of (AR) anthelmintic towards H. contortus.
... There are sluggish progresses in development of resistance in large ruminants as compared to the small ruminants, where it is very rapid. But now reports from the different part of world show that anthelmintic resistance in cattle parasites is emerging increasingly (Gasbarre et al., 2009a;Gasbarre et al., 2009b;Sutherland and Leathwick, 2011) and indicate a significant challenge to the cattle industry. However the knowledge of genetics and mechanism of drug resistance development is now succeeding but till there are much more facts that remain poorly understood (Beech et al., 2011). ...
... Different studies by Pinheiro [27], Amarante et al. [4], Jacquiet et al. [19], Achi et al. [1], Gasbarre et al., [16,17], and Brasil et al. [6] demonstrated the occurrence of crossed infections of H. placei and H.contortus in sheep, goats, cattle and buffalo. Mixed grazing strategy with different species of ruminants is an alternative option for decontamination of pastures assisting the anthelmintic control; however, the strategy of shared grazing areas possibly may favor crossed infections as observed in our study [8,25]. ...
Background
Reports of a lack of efficacy of most of the anthelmintic compounds for ruminants associated with the long-time necessity for creating new molecules have stressed the urgency to adopt alternative methods to control gastrointestinal parasites infection, such as strategies of sharing grazing areas. Therefore, this study aimed to evaluate nematode populations affecting cattle and sheep that share grazing areas before and after treatment with different anthelmintic compounds, and investigate the efficacy of anthelmintic treatment in these naturally infected ruminants at farms in the state of Rio Grande do Sul, Brazil.
Methods
The presence of co-infections by Haemonchus species was investigated by polymerase chain reaction (PCR) for groups treated with a benzimidazole. Farms were selected by: farmers’ consent, presence of 42–60 (or more) calves and sheep per farm with counts of ≥ 200 eggs per gram of feces (EPG), availability of calves and lambs aging from 6 to 9 months, absence of anthelmintic treatment for both species for 60 days before the experimental period, and shared grazing areas between this species on each farm. Animals were distributed into six treatment groups for each ruminant species per farm and treated with: ivermectin, doramectin, moxidectin, levamisole, albendazole, and closantel.
Results
Levamisol was the most effective anthelmintic compound for both ruminant species. In general, Cooperia spp., Haemonchus spp., and Trichostrongylus spp. were the genus present after tested treatments that were ineffective. PCR showed the presence of Haemonchus species co-infections between cattle and sheep.
Conclusion
Therefore, this study demonstrated the similarity between nematode population, the presence of multi-resistant nematodes, and the presence of Haemonchus species co-infections affecting different ruminant species that share pastures.
... On the other hand, cattle parasite resistance has been documented but its prevalence has yet to be determined; making it an emerging resistance (Kaplan 2004). Even the American cattle production industry showed little concern in regards to the effect of cattle parasite resistance on their industry (Gasbarre et al. 2009). However, through the use of multiple classes of drugs, multi-drug resistant strains of nematodes are slowly emerging (Kaplan 2004;Chaudhry, Miller, et al. 2014b;Prichard 2001). ...
Anthelmintic resistance (AR) is a major problem in the profitable production of livestock. Therefore, this study evaluated AR status in cattle farms at Mymensingh Sadar using in vivo, fecal egg count reduction test (FECRT) and in vitro, egg hatch assay (EHA) techniques. For this, ten cattle farms and forty animals from individual farms with more than 200 eggs per gram (EPG) of feces were selected by employing the McMaster technique. For FECRT, four groups having ten animals in each group were designed and animals of group I were treated with albendazole (ABZ), group II with levamisole (LEV), group III with ivermectin (IVM) according to the bodyweight and group IV was served as control (untreated). Fecal samples were collected at day 0 (pre-treatment) and day 14 of post-treatment (p. t) from animals of all treated and untreated groups directly from the rectum to calculate EPG and subsequently considered for copro-culture to detect resistant parasitic larvae. For EHA, following the collection of pooled fecal samples from ten farms, eggs were isolated and incubated with different concentrations of albendazole such as 0.05, 0.1, 0.2, 0.3 and 0.5 µg/ml. In FECRT, the result revealed that all three drugs such as ABZ, LEV and IVM were resistant in all farms except one where IVM was suspected resistance (SR). The identified resistant larvae from copro-culture were Haemonchus, Trichostrongylus and Oesophagostomum. In EHA, the EC50 value of ABZ ranged from 0.14 to 0.29 µg ABZ/ml (> 0.1 µg/ml designated as resistance) with the coefficient of correlation (R2) > 0.97 confirming ABZ resistance in all cattle farms. The present study suggests that AR is increasing and creates an alarming condition in controlling GI nematodes in Bangladesh.
