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Prevalence of gastrointestinal helminths and anthelmintic resistance on small-scale farms in Gauteng Province, South Africa

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Abstract

The present study was conducted to determine the prevalence and distribution of gastrointestinal helminths, to detect the presence of anthelmintic resistance in livestock from small-scale farms and to determine the level of helminthosis awareness among small-scale farmers in Gauteng Province, South Africa. Blood and faecal samples were collected from cattle (n = 314), sheep (n = 256) and goats (n = 311). Faecal egg counts and cultures were done, helminth genera identified and packed cell volume was assessed to detect anaemia. A faecal egg count reduction test was used to determine anthelmintic resistance against albendazole (7.5 mg/kg), levamisole (5 mg/kg) and ivermectin (0.2 mg/kg) on five small ruminant farms. A high prevalence of both nematodes and trematodes was observed; however, only 1 % of cattle had high nematode egg counts compared to goats (30 %) and sheep (32 %). Only 5 % of the animals were anaemic. Haemonchus and Calicophoron were the most dominant helminth genera in the studied ruminants. Anthelmintic resistance was detected against the three tested drugs on all the screened farms, except against albendazole and levamisole in sheep from Hammanskraal and Nigel, respectively. About 88 % of interviewed farmers were aware of veterinary helminthosis, 67 % treated against helminths and 83 % provided their livestock with nutritional supplements. This study showed that a high prevalence of helminthosis and anthelmintic resistance does occur in the study area, thus relevant strategic interventions are recommended.

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References

  • Ademola, I.O., Eloff, J.N., 2010. In vitro anthelmintic activity of Combretum molle (R.Br. ex G. Don) (Combretaceae) against Haemonchus contortus ova and larvae. Veterinary Parasitology, 169, 198–203.

    Article  PubMed  CAS  Google Scholar 

  • Bakunzi, F.R., 2003. Anthelminic resistance of nematodes in communally grazed goats in a semi-arid area of South Africa. Journal of the South African Veterinary Association, 74, 82–83.

    Article  PubMed  CAS  Google Scholar 

  • Bakunzi, F.R., 2008. Efficacy of 3 anthelmintics in communally grazed sheep as reflected by faecal egg count reduction tests in a semi arid area of South Africa. Journal of the South African Veterinary Association, 79, 54–5.

    Article  PubMed  CAS  Google Scholar 

  • Bath, G.F., Malan, F.S., van Wyk, J.A., 1996. The FAMACHA© ovine anaemia guide to assist with the control of haemonchosis. In: Proceedings of the 7th Annual Congress of Livestock Health and Production Group of the South African Veterinary Association, Port Elizabeth, June 5–7. p. 5.

  • Boomker, J., Horak, I.G., Ramsay, K.A., 1994. Helminth and arthropod parasites of indigenous goats in the northern Transvaal. Onderstepoort Journal of Veterinary Research, 61, 13–20.

    PubMed  CAS  Google Scholar 

  • Bricarello, P.A., Amarante, A.F.T., Rocha, R.A., Cabral Filho, S.L., Huntley, J.F., Houdijk, J.G.M., Abdalla, A.L., Gennari, S.M., 2005. Influence of dietary protein supply on resistance to experimental infections with Haemonchus contortus in Ile de France and Santa Ines lambs. Veterinary Parasitology, 134, 99–109.

    Article  PubMed  CAS  Google Scholar 

  • Busch, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W., 1997. Parasitology meets ecology on its own terms: Margolis et al. revisited. Journal of Parasitology, 83, 575–583.

    Article  Google Scholar 

  • Carmichael, I., Visser, R., Schneider, D., Soll, M., 1987. Haemonchus contortus resistance to ivermectin. Journal of the South African Veterinary Association, 58, 93.

    PubMed  CAS  Google Scholar 

  • Coles, G.C., Bauer, C., Borgsteede, F.H.M., Geerts, S., Klei, T.R., Taylor, M.A., Waller, P.J. 1992. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P) methods for the detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology, 44, 35—44.

    Article  PubMed  CAS  Google Scholar 

  • Coles, G.C., Jackson, F., Pomroy, W.E., Prichard, R.K., Von Samson-Himmelstjerna, G., Silvestre, A., Taylor, M.A. Vercruysse, J., 2006. The detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary Parasitology, 136, 167–185.

    Article  PubMed  CAS  Google Scholar 

  • De Villiers, J.F., Gcumisa, S.T., Gumede, S.A., Thusi, S.P., Dugmore, T.J., Cole, M., Du Toit, J.F., Vatta, A.F., Stevens, C., 2009. Estimation of live body weight from the heart girth measurement in KwaZulu–Natal goats. Applied Animal Husbandry and Rural Development, 1, 1–8.

