- Open Access
The effectiveness of faecal removal methods of pasture management to control the cyathostomin burden of donkeys
© Corbett et al.; licensee BioMed Central Ltd. 2014
- Received: 2 August 2013
- Accepted: 22 January 2014
- Published: 24 January 2014
The level of anthelmintic resistance within some cyathostomin parasite populations has increased to the level where sole reliance on anthelmintic-based control protocols is not possible. Management-based nematode control methods, including removal of faeces from pasture, are widely recommended for use in association with a reduction in anthelmintic use to reduce selection pressure for drug resistance; however, very little work has been performed to quantitatively assess the effectiveness of such methods.
We analysed data obtained from 345 donkeys at The Donkey Sanctuary (Devon, UK), managed under three different pasture management techniques, to investigate the effectiveness of faeces removal in strongyle control in equids. The management groups were as follows: no removal of faeces from pasture, manual, twice-weekly removal of faeces from pasture and automatic, twice-weekly removal of faeces from pasture (using a mechanical pasture sweeper). From turn-out onto pasture in May, monthly faecal egg counts were obtained for each donkey and the dataset subjected to an auto regressive moving average model.
There was little to no difference in faecal egg counts between the two methods of faecal removal; both resulted in significantly improved cyathostomin control compared to the results obtained from the donkeys that grazed pasture from which there was no faecal removal.
This study represents a valuable and unique assessment of the effectiveness of the removal of equine faeces from pasture, and provides an evidence base from which to advocate twice-weekly removal of faeces from pasture as an adjunct for equid nematode control. Widespread adoption of this practice could substantially reduce anthelmintic usage, and hence reduce selection pressure for nematode resistance to the currently effective anthelmintic products.
- Environmental control
For the last 50 years, control of nematode parasites of equids in the western world and beyond has focussed on the regular use of anthelmintic compounds. Anthelmintic compounds have been highly effective in controlling large strongyle spp., including the highly pathogenic Strongylus vulgaris[2, 3], shifting focus towards the previously less problematic smaller strongyles (cyathostomins). Anthelmintic resistance in cyathostomin species was first detected within a few years of the licensing of these products for use in equids, closely corresponding to the widespread adoption of six to eight-week interval dosing and resistance has developed to each anthelmintic after its introduction[6, 7]. Despite a decline in the prevalence of S. vulgaris and the introduction of targeted anthelmintic treatment protocols in the 1990s, interval dosing with anthelmintics was still common practice in 2002[8, 9]. Targeted threshold dosing involves selecting which animals to dose using faecal worm egg counts (FWEC), typically using an arbitrary lower threshold of 200 eggs per gram (EPG)[2, 10]. This strategy is appealing because of the high levels of over-dispersion of nematodes within populations[10, 11]. As only a few individual animals theoretically host the majority of the ‘in host’ worm population[12, 13], targeted dosing of these animals should only be sufficient to substantially reduce nematode contamination on pasture. Despite a gradual move towards more selective anthelmintic use such as this, the prevalence of anthelmintic resistance in some equine populations is now very high, with resistance now reported to every class available for use in equids[14–16]. The widespread prevalence of anthelmintic resistance in cyathostomins in equids provides strong motivation to develop alternative control methods that do not rely solely on the use of anthelmintic compounds. Commonly adopted practices aim to break the transmission cycle of the parasites by preventing or reducing re-infection of animals through grazing. Methods such as dung removal from pasture[7, 17, 18], strip grazing and resting pasture have been advocated, although few quantitative studies have been undertaken to truly demonstrate their effectiveness.
