Hostname: page-component-cd9895bd7-q99xh Total loading time: 0 Render date: 2024-12-27T18:57:59.608Z Has data issue: false hasContentIssue false
  • English
  • Français

Toxoplasma gondii coinfection with diseases and parasites in wild rabbits in Scotland

Published online by Cambridge University Press:  06 July 2015

SAM MASON ,
J. P. DUBEY ,
JUDITH E. SMITH  and
BRIAN BOAG
SAM MASON*
Affiliation:
School of Biology, Miall Building, University of Leeds, Leeds LS2 9JT, UK
J. P. DUBEY
Affiliation:
United States Department of Agriculture, Agricultural Research Service, Beltsville Agricultural Research Center, Animal Parasitic Diseases Laboratory, Building 1001, BARC-East, Beltsville, Maryland 20705-2350, USA
JUDITH E. SMITH
Affiliation:
School of Environment and Life Sciences, Peel Building, University of Salford, Salford M5 4WT, UK
BRIAN BOAG
Affiliation:
James Hutton Institute, Invergowrie, Dundee DD2 5DA, UK
*
* Corresponding author. School of Biology, Miall Building, University of Leeds, Leeds LS2 9JT, UK. Tel:xxx. Fax:xxx. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

In wild rabbits (Oryctolagus cuniculus) on an estate in Perthshire, central Scotland, the seroprevalence of Toxoplasma gondii was 18/548 (3·3%). The wild rabbit could be a T. gondii reservoir and it has potential value as a sentinel of T. gondii in environmental substrates. Toxoplasma gondii was associated with female sex (P < 0·001) and with relatively heavy infections by Eimeria stiedae (P = 0·036). It was not associated with the intensity of coccidial oocysts, the severity of myxomatosis caused by the virus Myxomatosis cuniculi, the intensity of roundworm eggs, the year or season, rabbit age or distance from farm buildings. Coinfections could have been affected by gestational down regulation of type 1 T helper cells. A sudden influx or release of T. gondii oocysts might have occurred. This is the first report of T. gondii in any wild herbivore in Scotland and also the first report of lapine T. gondii as a coinfection with E. stiedae, M. cuniculi and helminths.