We describe a new fixed-dose combination injectable (FDCI) formulated with doramectin and levamisole hydrochloride (HCl) to target broad and overlapping spectra of gastrointestinal nematodes (GINs) through two distinct modes of action. Here, we demonstrate the superior efficacy of the FDCI against mixed populations of cattle GINs in two dose confirmation studies conducted in Australia using artificially induced adult (Study 1) and immature (Study 2) GIN infections. Artificial infections consisted of Cooperia spp., Haemonchus placei, Ostertagia ostertagi, and Trichostrongylus axei. In both studies, cattle were inoculated with third-stage larvae and infections were confirmed by fecal egg count (FEC). Treatment groups in both studies were as follows: (1) negative control (saline, 0.9% sodium chloride), (2) positive control injectable endectocide (Study 1-0.2 mg/kg ivermectin; Study 2-0.2 mg/kg doramectin), (3) positive control injectable anthelmintic (7.5 mg/kg levamisole HCl), and (4) FDCI (0.2 mg/kg doramectin + 6.0 mg/kg levamisole HCl). Cattle were treated either 28 days (Study 1) or 6 days (Study 2) post-infection. On Days 14-16 (Study 1) or Days 20-21 (Study 2) post-treatment, cattle were euthanized and necropsied for the recovery, identification, and enumeration of worms. Treatment efficacy was calculated as reduction in worm burdens of treated cattle compared to saline-treated cattle, and treatments were considered effective if the geometric mean worm burden in the treatment group was reduced by ≥ 95% compared to the negative control group. In both studies, saline-treated cattle remained positive for GIN infections for the study duration. Ivermectin was less than 95% effective against Cooperia spp. (80.2%) and H. placei (24.8%) in Study 1, and levamisole HCl was less than 95% effective against Ostertagia spp. (47.1%) in Study 2. In contrast, the novel FDCI was 100% effective in treating adult and immature life stages of all cattle GINs included in the artificial infections, with no worms recovered at necropsy from doramectin + levamisole HCl-treated cattle. These data show a single administration of the FDCI provides broad-spectrum treatment of economically important cattle GINs.
Intensive farming practices and heavy reliance on anthelmintics have contributed significantly to the problem of macrocyclic lactone (ML) resistance in New Zealand. Farmers now have few options for effectively controlling cattle gastrointestinal nematodes (GINs) and regularly experience sub-optimal efficacy against economically important species. We present a novel fixed-dose combination injectable (FDCI) that simultaneously delivers 0.2 mg/kg doramectin and 6 mg/kg levamisole hydrochloride (HCl) to target a broad spectrum of cattle GINs in a single dose, providing an additional solution to endoparasite control in an environment of anthelmintic resistance. A dose confirmation study was conducted using naturally acquired infections of GINs in beef cattle in New Zealand. Cattle with GIN infections confirmed by fecal egg count (FEC) were randomly allocated (n = 12 per group) to the control (saline-treated), FDCI-treated or doramectin-treated group. On Day 0, cattle were weighed and administered a single subcutaneous injection of saline or endectocide. Rectal fecal samples were collected from each animal on Day 7 for individual duplicate fecal egg count (FEC) analysis, and coprocultures were conducted on pooled fecal samples within each treatment group. All animals were euthanized and necropsied for worm recovery on Days 14 through 16. Treatment efficacy was calculated based on reduction in FECs and worm burdens. All enrolled cattle were positive for GINs based on Day -5 FECs, with geometric mean (GM) FECs ranging from 337 to 521 eggs per gram (EPG). All saline-treated cattle remained positive for GIN infections for the study duration (Day 7 GM FEC = 427 EPG). Necropsy and worm recoveries revealed the presence of doramectin-resistant Cooperia oncophora, C. surnabada and Trichostrongylus longispicularis, as evidenced by ≤ 72.3 % efficacy of doramectin against these species. The new FDCI was ≥ 99.8 % effective against all GIN species, including ML-resistant C. oncophora, C. surnabada and T. longispicularis, providing broad-spectrum efficacy and eliminating economically important cattle GINs, including ML-resistant populations.
Reports of macrocyclic lactone (ML) loss of efficacy suggest ML resistance in gastrointestinal nematodes (GINs) is a growing problem in the US cattle industry. Empirical and modeling data support combining an ML and second anthelmintic from a different drug class to help ML resistance development while effectively treating existing resistant parasite populations. Here, we present a novel fixed-dose combination injectable (FDCI) solution for cattle that delivers 0.2 mg of doramectin and 6.0 mg of levamisole hydrochloride (HCl) per kg of body weight. Field studies were conducted at six sites across the Midwest United States to investigate the efficacy of a single administration of the FDCI in treating common cattle GINs. Cattle (n = 425) with GIN infections confirmed by fecal egg count (FEC) on Day -10( ± 2) were randomly allocated to the control (saline) or treatment (FDCI) group. On Day 0, pre-treatment fecal samples were collected, and cattle were administered a single subcutaneous injection of saline (n = 106) or FDCI (n = 319). Post-treatment fecal samples were collected on Day 14. Fecal egg count reduction tests (FECRTs) were conducted using Day 0 and Day 14 FECs. Efficacy was evaluated using Day 14 FECs (FDCI-treated versus saline-treated). Within treatment, samples collected on Days 0 and 14 with ≥ 20 eggs per gram (EPG) were cultured for nematode larvae recovery and identification. Day -10 FECs for enrolled animals were similar between treatment groups. Coprocultures from cattle with FEC ≥ 20 EPG (n = 68 saline; n = 211, FDCI) on Day 0 showed the presence of Cooperia punctata, Ostertagia spp., Haemonchus spp., C. oncophora, Oesophagostomum spp. and Trichostrongylus spp. Day 14 FECs for FDCI-treated cattle were significantly reduced (0-3 EPG) compared to saline-treated cattle (0-1252 EPG) (p ≤ 0.0042). At all study sites, the efficacy of the new FDCI was ≥ 99.4% and the FECR was 0.99 or 1.00. Day 14 coprocultures from control cattle showed infections of common GIN genera, confirming the efficacy of the FDCI against GINs in the field. A single administration of the doramectin + levamisole HCl combination injectable effectively treats common and economically important cattle GINs.