Under optimum environmental conditions, cyathostomin infective third stage larvae (L3) can develop in faeces within three to four days. In Scotland the shortest interval measured for L3 to translate onto pasture after faecal contamination was two weeks under summer weather conditions. Cyathostomin L3 become markedly less infective after eight days at 38°C, exhibiting improved survival at lower temperatures. Dung removal is thought to remove parasite eggs before the first stage larvae (L1) hatch and develop to L3, which then migrate from the faeces onto the pasture. As well as these commonly used control measures outlined above, other methods such as altering diets, and administration of nematophagous fungi have also been investigated for controlling nematodes[24, 25]. The wide variety of alternatives to anthelmintic dosing currently being investigated demonstrates the importance of alternative control measures. There is therefore a need for clear scientific evidence to support or contradict the adopted practices. Here, we seek to provide such evidence by examining the effect of removal of faeces from pasture on the individual monthly FWEC of co-grazed donkeys.
All donkeys in this study resided at The Donkey Sanctuary, Devon, UK. This is a charity, comprised of seven farms in England that house over 2,500 donkeys at any one time. The animals are managed in distinct groups in separate fields and are generally grouped by age and medical condition, with group sizes ranging from two up to over one hundred. On most pastures, faecal removal is practiced for parasite control; however, on steeper, less accessible fields there is no faecal removal. Helminth control varies slightly between the farms, although the general routine (and the routine used in this study) involves taking faecal samples from every animal at four-weekly intervals, FWEC analysis for strongyle (and other nematode species) eggs and anthelmintic dosing based on varying FWEC thresholds. To ensure that the welfare of the donkeys involved in the study was not compromised, any individuals with a FWEC of 2,000 EPG or over at any sampling received a clinical examination by a veterinary surgeon and where appropriate an immediate dose with pyrantel embonate at a dosage of 19 mg/kg was administered. However, there is known resistance in cyathostomins to this compound at the UK Donkey Sanctuary. After consultation with the University of Glasgow School of Veterinary Medicine ethics committee, this study was exempt from formal ethical approval requirements as it was part of standard husbandry techniques.
FWEC data were obtained from the routine parasite monitoring protocol used at the Donkey Sanctuary to control clinical disease due to parasitism. A total of 345 donkeys (147 females and 198 geldings), split among eleven fields, were used here. Of these animals there was an age range from 1 to 46 years old, where 61% were over 20 years old, 24% between 11 and 20 years old and only 15% between 1 and 10 years old. The animals were managed using three different pasture management strategies according to their respective field; these were, “No Removal”, where no faecal removal took place, “Manual”, where faeces were removed manually (using a dung scoop and/or manual removal with gloves) at least twice a week, and “Automated”, where faeces were removed by an automated pasture sweeper (Terra-Vacc, Sweeper, Terra-Vac Ltd, Suffolk, UK) approximately twice a week when weather conditions allowed. A total of 112 donkeys were on fields where no removal took place (split into three fields of 33, 33 and 42 donkeys), 96 donkeys were on fields where manual faecal collection occurred (split into four fields of 16, 17, 23 and 40 donkeys) and 137 donkeys were on fields where automated faecal collection occurred (split into four fields of 15, 27, 33 and 62 donkeys). Monthly FWEC were analysed using a modified McMaster technique with a sensitivity of 50 EPG. This resulted in 1,885 separate FWEC spread over seven consecutive 28-day periods from the 11th of May to the 28th of October 2010, with a total of 274 missing FWEC observations due to individuals not passing faeces during the sampling window for that month. Faeces were collected immediately after being voided and placed into plastic bags voided of air before being processed at the Sanctuary’s laboratory within 24 hours. One pasture sample was obtained from each field at four-week intervals by collecting 400 evenly spaced “plucks” of grass (the amount pinched between forefinger and thumb) per field. Each sample was processed for L3 extraction using the method described by Jorgensen but with the washing by hand replaced by washing in an electrical washing machine (‘Good ideas mini washing machine’, XPB15-2318, Tensor Marketing Ltd. Darlington).
