Endoparasite control management on horse farms – lessons from worm prevalence and questionnaire data

Reasons for performing study: Increasing prevalence of anthelmintic resistance in equine nematodes calls for a reexamination of current parasite control programmes to identify factors influencing control efficacy and development of resistance. Objectives: To investigate if associations occur between prevalence of parasitic nematodes and management practices. Methods: German horse farms (n = 76) were investigated in 2003 and 2004. Information on farm and pasture management with respect to endoparasite control measures obtained using a questionnaire survey. Faecal examinations were performed in parallel. Results: Horses (n = 2000) were examined by faecal nematode egg counts, grouped into foals, yearlings and mature individuals for statistical analyses. Farms were categorised into 3 types, riding, stud farms and small holdings. Count regression models were used to analyse strongyle faecal egg count data. Following dichotomisation of faecal egg count (FEC) data, prevalence of strongyle and Parascaris equorum infections were assessed by logistic regression models as a function from various management factors. Yearlings on stud farms showed a 2‐fold higher risk of being positive for strongyle FEC, higher (i.e. ≥3 per year) anthelmintic drug treatment frequencies were associated with reduced strongyle infection rates only in mature individuals but not in foals or yearlings, foals on farms fertilising pastures with horse manure had a significantly higher risk of being P. equorum FEC positive and yearlings on stud farms were more often showing incomplete FECR following anthelmintic treatment compared to yearlings on other farm types. The mean yearly treatment frequencies per age group were: foals 4.52, yearlings 3.26 and mature horses 2.72 times, respectively. Conclusion and potential relevance: To delay the development of anthelmintic, resistance management should include additional nonchemotherapeutic parasite control strategies, FEC‐monitoring, controlled quarantine treatment of new arrivals and control of efficacy by the faecal egg count reduction test on a regular basis.     

High-level pyrantel resistance in the hookworm Ancylostoma caninum

While anthelmintic resistance is now a widely recognized issue in the livestock industries, its existence within companion animal medicine has been rarely established conclusively. We undertook a placebo-controlled in vivo trial to measure the efficacy of pyrantel embonate against pooled isolates of the hookworm Ancylostoma caninum from Brisbane, Australia. A statistically significant fall in adult worm burden was observed among dogs in the pyrantel treatment group compared to the control dogs (178.0+/-24.5 versus 239.7+/-14.0; p=0.02), equating to an efficacy of just 25.7% (95% CI, 15.0-35.1%), as based upon reduction in mean worm burden. Analysis of faecal egg count trends through the course of the study revealed that egg counts rose in both control and pyrantel-treated dogs, with a greater rise observed in the latter group (11.6+/-8.3% versus 17.3+/-7.6%; p=0.04), despite the decrease in adult worm numbers in this group. Our results indicate that high-level anthelmintic resistance does occur in companion animal medicine, and highlight the need for greater vigilance and more judicious use of anthelmintics in small animal practice. They further indicate that the faecal egg count reduction test needs to be used with caution with this parasite.     

Frequent deworming in horses; it usually does not do any good, but it often harms

Due to excessive and inappropriate use of dewormers anthelmintic resistance has developed as a significant problem in horse parasites in the Netherlands. Since it is unlikely that new classes of anthelmintics against horse nematodes will be introduced in the near future, it is important to use the present drugs wisely. Veterinarians should advice horse owners about worm control programs with a more targeted approach. The number of anthelmintic treatments should be reduced and, through selective anthelmintic treatments, further development of anthelmintic resistance should be delayed. Preferably, horses with a low faecal egg count should not be treated at all to ascertain a reduction of the selection pressure for anthelmintic resistance. The propensity for low faecal egg counts is hereditary. This implies that mature horses with consistent low egg counts can be detected by faecal examination and that it is not necessary to repeat faecal examination each time in these animals. New horses on the farm should always be dewormed on arrival and should be introduced only after the efficacy of treatment has been determined. Anthelmintic resistance can also be introduced with the arrival of a new animal that is infected with drug-resistant parasites.     