Many factors influence the spectrum and magnitude of helminth populations in stocker cattle. Calves are placed into stocker operations during all seasons, from all regions of the country, and with a broad range of prior parasite exposure and parasiticide treatment. This makes it unlikely that a generalized or generic parasite control program will be effective for all animals at receiving. Follow-up treatment recommendations are equally problematic, contingent upon the success of the treatment protocol utilized when cattle arrived at the stocker operation, residual activity of the anthelmintic(s) used at arrival, parasite challenge during the stocker phase, general animal health, and producer expectations. At the farm or ranch level, the more troublesome and conflicted considerations regarding parasite control are often ignored, and treatments are based on what appears to have worked in the past or the current cost of treatment options. This paper is not intended to make detailed recommendations about worm control, but is instead a discussion of factors at play in stocker cattle, including the species of the parasites, biology of the parasites, parasiticides, and the interaction and effect of these factors on the health and productivity of stocker cattle.
The rational use of drugs in veterinary medicine has various significances, such as reducing the risk of drug resistance, increasing efficacy, reducing drug residue, and decreasing adverse drug reactions. The objectiveof this study is to evaluate types of rational use of veterinary drugs prescribed by veterinarians in the veterinary clinics of the Masha district. A sample was selected using a systematic random sampling method and the sampling unit was an animal patient encountered at Ateso veterinary clinic for the treatment of acute and/or chronic illness. A retrospective study was conducted to assess veterinary drug prescribing practices at Ateso woreda veterinary clinics in the south west areas of Ethiopia. A total of 920cases were recorded from the case registration books at the Ateso Veterinary clinic for diseases treated between January 2021 and February 2022. The study indicates thatin Atesoveterinary clinic, 111(12.1%) young,548(59.6%) adult and 261(28.4%) wereold.In this retrospective study, 654(71.1%) cattle, 62(6.7%) chicken, 66(7.2%) goat and 138(15.0%) were sheep in diagnosed animals. Regarding the agro-ecological partition in studyarea, 542(58.9%), 129(14.0%) and 249(27.1%) of diagnosed animals were highland, lowland and midland respectively.Thestudy resultsshowed that for a total of 920 cases diagnosed at clinic, 1788different drugs were prescribed, with an average per encounter of 1.9.Among the total drugs,Penstrep(31.7%), Albendazole (23.3%),Oxytetracycline(19.4%),Ivermectine(12.3%,Sulfa drugs (6.7%),Isomitamidium chloride (3.7%) and Veridium(2.9%) were the most leading prescribed drugs. All drugs were prescribed by the generic name without any laboratory support of the disease. The prescribing practices showed 51.1% of antibiotics and 23.3%of anthelmintic was prescribed for veterinary diseases treatment at Ateso veterinary clinic. Of the prescribed drugs, 7 % Anthelmentics (Albendazole) was prescribed irrationally to treat diseases that were tentatively diagnosed as infectious diseases. Similarly, 2.1 % Antibiotics were prescribed for parasitic disease. In conclusion, this study revealed problems in antibiotics andAnthelmintics use, description of routes of administration and length of treatment, and shortage of laboratory diagnostic facilities. Therefore, veterinary drugs particularly Antibiotics and Anthelmintics should be used appropriately to safeguard the public from residual drug impacts and resistance development.
In an effort to generate data for regulatory purposes on the therapeutic efficacy of eprinomectin 5% w/v extended-release injection (Eprinomectin ERI) (LongRange®, Boehringer Ingelheim) against infections of immature and adult stages of some nematode species (or stages) which are generally less common or predominantly seen in younger cattle, nine studies (minimum two per parasite and stage) were conducted in the USA and Germany. A total of 218 young cattle were included in seven experimentally induced infection studies (180 animals) and two studies with naturally acquired nematode infections (38 animals), which were compliant with WAAVP and VICH guidelines. In each study, cattle were randomly assigned into groups which received 1 mL per 50 kg body weight of either saline (controls) or Eprinomectin ERI (equivalent to 1 mg eprinomectin per kg body weight) via subcutaneous injection when the parasites were developing fourth-stage larval (L4) or adult nematodes. Following necropsy and parasite recovery, percentage efficacy was calculated based on the comparison of geometric mean nematode counts of the Eprinomectin ERI- vs. the saline-treated animals. Eprinomectin ERI-treated cattle had significantly (p < 0.05) lower counts of each species and stage of nematodes than the controls. Eprinomectin ERI treatment was demonstrated to be efficacious (> 90%) against L4 and adult Bunostomum phlebotomum and Nematodirus helvetianus; against L4 Haemonchus placei, Oesophagostomum radiatum, and Trichostrongylus colubriformis; and against adult H. contortus. Percentage efficacy against L4 H. contortus was variable (69.6 to 100%). All treatments were well accepted, and no treatment-related health problems were observed in any study.