FWEC data were modelled using a latent class first order auto regressive moving average (ARMA) model to describe the seven, consecutive monthly FWEC data obtained from each donkey. The observed egg counts were described using an over-dispersed Poisson distribution, with a log link function. The latent states of the initial observation from each donkey were described using a mixed model with random effects of animal and field, a linear effect of age, and fixed effect of gender. Subsequent observations were modelled as dependent on the latent state corresponding to the previous months observation from that individual, as well as a random effect of sampling point (month), fixed effect of anthelmintic dosing after the previous months sampling (where relevant), and a separate moving average effect for each of the three pasture management types representing the force of re-infection from pasture.
The latent class model was fitted using Bayesian Markov chain Monte Carlo (MCMC) methods, using JAGS run from inside R using the runjags package. Minimally informative priors were used for each parameter, and the model was run to convergence as assessed visually using trace plots for each parameter. Model fit using the deviance information criterion (DIC) was used to determine the best fitting candidate model excluding each of the effects of age and gender.
Table showing median and 95% confidence intervals for each parameter in the model of best fit
Gender (gelding vs female)
Automated vs. manual removal
Automated vs. no removal
Manual vs. no removal
This study represents the first large-scale quantitative validation of pasture hygiene as a viable method of nematode control in equids. Previous studies have shown faecal removal to be highly effective[18, 33, 34] but lacked the large sample size and rigorous statistical methods applied here. Our findings demonstrate that removing faeces from pasture approximately twice weekly is an effective adjunct to strongyle control in groups of donkeys. There does not appear to be any difference between manual and automated methods of pasture hygiene in terms of FWEC, suggesting that either method works equally well. This is an important finding because although some pasture sweepers may act to partially disperse the faeces during use, there appears to be no effect on cyathostomin reinfection as measured by FWEC. Although, a qualitative difference was observed between automated and manual removal of faeces as measured by pasture larval counts. The pasture samples were collected in an attempt to quantify the amount of strongyle larvae on the pasture and therefore the relative levels of infectivity. However, inconsistent recovery of L3 as seen in Figure 3 resulting in extreme variability of pasture larval counts within a field precluded statistically meaningful analysis of this data. This suggests that although pasture larval counts are philosophically attractive as providing the most direct measurement of pasture contamination, difficulties relating to the highly variable nature of this data make this technique less precise in practice. With most strongylid larvae found within 30 cm of bovine and equine faeces[35, 36], a study in Queensland, Australia focused on free living stages of strongylids of horses and found that migration from the faecal matter is highly influenced by rainfall and temperature. The lack of information about weather conditions and distance from faecal pats of each sample could explain the inconsistent recovery of our pasture larval counts. It must also be noted that as larvae also migrate into the upper layers of the soil, those obtained from the grass only represent a proportion of the total on the pasture.
The computationally intensive statistical techniques used in this paper are increasingly being recommended for use in parasitology[38, 39]. The long-standing advice for analysis of FWEC data has been to use a generalized linear model (GLM) with an over-dispersed (commonly negative binomial) response, because of the potential for erroneous inference associated with log transforming count observations. Bayesian methods have been shown to produce superior inference than older methods of analysis for FWEC data and for analysis of the faecal egg count reduction test (FECRT) data. The MCMC method used here is necessary to fit the latent class model required to describe the complex structure of the data. In particular, the combination of a latent class ARMA model with over-dispersed Poisson response and the additional complication of some missing observations would not have been possible using other modelling frameworks.
With a dosing threshold of 2,000 EPG in this population, the absolute effect of a 20% decrease in egg shedding could be as much as tenfold larger than would be expected in most equine holdings, which use a threshold in the region of 200 EPG. Because of this, and the potential subtle differences in life cycle between donkeys and horses, it is not clear to what extent these conclusions can be extrapolated to other situations; although for parasites with similar lifecycles it would be reasonable to expect a comparable decrease in pasture contamination. Such a decrease would allow less frequent dosing of animals, reducing the amount of anthelmintic used, and therefore slowing the development of anthelmintic resistance. This potentially justifies the expenditure of effort in pasture management in order to reduce the probability of treatment failure due to resistance for clinical cases of parasitism occurring when animals have become heavily parasitised. It is worth noting that FWEC can only be used as an indicator for the number of egg producing adult strongyles. An arbitrary figure of over 1,000 has been described as high, but donkeys in this study had FWEC in excess of 5,000 EPG without any observed clinical effects. It is possible that the potential for clinical disease is reduced in donkeys compared to horses.