Equine helminth infections: control by selective chemotherapy

A programme of selective anthelmintic therapy was used in a herd of 31 horses. Faecal egg counts were done during the months of September, November, January, March, May and the following September. Horses with greater than or equal to 100 eggs per gram (epg) were treated with ivermectin, and those with less than 100 epg were not treated. The criteria for adequate internal parasite control in the herd was a median herd faecal egg count of less than or equal to 100 epg. Effectiveness of selective therapy was assessed by faecal egg count after nine months of treatment and was determined to be adequate when a median herd egg count of 0 epg was obtained. However, on returning from pasture the following September, median herd egg count had risen to 325 epg. A statistically significant correlation was seen in the paired September faecal egg counts of the horses in that initial September faecal egg count was predictive for the following September. Initial September faecal egg count was related to the number of anthelmintic treatments required during the period of selective therapy, whereas age of horse was not. We propose that faecal egg counts be incorporated into strategic anthelmintic programmes as an economical tool for identifying and targeting herd members predisposed to shedding elevated numbers of helminth eggs.     

Strongyle egg shedding consistency in horses on farms using selective therapy in Denmark

Knowledge of horses that shed the same number of strongyle eggs over time can lead to the optimization of parasite control strategies. This study evaluated shedding of strongyle eggs in 424 horses on 10 farms when a selective anthelmintic treatment regime was used over a 3-year period. Faecal egg counts were performed twice yearly, and horses exceeding 200 eggs per gram (EPG) of faeces were treated. The results are presented as probabilities of the egg count outcome, when two previous egg counts are known. A horse with no strongyle eggs detected in the two previous faecal examinations had an 82% probability of a zero, and a 91% of being below 200 eggs per gram in the third examination. A horse with the two previous egg counts below 200 EPG had an 84% probability of being below 200 EPG the third time as well. When faecal egg counts exceeded 200 EPG on the previous two counts, the probability for a horse exceeding 200 EPG the third time was 59%. In conclusion, these data demonstrate consistent shedding from one grazing season to another in a majority of horses despite treatment of horses exceeding 200 EPG.     

Criteria for diagnosing anthelmintic resistance by the faecal egg count reduction test

This study examines the possible outcome of adopting criteria recommended by the Australian Working Party for defining anthelmintic resistance by the faecal egg count reduction test, namely a mean percentage reduction of less than 95%, together with a lower 95% confidence limit of less than or equal to 90%. Based on an analysis of 313 veterinary diagnostic cases submitted for faecal egg count reduction testing in sheep and goats over a 7-year period, it was found that lower confidence limits of 90% or less were always associated with mean percentage reductions of less than 95%. These results suggest that if anthelmintic resistance is to be defined on the basis of mean faecal egg count reductions of this magnitude, then little practical purpose is likely to be served by further consideration of the lower confidence limits of these estimates.     

Multiple anthelmintic resistance in Haemonchus contortus on a sheep farm in India

Multiple resistance to benzimidazoles (fenbendazole, albendazole and mebendazole) in a strain of Haemonchus contortus in sheep was detected on a farm where fenbendazole resistance had already been identified. Following a faecal egg count reduction test, this was confirmed by both critical and controlled anthelmintic tests. Different groups of sheep infected naturally or given an experimental infection with the fenbendazole-resistant strain were treated with the recommended doses of various anthelmintics. Compared to the control group, percentage reductions in faecal egg counts of sheep treated with fenbendazole, albendazole, mebendazole, levamisole and morantel varied between 56% and 81% and worm counts between 71% and 86%. The results indicate the presence of multiple anthelmintic resistance in this strain of H. contortus on this farm. Sheep treated with ivermectin and closantel showed 100% reductions in faecal egg and worm counts, suggesting high efficacy of these drugs against the population of H. contortus on this farm.     

