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Helminth egg excretion with regard to age, gender and management practices on UK Thoroughbred studs

Published online by Cambridge University Press:  25 January 2013

V. E. RELF ,
E. R. MORGAN ,
J. E. HODGKINSON  and
J. B. MATTHEWS
V. E. RELF*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Midlothian EP26 0PZ, UK
E. R. MORGAN
Affiliation:
School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK
J. E. HODGKINSON
Affiliation:
Institute of Infection and Global Health, University of Liverpool, Liverpool L3 5RF, UK
J. B. MATTHEWS
Affiliation:
Moredun Research Institute, Pentlands Science Park, Midlothian EP26 0PZ, UK
*
* Corresponding author: Moredun Research Institute, Pentlands Science Park, Midlothian EP26 0PZ, UK. Tel: +44 131 445 5111. Fax: +44 131 445 6235. E-mail: valerie.relf@moredun.ac.uk
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Summary

Few studies have described the combined effect of age, gender, management and control programmes on helminth prevalence and egg shedding in grazing equines. Here, fecal samples collected from 1221 Thoroughbred horses, residing at 22 studs in the UK, were analysed. The distribution of strongyle eggs amongst individuals in relation to age, gender and management practices was investigated. Fecal worm egg counts (FWECs), described as the number of eggs per gramme (epg) of feces, were determined using a modification of the salt flotation method. The FWEC prevalence (mean%) of strongyles, Parascaris equorum, tapeworm spp. and Strongyloides westeri was 56, 9, 4 and 8%, respectively. Strongyle, P. equorum, tapeworm spp. and S. westeri infections were detected on 22 (100%), 11 (50%), 9 (41%) and 8 (36%) of studs, respectively. Within all age and gender categories, strongyle FWECs were highly over-dispersed (arithmetic mean = 95 epg, aggregation parameter k=0·111) amongst horses. Animal age, last anthelmintic type administered and management practices (for example, group rotation on grazing) most strongly influenced strongyle prevalence and level of egg shedding (P < 0·05). Overall, 11% of equines (range: 234–2565 epg) were responsible for excreting 80% of the strongyle eggs detected on FWEC analysis. The results confirm that the judicious application of targeted treatments has potential to control equine strongyle populations by protecting individual horses from high burdens, whilst promoting refugia for anthelmintic susceptible genotypes.

Keywords

horsehelminthsprevalencefecal egg sheddingagegendermanagement practicesaggregation

Information

Type
Research Article
Information
Parasitology , Volume 140 , Issue 5 , April 2013 , pp. 641 - 652
Copyright
Copyright © Cambridge University Press 2013