Although the vast majority of the work on cyathostomins has been undertaken with horses and ponies, it is generally assumed that for the most part these findings apply to all equids providing that the management is similar. The life cycles of the small strongyles are very similar within the two species of equid; encystation of the larval stages is known to occur in the large intestine of horses[5, 34] and has also been found in donkeys[44, 45]. The reduction of FWEC to zero of donkeys dosed with ivermectin (via intramuscular injection) also appears to be in line with that previously noted in horses. These noted similarities suggest that despite this study being performed in donkeys, the findings and advice could be extended to other equids. If pasture hygiene is combined with strategic anthelmintic dosing, there may be excessive reduction of the cyathostomin population in refugia. This might increase the likelihood of anthelmintic resistance but there is no evidence basis on which we can truly assess the impact of faecal removal on refugia. Certainly, it might be appropriate to increase the arbitrary dosing threshold FWEC of 200 EPG[2, 10] in situations when high level parasite hygiene is performed concurrently with an anthelmintic dosing programme.
Evidence of increased FWEC with donkey age suggests a reduced capability to naturally deal with cyathostomins as an animal gets older. Previous findings in younger horses, however, have found FWEC to decrease with age, but then increase again with older horses. With only 9 of the 345 donkeys studied under 6 years old (and 85% over 10 years old) these findings are only applicable for middle aged to older donkeys, with a linear effect being less appropriate for a larger age range.
In summary, we have demonstrated and quantified the effectiveness of twice weekly removal of faeces as an adjunct to nematode control in donkeys in a geographical region with a temperate climate and moderate rainfall. These findings support the frequently-given advice to use pasture hygiene for helminth control in equids[17, 48], and suggest that a substantial reduction in anthelmintic usage can be achieved. This will result in a reduction in the selection pressure for anthelmintic resistance, potentially prolonging the useful lifespan of the currently effective drugs.
Twice weekly removal of faecal material from pasture significantly reduced the number of strongyle eggs shed in faeces from groups of co-grazed donkeys. This statistically verifies this form of pasture hygiene as a useful management based control of strongyles in equines. Use of this management control reduces the reliance and use of anthelmintic drugs, reducing the selection pressure towards cyathostomin resistance against these drugs.
This study had financial support from The Donkey Sanctuary in Devon. We would also like to thank The Donkey Sanctuary’s research staff and laboratory team for performing the faecal worm egg counts and collecting the pasture samples and Mr James McGoldrick for counting the pasture samples. Thanks to Nicole Du Toit and Andrew Trawford for their guidance and support at the inception of this project.