Multiple Anthelmintic Resistance in Haemonchus Contortus on a Sheep Farm in Kenya

Multiple resistance to albendazole, thiophanate, levamisole and orally administered ivermectin was detected in an isolate of Haemonchus contortus in sheep on a farm where benzimidazole resistance had already been identified. Following a faecal egg count reduction test, this was confirmed by both critical and controlled anthelmintic tests. Different groups of sheep infected naturally or given an experimental infection with the benzimidazole-resistant isolate were treated with the recommended doses of various anthelmintics. Compared to the control group, the percentage reductions in the faecal egg counts of sheep treated with albendazole, thiophanate, levamisole and ivermectin varied between 38.2% and 79.1% and the residual worm counts between 27.3% and 57.5%. The results indicate the presence of multiple anthelmintic resistance in this isolate of H. contortus. Sheep treated with closantel showed 100% reductions in faecal egg and worm counts, indicating that this drug was very effective against the population of H. contortus on the farm.     

Criteria for diagnosing anthelmintic resistance by the faecal egg count reduction test

This study examines the possible outcome of adopting criteria recommended by the Australian Working Party for defining anthelmintic resistance by the faecal egg count reduction test, namely a mean percentage reduction of less than 95%, together with a lower 95% confidence limit of less than or equal to 90%.

Based on an analysis of 313 veterinary diagnostic cases submitted for faecal egg count reduction testing in sheep and goats over a 7-year period, it was found that lower confidence limits of 90% or less were always associated with mean percentage reductions of less than 95%. These results suggest that if anthelmintic resistance is to be defined on the basis of mean faecal egg count reductions of this magnitude, then little practical purpose is likely to be served by further consideration of the lower confidence limits of these estimates.     

Methods to determine resistance to anthelmintics when continuing larval development occurs

The in vivo faecal egg count reduction test (FECRT) is the most commonly used test to detect anthelmintic resistance (AR) in gastrointestinal nematodes (GIN) of ruminants in pasture based systems. However, there are several variations on the method, some more appropriate than others in specific circumstances. While in some cases labour and time can be saved by just collecting post-drench faecal worm egg counts (FEC) of treatment groups with controls, or pre- and post-drench FEC of a treatment group with no controls, there are circumstances when pre- and post-drench FEC of an untreated control group as well as from the treatment groups are necessary. Computer simulation techniques were used to determine the most appropriate of several methods for calculating AR when there is continuing larval development during the testing period, as often occurs when anthelmintic treatments against genera of GIN with high biotic potential or high re-infection rates, such as Haemonchus contortus of sheep and Cooperia punctata of cattle, are less than 100% efficacious. Three field FECRT experimental designs were investigated: (I) post-drench FEC of treatment and controls groups, (II) pre- and post-drench FEC of a treatment group only and (III) pre- and post-drench FEC of treatment and control groups.To investigate the performance of methods of indicating AR for each of these designs, simulated animal FEC were generated from negative binominal distributions with subsequent sampling from the binomial distributions to account for drench effect, with varying parameters for worm burden, larval development and drench resistance. Calculations of percent reductions and confidence limits were based on those of the Standing Committee for Agriculture (SCA) guidelines. For the two field methods with pre-drench FEC, confidence limits were also determined from cumulative inverse Beta distributions of FEC, for eggs per gram (epg) and the number of eggs counted at detection levels of 50 and 25. Two rules for determining AR: (1) %reduction (%R) < 95% and lower confidence limit <90%; and (2) upper confidence limit <95%, were also assessed. For each combination of worm burden, larval development and drench resistance parameters, 1000 simulations were run to determine the number of times the theoretical percent reduction fell within the estimated confidence limits and the number of times resistance would have been declared.When continuing larval development occurs during the testing period of the FECRT, the simulations showed AR should be calculated from pre- and post-drench worm egg counts of an untreated control group as well as from the treatment group. If the widely used resistance rule 1 is used to assess resistance, rule 2 should also be applied, especially when %R is in the range 90 to 95% and resistance is suspected.     

