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Investigating the role of wild carnivores in the epidemiology of bovine neosporosis

Published online by Cambridge University Press:  15 October 2012

PETER STUART ,
ANNETTA ZINTL ,
THEO DE WAAL ,
GRACE MULCAHY ,
CONALL HAWKINS  and
COLIN LAWTON
PETER STUART*
Affiliation:
Finnish Forest Research Institute, Suonejoki Research Unit, Finland
ANNETTA ZINTL
Affiliation:
School of Veterinary Medicine, University College Dublin, Belfield, Dublin, Ireland
THEO DE WAAL
Affiliation:
School of Veterinary Medicine, University College Dublin, Belfield, Dublin, Ireland
GRACE MULCAHY
Affiliation:
School of Veterinary Medicine, University College Dublin, Belfield, Dublin, Ireland
CONALL HAWKINS
Affiliation:
Mammal Ecology Group, School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
COLIN LAWTON
Affiliation:
Mammal Ecology Group, School of Natural Sciences, National University of Ireland Galway, Galway, Ireland
*
*Corresponding author: Finnish Forest Research Institute, Suonejoki Research Unit, Finland. Tel: 00358 408015316. E-mail: peterdstuart@hotmail.com
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Summary

Neospora caninum is a protozoan parasite, primarily associated with bovine abortion. The only definitive hosts discovered to date are carnivores. This study aimed to identify the role of mammalian carnivores in the epidemiology of bovine neosporosis. A sample bank of serum, fecal and brain samples was established: American mink (Mustela vison), red foxes (Vulpes vulpes), pine martens (Martes martes), badgers (Meles meles), stoats (Mustela erminea), otters (Lutra lutra) and feral ferrets (Mustela putorius). Approximately 1% of mink and 1% of fox samples were positive by IFAT. According to PCR analysis of DNA extracted from brain tissue, 3% of the mink, 4% of the otters and 6% of the foxes examined were infected with N. caninum. All fecal samples tested negative for N. caninum DNA (n = 311), suggesting that the species that tested positive were intermediate not definitive hosts. This is the first time that tissues from mustelids have tested positive for N. caninum. The need to test 2 relatively large (∼200 mg) targeted parts of the brain to avoid false negatives was also identified. The relatively low prevalence of N. caninum in Irish carnivores suggests that the local ecology of a species has an important influence on its epidemiological role.

Keywords

Neospora caninumwildlifecarnivoremustelid
Type
Research Article
Information
Parasitology , Volume 140 , Issue 3 , March 2013 , pp. 296 - 302
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Almería, S., Ferrer, D., Pabón, M., Castellà, J. and Mañas, M. L. (2002). Red foxes (Vulpes vulpes) are natural intermediate hosts of Neospora caninum. Veterinary Parasitology 107, 287–294.CrossRefGoogle Scholar
Anderson, T., Dejardin, A., Howe, D. K., Dubey, J. P. and Michalski, M. L. (2007) Neospora caninum antibodies detected in Midwestern white-tailed deer (Odocoileus virginianus) by western blot ELISA. Vp 145, 152–155.Google Scholar
Antony, A. and Williamson, N. B. (2003). Prevalence of antibodies to Neospora caninum in dogs of rural or urban origin in central New Zealand. New Zealand Veterinary Journal 51, 232–237.CrossRefGoogle ScholarPubMed