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References

REFERENCES

Becher, A. M., Mahling, M., Nielsen, M. K. and Pfister, K. (2010). Selective anthelmintic therapy of horses in the Federal states of Bavaria (Germany) and Salzburg (Austria): An investigation into strongyle egg shedding consistency. Veterinary Parasitology 171, 116–122.Google Scholar
Beelitz, P., Göbel, E. and Gothe, R. (1996). Spectrum of species and incidence of endoparasites in foals and their mother mares from breeding farms with and without anthelmintic prophylaxis in upper Bavaria. Tierärztliche Praxis 24, 48–54.Google Scholar
Boersema, J. H., Eysker, M., Maas, J. and van der Aar, W. M. (1996). Comparison of the reappearance of strongyle eggs on foals, yearlings and adult horses after treatment with ivermectin or pyrantel. Veterinary Quarterly 18, 7–9.Google Scholar
Bouman, A., Heineman, M. J. and Faas, M. M. (2005). Sex hormones and the immune response in humans. Human Reproduction Update 11, 411–423. doi: 10.1093/humupd/dmi008.Google Scholar
Bucknell, D. G., Gasser, R. B. and Beveridge, I. (1995). The prevalence and epidemiology of gastrointestinal parasites of horses in Victoria, Australia. International Journal for Parasitology 25, 711–724.Google Scholar
Döpfer, D., Kerssens, C. M., Meijer, Y. G. M., Boersema, J. H. and Eysker, M. (2004). Shedding consistency of strongyle-type eggs in Dutch boarding horses. Veterinary Parasitology 124, 249–258.Google Scholar
Epe, C., Coati, N. and Schnieder, T. (2004). Results of parasitological examinations of faecal samples from horses, ruminants, pigs, dogs, cats, hedgehogs and rabbits between 1998 and 2002. Deutsche Tierärztlicher Wochenschrift 111, 243–247.Google Scholar
Epe, C., Ising-Volmer, S. and Stoye, M. (1993). Parasitological fecal studies of equids, dogs, cats and hedgehogs during the years 1984–1991. Deutsche Tierärztlicher Wochenschrift, 100, 426–428.Google Scholar
Eysker, M., Bakker, J., van den Berg, M., van Doorn, D. C. K. and Ploeger, H. W. (2008). The use of age-clustered pooled faecal samples for monitoring worm control in horses. Veterinary Parasitology 151, 249–255.Google Scholar
Eysker, M., Boersema, J. H. and Kooyman, F. N. J. (1992). The effect of ivermectin treatment against inhibited early third stage, late third stage and fourth stage larvae and adult stages of the cyathostomes in Shetland ponies and spontaneous expulsion of these helminths. Veterinary Parasitology 42, 295–302.Google Scholar
Fritzen, B., Rohn, K., Schnieder, T. and Von Samson-Himmelstjerna, G. (2010). Endoparasite control management on horse farms – lessons from worm prevalence and questionnaire data. Equine Veterinary Journal 42, 79–83. doi: 10.2746/042516409x471485.Google Scholar
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites. Science 218, 384–387.Google Scholar
Herd, R. P. and Willardson, K. L. (1985). Seasonal distribution of infective strongyle larvae on horse pastures. Equine Veterinary Journal 17, 235–237. doi: 10.1111/j.2042-3306.1985.tb02481.x.Google Scholar
Hilborn, R. and Mangel, M. (1997). The Ecological Detective: Confronting Models with Data, Princeton University Press, Princeton, NJ, USA.Google Scholar
Hinney, B., Wirtherle, N., Kyule, M., Miethe, N., Zessin, K.-H. and Clausen, P.-H. (2011). Prevalence of helminths in horses in the state of Brandenburg, Germany. Parasitology Research 108, 1083–1091. doi: 10.1007/s00436-011-2362-z.Google Scholar
Höglund, J., Ljungström, B. L., Nilsson, O., Lundquist, H., Osterman, E. and Uggla, A. (1997). Occurrence of Gasterophilus intestinalis and some parasitic nematodes of horses in Sweden. Acta Veterinaria Scandinavica 38, 157–165.Google Scholar
Jackson, F. (1974). New technique for obtaining nematode ova from sheep faeces. Laboratory Practice 23, 65–66.Google Scholar
Jasko, D. J. and Roth, L. (1984). Granulomatous colitis associated with small strongyle larvae in a horse. Journal of the American Veterinary Medical Association 185, 553–554.Google Scholar
Kaplan, R. M. (2002). Anthelmintic resistance in nematodes of horses. Veterinary Research 33, 491–507.Google Scholar
Kaplan, R. M. (2004). Drug resistance in nematodes of veterinary importance: a status report. Trends in Parasitology 20, 477–481.Google Scholar
Klein, S. L. (2004). Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology 26, 247–264. doi: 10.1111/j.0141-9838.2004.00710.x.Google Scholar
