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Determining Treatment to Control Two Multidrug-Resistant Parasites on a Texas Horse Farm
Abstract
A study was undertaken at the Texas A&M Horse Center to evaluate and compare the effectiveness of three anthelmintics—ivermectin, fenbendazole, and a combination of ivermectin and pyrantel pamoate—on fecal egg count reductions of cyathostomes and Parascaris equorum in 30 naturally infected foals. The foals were randomized into three treatment groups, with individuals being rerandomized after each 8-week observation period. The treatments of ivermectin and fenbendazole were given at the manufacturer's recommended doses, and the pyrantel treatment was given at two times the manufacturer's recommended dose. Fecal egg counts were performed at the time of treatment and at 2-week intervals after treatment for a total of 8 weeks. Each foal received a total of three treatments during the course of the study. Fecal egg counts were performed by a modified McMaster's test, with a sensitivity of 25 eggs per gram of feces, and by the modified Wisconsin double centrifugal flotation technique, with a sensitivity of 0.2 eggs per gram of feces. Fecal egg reduction percentages were calculated. Analysis of the results showed that ivermectin, either used alone or with pyrantel, was a more effective anthelmintic for cyathostome (small strongyle) control than fenbendazole. Fenbendazole and pyrantel showed a higher initial reduction in Parascaris egg counts when compared with the ivermectin-only-treated group, but this difference lessened over time. The use of the combination treatment showed the best results for controlling both parasites, indicating that a combination of anthelmintics may be necessary to control parasites on some equine farms.
... Small strongyles, also known as cyathostomes, are considered the most relevant helminths due to their prevalence, pathogenic potential and ability to develop resistance to anthelmintics [16]. These can parasitize horses of all ages, but are more pathogenic in young animals [17,18]. The most common genera of small strongyles are Cyathostomum spp. ...
Equine farming faces growing challenges with helminthoses, aggravated by the indiscriminate use of anthelmintics without technical criteria. This practice favors resistance to these drugs, generates residues in animal products, compromises food safety and human health, and, when excreted in large quantities, negatively impacts environmental health by affecting invertebrates and fecal microorganisms. This highlights the importance of the One Health approach. A promising alternative is biological control with nematophagous or helminthophagous fungi such as Duddingtonia flagrans, Pochonia chlamydosporia, Arthrobotrys oligospora, Monacrosporium thaumasium, Mucor circinelloides and Purpureocillium lilacinum. Due to their different mechanisms of action, ovicidal and predatory fungi, when used together, can act in a complementary and synergistic way in the biological control of helminths, increasing their effectiveness in reducing parasitic infections. The use of these fungi through biosynthesized nanoparticles from fungal filtrates is also emerging as a new approach to nematode control. It can be administered through feed supplementation in commercial formulations. The aim of this review is to explore the use of helminthophagous fungi in the control of helminthiases in horses, highlighting their potential as a biological alternative. It also aims to understand how these fungi can contribute effectively and sustainably to parasite management in horses.
... In addition, most researchers agree that assessment of fecal egg count (FEC) should be incorporated into parasite control practices and that climate and other factors, such as housing and sanitation, should be considered in determining frequency and timing of anthelmintic strategies (Brady & Nichols, 2009;Matthews, 2014). Importantly, horse owners need to be informed about the decreased effectiveness of some anthelmintics used to treat horses for internal parasites (Luksovsky, Craig, Bingham, Cyr, & Forrest, 2013). ...
We conducted a survey to assess parasite control programs used by three groups of horse owners. The majority of those surveyed indicated that they received information on parasite control from veterinarians, with only 6% indicating reliance on Extension materials for such information. Most participants did not use fecal egg counts as part of their parasite control programs, and most were not aware of parasite resistance to anthelmintics. Our survey results highlight areas in which education for horse owners may be needed.
... Moreover, macrocyclic lactones are able to eliminate tissue migrating larval stages of Parascaris spp. (Reinemeyer and Nielsen 2017;Lyons and Tolliver 2012;Lindgren et al. 2008) and this property is expected to cause the better/longer lasting protection than pyrantel and fenbendazole, which are both only active against gut luminal stages of the parasite (Luksovsky et al. 2013;Armstrong et al. 2014;Lindgren et al. 2008). ...