Barber, J. S. and Trees, A. J. (1996). Clinical aspects of 27 cases of neosporosis in dogs. The Veterinary Record 139, 439–443.CrossRefGoogle ScholarPubMed
Barber, J. S., Gasser, R. B., Ellis, J., Reichel, M. P., McMillan, D. and Trees, A. J. (1997). Prevalence of antibodies to Neospora caninum in different canid populations. Journal of Parasitology 83, 1056–1058.CrossRefGoogle ScholarPubMed
Basso, W., Venturini, L., Venturini, M. C., Moore, P., Rambeau, M., Unzaga, J. M., Campero, C., Bacigalupe, D. and Dubey, J. P. (2001). Prevalence of Neospora caninum infection in dogs from beef-cattle farms, dairy farms, and from urban areas of Argentina. Journal of Parasitology 87, 906–907.CrossRefGoogle ScholarPubMed
Boom, R., Sol, C. J., Salimans, M. M., Jansen, C. L., Wertheim-Van Dillen, P. M. and Van Der Noordaa, J. (1990). Rapid and simple method for purification of nucleic acids. Journal of Clinical Microbiology 28, 495–503.CrossRefGoogle ScholarPubMed
Boyle, K. and Whelan, J. (1990). Changes in the diet of the badger Meles meles L. from autumn to winter. The Irish Naturalists' Journal 23, 199–202.Google Scholar
Buxton, D., Maley, S. W., Innes, E. A., Pastoret, P. P. and Brochier, B. (1997). Examination of red foxes (Vulpes vulpes) from Belgium for antibody to Neospora caninum and Toxoplasma gondii. The Veterinary Record 141, 308–309.CrossRefGoogle ScholarPubMed
Buxton, D., Maley, S. W., Wright, S., Thomson, K. M., Rae, A. G. and Innes, E. A. (1998). The pathogenesis of experimental neosporosis in pregnant sheep. Journal of Comparative Pathology 118, 267–279.CrossRefGoogle ScholarPubMed
Cleary, G. P., Corner, L. A. L., O'Keeffe, J. and Marples, N. M. (2009). The diet of the badger Meles meles in the Republic of Ireland. Mammalian Biology – Zeitschrift für Säugetierkunde 74, 438–447.CrossRefGoogle Scholar
De Marez, T., Liddell, S., Dubey, J. P., Jenkins, M. C. and Gasbarre, L. (1999). Oral infection of calves with Neospora caninum oocysts from dogs: humoral and cellular immune responses. International Journal for Parasitology 29, 1647–1657.CrossRefGoogle ScholarPubMed
Dijkstra, T., Eysker, M., Schares, G., Conraths, F. J., Wouda, W. and Barkema, H. W. (2001). Dogs shed Neospora caninum oocysts after ingestion of naturally infected bovine placenta but not after ingestion of colostrum spiked with Neospora caninum tachyzoites. International Journal for Parasitology 31, 747–752.CrossRefGoogle Scholar
Dubey, J. P., Carpenter, J. L., Speer, C. A., Topper, M. J. and Uggla, A. (1988). Newly recognized fatal protozoan disease of dogs. Journal of the American Veterinary Medical Association 192, 1269–1285.Google ScholarPubMed
Dubey, J. P., Jenkins, M. C., Rajendran, C., Miska, K., Ferreira, L. R., Martins, J., Kwok, O. C. H. and Choudhary, S. (2011). Gray wolf (Canis lupus) is a natural definitive host for Neospora caninum. Veterinary Parasitology 181, 382–387.CrossRefGoogle ScholarPubMed
Dubey, J. P., Lindsay, D. S., Adams, D. S., Gay, J. M., Baszler, T. V., Blagburn, B. L. and Thulliez, P. (1996). Serologic responses of cattle and other animals infected with Neospora caninum. American Journal of Veterinary Research 57, 329–336.Google ScholarPubMed