- von Samson-Himmelstjerna G: Anthelmintic resistance in equine parasites - detection, potential clinical relevance and implications for control. Vet Parasitol. 2012, 185: 2-8. 10.1016/j.vetpar.2011.10.010.View ArticlePubMedGoogle Scholar
- Nielsen MK, Vidyashankar AN, Olsen SN, Monrad J, Thamsborg SM: Strongylus vulgaris associated with usage of selective therapy on Danish horse farms — Is it reemerging?. Vet Parasitol. 2012, 189: 260-266. 10.1016/j.vetpar.2012.04.039.View ArticlePubMedGoogle Scholar
- Brady HA, Nichols WT: Drug resistance in equine parasites: an emerging global problem. J Equine Vet Sci. 2009, 29: 285-295. 10.1016/j.jevs.2009.04.186.View ArticleGoogle Scholar
- Love S, Duncan JL: Could the worms have turned?. Equine Vet J. 1991, 23: 152-154. 10.1111/j.2042-3306.1991.tb02745.x.View ArticlePubMedGoogle Scholar
- Kaplan RM: Anthelmintic resistance in nematodes of horses. Vet Res. 2002, 33: 491-507. 10.1051/vetres:2002035.View ArticlePubMedGoogle Scholar
- Trawford AF, Burden FA: Drug resistant cyathostomins in donkey herds; lessons in management for All equids. J Equine Vet Sci. 2012, 32: 43-View ArticleGoogle Scholar
- Herd RP: Control strategies for ruminant and equine parasites to counter resistance, encystment, and ecotoxicity in the USA. Vet Parasitol. 1993, 48: 327-336. 10.1016/0304-4017(93)90166-K.View ArticlePubMedGoogle Scholar
- Earle CG, Kington HA, Coles GC: Helminth control used by trainers of thoroughbreds in England. Vet Rec. 2002, 150: 405-408. 10.1136/vr.150.13.405.View ArticlePubMedGoogle Scholar
- Relf VE, Morgan ER, Hodgkinson JE, Matthews JB: A questionnaire study on parasite control practices on UK breeding thoroughbred studs. Equine Vet J. 2012, 44: 466-471. 10.1111/j.2042-3306.2011.00493.x.View ArticlePubMedGoogle Scholar
- Relf VE, Morgan ER, Hodgkinson JE, Matthews JB: Helminth egg excretion with regard to age, gender and management practices on UK thoroughbred studs. Parasitology. 2013, 140: 641-652. 10.1017/S0031182012001941.View ArticlePubMedGoogle Scholar
- Wood ELD, Matthews JB, Stephenson S, Slote M, Nussey DH: Variation in fecal egg counts in horses managed for conservation purposes: individual egg shedding consistency, age effects and seasonal variation. Parasitology. 2013, 140: 115-128. 10.1017/S003118201200128X.View ArticlePubMedGoogle Scholar
- Molnar V, Kassai T: The distribution of nematode egg counts and larval counts in grazing sheep and their implications for parasite control. Vet Parasitol. 1994, 24 (I): 103-108.Google Scholar
- Nielsen MK, Haaning N, Olsen SN: Strongyle egg shedding consistency in horses on farms using selective therapy in Denmark. Vet Parasitol. 2006, 135: 333-335. 10.1016/j.vetpar.2005.09.010.View ArticlePubMedGoogle Scholar
- Lyons ET, Tolliver SC, Drudge JH: Historical perspective of cyathostomes: prevalence, treatment and control programs. Vet Parasitol. 1999, 85: 97-111. 10.1016/S0304-4017(99)00091-6. discussion 111–2, 215–25View ArticlePubMedGoogle Scholar
- Matthews JB: An update on cyathostomins: anthelmintic resistance and worm control. Equine Vet Educ. 2008, 20: 552-560. 10.2746/095777308X363912.View ArticleGoogle Scholar
- Molento MB, Antunes J, Bentes RN, Coles GC: Anthelmintic resistant nematodes in Brazilian horses. Vet Rec. 2008, 162: 384-385. 10.1136/vr.162.12.384.View ArticlePubMedGoogle Scholar