Gastrointestinal nematodes are ubiquitous parasites of grazing equines with Parascaris spp., and strongyles being the most relevant ones regarding the prevalence and potential disease severity. Despite their importance, epidemiological data regarding the presence and egg-shedding intensities of these parasites are scarce. Data from 1067 horse samples collected on German horse farms initially to compare diagnostic methods were used for epidemiological analyses. Due to its higher sensitivity, presence/absence data were based on a combined sedimentation/flotation technique while faecal egg counts were based on Mini-FLOTAC. For strongyles, 46.5% of the samples were positive and the median egg-shedding intensity was 40 (range 5–2590). In multivariate analyses, prevalence and egg-shedding intensity were significantly influenced by season, age group and sample type. The drug used for the last treatment and the number of foals on the yard only affected prevalence while the number of horses on the yard and sex were only significant for egg-shedding intensity. For Parascaris spp., a prevalence of 4.6% and a median egg-shedding intensity of 0 (range 5–905) were observed. In multivariate analyses, the age group, the time since the last anthelmintic treatment, presence and number of foals had significant effects on ascarid prevalence whereas egg-shedding intensity was significantly influenced by age group and season only. Parascaris occurred only on yards with foals, but with an increasing number of foals, Parascaris egg-shedding intensity decreased. Prevalence and egg-shedding intensity were influenced by different but partially overlapping variables for Parascaris and strongyles.
... Foal owners should comply deworming instructions recommended by their own veterinarian. As a result from one study among foals, the use of combination therapy of ivermectinpyrantel against small strongyles and parascaris has been recommended (Luksovsky et al., 2013). Various drugs and drug combinations have been used among foals in Finland (Näreaho et al., 2011) and because of observed increase in anthelmintic resistance among horse population worldwide, it is recommended by Finnish veterinary practitioners that the efficacy of anthelmintic should be tested by taking fecal samples before and after the grazing season (Recommendation of Finnish Veterinary Practitioners, 2019; Horse Information Centre of Finland, 2019). ...
Objective:
To compare larvicidal regimens of fenbendazole and moxidectin for reduction and suppression of cyathostomin fecal egg counts (FEC) in a transient herd of embryo transfer-recipient mares.
Design:
Randomized, complete block, clinical trial.
Animals:
120 mares from 21 states, residing on 1 farm.
Procedures:
An initial fecal sample was collected from each mare; mares with an FEC ≥ 200 eggs/g were assigned to treatment groups. Eighty-two horses received fenbendazole (10.0 mg/kg [4.5 mg/lb], PO, q 24 h for 5 days) or moxidectin (0.4 mg/kg [0.18 mg/lb], PO, once); FEC data were analyzed 14, 45, and 90 days after treatment.
Results:
Mean FEC reduction was 99.9% for moxidectin-treated mares and 41.9% for fenbendazole-treated mares 14 days after treatment. By 45 days, mean FEC of fenbendazole-treated mares exceeded pretreatment counts; however, FECs of moxidectin-treated mares remained suppressed below pretreatment values for the duration of the 90-day study. Fecal egg counts were significantly different between groups at 14, 45, and 90 days after treatment.
Conclusions and clinical relevance:
Failure of the 5-day regimen of fenbendazole to adequately reduce or suppress FEC suggested inadequate adulticidal and larvicidal effects. In contrast, a single dose of moxidectin effectively reduced and suppressed FEC for an extended period. Given the diverse geographic origins of study mares, these results are likely representative of cyathostomin-infected mares in much of the United States, confirming previous findings indicating that fenbendazole resistance in cyathostomins is widespread and that moxidectin remains an effective treatment for control of these important parasites.
A study was conducted to determine the efficacy of a benzimidazole anthelmintic (fenbendazole) on horse farms in Slovakia. Nine stud farms with a total number of 80 horses were selected for the faecal egg count reduction (FECR) test. Resistance was assumed if egg count reduction was less than 90%. A low level of benzimidazole resistance was found on three farms (84.4-89.0%). On the remaining farms the results of the FECR test indicated substantial reduction in faecal egg output after treatment (92.5-99.4%). Larval identification before treatment revealed Cyathostominea larvae as being predominant.