Dubey, J. P. and Schares, G. (2006). Diagnosis of bovine neosporosis. Veterinary Parasitology 140, 1–34.CrossRefGoogle ScholarPubMed
Dubey, J. P., Schares, G. and Ortega-Mora, L. M. (2007). Epidemiology and control of neosporosis and Neospora caninum. Clinical Microbiology Review 20, 323–367.CrossRefGoogle ScholarPubMed
Fairley, J. S. (1967). An indication of the food of the badger in North-East Ireland. The Irish Naturalists' Journal 15, 267–269.Google Scholar
Fairley, J. S. (2001). A Basket of Weasels. Published privately. Belfast, Northern Ireland.Google Scholar
Ferroglio, E., Pasino, M., Romano, A., Grande, D., Pregel, P. and Trisciuoglio, A. (2007). Evidence of Neospora caninum DNA in wild rodents. Veterinary Parasitology 148, 346–349.CrossRefGoogle ScholarPubMed
Gondim, L. F. P. (2006). Neospora caninum in wildlife. Trends in Parasitology 22, 247–252.CrossRefGoogle ScholarPubMed
Gondim, L. F. P., Gao, L. and McAllister, M. M. (2002). Improved production of Neospora caninum oocysts, cyclical oral transmission between dogs and cattle, and in vitro isolation from oocysts. Journal of Parasitology 88, 1159–1163.CrossRefGoogle ScholarPubMed
Gondim, L. F. P., McAllister, M. M., Mateus-Pinilla, N. E., Pitt, W. C., Mech, L. D. and Nelson, M. E. (2004 b). Transmission of Neospora caninum between wild and domestic animals. Journal of Parasitology 90, 1361–1365.CrossRefGoogle ScholarPubMed
Gondim, L. F. P., McAllister, M. M., Pitt, W. C. and Zemlicka, D. E. (2004 a). Coyotes (Canis latrans) are definitive hosts of Neospora caninum. International Journal for Parasitology 34, 159–161.CrossRefGoogle ScholarPubMed
Hamilton, C. M., Gray, R., Wright, S. E., Gangadharan, B., Laurenson, K., Innes, E. A. (2005). Prevalence of antibodies to Toxoplasma gondii and Neospora caninum in red foxes (Vulpes vulpes) from around the UK. Veterinary Parasitology 130, 169–173.CrossRefGoogle ScholarPubMed
Hewson, R. (1984). Scavening and predation upon sheep and lambs in West Scotland. Journal of Applied Ecology 21, 843–868.CrossRefGoogle Scholar
Ho, M. S. Y., Barr, B. C., Rowe, J. D., Anderson, M. L., Sverlow, K. W., Packham, A., Marsh, A. E. and Conrad, P. A. (1997). Detection of Neospora sp. from infected bovine tissues by PCR and probe hybridization. Journal of Parasitology 83, 508–514.CrossRefGoogle ScholarPubMed
Hobson, J. C., Duffield, T. F., Kelton, D., Lissemore, K., Hietala, S. K., Leslie, K. E., McEwen, B. and Peregrine, A. S. (2005). Risk factors associated with Neospora caninum abortion in Ontario Holstein dairy herds. Veterinary Parasitology 127, 177–188.CrossRefGoogle ScholarPubMed
Hughes, J. M., Thomasson, D., Craig, P. S., Georgin, S., Pickles, A. and Hide, G. (2008). Neospora caninum: Detection in wild rabbits and investigation of co-infection with Toxoplasma gondii by PCR analysis. Experimental Parasitology 120, 255–260.CrossRefGoogle ScholarPubMed
Hughes, J. M., Williams, R. H., Morley, E. K., Cook, D. A. N., Terry, R. S., Murphy, R. G., Smith, J. E. and Hide, G. (2006). The prevalence of Neospora caninum and co-infection with Toxoplasma gondii by PCR analysis in naturally occurring mammal populations. Parasitology 132, 29–36.CrossRefGoogle ScholarPubMed
Hurková, L. and Modrý, D. (2006). PCR detection of Neospora caninum, Toxoplasma gondii and Encephalitozoon cuniculi in brains of wild carnivores. Veterinary Parasitology 137, 150–154.CrossRefGoogle ScholarPubMed