- Hinney B, Wirtherle NC, Kyule M, Miethe N, Zessin K-H, Clausen P-H: A questionnaire survey on helminth control on horse farms in Brandenburg, Germany and the assessment of risks caused by different kinds of management. Parasitol Res. 2011, 109: 1625-1635. 10.1007/s00436-011-2434-0.View ArticlePubMedGoogle Scholar
- Krecek RC, Waller PJ: Towards the implementation of the “basket of options” approach to helminth parasite control of livestock: emphasis on the tropics/subtropics. Vet Parasitol. 2006, 139: 270-282. 10.1016/j.vetpar.2006.04.018.View ArticlePubMedGoogle Scholar
- Francisco R, Paz-Silva A, Francisco I, Cortiñas FJ, Miguélez S, Suárez JL, Cazapal-Monteiro CF, Arias MS, Sánchez-Andrade R: Preliminary analysis of the results of selective therapy against strongyles in pasturing horses. J Equine Vet Sci. 2012, 32: 274-280. 10.1016/j.jevs.2011.09.074.View ArticleGoogle Scholar
- Nielsen MK, Kaplan RM, Thamsborg SM, Monrad J, Olsen SN: Climatic influences on development and survival of free-living stages of equine strongyles: implications for worm control strategies and managing anthelmintic resistance. Vet J. 2007, 174: 23-32. 10.1016/j.tvjl.2006.05.009.View ArticlePubMedGoogle Scholar
- Ramsey YH, Christley RM, Matthews JB, Hodgkinson JE, McGoldrick J, Love S: Seasonal development of Cyathostominae larvae on pasture in a northern temperate region of the United Kingdom. Vet Parasitol. 2004, 119: 307-318. 10.1016/j.vetpar.2003.11.014.View ArticlePubMedGoogle Scholar
- Ogbourne CP: Survival on herbage plots of infective larvae of strongylid nematodes of the horse. J Helminthol. 1973, 47: 9-16. 10.1017/S0022149X00023695.View ArticlePubMedGoogle Scholar
- Matthee S, Krecek RC, Milne SA, Boshoff M, Guthrie AJ: Impact of management interventions on helminth levels, and body and blood measurements in working donkeys in South Africa. Vet Parasitol. 2002, 107: 103-113. 10.1016/S0304-4017(02)00113-9.View ArticlePubMedGoogle Scholar
- Paraud C, Hoste H, Lefrileux Y, Pommaret A, Paolini V, Pors I, Chartier C: Administration of Duddingtonia flagrans chlamydospores to goats to control gastro-intestinal nematodes: dose trials. Vet Res. 2005, 36: 157-166. 10.1051/vetres:2004060.View ArticlePubMedGoogle Scholar
- Waller PJ: International approaches to the concept of integrated control of nematode parasites of livestock. Int J Parasitol. 1999, 29: 155-164. 10.1016/S0020-7519(98)00178-7. discussion 183–4View ArticlePubMedGoogle Scholar
- Matthews JB, Burden FA: Common helminth infections of donkeys and their control in temperate regions. Equine Vet Educ. 2013, 25 (9): 461-467. 10.1111/eve.12018.View ArticleGoogle Scholar
- MAFF: Manual of veterinary parasitological laboratory techniques. 1986, London: HMSO, 166-Google Scholar
- Jorgensen RJ: Isolation of infective Dictyocaulus Larvae from herbage. Vet Parasitol. 1975, 1: 61-67. 10.1016/0304-4017(75)90008-4.View ArticleGoogle Scholar
- Plummer M: Just Another Gibbs Sampler (JAGS). 2008Google Scholar
- R Core Team: R: A language and environment for statistical computing. 2013Google Scholar
- Denwood MJ: runjags: Run Bayesian MCMC models in the BUGS syntax from within R. 2013Google Scholar
- Spiegelhalter DJ, Best NG, Carlin BP, Van Der Linde A: Bayesian measures of model complexity and fit. J R Stat Soc Ser B (Statistical Methodol). 2002, 64: 583-639. 10.1111/1467-9868.00353.View ArticleGoogle Scholar