Keywords

Toxoplasma gondiiEimeria stiedaerabbitcoinfection
Type
Research Article
Information
Parasitology , Volume 142 , Issue 11 , September 2015 , pp. 1415 - 1421
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Almería, S., Calvete, C., Pagés, A., Gauss, C. and Dubey, J. P. (2004). Factors affecting the seroprevalence of Toxoplasma gondii infection in wild rabbits (Oryctolagus cuniculus) from Spain. Veterinary Parasitology 123, 265–270.Google Scholar
Alvarado-Esquivel, C., Torres-Berumen, J. L., Estrada-Martínez, S., Liesenfeld, O. and Mercado-Suarez, M. F. (2011). Toxoplasma gondii infection and liver disease: a case–control study in a northern Mexican population. Parasites and Vectors 4, 75.Google Scholar
Alvarado-Esquivel, C., Alvarado-Esquivel, D., Villena, I. and Dubey, J. P. (2013). Seroprevalence of Toxoplasma gondii infection in domestic rabbits in Durango State, Mexico. Preventive Veterinary Medicine 111, 325–328.Google Scholar
Aramini, J. J., Stephen, C., Dubey, J. P., Engelstoft, C., Schwantje, H. and Ribble, C. S. (1999). Potential contamination of drinking water with Toxoplasma gondii oocysts. Epidemiology and Infection 122, 305–315.Google Scholar
Barriga, O. O. and Arnoni, J. V. (1981). Pathophysiology of hepatic coccidiosis in rabbits. Veterinary Parasitology 8, 201–210.Google Scholar
Bertó-Moran, A., Pacios, I., Serrano, E., Moreno, S. and Rouco, C. (2013). Coccidian and nematode infections influence prevalence of antibody to myxoma and rabbit hemorrhagic disease viruses in European rabbits. Journal of Wildlife Diseases 49, 10–17.Google Scholar
Beverley, J. K. A., Beattie, C. P. and Roseman, C. (1954). Human Toxoplasma infection. Journal of Hygiene 52, 37–46.Google Scholar
Boag, B., Lello, J., Fenton, A., Tomkins, D. M. and Hudson, P. J. (2001). Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus). International Journal for Parasitology 31, 1421–1428.Google Scholar
Boag, B., Hernandez, A. D. and Cattadori, I. M. (2013). Observations on the epidemiology and interactions between myxomatosis, coccidiosis and helminth parasites in a wild rabbit population in Scotland. European Journal of Wildlife Research 59, 557–562.Google Scholar
Burrells, A., Bartley, P. M., Zimmer, I. A., Roy, S., Kitchener, A. C., Meredith, A., Wright, S. E., Innes, E. A. and Katzer, F. (2013). Evidence of the three main clonal Toxoplasma gondii lineages from wild mammalian carnivores in the UK. Parasitology 140, 1768–1776.Google Scholar
Cattadori, I. M., Boag, B., Bjørnstad, O. N., Cornell, S. J. and Hudson, P. J. (2005). Peak shift and epidemiology in a seasonal host–nematode system. Proceedings of the Royal Society B 272, 1163–1169.Google Scholar
Cattadori, I. M., Boag, B. and Hudson, P. J. (2008). Parasite co-infection and interaction as drivers of host heterogeneity. International Journal for Parasitology 38, 371–380.Google Scholar
Conrad, P. A., Miller, M. A., Kreuder, C., James, E. R., Mazet, J., Dabritz, H., Jessup, D. A., Gulland, F. and Grigg, M. E. (2005). Transmission of Toxoplasma: clues from the study of sea otters as sentinels of Toxoplasma gondii flow into the marine environment. International Journal for Parasitology 35, 1155–1168.Google Scholar
Cox, F. E. G. (2001). Concomitant infections, parasites and immune responses. Parasitology 122(Suppl. S1), S23–S38.Google Scholar
Cox, J. C., Edmonds, J. W. and Shepherd, R. C. H. (1981). Toxoplasmosis and the wild rabbit Oryctolagus cuniculus in Victoria, Australia with suggested mechanisms for dissemination of oocysts. Journal of Hygiene 87, 331–337.Google Scholar
Darwich, L., Cabezón, O., Echeverria, I., Pabón, M., Marco, I., Molina-López, R., Alarcia-Alejos, O., López-Gatius, F., Lavín, S. and Almería, S. (2012). Presence of Toxoplasma gondii and Neospora caninum DNA in the brain of wild birds. Veterinary Parasitology 183, 377–381.Google Scholar
Dubey, J. P. (2008). The history of Toxoplasma gondii – the first 100 years. Journal of Eukaryotic Microbiology 55, 467–475.Google Scholar
Dubey, J. P. (2010). Toxoplasmosis of Animals and Humans, 2nd Edn. CRC Press, Boca Raton, FL, USA.Google Scholar
Dubey, J. P. and Beattie, C. P. (1988). Toxoplasmosis of Animals and Man. CRC Press, Boca Raton, FL, USA.Google Scholar
Dubey, J. P. and Desmonts, G. (1987). Serological responses of equids fed Toxoplasma gondii oocysts. Equine Veterinary Journal 19, 337–339.Google Scholar