    Google Scholar 

  • Delannoy-Normand, A., Cortet, J., Cabaret, J., Neveu, C., 2010. A suite of genes expressed during transition to parasitic lifestyle in the trichostrongylid nematode Haemonchus contortus encode potentially secreted proteins conserved in Teladorsagia circumcincta. Veterinary Parasitology, 174, 106–114.

    Article  PubMed  CAS  Google Scholar 

  • Dorny, P., Stoliaroff, V., Charlier, J., Meas, S., Sorn, S., Chea, B., Holl, D., Van Aken, D., Vercruysse, J., 2011. Infections with gastrointestinal nematodes, Fasciola and Paramphistomum in cattle in Cambodia and their association with morbidity parameters. Veterinary Parasitology, 175, 293–299.

    Article  PubMed  Google Scholar 

  • Dreyer, K., Fourie, L.J., Kok, D.J., 1999. Assessment of cattle owner’s perceptions and expectations, and identification of constraints on production in a peri-urban, emerging environment. Onderstepoort Journal of Veterinary Research, 66, 95–102.

    PubMed  CAS  Google Scholar 

  • Dupuy, J., Chartier, C., Sutra, J.F., Alvinerie, M., 2001. Eprinomectin in dairy goats; dose influence on plasma levels and excretion in milk. Parasitology Research, 87, 294-298.

    Article  PubMed  CAS  Google Scholar 

  • El-Abdellati, A., Charlier, J., Geldhof, P., Lavecke, B., Demeler, J., von Samson-Himmelstjerna, G., Claerebout, E., Vercruysse, J., 2010. The use of a simplified faecal egg count reduction test for assessing anthelmintic efficacy on Belgian and German cattle farms. Veterinary Parasitology, 169, 352–357.

    Article  PubMed  CAS  Google Scholar 

  • Garg, R., Yadav, C.L., 2008. Genotyping of benzimidazoles susceptible and resistant alleles in different populations of Haemonchus contortus from Himalayan and sub-Himalayan regions of North Western India. Tropical Animal Health and Production, doi:10.1007/s11250-008-9292-5.

  • Grace, D., Humstedt, I., Sidibe, T., Randolph, P., Clansen, H., 2007. Comparing FAMACHA eye colour chart and hemoglobin colour scale for detecting anaemia and improving treatment of bovine trypanomosis in West Africa. Veterinary Parasitology, 14, 26–39.

    Article  Google Scholar 

  • Gray, G.D., Connell, J.G., Phimphachanhvongsod, V., 2012. Worms in smallholder livestock system: technologies and practices that make a difference. Veterinary Parasitology, 186, 124–131.

    Article  PubMed  CAS  Google Scholar 

  • Horak, I.G., 1966. The pathogenesis and symptoms of paramphistomiasis in sheep. Journal of the South African Veterinary Medical Association, 37, 428–430.

    Google Scholar 

  • Horak, I.G., 1978. Parasites of domestic and wild animals in South Africa. V. Helminths in sheep on dryland pasture on the Transvaal Highveld. Onderstepoort Journal of Veterinary Research, 45, 1–6.

    PubMed  CAS  Google Scholar 

  • Horak, I.G., Louw, J.P., 1977. Parasites of domestic and wild animals in South Africa. IV. Helminths in sheep on irrigated pasture on the Transvaal Highveld. Onderstepoort Journal of Veterinary Research, 44, 261–270.

    PubMed  CAS  Google Scholar 

  • Hoste, H., Sotiraki, S., Landau, S.Y., Jackson, F., Beveridge, I., 2010. Goat-nematode interactions: think differently! Trends in Parasitology, 26, 376–381.

    Article  PubMed  Google Scholar 

  • Jackson, F., Greer, A.W., Huntley, J., McAnulty, R.W., Bartley, D.J., Stanley, A., Stenhouse, L., Stankiewics, M., Sykes, A.R., 2004. Studies using Teladorsagia circumcinta in an in vitro direct challenge method using abomasal tissue explants. Veterinary Parasitology, 124, 73–89.

    Article  PubMed  CAS  Google Scholar 

  • Jackson, F., Varaday, M., Bartley, D.J., 2012. Managing anthelmintic resistance in goats—can we learn lessons from sheep? Small Ruminant Research, 103, 3–9.

    Article  Google Scholar 

  • Jurasek, M.E., Bishop-Stewart, J.K., Storey, B.E., Kaplan, R.M., Kent, M.L., 2010. Modification and further evaluation of a fluorescein-labeled peanut agglutinin test for identification of Haemonchus contortus eggs. Veterinary Parasitology, 169, 209–213.