Ibarra, J. T. S., Fasola, L., Macdonald, D. W., Rozzi, R. and Bonacic, C. N. (2009). Invasive American mink Mustela vison in wetlands of the Cape Horn Biosphere Reserve, southern Chile: what are they eating? Oryx 43, 87–90.CrossRefGoogle Scholar
Jakubek, E. B., Bröjer, C., Regnersen, C., Uggla, A., Schares, G. and Björkman, C. (2001). Seroprevalences of Toxoplasma gondii and Neospora caninum in Swedish red foxes (Vulpes vulpes). Veterinary Parasitology 102, 167–172.CrossRefGoogle ScholarPubMed
Jenkins, M. C., Parker, C., Hill, D., Pinckney, R. D., Dyer, R. and Dubey, J. P. (2007). Neospora caninum detected in feral rodents. Veterinary Parasitology 143, 161–165.CrossRefGoogle ScholarPubMed
King, J. S., Slapeta, J., Jenkins, D. J., Al-Qassab, S. E., Ellis, J. T. and Windsor, P. A. (2010). Australian dingoes are definitive hosts of Neospora caninum. International Journal for Parasitology 40, 945–950.CrossRefGoogle ScholarPubMed
Lasri, S., De Meerschman, F., Rettigner, C., Focant, C. and Losson, B. (2004). Comparison of three techniques for the serological diagnosis of Neospora caninum in the dog and their use for epidemiological studies. Veterinary Parasitology 123, 25–32.CrossRefGoogle ScholarPubMed
Lindsay, D. S., Dubey, J. P. and Duncan, R. B. (1999). Confirmation that the dog is a definitive host for Neospora caninum. Veterinary Parasitology 82, 327–333.CrossRefGoogle ScholarPubMed
Lindsay, D. S., Weston, J. L. and Little, S. E. (2001). Prevalence of antibodies to Neospora caninum and Toxoplasma gondii in gray foxes (Urocyon cinereoargenteus) from South Carolina. Veterinary Parasitology 97, 159–164.CrossRefGoogle ScholarPubMed
Marnell, F., Kingston, N. and Looney, D. (2009). Ireland Red List No. 3: Terrestrial Mammals. National Parks and Wildlife Service, Department of the Environment, Heritage and Local Government, Dublin, Eire.Google Scholar
McAllister, M. M., Dubey, J. P., Lindsay, D. S., Jolley, W. R., Wills, R. A. and McGuire, A. M. (1998). Rapid communication: Dogs are definitive hosts of Neospora caninum. International Journal for Parasitology 28, 1473–1479.CrossRefGoogle Scholar
McLauchlin, J., Pedraza-Diaz, S., Amar-Hoetzeneder, C. and Nichols, G. L. (1999). Genetic characterization of Cryptosporidium strains from 218 patients with diarrhea diagnosed as having sporadic cryptosporidiosis. Journal of Clinical Microbiology 37, 3153–3158.CrossRefGoogle ScholarPubMed
Melo, C. B., Leite, R. C. and Leite, F. S. C. (2002). Serological surveillance on South American wild canids for Neospora caninum. Arquivo Brasileiro de Medicina Veterinária e Zootecnia 54, 444–447.CrossRefGoogle Scholar
Murphy, T. M., Walochnik, J., Hassl, A., Moriarty, J., Mooney, J., Toolan, D., Sanchez-Miguel, C., O'Loughlin, A. and McAuliffe, A. (2007). Study on the prevalence of Toxoplasma gondii and Neospora caninum and molecular evidence of Encephalitozoon cuniculi and Encephalitozoon (Septata) intestinalis infections in red foxes (Vulpes vulpes) in rural Ireland. Veterinary Parasitology 146, 227–234.CrossRefGoogle Scholar
O'Mahony, D., O'Reilly, C. and Turner, P. (2012). Pine marten (Martes martes) distribution and abundance in Ireland: A cross-jurisdictional analysis using non-invasive genetic survey techniques. Mammalian Biology 77, 351–357.CrossRefGoogle Scholar