ABSTRACT : Since 2002, macrocyclic lactone resistance has been reported in populations of Parascaris equorum from several countries. It is apparent that macrocyclic lactone resistance developed in response to exclusive and/or excessively frequent use of ivermectin or moxidectin in foals during the first year of life. The development of anthelmintic resistance was virtually inevitable, given certain biological features of Parascaris and unique pharmacologic characteristics of the macrocyclic lactones. Practitioners can utilize the Fecal Egg Count Reduction Test to detect anthelmintic resistance in Parascaris, and the same technique can be applied regularly to confirm the continued efficacy of those drugs currently in use. In the face of macrocyclic lactone resistance, piperazine or anthelmintics of the benzimidazole or pyrimidine classes can be used to control ascarid infections, but Parascaris populations that are concurrently resistant to macrocyclic lactones and pyrimidine drugs have been reported recently from Texas and Kentucky. Compared to traditional practices, future recommendations for ascarid control should feature: 1) use of only those anthelmintics known to be effective against indigenous populations, 2) initiation of anthelmintic treatment no earlier than 60 days of age, and 3) repetition of treatments at the longest intervals which prevent serious environmental contamination with Parascaris eggs. In the interest of decreasing selection pressure for anthelmintic resistance, horse owners and veterinarians must become more tolerant of the passage of modest numbers of ascarid eggs by some foals. Anthelmintic resistance is only one of several potential responses to genetic selection. Although still only theoretical, changes in the immunogenicity of ascarid isolates or reduction of their prepatent or egg reappearance periods could pose far greater challenges to effective control than resistance to a single class of anthelmintics.
By collecting fecal samples every 2 weeks beginning at 2 months of age, 32 foals from a single Texas farm were monitored. The foals were administered ivermectin paste at the time of the first collection and again monthly. When foals had Parascaris egg counts higher 2 weeks after ivermectin treatment than at treatment, they were administered pyrantel pamoate at the manufacturer's recommended dose (6.6 mg/kg) or at twice the recommended dose (13.2 mg/ kg) when tapeworm eggs were also detected. An elevation or only minimal reduction (less than 75%) in Parascaris egg counts was seen 2 weeks after ivermectin treatment until the foals were 8 months of age, at which time there was an 85% reduction in fecal egg count after treatment. When pyrantel was administered at the manufacturer's recommended dose, a 42% to 84% reduction in egg counts occurred, but at 13.2 mg/kg there was a 98% to 100% reduction in fecal egg counts 2 weeks posttreatment. However, pyrantel failed to control strongylate egg counts even at the elevated dose, whereas ivermectin reduced strongylate fecal egg counts by greater than 99%, determined 2 weeks posttreatment. Pyrantel, but not ivermectin, lowered Parascaris egg counts. Ivermectin, but not pyrantel, lowered strongyle egg counts 2 weeks post administration. A single drug for all ages of horses approach to parasite control requires rethinking. Combinations of drugs or more careful evaluation of anthelmintics in foals may be necessary for continued parasite control.
Over the past 20 years a series of surveys based on worm egg counts has been conducted on the prevalence of worm parasitisms in Wisconsin dairy cattle. In full acceptance of the many uses, limitations and interpretations of egg counts, these nevertheless have led us to conclude that, when eggs are found, live worms are prey sent within the cattle, that is, that active and important parasitisms are present. Our first state-wide surveys of Wisconsin dairy herds, conducted in the early 1950s, established universal prevalence of active worm parasitisms in the herds, and the latest state-wide surveys in the 1970s established the same continuous prevalence (Cox and Todd, 1962; Meyers, 1970; Todd et al 1972; Bliss, 1973; Bliss and Todd, 1973). In the past 20 years the parasitisms have not been controlled, have scarcely ever been treated until recent years, and have not declined. In three recent field studies conducted in commercial herds the worm eggs found in 5 g faeces averaged 36 in 1028 cows, 16.3 in 1003 cows and 10.2 in 488 cows…
Possible anthelmintic resistance on a breeding farm where a rapid rotation anthelmintic programme had been implemented for 9 years was investigated. Cyathostomins resistant to fenbendazole and pyrantel were documented by faecal worm egg count reduction test (FWECRT).
To 1) manage small strongyle transmission in a herd of horses in which resistance to both pyrantel pamoate and fenbendazole was identified and thereby reduce the risk of clinical disease in the individual animal, 2) monitor the change in resistance patterns over time and 3) monitor the efficacy of ivermectin over the study period.
Targeted ivermectin treatment of horses on the farm was instituted for mature horses with faecal worm egg counts (FWEC) > 200 eggs/g (epg) and for horses < age 2 years with FWEC > 100 epg.
Over a 30 month period, targeted ivermectin treatment achieved acceptable control in mares, as judged by FWEC, and improved control of patent cyathostome infection in consecutive foal crops. Egg reappearance time (ERT) after treatment with ivermectin was < 8 weeks in mares and foals more frequently in the second year of the study than in the first year. Numbers of anthelmintic treatments were reduced by 77.6 and 533% in the mare and foal group, respectively.
Targeted ivermectin treatment may be an economically viable method of managing multiple drug resistant cyathostominosis.
Use of ivermectin should be monitored closely for development of resistance.
To determine prevalence of anthelmintic resistance in cyathostome nematodes of horses in the southern United States.