    Article  PubMed  CAS  Google Scholar 

  • Kanyari, P.W.N., Kagira, J.M., Mhoma, R.J., 2009. Prevalence and intensity of endoparasites in small ruminants kept by farmers in Kisumu Municipality, Kenya. Livestock Research for Rural Development, 21, 1–10.

    Google Scholar 

  • Kochapakdee, S., Pandey, V.S., Pralomkan, W., Chlodumrongkul, S., Ngampongsai, W., Lawpetchara, A., 1995. Anthelmintic resistance in goats in southern Thailand. Veterinary Record, 137, 124–125.

    Article  PubMed  CAS  Google Scholar 

  • Leignel, V., Silvestre, A., Humbert, J.F., Cabaret, J., 2010. Alternation of anthelmintic treatments: a molecular evaluation for benzimidazole resistance in nematodes. Veterinary Parasitology, 172, 80–88.

    Article  PubMed  CAS  Google Scholar 

  • Lespine, A., Chartier, C., Hoste, H., Alvinerie, M., 2012. Endectocides in goats: pharmacology, efficacy and use conditions in the context of anthelmintic resistance. Small Ruminant Research, 103, 10–17.

    Article  Google Scholar 

  • Malan, F.S., Van Wyk, J.A., Wessels, C.D., 2001. Clinical evaluation of anaemia in sheep: early trials. Onderstepoort Journal of Veterinary Research, 61, 165–174.

    Google Scholar 

  • Mederos, A., Fernandez, S., Van Leeuwen, J., Peregrine, A.S., Kelton, D., Menzies, P., LeBoeuf, A., Martin, R., 2010. Prevalence and distribution of gastrointestinal nematodes on 32 organic and conventional commercial sheep farms in Ontario and Quebec, Canada (2006–2008). Veterinary Parasitology, 170, 244–252.

    Article  PubMed  CAS  Google Scholar 

  • NCCLS, 2000. Procedure for determining packed cell volume by the microhematocrit method. Approved standard, 3rd ed. NCCLS document H7-A3 (ISBN 1-56238-413-9).

  • Paolini, V., De La Farge, F., Prevot, F., Dorchies, Ph., Hoste, H., 2005. Effects of the repeated distribution of sainfoin hay on the resistance and the resilience of goats naturally infected with gastrointestinal nematodes. Veterinary Parasitology, 127, 277–283.

    Article  PubMed  CAS  Google Scholar 

  • Payne, R.W., Murray, D.D.A., Harding, S.A., 2010. An introduction to the GenStat Command Language (13th edition). VSN International, Hemel Hempstead, UK.

    Google Scholar 

  • Rayner, A.A., 1969. A first course in Biometry for agriculture students. University of Natal Press, Pietermaritzburg.

    Google Scholar 

  • Reinecke, R.K., 1983. Veterinary helminthology. Butterworths: Oxford, UK.

    Google Scholar 

  • Rinaldi, L., Veneziano, V., Morgoglione, M.E., Pennacchio, S., Santaniello, M., Schioppi, M., Musella, V., Fedele, V., Cringoli, G., 2009. Is gastrointestinal strongyle faecal egg count influenced by hour of sample collection and worm burden in goats? Veterinary Parasitology, 163, 81–86.

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute, Inc. (1999), SAS/STAT user’s guide, version 9, 1st printing, volume 2. SAS Institute Inc, SAS Campus Drive, Cary, North Carolina 27513.

    Google Scholar 

  • Suarez, V.H., 2002. Helminthic control of grazing ruminants and environmental risks in South America. Veterinary Research, 33, 563–573.

    Article  PubMed  CAS  Google Scholar 

  • Torres-Acosta, J.F.J., Mendoza-de-Gives, P., Aguilar-Caballero, A.J., Cuellar-Ordaz, J.A., 2012. Anthelmintic resistance in sheep farms: update of the situation in the American continent. Veterinary Parasitology 189(1):89–96.

    Article  PubMed  CAS  Google Scholar 

  • Tsotetsi, A.M., Mbati, P.A., 2003. Parasitic helminths of veterinary importance in cattle, sheep and goats on communal farms in the north eastern Free State, South Africa. Journal of the South African Veterinary Association, 74, 45–48.

    Article  PubMed  CAS  Google Scholar 

  • Van Wyk, J.A., Malan, F.S., 1988. Resistance of field strains of Haemonchus contortus to ivermectin, closantel, rafoxanide and the benzimidazoles in South Africa. Veterinary Record, 123, 226–228.