Dubey, J. P., Brown, C. A., Carpenter, J. L. and Moore, J. J. (1992). Fatal toxoplasmosis in domestic rabbits in the USA. Veterinary Parasitology 44(3–4), 305–309.Google Scholar
Dubey, J. P., Rollor, E. A., Smith, K., Kwok, O. C. H. and Thulliez, P. (1997). Low seroprevalence of Toxoplasma gondii in feral pigs from a remote island lacking cats. Journal of Parasitology 83, 839–841.Google Scholar
Dubey, J. P., Passos, L. M. F., Rajendran, C., Ferreira, L. R., Gennari, S. M. and Su, C. (2011). Isolation of viable Toxoplasma gondii from guinea fowl (Numida meleagris) and domestic rabbits (Oryctolagus cuniculus) from Brazil. Journal of Parasitology 97, 842–845.Google Scholar
Faull, W. B., Clarkson, M. J. and Winter, A. C. (1986). Toxoplasmosis in a flock of sheep: some investigations into its source and control. Veterinary Record 119, 491–493.Google Scholar
Foundation for Statistical Computing (2011). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Fröhlich, S., Entzeroth, R. and Wallach, M. (2012). Comparison of protective immune responses to apicomplexan parasites. Journal of Parasitology Research Article ID 852591, doi: 10.1155/2012/852591.Google Scholar
Garcia-Bocanegra, I., Astorga, R. J., Napp, S., Casal, J., Huerta, B., Borge, C., and Arenas, A. (2010 a). Myxomatosis in wild rabbit: design of control programs in Mediterranean ecosystems. Preventive Veterinary Medicine 93, 42–50.Google Scholar
Garcia-Bocanegra, I., Dubey, J. P., Martínez, F., Vargas, A., Cabezón, O., Zorrilla, I., Arenas, A. and Almería, S. (2010 b). Factors affecting seroprevalence of Toxoplasma gondii in the endangered Iberian lynx (Lynx pardinus). Veterinary Parasitology 167, 36–42.Google Scholar
Graham, A. L., Cattadori, I. M., Lloyd-Smith, J. D., Ferrari, M. J. and Biømstad, O. M. (2007). Transmission consequnces of coinfection: cytokines writ large. Trends in Parasitology 23, 284–291.Google Scholar
Hejlícek, K., Literák, I. and Nezval, J. (1997). Toxoplasmosis in wild mammals from the Czech Republic. Journal of Wildlife Diseases 33, 480–485.Google Scholar
Hobbs, R. P., Twigg, L. E., Elliot, A. D. and Wheeler, A. G. (1999). Factors influencing the fecal egg and oocyst counts of parasites of wild European rabbits Oryctolagus cuniculus (L.) in Southern Western Australia. Journal of Parasitology 85, 796–802.Google Scholar
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.Google Scholar
Jeklova, E., Leva, L., Matiasovic, J., Kovarcik, K., Kudlackova, H., Nevorankova, Z., Psikal, I. and Falyna, M. (2008). Characterisation of immunosuppression in rabbits after infe4ction with the myxoma virus. Veterinary Microbiology 129, 117–130.Google Scholar
Kapperud, G. (1978). Survey for toxoplasmosis in wild and domestic animals from Norway and Sweden. Journal of Wildlife Diseases 14, 157–162.Google Scholar
Kijlstra, A. and Jongert, E. (2009). Toxoplasma-safe meat: close to reality? Trends in Parasitology 25, 18–22.Google Scholar
Lello, J., Boag, B. and Hudson, P. J. (2005). The effect of single and concomitant pathogenic infections on the condition and fecundity of the wild rabbit (Oryctolagus cuniculus). International Journal for Parasitology 35, 1509–1515.Google Scholar
Mecca, J. N., Meireles, L. R. and de Andrade, H. F. (2011). Quality control of Toxoplasma gondii in meat packages: standardization of an ELISA test and its use for detection in rabbit meat cuts. Meat Science 88, 584–589.Google Scholar
Moffett, A. and Loke, C. (2006). Immunology of placentation in eutherian mammals. Nature Review Immunology 6, 584–594.Google Scholar
Molina, X., Casanova, J. C. and Feliu, C. (1999). Influence of host weight, sex and reproductive status on helminth parasites of the wild rabbit, Oryctolagus cuniculus, in Navarra, Spain. Journal of Helminthology 73, 221–225.Google Scholar
Sroka, J., Zwolinski, J., Dutkiewicz, J., Tos-Luty, S. and Latuszynska, J. (2003). Toxoplasmosis in rabbits confirmed by strain isolation: a potential risk of infection among agricultural workers. Annals of Agriculture and Environmental Medicine 10, 125–128.Google Scholar
Sroka, J., Wojcik-Fatla, A. and Dutkiewicz, J. (2006). Occurrence of Toxoplasma gondii in water from wells located on farms. Annals of Agriculture and Environmental Medicine 13, 169–175.Google Scholar
Su, C., Shwab, E. K., Zhou, P., Zhu, X. Q. and Dubey, J. P. (2010). Moving towards an integrated approach to molecular detection and identification of Toxoplasma gondii . Parasitology 137, 1–11.Google Scholar