The objective of this controlled study was to determine the anthelmintic efficacy of eprinomectin 5% w/v extended-release injection (Eprinomectin ERI; LONGRANGE®, Boehringer Ingelheim Animal Health) against primarily ovine-adapted gastrointestinal strongylid nematode (GIN) parasites in naturally infected young cattle. Eighteen calves which grazed on a sheep-dominated mixed sheep-cattle farm were randomly allocated into two equal groups (saline [control] or Eprinomectin ERI, administered each at 1 mL/50 kg body weight once subcutaneously), treated and euthanized 14 days thereafter for a differential GIN count. Ten species of strongylid nematodes were recovered from the control calves (ovine-adapted Haemonchus contortus, Teladorsagia circumcincta, Trichostrongylus colubriformis, Cooperia curticei, Nematodirus battus, Chabertia ovina; bovine-adapted Ostertagia ostertagi, Cooperia oncophora, Nematodirus helvetianus; 'generalist' Trichostrongylus axei). Adult GIN counts ranged from 1,540 to 5,244 for the control calves and from zero to 110 for the Eprinomectin ERI-treated calves. Accepting the International Cooperation on Harmonisation of Technical Requirements for Registration of Veterinary Medicinal Products anthelmintic guidelines criteria on adequacy of infections to be demonstrated in the control animals, this study showed that Ch. ovina, C. curticei, H. contortus, N. battus, T. axei, and T. colubriformis were reduced significantly (p < 0.0001) by ≥ 98.7% in the animals treated with Eprinomectin ERI. In conclusion, Eprinomectin ERI treatment was efficacious against a range of ovine-adapted nematode parasites in naturally infected young cattle.
The efficacy of the anthelmintic albendazole (ALB), doramectin (DOR) and ivermectin (IVM) were evaluated in Holstein and Holstein crossbreed dairy heifers using the fecal egg count reduction test (FECRT). Dairy heifers (n=420; ~6 months of age; BW = 149 ± 39.6 kg) were evaluated in 21 dairy farms. All heifers were required to be on pasture and not have been exposed to anthelmintic treatment for a minimum of 3 months. At each dairy farm, a priori, groups of at least 18 heifers were randomly divided to be treated with IVM, or DOR, or ALB following manufacturer's instructions. Fecal samples were collected directly from the rectum 7 days before anthelmintic treatment (d-7), at the time of the treatment (d0), and 14 days after treatment (d14). Only heifers that had an average FEC ³ 100 eggs per gram of feces (average of FEC from day d-7 and d0) were considered in the FECRT. The FECRT was determined by the modified McMaster technique. Of the three-anthelmintic used, ALB (n=142) proved to be the most effective (P < 0.0005) with an efficacy of 67.47% ± 8.43. The efficacy of DOR and IVM did not differ (P = 0.8713). While DOR (n = 130) exhibited a efficacy of 25.50% ± 18.00, IVM (n = 148) exhibited a efficacy of -8.13% ± 19.89 due to an increase in FEC after treatment. Dairy farmers should implement integrated methods of nematode control to preserve the effectiveness of currently available anthelmintics.
Background
The species composition of cattle gastrointestinal nematode (GIN) communities can vary greatly between regions. Despite this, there is remarkably little large-scale surveillance data for cattle GIN species which is due, at least in part, to a lack of scalable diagnostic tools. This lack of regional GIN species-level data represents a major knowledge gap for evidence-based parasite management and assessing the status and impact of factors such as climate change and anthelmintic drug resistance.
Methods
This paper presents a large-scale survey of GIN in beef herds across western Canada using ITS-2 rDNA nemabiome metabarcoding. Individual fecal samples were collected from 6–20 randomly selected heifers (n = 1665) from each of 85 herds between September 2016 and February 2017 and 10–25 first season calves (n = 824) from each of 42 herds between November 2016 and February 2017.
Results
Gastrointestinal nematode communities in heifers and calves were similar in Alberta and Saskatchewan, with Ostertagia ostertagi and Cooperia oncophora being the predominant GIN species in all herds consistent with previous studies. However, in Manitoba, Cooperia punctata was the most predominant species overall and the most abundant GIN species in calves from 4/8 beef herds.
Conclusions
This study revealed a marked regional heterogenicity of GIN species in grazing beef herds in western Canada. The predominance of C. punctata in Manitoba is unexpected as although this parasite is often the most predominant cattle GIN species in more southerly latitudes, it is generally only a minor component of cattle GIN communities in northern temperate regions. We hypothesize that the unexpected predominance of C. punctata at such a northerly latitude represents a range expansion, likely associated with changes in climate, anthelmintic use, management, and/or animal movement. Whatever the cause, these results are of practical concern since C. punctata is more pathogenic than C. oncophora, the Cooperia species that typically predominates in cooler temperate regions. Finally, this study illustrates the value of ITS-2 rDNA nemabiome metabarcoding as a surveillance tool for ruminant GIN parasites.