The detection of anthelmintic resistance by the faecal egg count reduction test: An examination of some of the factors affecting performance and interpretation

This study examines and compares the possible effects of several procedural variants with those of a currently recommended faecal egg count reduction test for the detection of anthelmintic resistance. The results suggest that the failure of an anthelmintic to reduce the arithmetic mean egg counts of 10–15 animals by at least 90%, from either their pre-treatment levels or from those of an untreated control group 5–10 days later, is likely to be an appropriate procedure. It is recommended that such evaluations of drench performance be regularly conducted on farms. Some suggestions as to how this might be encouraged are made, and the role of larval cultures both in increasing the sensitivity and in enhancing the value of the faecal egg count reduction test are discussed.     

河北省坝上地区绵羊消化道线虫对丙硫苯咪唑抗药性的检测

目的　为了查明绵羊消化道线虫对丙硫苯咪唑的抗药性。方法　应用粪便虫卵减少试验 (FECRT)对河北省坝上地区绵羊消化道线虫的抗药性进行了检测。结果　应用 5 m g/ kg丙硫苯咪唑对 5组绵羊进行驱虫的虫卵减少率分别为 4 3.9% ,38.4 6 % ,4 9.0 9% ,37.6 3%和 4 3.35 % ,驱净率分别为 2 0 % ,15 % ,15 % ,2 5 %和 10 %。结论　根据 FECRT 95 %置信域小于 90 % ,表明试验羊对该药有抗药性     

Anthelmintic resistance and sheep management practices in south western Victoria

Twenty-eight farms in 7 shires in south western Victoria were selected and tested for presence of benzimidazole-resistant nematodes between November 1979 and June 1981. Mean faecal egg counts of sheep were less than 100 strongyloid eggs/g on 11 farms. Faecal egg count reduction tests were conducted on the remaining 17 farms and thiabendazole was less than 90% efficient in reducing egg counts in sheep from 5 (29%) of these farms. Thiabendazole-resistant Teladorsagia circumcincta were identified at necropsy of experimentally infected treated sheep. In further studies a survey of 104 farms was conducted in the Mount Rouse and Dundas shires of western Victoria in 1981 and 1982 respectively to determine the prevalence of anthelmintic resistance in these shires. Mean faecal egg counts among weaner sheep in the winter-spring of both years were less than 100 eggs/g which indicated low levels of parasitic nematode populations. A faecal egg count reduction test was conducted on 10 farms and thiabendazole was less than 90% efficient on 3; levamisole was greater than 90% efficient in all 10 tests. Most of the surveyed farms carried Merino or Merino crossbred sheep at 10 to 15 dry sheep equivalents per ha and weaners were treated with anthelmintics 3 to 6 times per year. Management procedures based mainly on anthelmintic therapy were effective in controlling nematode populations in weaner sheep, although many producers alternated between different groups of anthelmintics within the same year contrary to current recommendations for long-term preservation of anthelmintic efficacy. It was concluded that anthelmintic resistance was not of practical importance to the majority of sheep producers in the region.     

The detection of anthelmintic resistance by the faecal egg count reduction test: an examination of some of the factors affecting performance and interpretation

This study examines and compares the possible effects of several procedural variants with those of a currently recommended faecal egg count reduction test for the detection of anthelmintic resistance. The results suggest that the failure of an anthelmintic to reduce the arithmetic mean egg counts of 10-15 animals by at least 90%, from either their pre-treatment levels or from those of an untreated control group 5-10 days later, is likely to be an appropriate procedure. It is recommended that such evaluations of drench performance be regularly conducted on farms. Some suggestions as to how this might be encouraged are made, and the role of larval cultures both in increasing the sensitivity and in enhancing the value of the faecal egg count reduction test are discussed.     