Cross-sectional study.
786 horses on 44 farms and stables in Georgia, South Carolina, Florida, Kentucky, and Louisiana.
Fecal egg count (FEC) reduction tests were performed on 44 large farms and stables. Horses on each farm were treated with an oral paste formulation of fenbendazole, oxibendazole, pyrantel pamoate, or ivermectin at recommended label dosages. A mixed linear model was fitted to the percentage reduction in FEC, accounting for differences among farms, states, ages, treatments, and treatment by state interactions.
By use of a conservative measure of resistance (< 80% reduction), the percentage of farms with anthelmintic-resistant cyathostomes was 97.7%, 0%, 53.5%, and 40.5% for fenbendazole, ivermectin, oxibendazole, and pyrantel pamoate, respectively. Mean percentage reductions in FEC for all farms were 24.8%, 99.9%, 73.8%, and 78.6% for fenbendazole, ivermectin, oxibendazole, and pyrantel pamoate, respectively. Pairwise contrasts between states for each treatment revealed that in almost all instances, there were no significant differences in results between states.
The prevalence of resistance found in this study was higher than that reported previously, suggesting that anthelmintic resistance in equine cyathostomes is becoming a major problem. Furthermore, data from these 5 southern states, which are geographically and physiographically distinct, were remarkably similar. This suggests that drug resistance in cyathostomes is highly prevalent throughout the entire southern United States and probably nationwide.
The study was undertaken to evaluate adverse effects of larvicidal treatment in horses naturally infected with cyathostomins. Out of 24 ponies kept on pasture, four animals were housed in September and anthelmintically cured to serve as worm-free controls (group C-0). The others were housed in December. Eight animals each were treated 8 weeks later with 5 x 7.5mg/kg fenbendazole (FBZ) or 1 x 0.4 mg/kg moxidectin (MOX). Four animals remained untreated (group C-i). Two, 4, 6 and 14 days after the end of treatment two animals of each of the treated groups were necropsied together with group C-0 and C-i animals. Infected animals before treatment showed weight loss, eosinophilia, increased plasma protein and globulin contents. Treatment was followed by weight gain and temporal plasma protein and globulin increase. Proportions of CD4+ and CD8+ T lymphocytes in the peripheral blood did not differ between the groups before treatment but dropped significantly temporally after FBZ treatment. Group C-0 was worm-free at necropsy. Group C-i animals contained variable numbers of luminal and tissue cyathostomins. Histological sections showed larval stages in the lamina propria und submucosa surrounded by macrophages. Either treatment was effective against luminal parasites and reduced the number of larvae in the bowel wall beginning 4-6 days after FBZ and 6-14 days after MOX treatment. Histologically, as a first reaction after FBZ application T lymphocytes accumulated around morphologically intact L4 in the submucosa. Subsequently T lymphocytes associated with eosinophils infiltrated the submucosa. Parasites became enclosed by granulomas with eosinophils adhering to and invading the larvae which started to disintegrate on day 4. Later on, particularly on day 14 inflammation extended into the mucosa and was frequently associated with ulcerations. Third stage larvae in general and L4 in the lamina propria, however, seemed not to be affected until day 14 and even then, parasites did usually not generate extensive inflammation. After MOX treatment severe morphologically detectable alterations of tissue larvae could not be observed earlier than day 14. Different from FBZ treatment, larvae disintegrated and were obviously resorbed without causing severe inflammation in the gut wall. In conclusion treatment with either drug was efficacious against tissue larvae of cyathostomins but there may be different clinical consequences: in contrast to MOX effects, killing of larvae due to FBZ was associated with severe tissue damage, which clinically may correspond to reactions caused by synchronous mass emergence of fourth stage larvae, i.e., may mimic larval cyathostominosis.
In 2003 and 2004, on a total of 63 different German horse farms, a survey using the faecal egg count reduction (FECR) test was performed to investigate the efficacy of ivermectin (IVM, Ivomec) and pyrantel (PYR, Banminth) treatment against gastro-intestinal nematodes in a total of 767 horses. IVM treatment resulted in 100% reduction of the cyathostomin egg production 14 and 21 days post-treatment (d.p.t.) on 37 farms. On the remaining five farms, the mean faecal egg count reduction ranged between 97.7 and 99.9%. The mean cyathostomin FECR following PYR treatment ranged between 92.2 and 100% on the 25 farms tested. Therefore, based on the 90% FECR threshold suggested for detection of anthelmintic resistance in horses, neither IVM nor PYR anthelmintic resistance was detected. However, if the thresholds recommended for the detection of resistance in small ruminants were applied, on one and four farms signs of reduced IVM and PYR efficacy, respectively, were observed. In 2005, to further investigate these findings, the cyathostomin egg-reappearance period (ERP) following IVM treatment was examined on six selected farms, two of which were found to show less than 99.8% FECR in the previous survey. On these two latter farms, the ERP was less than 5 weeks, while on the other four it was at least 8 weeks. Earlier investigations described IVM cyathostomin ERP of at least 9 weeks. The efficacy of IVM to reduce Parascaris equorum egg excretion was also studied. On one farm in 2 consecutive years, IVM treatment did not lead to a significant reduction in P. equorum faecal egg counts in one and five young horses, respectively.