Fecal samples were collected from cows (n = 1458), calves (n = 1188), and replacement heifers (n = 921) between 2012 and 2014 from 199 herds and generalized estimating equations were used to predict mean fecal egg counts and prevalence of egg-positive samples. Replacement heifers had the highest prevalence of Trichostrongylid-type eggs at 83% [95% confidence interval (CI): 78% to 87%], and cows had the lowest at 75% (95% C: 70% to 81%). Nematodirus spp. was most frequently present in calves [predicted prevalence: 34% (95% CI: 28% to 40%)]. Mean fecal egg counts were highest in calves with 5.9 (95% CI: 3.9 to 7.8) Trichostrongylid-type eggs per gram (EPG) of feces and 1.0 (95% CI: 0.7 to 1.4) Nematodirus spp. EPG. Although mean egg counts were low to moderate, the high prevalence highlights the need to further investigate the epidemiology of gastrointestinal nematodes in western Canada. This is particularly relevant considering management changes, increasing herd sizes, climate change, and threatening anthelmintic resistance.
The study investigated the presence of resistance to benzimidazoles in Haemonchus contortus helminths from ruminant species in Greece through the detection of the Phe/Tyr polymorphism in the amino acid at position 200 of the β-tubulin protein. In total, 288 adult female H. contortus helminths collected from the abomasum of various ruminant animals in Greece were tested. Of these, 96 were collected from sheep, 96 from goats, 48 from cattle, and 48 from buffaloes. The frequencies of the homozygous and heterozygous resistant genotypes at the position 200 of the β-tubulin gene of helminths recovered from sheep were 96.9% and 3.1%, respectively. The frequencies of the homozygous and heterozygous resistant genotypes, respectively, were 100.0% and 0.0% in helminths from goats, 25.0% and 75.0% in helminths from cattle and 8.3% and 91.7% in helminths from buffaloes. In all parasitic populations, no homozygous susceptible genotypes were detected. The present study highlighted, for the first time, the emergence of benzimidazole-resistant H. contortus in goats, cattle, and buffaloes in Greece, using an allele-specific PCR. It is postulated that benzimidazole-resistant alleles were transferred from sheep or goats to cattle and buffaloes at the commonly grazing pastures in Greece.
There is a paucity of information from western Canadian beef cow-calf producers about how they control gastrointestinal nematodes. The objectives of this study were to describe cow-calf producers' management practices related to control of gastrointestinal nematodes including pasture management and use of parasite control products. A questionnaire was distributed to 105 producers in May 2015. Responses from 97 producers revealed the almost uniform dependence on the use of a pour-on macrocyclic lactone parasite control product in the fall as part of a routine farm management program. Control of external parasites was the primary reason for treatment, while none of the producers chose to treat specifically to manage internal parasites. The predominant management practices identified through this study increase the risk of development of anthelmintic resistance. The results also highlight the need to raise awareness of the importance of an evidence-based gastrointestinal nematode control program in beef cow-calf herds.
Copyright and/or publishing rights held by the Canadian Veterinary Medical Association.
Parasite species infecting cattle throughout northern North American are generally the same as those found throughout North America. Throughout Canada, cattle are primarily infected with Ostertagia ostertagi and Cooperia oncophora, whose larvae survive cold winters within soil of pastures. Overwintering larvae of these species maintain a temporary population of refugia available in spring to grazing cattle. Cattle from northern United States are also infected with Cooperia punctata and Haemonchus placei, whose larvae cannot survive cold winters within pastures. Anthelmintics with persistent activity are used during spring to recover some of these losses; however, anthelmintic resistance limits effectiveness of this strategy.
To determine the prevalence, mean fecal egg count intensities, and predominant gastrointestinal nematode species, fresh environmental fecal samples were collected from 30 grazing heifers at monthly intervals (June, July, and August) on 6 Saskatchewan dairy farms in 2016. The population average strongylid prevalence ranged from 67.2% [95% confidence interval (CI): 49.5% to 84.9%] in June to 88.3% (95% CI: 76.7% to 100.0%) in August (P = 0.05) while the mean fecal egg count ranged from 1.7 in June to 9.3 eggs/g of feces in August (P < 0.003). The predominant nematode species were identified using a deep-sequencing nemabiome assay targeting the internal transcribed spacer rDNA genomic locus of both L1 and L3-stage larvae. Cooperia oncophora and Ostertagia ostertagi were predominant on all farms, accounting for > 85% of the species. The results provide important previously unavailable data on the epidemiology of gastrointestinal nematodes (GIN) in fecal samples from these grazing heifers in Saskatchewan.
Copyright and/or publishing rights held by the Canadian Veterinary Medical Association.