A comparison of the FECPAK and Mini-FLOTAC faecal egg counting techniques

Faecal egg counts (FECs) are used for detecting and quantifying nematode infections and are the basis for determining drug efficacy and anthelmintic resistance in faecal egg count reduction tests (FECRTs). Currently, several FEC techniques are available for detecting and quantifying eggs of sheep nematodes. A comparison of the egg counts from the FECPAK (with a minimum detection limit of 30 eggs per gram (epg)) and Mini-FLOTAC (with a minimum detection limit of 5 epg) showed better diagnostic performance with Mini-FLOTAC in terms of measurement error (level of over- or under-estimation of FEC) and precision (variability in FEC). A tendency to under-estimate FEC was observed with the FECPAK particularly at egg densities of less than 500 epg. It is concluded that Mini-FLOTAC is a reliable diagnostic tool offering reduced measurement error and a higher level of precision.     

Doramectin resistance in Haemonchus contortus on an alpaca farm in Belgium

Parasitism by gastrointestinal nematodes is a health concern in New World Camelids (NWC) worldwide, and anthelmintic treatment is often needed for parasite control. Although anthelmintic resistance has been reported in ruminants worldwide, data in NWC are only scarce. In the present study, a case of suspected doramectin resistance in alpacas was examined. A field efficacy study was conducted for the evaluation of two different dosages of doramectin using a faecal egg count reduction test. A group of 8 alpacas was treated with a subcutaneous injection of doramectin at 0.2mg/kg bodyweight. Individual faecal samples were collected before treatment and 7 days after treatment. The faecal egg counts indicated a treatment efficacy of only 68%. To determine whether the treatment failure was caused by true anthelmintic resistance or suboptimal dosage in this animal species, a group of 4 alpacas was subsequently treated at 0.3mg/kg bodyweight. Faecal egg counts 7 days post treatment were reduced by only 41%, indicating that the treatment failure was more likely to be caused by the presence of resistant parasites on this farm. Coprocultures of faecal samples collected after treatment indicated the presence of 98.5% Haemonchus contortus and a small percentage of Cooperia oncophora (<1.5%). A controlled efficacy trial in sheep, for which the optimal dosage of doramectin is known, was conducted to ensure that this truly was a case of resistant parasites. Infective larvae collected from the faeces of these alpacas were used to infect eight nematode-free lambs. These lambs were assigned to one of two groups based on faecal egg counts post infection. One group was treated with doramectin injectable at 0.2mg/kg bodyweight, the other group served as a non treated control group. Pharmacokinetics indicated that the doramectin treatment was adequate, yet an efficacy of only 16% was determined on day 7 after treatment. Identification of the larvae after treatment revealed 100% H. contortus. On day 7 after treatment, H. contortus worm counts were only reduced by 8% in the treated lambs. The results of the present study report for the first time a case of doramectin resistance in alpacas, mainly in H. contortus.     

Multiple anthelmintic resistance and the possible contributory factors in Beetal goats in an irrigated area (Pakistan)

This paper presents the first report of multiple anthelmintic resistance in the gastrointestinal nematodes of goats and its possible contributory factors in an irrigated area (Pakistan). A total of 18 privately owned Beetal goat flocks were selected in order to determine the anthelmintic resistance against commonly used anthelmintics. Forty to 48 animals from each flock were selected according to their weight and egg count. The three anthelmintics viz., oxfendazole, levamisole and ivermectin, were given to three groups at manufacturer’s recommended dose while one group was kept as untreated control. Anthelmintic resistance was determined through faecal egg count reduction and egg hatch tests while assessment of the contributory factors of anthelmintic resistance was measured through the rural participatory approach. Faecal egg count reduction test revealed high prevalence of anthelmintic resistance (83.3%) and it was either single (levamisole) or multiple (oxfendazole and levamisole). Egg hatch test confirmed the resistance against oxfendazole as detected with faecal egg count reduction test. None of the goat flocks was resistant to ivermectin. Copro-cultures revealed that Haemonchus contortus, Trichostrongylus colubriformis and Teladorsagia circumcincta were the most common species exhibiting resistance to levamisole and oxfendazole. Step-wise logistic regression of the data on worm control practices revealed significant role of under-dosing, low-protein diets, healthcare supervision by the traditional healers and mass treatments.     