Kornas, S., Cabaret, J., Skalska, M. and Nowosad, B. (2010). Horse infection with intestinal helminths in relation to age, sex, access to grass and farm system. Veterinary Parasitology 174, 285–291.Google Scholar
Kuzmina, T. A. and Kharchenko, V. O. (2008). Anthelmintic resistance in cyathostomins of brood horses in Ukraine and influence of anthelmintic treatments on strongylid community structure. Veterinary Parasitology 154, 277–288.Google Scholar
Kyvsgaard, N. C., Lindbom, J., Andreasen, L. L., Luna-Olivares, L. A., Nielsen, M. K. and Monrad, J. (2011). Prevalence of strongyles and efficacy of fenbendazole and ivermectin in working horses in El Sauce, Nicaragua. Veterinary Parasitology 181, 248–254.Google Scholar
Lamason, R., Zhao, P., Rawat, R., Davis, A., Hall, J., Chae, J., Agarwal, R., Cohen, P., Rosen, A., Hoffman, E. and Nagaraju, K. (2006). Sexual dimorphism in immune response genes as a function of puberty. BMC Immunology 7, 2.Google Scholar
Larsen, M., Lendal, S., Chriel, M., Olsen, S. and Bjorn, H. (2002). Risk factors for high endoparasitic burden and the efficiency of a single anthelmintic treatment of Danish horses. Acta Veterinaria Scandinavica 43, 99–106.Google Scholar
Leathwick, D. M., Miller, C. M., Atkinson, D. S., Haack, N. A., Waghorn, T. S. and Oliver, A. M. (2008). Managing anthelmintic resistance: Untreated adult ewes as a source of unselected parasites, and their role in reducing parasite populations. New Zealand Veterinary Journal 56, 184–195. doi: 10.1080/00480169.2008.36832.Google Scholar
Lind, E. O., Höglund, J., Ljungström, B. L., Nilsson, O. and Uggla, A. (1999). A field survey on the distribution of strongyle infections of horses in Sweden and factors affecting faecal egg counts. Equine Veterinary Journal 31, 68–72. doi: 10.1111/j.2042-3306.1999.tb03793.x.Google Scholar
Love, S., Murphy, D. and Mellor, D. (1999). Pathogenicity of cyathostome infection. Veterinary Parasitology 85, 113–122.Google Scholar
Ludwig, K. G., Craig, T. M., Bowen, J. M., Ansari, M. M. and Ley, W. B. (1983). Efficacy of ivermectin in controlling Strongyloides westeri infections in foals. American Journal of Veterinary Research 44, 314–316.Google Scholar
Lyons, E. T., Drudge, J. H. and Tolliver, S. C. (1973). On the life cycle of Strongyloides westeri in the equine. Journal of Parasitology 59, 780–787.Google Scholar
Lyons, E. T. and Tolliver, S. C. (2004). Prevalence of parasite eggs (Strongyloides westeri, Parascaris equorum and strongyles) and oocysts (Emeria leuckarti) in the feces of Thoroughbred foals on 14 farms in central Kentucky in 2003. Parasitology Research 92, 400–404. doi: 10.1007/s00436-003-1068-2.Google Scholar
Lyons, E. T., Tolliver, S. C., Harold Drudge, J., Granstrom, D. E. and Collins, S. S. (1993). Natural infections of Strongyloides westeri: prevalence in horse foals on several farms in central Kentucky in 1992. Veterinary Parasitology 50, 101–107.Google Scholar
Matthews, J. B. (2008). An update on cyathostomins: Anthelmintic resistance and worm control. Equine Veterinary Education 20, 552–560. doi: 10.2746/095777308x363912.Google Scholar
Mfitilodze, M. W. and Hutchinson, G. W. (1989). Prevalence and intensity of non-strongyle intestinal parasites of horses in northern Queensland. Australian Veterinary Journal 66, 23–26. doi: 10.1111/j.1751-0813.1989.tb09708.x.Google Scholar
Mfitilodze, M. W. and Hutchinson, G. W. (1990). Prevalence and abundance of equine strongyles (Nematoda: Strongyloidea) in tropical Australia. Journal of Parasitology 76, 487–494.Google Scholar
Ministry of Agriculture, Fisheries and Food (1986). Manual of Veterinary Parasitological Laboratory Techniques. In Reference Book 418 pp. 36–39. HMSO, London, UK.Google Scholar
Monteiro, R. V., Dietz, J. M., Beck, B. B., Baker, A. J., Martins, A. and Jansen, A. M. (2007). Prevalence and intensity of intestinal helminths found in free-ranging golden lion tamarins (Leontopithecus rosalia, Primates, Callitrichidae) from Brazilian Atlantic forest. Veterinary Parasitology 145, 77–85.Google Scholar
Morgan, E. R., Cavill, L., Curry, G. E., Wood, R. M. and Mitchell, E. S. E. (2005). Effects of aggregation and sample size on composite faecal egg counts in sheep. Veterinary Parasitology 131, 79–87.Google Scholar
Morgan, E. R. and Wall, R. (2009). Climate change and parasitic disease: farmer mitigation? Trends in Parasitology 25, 308–313.Google Scholar