The six species of Nematodirus parasitic in domestic ruminants of North America have been identified previously on the basis of characteristics of the bursa and tips of the spicules, and females could not be identified. In an effort to find additional diagnostic characteristics of both sexes, cuticular ridges were studied with light and scanning electron microscopy and in whole mounts and cross sections. After the cuticular ridges of males were characterized, females were matched with males by means of cuticular ridges, except for the rare species N. davtiani. Five of the six species have variations of an 18-ridge bilaterally symmetrical system in the cervical region. The sixth species has 26 cervical ridges. Two groups of species were recognized on the basis of cuticular characteristics correlated with other morphological characters. The two species in Group I, Nematodirus filicollis and N. dalviani, lose ridges laterally in the postcervical region and have 14 ridges at midbody. They can be identified by their anteriorly extended pattern of ridges in the cervical region. These two species also share the characteristics of finlike ridges, a small number (30-35) of perioral denticles, a short cephalic expansion, and a large bursa without a separate dorsal lobe. Nematodirus davtiani can be distinguished from N. filicollis by its prominent dorsalmost and ventralmost ridges and its distinctive dorsal ray. In contrast, the four species of Group II, N. helvetianus, N. oiratianus interruptus ssp. n., N. abnormalis, and N. spathiger, share the characteristics of a more posteriorly distributed pattern of ridges in the cervical region, 18 or more ridges near midbody, smaller dorsal and ventral ridges, a larger number (50-65) of perioral denticles, a longer cephalic expansion, and a smaller bursa with separate dorsal lobes. Nematodirus helvetianus and N. oiratianus interruptus add ridges in the cervical and postcervical regions, and are characterized by having more than 18 ridges for most of their length; they do not add ventral ridges in the last quarter of the males. Nematodirus helvetianus has more ridges (30-36 at midbody) than any of the other species. Nematodirus oiratianus interruptus can be easily separated from all other species by its discontinuous ridges in the cervical region. Nematodirus oiratianus oiratianus from Asia and South America have continuous ridges. Nematodirus spathiger and S. abnormalis have 18 ridges for most of their length; they lose all dorsal ridges and add a few ventral ridges in the last quarter of the males. Nematodirus abnormalis can be distinguished from N. spalhiger by the cervical discontinuities in ridges numbered 2 and 8, by spicular and bursal characteristics, and a more anterior vulva position. Possible evolutionary relationships among the six species are described in a cladogram and a key to species.
Trichostrongyloid nematodes are usually identifed by characteristics of the males. In an effort to find additional diagnostic characteristics of both sexes of Nematodirella of North American ruminants, cuticular ridges were studied. Four distinct cuticular morphotypes were found among specimens from North American ruminants. The four cuticular morphotypes represent three species previously reported in North America and a fourth Asian species not previously reported in North America. One species has numerous ridges that are discontinuous in a regular pattern: N. antilocaprae, parasitic in the pronghorn antelope, Antilocaprae americana, is believed to be confined to North America. Two species have numerous continuous ridges and are parasites of Holarctic cervids, namely, N. longissimespiculata with 44–52 cervical ridges, parasitic in the reindeer, Rangifer tarandus, and N. alcidis with 28–34 cervical ridges, parasitic in the moose, Alces alces. The fourth species, N. gazelli, has 14 cervical ridges, and is parasitic in Holarctic bovids including Ovis aries. A fifth species, not known to occur in North America, was also studied — N. dromedarii with 22 cervical ridges is parasitic in the camel, Camelus dromedarius. The cuticular characteristics are correlated with other characteristics in a key to species and the evolution of the species of Nematodirella is discussed. Numerous redeterminations are made of specimens from earlier reports. ac]19821013
Methods have been described to assist in the detection of anthelmintic resistance in strongylid nematodes of ruminants, horses and pigs. Two tests are recommended, an in vivo test, the faecal egg count reduction test for use in infected animals, and an in vitro test, the egg hatch test for detection of benzimidazole resistance in nematodes that hatch shortly after embryonation. Anaerobic storage for submission of faecal samples from the field for use in the in vitro test is of value and the procedure is described. The tests should enable comparable data to be obtained in surveys in all parts of the world.
Previous studies have indicated that host genetics significantly affects the number of gastrointestinal nematode eggs per gram (epg) in the feces of calves during their first grazing season. An entire calf crop of approximately 190 animals was monitored monthly until weaning to verify these earlier results, and to begin to discern the basis for this phenomenon. A significant genetic effect on fecal epg values was not observed until calves had been on pasture for 2-3 months, and was demonstrable until late in the grazing season when the effect was lost. The loss of a genetic effect coincided with the appearance of significant numbers of the more highly fecund nematode species Haemonchus placei and Oesophagostomum radiatum, and with an apparent increase in Ostertagia ostertagi transmission, indicating that the observed genetic control of epg values may be species specific, dose dependent or both. Calves were selected from the population, and grouped according to their epg phenotype over the grazing season as either high or low epg calves. Postmortem examination of some of these calves indicated that worm burdens in the low epg calves were 60% of those of the high epg calves. Experimental challenge inoculation of the remaining calves indicated that: (1) challenge with Cooperia oncophora resulted in low epg calves harboring worm numbers that were 65% of those of high epg calves; (2) challenge with O. ostertagi resulted in similar numbers of worms in both groups, but the fecundity of worms in the low epg groups was significantly lower (P less than 0.05) than in the high epg group. Analysis of serum anti-Ostertagia antibody levels in the grazing calf population showed rises in serum IgG1, IgG2, IgM and IgA antibody levels during the grazing season. Peak serum IgG2 and IgG1 anti-Ostertagia antibody levels were found to be significantly affected by host genetic factors while IgA and IgM levels were not under such control.