- Herd RP: Epidemiology and control of equine strongylosis at newmarket. Equine Vet J. 1986, 18: 447-452. 10.1111/j.2042-3306.1986.tb03684.x.View ArticlePubMedGoogle Scholar
- Matthee S, McGeoch MA: Helminths in horses: use of selective treatment for the control of strongyles. J S Afr Vet Assoc. 2004, 75: 129-136.View ArticlePubMedGoogle Scholar
- Durie PH: Parasitic gastro-enteritis of cattle: the distribution and survival of infective strongyle larvae on pasture. Aust J Agric Res. 1961, 12: 1200-1211. 10.1071/AR9611200.View ArticleGoogle Scholar
- English AW: The epidemiology of equine strongylosis in Southern Queensland 1. The Bionomics of the free-living stages in faeces and on pasture. Aust Vet J. 1979, 55: 299-305. 10.1111/j.1751-0813.1979.tb00413.x.View ArticlePubMedGoogle Scholar
- Larsen M: Biological control of helminths. Int J Parasitol. 1999, 29: 139-146. 10.1016/S0020-7519(98)00185-4.View ArticlePubMedGoogle Scholar
- Basáñez MG, Marshall C, Carabin H, Gyorkos T, Joseph L: Bayesian statistics for parasitologists. Trends Parasitol. 2004, 20: 85-91. 10.1016/j.pt.2003.11.008.View ArticlePubMedGoogle Scholar
- Paterson S, Lello J: Mixed models: getting the best use of parasitological data. Trends Parasitol. 2003, 19: 370-375. 10.1016/S1471-4922(03)00149-1.View ArticlePubMedGoogle Scholar
- Wilson K, Grenfell BT: Generalized linear modelling for parasitologists. Parasitol Today. 1997, 13: 33-38. 10.1016/S0169-4758(96)40009-6.View ArticlePubMedGoogle Scholar
- O’Hara RB, Kotze DJ: Do not log-transform count data. Methods Ecol Evol. 2010, 1: 118-122. 10.1111/j.2041-210X.2010.00021.x.View ArticleGoogle Scholar
- Denwood MJ, Stear MJ, Matthews L, Reid SWJ, Toft N, Innocent GT: The distribution of the pathogenic nematode Nematodirus battus in lambs is zero-inflated. Parasitology. 2008, 135: 1225-1235.View ArticlePubMedGoogle Scholar
- Denwood MJ, Reid SWJ, Love S, Nielsen MK, Matthews L, McKendrick IJ, Innocent GT: Comparison of three alternative methods for analysis of equine faecal Egg count reduction test data. Prev Vet Med. 2010, 93: 316-323. 10.1016/j.prevetmed.2009.11.009.View ArticlePubMedGoogle Scholar
- Matthee S, Krecek RC, Guthrie AJ: Effect of management interventions on the helminth parasites recovered from donkeys in South Africa. J Parasitol. 2002, 88: 171-179.View ArticlePubMedGoogle Scholar
- Oryan A, Farjani Kish G, Rajabloo M: Larval cyathostominosis in a working donkey. J Parasit Dis. 2013,http://link.springer.com/journal/12639/onlineFirst/page/6,Google Scholar
- Seri HI, Abakar AD, Abdelrahman A, Tigani TA: Efficacy of Ivermectin in an injectable formulation against gastrointestinal nematodes of donkeys ( Equus asinus ). Vet Arh. 2005, 75: 369-374.Google Scholar
- Döpfer D, Kerssens CM, Meijer YGM, Boersema JH, Eysker M: Shedding consistency of strongyle-type eggs in Dutch boarding horses. Vet Parasitol. 2004, 124: 249-258. 10.1016/j.vetpar.2004.06.028.View ArticlePubMedGoogle Scholar
- Von S-HG, Traversa D, Demeler J, Rohn K, Milillo P, Schurmann S, Lia R, Perrucci S, Di Regalbono AF, Beraldo P, Barnes H, Cobb R, Boeckh A: Effects of worm control practices examined by a combined faecal egg count and questionnaire survey on horse farms in Germany, Italy and the UK. Parasit Vectors. 2009, 2 Suppl 2: S3-Google Scholar
This article is published under license to BioMed Central Ltd. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.