Reichel, M. P. and Ellis, J. T. (2009). Neospora caninum - How close are we to development of an efficacious vaccine that prevents abortion in cattle? International Journal for Parasitology 39, 1173–1187.CrossRefGoogle ScholarPubMed
Selva, N. (2004) Life after death - scavenging on ungulate carcasses. In Essays on Mammals of Bialowieza Forest (ed. Jedrzejewska, B. and Wojcik, J. M.), pp. 59–68. Mammal Research Institute, Polish Academy of Sciences, Bialowieza, Poland.Google Scholar
Simpson, V. R., Monies, R. J., Riley, P. and Cromey, D. S. (1997). Foxes and neosporosis. The Veterinary Record 8, 503.Google Scholar
Sleeman, D. P. (1992). Diet of Irish stoats. The Irish Naturalists' Journal 24, 151–153.Google Scholar
Sleeman, D. P., Davenport, J. and Fitzgerald, A. (2008). Incidence of visits by badgers to farmyards in Ireland in winter. The Veterinary Record 163, 724.CrossRefGoogle ScholarPubMed
Smith, G. C., Gangadharan, B., Taylor, Z., Laurenson, M. K., Bradshaw, H., Hide, G., Hughes, J. M., Dinkel, A., Romig, T. and Craig, P. S. (2003). Prevalence of zoonotic important parasites in the red fox (Vulpes vulpes) in Great Britain. Veterinary Parasitology 118, 133–142.CrossRefGoogle ScholarPubMed
Sobrino, R., Dubey, J. P., Pabón, M., Linarez, N., Kwok, O. C., Millán, J., Arnal, M. C., Luco, D. F., López-Gatius, F., Thulliez, P., Gortázar, C. and Almería, S. (2008). Neospora caninum antibodies in wild carnivores from Spain. Veterinary Parasitology 155, 190–197.CrossRefGoogle ScholarPubMed
Thilsted, J. and Dubey, J. (1989). Neosporosis-like abortions in a herd of dairy cattle. The Journal of Veterinary Diagnostic Investigation 1, 205–209.CrossRefGoogle Scholar
Thomasson, D., Wright, E. A., Hughes, J. M., Dodd, N. S., Cox, A. P., Boyce, K., Gerwash, O., Abushahma, M., Lun, Z. R., Murphy, R. G., Rogan, M. T. and Hide, G. (2011). Prevalence and co-infection of Toxoplasma gondii and Neospora caninum in Apodemus sylvaticus in an area relatively free of cats. Parasitology 138, 1117–1123.CrossRefGoogle Scholar
Tosh, D. G., McDonald, R. A., Bearhop, S., Lllewellyn, N. R., Fee, S., Sharp, E. A., Barnett, E. A. and Shore, R. F. (2011). Does small mammal prey guild affect the exposure of predators to anticoagulant rodenticides? Environmental Pollution 159, 3106–3112.CrossRefGoogle ScholarPubMed
Wapenaar, W., Barkema, H. W., Schares, G., Rouvinen-Watt, K., Zeijlemaker, L., Poorter, B., O'Handley, R. M., Kwok, O. C. H. and Dubey, J. P. (2007). Evaluation of four serological techniques to determine the seroprevalence of Neospora caninum in foxes (Vulpes vulpes) and coyotes (Canis latrans) on Prince Edward Island, Canada. Veterinary Parasitology 145, 51–58.CrossRefGoogle ScholarPubMed
Whelan, R. (2008). An examination of fox (Vulpes vulpes) diet through stomach content analysis. Zoology BSc Thesis. National University of Ireland, Galway, Ireland.Google Scholar
Wolfe, A., Hogan, S., Maguire, D., Fitzpatrick, C., Mulcahy, G., Vaughan, L., Wall, D. and Hayden, T. J. (2001). Red foxes (Vulpes vulpes) in Ireland as hosts for parasites of potential zoonotic and veterinary significance. The Veterinary Record 149, 759–763.CrossRefGoogle Scholar