Application of in vitro anthelmintic sensitivity assays to canine parasitology: detecting resistance to pyrantel in Ancylostoma caninum

Resistance of the canine hookworm Ancylostoma caninum to anthelmintic therapy with pyrantel is an emerging problem in canine veterinary practice. Detecting anthelmintic resistance in parasites of pets is problematic because traditional resistance-monitoring techniques used with livestock parasites, such as the faecal egg count reduction test, are often impractical for use in small animals. We used two field-collected isolates of A. caninum in an abbreviated critical trial to test their pyrantel resistance status. The strains showed high-level and low-level resistance, with in vivo pyrantel efficacies of 28% and 71%, respectively. We noted a distinct worm density dependence effect on faecal egg count during the critical trial; egg counts in the dogs containing the low-level resistant isolate were 41% higher 6 days after drug treatment, despite the removal of 71% of the adult worms by the drug treatment. We then assessed four candidate in vitro assays for their ability to detect pyrantel resistance in A. caninum larvae, using these two isolates. The assays included a new format termed the larval arrested morphology assay (LAMA), based on observation of the effects of pyrantel on the body shape adopted by infective stage A. caninum larvae in vitro. Our data suggests that three of these assays, the LAMA, the larval motility assay (LMA), and larval feeding inhibition assay (LFIA) show promise with regards to detection of pyrantel resistance in A. caninum, but the complexity of the LFIA would likely limit its suitability for field studies. In vivo pyrantel efficacies of 28% and 71% in the two A. caninum isolates were associated with a 17-fold shift in the in vitro IC(50) values measured using the LAMA. Further testing with isolates of varying degrees of resistance is required to determine which of these assays is suitable as a rapid in vitro laboratory test for pyrantel resistance in A. caninum. The present study also indicates that potential exists for the novel LAMA or the LMA to be of use in detecting pyrantel resistance in the human hookworms, Necator americanus and Ancylostoma duodenale.     

Prevalence of anthelmintic-resistant nematodes in fibre-producing goats in Scotland.

Six cashmere goat herds in Scotland were surveyed to assess the prevalence of anthelmintic resistance and the species of nematode involved. Resistance was determined in vivo by a faecal egg count reduction test and in vitro using an egg hatch assay and specific faecal egg identification techniques. Benzimidazole resistance was present in five of the herds, insufficient eggs were obtained from the other herd to draw firm conclusions. Teladorsagia (Ostertagia) species predominated in four of the five herds in which resistance was detected and Haemonchus contorus was the dominant species in the other.     

Multispecies and multiple anthelmintic resistance on cattle nematodes in a farm in Argentina: the beginning of high resistance?

There are very few resistance records on cattle nematodes. South American successive records have been increasing rapidly since the year 2000. In Argentina, increasing dissatisfaction based on the exclusive use of macrocyclic lactones has prompted the use of benzimidazoles in the Pampean region. The studied farm is located in the Argentina humid Pampas and had apparently poor results after anthelmintic treatments. Evaluation of resistance was firstly based on faecal egg reduction after treatment in November 2001 and June 2002 and was complemented with worm counts obtained by necropsy in June 2002. The study reports that the reduction of faecal egg excretion after benzimidazole (reduction 31-79%) or ivermectin treatments (76-97%) in November 2001 was insufficient and these poor results were confirmed in June 2002 (benzimidazoles (65-89%) and ivermectin (47-77%)). Several methods for evaluating faecal egg count reduction were performed and yielded different results. A new method based on the estimated faecal egg counts (corrected from the initial faecal egg counts and animal type using a general linear model) was used and gave higher flexibility in the interpretation of putative resistance to anthelmintics. From necropsy results, it could be concluded that Cooperia oncophora was resistant to avermectins and benzimidazoles and that Cooperia punctata, Ostertagia ostertagi and Haemonchus placei were resistant to benzimidazoles. This case of multispecies and multidrug resistance is probably not unique and could reflect the emergence of resistances in Argentina. This emergence is probably due to the intensive use of anthelmintics, the absence of refugia, and the frequent circulation of infected cattle.