Field studies (n=6) were completed on evaluation of activity of ivermectin (200 microg/kg) paste formulation against small strongyles in horses (foals, yearlings, and older animals) on a farm (Farm MC) in Central Kentucky in late 2006 and during 2007. A girth tape was used to estimate body weights which were then used to calculate the proper dose rate of ivermectin. The foals, yearlings, and some of the older horses were born and raised on the farm. However, most of the older horses which were not raised on the farm had been there for several years. The horse herd was given ivermectin exclusively, usually four times a year, since 1990. An exception was that during the foal's period of life fenbendazole, pyrantel pamoate, and oxibendazole were given occasionally besides ivermectin. Efficacy of drug activity was determined by pretreatment and posttreatment counts of strongyle eggs per gram of feces (EPGs). Culture of strongyle eggs in feces from some of the horses showed that only small strongyle larvae were present. The research included two studies (A and B) in foals (n=24) and four studies (C, D, E, and F) in yearlings (n=13) alone or with older horses (n=10). For each of the studies (B through F), there was a treated and a nontreated group. These groups were switched for each treatment, i.e., the treated group in one study was the nontreated group in the next study and vice versa. Eggs per gram of feces counts were determined at 1- or 2-week posttreatment intervals for 4 weeks for study A and 6 weeks for studies B through F. Also, for studies B, E, and F, counts of EPGs were done either two or three times during the third week posttreatment. The studies showed a similar posttreatment pattern of strongyle EPG counts beginning to return at about 4 weeks and increasing at 5 and 6 weeks posttreatment. Two horses in study E and one in study F had low EPG values toward the end of the third week posttreatment. The results of this ivermectin investigation showed that the strongyle EPG counts started returning about twice as quickly post-ivermectin-treatment of horses than when the drug was first marketed in the early 1980s.
Horse foals on five farms in Central Kentucky were used in field studies in 2007 evaluating activity of paste formulations of four compounds (fenbendazole-FBZ, ivermectin-IVM, oxibendazole-OBZ, and pyrantel pamoate-PRT) against internal parasites with emphasis on ascarids (Parascaris equorum). It has been well established the last few years that there is widespread resistance of P. equorum to ivermectin. The main purpose of the present research was to obtain current data on ascaridicidal activity of FBZ, OBZ, and PRT; also, to acquire further information on ascarid resistance to ivermectin. Additionally, data were documented on drug activity on small strongyles. Detection of ascarid and strongyle eggs in feces of foals was by a qualitative method (presence or absence) or a quantitative method (eggs per gram of feces). Strongyle eggs all were assumed to be from small strongyles. This is based on fecal cultures from horses on one farm and historic records from horses in this area on excellent deworming programs. A girth tape was used to estimate the body weight of each foal so that the appropriate dose rate of each drug could be given. Many of the foals were used in more than one cycle of treatments. Efficacy of the drugs, administered intraorally, was determined by calculating the average percentage reduction (% red.) of the number of foals passing eggs after vs. before treatment: (1) FBZ at 10 mg/kg was tested on four farms; 76 foals were examined, 50 with ascarid eggs (84% red.) and 62 with strongyle eggs (0% red.); (2) IVM at 200 microg/kg was tested on three farms; 58 foals were examined, 18 with ascarid eggs (0% red.) and 48 with strongyle eggs (100% red.); (3) OBZ at 10 mg/kg was tested on three farms; 181 foals were examined, 78 with ascarid eggs (94% red.) and 79 with strongyle eggs (0% red.); (4) PRT was tested on two farms, one farm at 1x (6.6 mg base/kg); 42 were foals examined, 16 with ascarid eggs (0% red.) and 33 with strongyle eggs (12% red.) and one farm at 2x (13.2 mg base/kg); 18 foals were examined, 13 with ascarid eggs (23% red.) and 15 with strongyle eggs (27% red.).