    Article  PubMed  Google Scholar 

  • Van Wyk, J.A., Malan, F.S., Gerber, H.M., Alves, R.M.R., 1987. Two field strains of Haemonchus contortus resistant to rafoxanide. Onderstepoort Journal of Veterinary Research, 54, 143–146.

    PubMed  Google Scholar 

  • Van Wyk, J.A., Malan, F.S., Randles, J.L., 1997. How long before resistance makes it impossible to control some field strains of Haemonchus contortus in South Africa with any of the anthelmintics? Veterinary Parasitology, 70, 111–112.

    Article  PubMed  Google Scholar 

  • Van Wyk, J.A. Stenson, M.O., Van der Merwe, J.S., Vorster, R.J., Viljoen, P.G., 1999. Anthelmintic resistance in South Africa: surveys indicate an extremely serious situation in sheep and goat farming. Onderstepoort Journal of Veterinary Research, 66, 273–284.

    PubMed  Google Scholar 

  • Van Wyk, J.A., Cabaret, J., Michael, L.M., 2004. Morphological identification of nematode larvae of small ruminants and cattle simplified. Veterinary Parasitology, 119, 277–306.

    Article  PubMed  Google Scholar 

  • Van Wyk, J.A., Hoste, H., Kaplan, R.M., Besier, R.B., 2006. Targeted selective treatment for worm management—how do we sell rational programs to farmers? Veterinary Parasitology, 139, 336–346.

    Article  PubMed  Google Scholar 

  • Vatta, A.F., Lindberg, A.L.E., 2006. Managing anthelmintic resistance in small ruminant livestock of emerging farmers in South Africa. Journal of the South African Veterinary Association, 77, 2–8.

    Article  Google Scholar 

  • Vatta, A.F., Letty, B.A., Van der Linde, M.J., Van Wijk, E.F., Hansen, J.W., Krecek, R.C., 2001. Testing for clinical anaemia caused by Haemonchus spp. in goats farmed under resource-poor conditions in South Africa using an eye colour chart developed for sheep. Veterinary Parasitology, 99, 1–14.

    Article  PubMed  CAS  Google Scholar 

  • Vatta, A.F., Krecek, R.C., Letty, B.A., van der Linde, M.J., Grimbeek, R.J., de Villiers, J.F., Motswatswe, P.W., Molebiemang, G.S., Boshoff, H.M., Hansen, J.W., 2002. Incidence of Haemonchus spp. and effect on haematocrit and eye colour in goats farmed under resource-poor conditions in South Africa. Veterinary Parasitology, 103, 119–131.

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank various colleagues for their constructive suggestions and the Gauteng Department of Agriculture and Rural Development (GDARD) for funding the project. The GDARD animal health technicians (John Manganye, William Kutu, Theo Serebolo, Thato Motlhaga, Malebo Molosiwa, Tsholofelo Mojanaga, Tsholanang Mojanaga, Sandy Moale, Sipho Nyambi, Jacob Monametsi, Emmanuel Hlatshwayo, Lucky Maphale and James Leshabane) and the Agricultural Research Council, Onderstepoort Veterinary Institute (ARC-OVI) Parasites, Vectors and Vector-Borne Diseases Programme technicians (Daniel Chipana, Frans Masubelle, David Letsoalo and Ellen Van Wijk) are acknowledged for technical assistance both in the field and laboratory. Our deepest gratitude goes to the Gauteng small-scale farmers for their cooperation, Dr Roy Williams (ARC-OVI) for map production and Liesl Morey and Frikkie Calitz (ARC-Biometry) for statistical analysis.

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  1. Agricultural Research Council, Onderstepoort Veterinary Institute, Onderstepoort, 0110, South Africa

    Ana Mbokeleng Tsotetsi & Stephen Njiro

  2. Gauteng Department of Agriculture and Rural Development, Gauteng Veterinary Services, Pretoria, 0001, South Africa

    Tendai Charles Katsande, Gugulethu Moyo, Faculty Baloyi & Jaison Mpofu

  3. Parasites, Vectors and Vector-Borne Diseases Programme, Agricultural Research Council, Onderstepoort Veterinary Institute, Private Bag X 05, Onderstepoort, 0110, South Africa

    Ana Mbokeleng Tsotetsi

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  1. Ana Mbokeleng Tsotetsi
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Correspondence to Ana Mbokeleng Tsotetsi.

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Tsotetsi, A.M., Njiro, S., Katsande, T.C. et al. Prevalence of gastrointestinal helminths and anthelmintic resistance on small-scale farms in Gauteng Province, South Africa. Trop Anim Health Prod 45, 751–761 (2013). https://doi.org/10.1007/s11250-012-0285-z

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