Macrocyclic lactone endectocides include two chemically distinct compounds moxidectin, a milbemycin, and ivermectin, an avermectin. The significance of the chemical differences between these compounds in relation to nematode resistance remains to be established. Reported studies indicate that moxidectin at the recommended dose rate of 0.2 mg/kg controls identified strains of nematodes, isolated from sheep and goats, with demonstrated resistance to ivermectin. This reflects the significantly greater potency of moxidectin against the 3 genera of nematodes most commonly involved in anthelmintic resistance, Haemonchus, Ostertagia and Trichostrongylus. Moxidectin, in recommended strategic treatment programmes, should reduce the risk of further development of resistance to the macrocylic lactone endectocides.
Despite the enormous advances over the last 50 years in the chemotherapeutic control of nematode parasites, the economic importance of these parasites to the grazing livestock industries remains as great as ever. Added to this, the emergence and rapid development of resistance to the new broad spectrum anthelmintics in the important nematode species now looms large as a major international threat. This particularly is of concern to the sheep industry, especially in the major sheep-raising countries of the Southern Hemisphere, but there are clear signs that the problem in Western Europe and North America is rapidly escalating. Resistance is also a serious concern in the intensive goat industry, but at present appears to occur only on isolated, individual cattle properties. To obtain a perspective of the development of anthelmintic resistance in relation to husbandry practices, this review focuses on the problem in the sheep industry in relation to its development, detection and management.
The large stomach worms Haemonchus contortus, Haemonchus placei, and Haemonchus similis are important pathogens of cattle and sheep. This paper describes characteristics of surface cuticular ridges (synlophe), which for the first time provide morphological criteria for identifying individual adult specimens of either sex. The diagnostic patterns of the synlophe on the anterior half of specimens can be observed at 400x in temporary mounts on glass slides. The synlophe can be studied in cleared preserved specimens or in living or freshly thawed frozen specimens mounted in water. The synlophe of H. contortus has 30 ridges in the region of the posterior half of the esophagus, 4 fewer than H. placei and H. similis. The 4 extra ridges of H. placei and H. similis are consistently located bilaterally to the 3 ventralmost and the 3 dorsalmost ridges. The 4 extra ridges of H. similis extend to the end of the synlophe posterior to midbody, but in H. placei they extend posteriorly only to the end of the anterior quarter of the nematode. A key is included to the 3 species of Haemonchus parasitic in domestic sheep and cattle using characteristics of spicules, female reproductive system, female tail, and the synlophe.
Studies of medium stomach worms (Subfamily Ostertagiinae) of domestic and wild ruminants in North America have refined our understanding of the systematics, host distribution and biogeography of these nematodes. Strong support for recognition of monophyly for the Ostertagiinae has resulted from preliminary phylogenetic analyses of morphological characters among these and other trichostrongylids. Evaluation of morphological and biochemical characters in our laboratory and elsewhere has not refuted the polymorphism hypothesis where paired major and minor morphotypes are postulated to represent polymorphic species within the genera Ostertagia (Ostertagia ostertagi/Ostertagia lyrata; Ostertagia leptospicularis/Ostertagia kolchida; Ostertagia gruehneri/Ostertagia arctica; Ostertagia mossi/Ostertagia dikmansi), Teladorsagia (Teladorsagia circumcincta/Teladorsagia trifurcata (= Teladorsagia davtiani), and Marshallagia (Marshallagia marshalli/Marshallagia occidentalis). The minor morphotype of Ostertagia bisonis, recognized in Eurasia (considered to be Teladorsagia kazakhstanica), has yet to be discovered in North America. The taxonomy of these species has remained stable since an earlier overview of Ostertagia spp. and Teladorsagia spp. in North American domestic stock at the 1986 Ostertagia Workshop. Investigations since 1986 have focused on comparative morphology and the clear differentiation of Ostertagiinae, primarily from wild ruminants, that have been reported or may potentially occur in domestic bovids. Among these are species which infect wild and domestic sheep (Marshallagia marshalli/Marshallagia occidentalis), bovids (Ostertagia bisonis), and cervids (Ostertagia mossi/Ostertagia dikmansi, Ostertagia leptospicularis/Ostertagia kolchida, Ostertagia gruehneri/Ostertagia arctica, Mazamastrongylus odocoilei and Mazamastrongylus pursglovei) in North America. A key is presented for identifying 15 species of the Subfamily Ostertagiinae that are parasitic in domestic and wild ruminants of North America. Four exotic species (Camelostrongylus mentulatus, Spiculopteragia spiculoptera (= Spiculopteragia boehmi), Spiculopteragia asymmetrica and Longistrongylus curvispiculum) have been reported in North America, but only in game farms and are not included in the key. Hyostrongylus rubidus, a member of the Ostertagiinae normally parasitic in pigs and only rarely reported from domestic ruminants, is not included in the keys. Additional data from comparative morphology and molecular analyses will promote a reassessment of the generic-level systematics of the Ostertagiinae and allow an evaluation of host-parasite evolution and historical biogeography.