Nielsen, M. K., Haaning, N. and Olsen, S. N. (2006). Strongyle egg shedding consistency in horses on farms using selective therapy in Denmark. Veterinary Parasitology 135, 333–335.Google Scholar
Nielsen, M. K., Kaplan, R. M., Thamsborg, S. M., Monrad, J. and Olsen, S. N. (2007). Climatic influences on development and survival of free-living stages of equine strongyles: Implications for worm control strategies and managing anthelmintic resistance. The Veterinary Journal 174, 23–32.Google Scholar
Osterman Lind, E., Hoglund, J., Ljungstrom, B., Nilsson, O. and Uggla, A. (1999). A field survey on the distribution of strongyle infections of horses in Sweden and factors affecting faecal egg counts. Equine Veterinary Journal 31, 68–72.Google Scholar
Proudman, C. J. and Edwards, G. B. (1992). Validation of a centrifugation/flotation technique for the diagnosis of equine cestodiasis. Veterinary Record 131, 71–72. doi: 10.1136/vr.131.4.71.Google Scholar
Reinemeyer, C. (2009). Diagnosis and control of anthelmintic-resistant Parascaris equorum . Parasites and Vectors 2(Suppl. 2), S8.Google Scholar
Relf, V. E., Morgan, E. R., Hodgkinson, J. E. and Matthews, J. B. (2012). A questionnaire study on parasite control practices on UK breeding Thoroughbred studs. Equine Veterinary Journal 44, 466–471. doi: 10.1111/j.2042-3306.2011.00493.x.Google Scholar
Shaw, D. J. and Dobson, A. P. (1995). Patterns of macroparasite abundance and aggregation in wildlife populations: a quantitative review. Parasitology 111(Suppl. S1), S111-S133.Google Scholar
Shaw, D. J., Grenfell, B. T. and Dobson, A. P. (1998). Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117, 597–610.Google Scholar
Sokal, R. and Rohlf, F. (1995). Biometry: The Principles and Practice of Statistics in Biological Research. W. H. Freeman and Co., New York, USA.Google Scholar
Stratford, C. H., McGorum, B. C., Pickles, K. J. and Matthews, J. B. (2011). An update on cyathostomins: Anthelmintic resistance and diagnostic tools. Equine Veterinary Journal 43, 133–139. doi: 10.1111/j.2042-3306.2011.00397.x.Google Scholar
Thienpont, D., Rochette, F. and Vanparijs, O. F. J. (1986). Diagnosing Helminthiasis by Coprological Examination, 2nd Edn. Janssen Research Foundation, Beerse, Belgium.Google Scholar
Torgerson, P. R., Paul, M. and Lewis, F. I. (2012). The contribution of simple random sampling to observed variations in faecal egg counts. Veterinary Parasitology 188, 397–401.Google Scholar
Torgerson, P. R., Schnyder, M. and Hertzberg, H. (2005). Detection of anthelmintic resistance: a comparison of mathematical techniques. Veterinary Parasitology 128, 291–298.Google Scholar
Traversa, D., Klei, T. R., Iorio, R., Paoletti, B., Lia, R. P., Otranto, D., Sparagano, O. A. E. and Giangaspero, A. (2007). Occurrence of anthelmintic resistant equine cyathostome populations in central and southern Italy. Preventive Veterinary Medicine 82, 314–320.Google Scholar
Uhlinger, C. (1992). Preliminary studies into factors affecting the variability of egg reappearance period and anthelmintic treatment intervals in the control of equine cyathostomes. In The 6th International Equine Infectious Diseases Conference pp. 157–161. R & W Publications Ltd, Newmarket, UK.Google Scholar
Uhlinger, C. (1993). Uses of faecal egg count data in equine practice. Compendium on Continuing Education for the Practicing Veterinarian 15, 742–748.Google Scholar
van Dijk, J., Sargison, N. D., Kenyon, F. and Skuce, P. J. (2010). Climate change and infectious disease: helminthological challenges to farmed ruminants in temperate regions. Animal 4, 377–392.Google Scholar
van Wyk, J. A. (2001). Refugia: overlooked as perhaps the most potent factor concerning the development of anthelmintic resistance. Onderstepoort Journal of Veterinary Research 68, 55–67.Google Scholar
Vidyashankar, A. N., Kaplan, R. M. and Chan, S. (2007). Statistical approach to measure the efficacy of anthelmintic treatment on horse farms. Parasitology 134, 2027–2039.Google Scholar
von Samson-Himmelstjerna, G. (2012). Anthelmintic resistance in equine parasites – detection, potential clinical relevance and implications for control. Veterinary Parasitology 185, 2–8.Google Scholar
Wessa, P. (2008). Maximum-likelihood Negative Binomial Distribution Fitting (v1.0.2) in Free Statistics Software (v1.1.23-r7). Office for Research Development and Education, URL http://www.wessa.net/rwasp_fitdistrnegbin.wasp/ Google Scholar
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