Since the first reports of resistance to the broad spectrum anthelmintics were made some three decades ago, this phenomenon has changed from being considered merely as a parasitological curiosity to a state of industry crisis in certain livestock sectors. This extreme situation exists with the small ruminant industry of the tropical/sub-tropical region of southern Latin America where resistance to the entire broad spectrum anthelmintic arsenal now occurs. In contrast, the cattle industry does not appear to be threatened--or so it seems. Although field reports of resistance have been made to the range of broad spectrum anthelmintics in nematode parasites of cattle, it appears that the evolution of resistance in cattle parasites is not as dramatic as for sheep worms. However, one cannot remain confident that this state of affairs will remain static. Concern is shared amongst parasitologists that we have not looked closely enough. In regions of the world where internal parasites are considered a problem in cattle and drenching occurs frequently, no widespread surveys have been carried out. It appears that because of the very high costs and risks associated with taking a new active drug down the development track to marketing, that the pharmaceutical industry has, in general, turned away from this activity. By implication, the international small ruminant industry is too small for these companies to make the necessary investment. This begs two questions: What is the fate of the sheep (and goat) industries in those parts of the world where resistance is rampant and immediate ameliorative parasite control options are required? What will be the response if significant resistance is found in cattle parasites? There is a body of opinion which suggests that if resistance becomes an issue in the control of cattle parasites then the pharmaceutical industry will find it commercially attractive to re-enter the anthelmintic discovery and development business. This is based on the simple commercial fact that by far the greatest anthelmintic sales are associated with the cattle industry. However, this market is specific and sectoral, with by far the greatest sales in North America and Western Europe, where the prevalence of resistance is likely to be low and remain so, more-or-less indefinitely. So the chances of the above scenario occurring must be considered low. Remarkable developments have recently occurred in non-chemotherapeutic parasite control options, for example worm vaccines, host selection and biological control. Also, there seems to be greater acceptance of various grazing management practices designed to reduce the frequency of anthelmintic treatment. However, they collectively cannot be expected to offer immediate salvation to farmers now faced with chemotherapeutic failure to control nematode parasites in their flocks. The future for these farmers must be considered bleak, because compounded with these problems are the poor commodity prices for sheep and goat meat and fibre, resulting in relentless reductions in funding for research to support these industries. Perhaps the major social issues associated with re-structuring and possibly abandonment of sheep and goat farming in affected areas may precipitate action? As veterinary parasitologists, who in general have an interest and expertise in parasite control, we must promote the importance of the problem of anthelmintic resistance and ways to tackle it.
A postal survey of worming practices on West Country dairy farms was undertaken and farmers were requested to send faecal samples for nematode egg counts. The majority of the farmers who responded had a nematode control policy which was based on a mixture of anthelmintics and pasture rotation. Sixty-five per cent turned out calves on to the same paddock each year and 57 per cent treated their stock with anthelmintics during the second year. Ninety farms submitted samples for analysis but only 16 samples contained sufficient eggs to justify repeat egg counts and only eight of these produced enough eggs for in vitro tests. The small number of positive samples, even into the latter part of the year suggests a heavy use of anthelmintics with relatively clean pasture. One Somerset farm had larvae which developed in high concentrations of ivermectin, and eggs were still being passed after two treatments with ivermectin at the manufacturer's recommended dose seven days apart. Of 100 male nematodes isolated from two of the calves, 88 were Cooperia species and 12 were Nematodirus species. A controlled trial with this isolate in eight Friesian male calves showed a 44 per cent reduction in egg counts at day 7 but no significant reduction in worm burden postmortem. This is the first reported case of ivermectin-resistant Cooperia species in cattle in the United Kingdom.
In April 2003, persistent scouring and ill-thrift that was reported in calves form an intensive beef rearing operation in central Argentina despite treatments with benzimidazole and ivermectin. In order to conduct a controlled faecal egg count reduction test on this herd, 40 calves 5-8-months-old were selected on the basis that they had a nematode eggs per gram (epg) of faeces count greater than 150. Animals were divided into four groups (1-4) of 10 calves. Calves of groups 1-3 were treated, respectively, with subcutaneous injection of ivermectin (200 mcg/kg), ricobendazole (4 mg/kg) and levamisole (7.5 mg/kg), while calves of group 4 remained as untreated controls. The egg count reductions carried out 10 days later were lower than 15% in calves treated with ivermectin and ricobendazole, but 100% in animals receiving levamisole. Pooled post-treatment faecal cultures showed larval percentages of 92 and 95 for Haemonchus and 8 and 5 for Cooperia in the faeces of calves treated with ivermectin and ricobendazole, respectively. This is the first reported case of Haemonchus parasiting cattle showing simultaneous resistance to avermectins and benzimidazole type anthelmintics.
The systematics of nematodes that cause Ostertagiasis in domestic and wild ruminants in North America with a key to species
- Lichtenfels