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Evidence of the three main clonal Toxoplasma gondii lineages from wild mammalian carnivores in the UK

Published online by Cambridge University Press:  19 August 2013

A. BURRELLS
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
P. M. BARTLEY
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
I. A. ZIMMER
Affiliation:
The Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, UK
S. ROY
Affiliation:
The Food and Environment Research Agency, Sand Hutton, York YO41 1LZ, UK
A. C. KITCHENER
Affiliation:
Department of Natural Sciences, National Museums Scotland, Chambers Street, Edinburgh EH1 1JF, UK Institute of Geography, School of GeoSciences, University of Edinburgh, Drummond Street, Edinburgh EH8 9XP, UK
A. MEREDITH
Affiliation:
Royal (Dick) School of Veterinary Studies, University of Edinburgh, Midlothian EH25 9RG, UK
S. E. WRIGHT
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
E. A. INNES
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
F. KATZER*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 0PZ, UK
*
*Corresponding author: Moredun Research Institute, Pentlands Science Park, Bush Loan, Midlothian EH26 OPZ, UK. E-mail: frank.katzer@moredun.ac.uk

Summary

Toxoplasma gondii is a zoonotic pathogen defined by three main clonal lineages (types I, II, III), of which type II is most common in Europe. Very few data exist on the prevalence and genotypes of T. gondii in the UK. Wildlife can act as sentinel species for T. gondii genotypes present in the environment, which may subsequently be transmitted to livestock and humans. DNA was extracted from tissue samples of wild British carnivores, including 99 ferrets, 83 red foxes, 70 polecats, 65 mink, 64 badgers and 9 stoats. Parasite DNA was detected using a nested ITS1 PCR specific for T. gondii, PCR positive samples were subsequently genotyped using five PCR–RFLP markers. Toxoplasma gondii DNA was detected within all these mammal species and prevalence varied from 6·0 to 44·4% depending on the host. PCR–RFLP genotyping identified type II as the predominant lineage, but type III and type I alleles were also identified. No atypical or mixed genotypes were identified within these animals. This study demonstrates the presence of alleles for all three clonal lineages with potential for transmission to cats and livestock. This is the first DNA-based study of T. gondii prevalence and genotypes across a broad range of wild British carnivores.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Anwar, A., Knaggs, J., Service, K. M., McLaren, G. W., Riordan, P., Newman, C., Delahay, R. J., Cheesman, C. and Macdonald, D. W. (2006). Antibodies to Toxoplasma gondii in Eurasian badgers. Journal of Wildlife Diseases 42, 179181. doi: 42/1/179.CrossRefGoogle ScholarPubMed
Aubert, D., Ajzenberg, D., Richomme, C., Gilot-Fromont, E., Terrier, M. E., de Gevigney, C., Game, Y., Maillard, D., Gibert, P., Darde, M. L. and Villena, I. (2010). Molecular and biological characteristics of Toxoplasma gondii isolates from wildlife in France. Veterinary Parasitology 171, 346349. doi: 10.1016/j.vetpar.2010.03.033.CrossRefGoogle ScholarPubMed
Bartley, P. M., Wright, S. E., Zimmer, I. A., Roy, S., Kitchener, A. C., Meredith, A., Innes, E. A. and Katzer, F. (2013). Detection of Neospora caninum in wild carnivorans in Great Britain. Veterinary Parasitology 192, 279283. doi: 10.1016/j.vetpar.2012.10.001.CrossRefGoogle ScholarPubMed
Berger-Schoch, A. E., Herrmann, D. C., Schares, G., Müller, N., Bernet, D., Gottstein, B. and Frey, C. F. (2011). Prevalence and genotypes of Toxoplasma gondii in feline faeces (oocysts) and meat from sheep, cattle and pigs in Switzerland. Veterinary Parasitology 177, 290297.CrossRefGoogle ScholarPubMed
Buxton, D., Wright, S., Maley, S. W., Rae, A. G., Lunden, A. and Innes, E. A. (2001). Immunity to experimental neosporosis in pregnant sheep. Parasite Immunology 23, 8591. doi: pim362.CrossRefGoogle ScholarPubMed
Carme, B., Demar, M., Ajzenberg, D. and Darde, M. L. (2009). Severe acquired toxoplasmosis caused by wild cycle of Toxoplasma gondii, French Guiana. Emerging Infectious Diseases 15, 656658.CrossRefGoogle ScholarPubMed
De Craeye, S., Speybroeck, N., Ajzenberg, D., Darde, M. L., Collinet, F., Tavernier, P., Van Gucht, S., Dorny, P. and Dierick, K. (2011). Toxoplasma gondii and Neospora caninum in wildlife: common parasites in Belgian foxes and Cervidae? Veterinary Parasitology 178, 6469. doi: 10.1016/j.vetpar.2010.12.016.CrossRefGoogle ScholarPubMed
de Sousa, S., Ajzenberg, D., Canada, N., Freire, L., da Costa, J. M., Dardé, M. L., Thulliez, P. and Dubey, J. P. (2006). Biologic and molecular characterization of Toxoplasma gondii isolates from pigs from Portugal. Veterinary Parasitology 135, 133136. doi: 10.1016/j.vetpar.2005.08.012.CrossRefGoogle ScholarPubMed
Dubey, J. P., Lindsay, D. S. and Speer, C. A. (1998). Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clinical Microbiology Reviews 11, 267299.CrossRefGoogle ScholarPubMed
Dubey, J. P., Sundar, N., Hill, D., Velmurugan, G. V., Bandini, L. A., Kwok, O. C., Majumdar, D. and Su, C. (2008). High prevalence and abundant atypical genotypes of Toxoplasma gondii isolated from lambs destined for human consumption in the USA. International Journal for Parasitology 38, 9991006. doi: 10.1016/j.ijpara.2007.11.012.CrossRefGoogle ScholarPubMed
Ferreira, I. M., Vidal, J. E., de Mattos, C. D., de Mattos, L. C., Qu, D., Su, C. and Pereira-Chioccola, V. L. (2011). Toxoplasma gondii isolates: multilocus RFLP-PCR genotyping from human patients in Sao Paulo State, Brazil identified distinct genotypes. Experimental Parasitology 129, 190195. doi: 10.1016/j.exppara.2011.06.002.CrossRefGoogle Scholar
Grigg, M. E., Ganatra, J., Boothroyd, J. C. and Margolis, T. P. (2001). Unusual abundance of atypical strains associated with human ocular toxoplasmosis. Journal of Infectious Diseases 184, 633639. doi: JID000439.CrossRefGoogle ScholarPubMed
Hamilton, C. M., Gray, R., Wright, S. E., Gangadharan, B., Laurenson, K. and 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, 169173. doi: 10.1016/j.vetpar.2005.03.020.CrossRefGoogle ScholarPubMed
Herrmann, D. C., Maksimov, P., Maksimov, A., Sutor, A., Schwarz, S., Jaschke, W., Schliephake, A., Denzin, N., Conraths, F. J. and Schares, G. (2012). Toxoplasma gondii in foxes and rodents from the German Federal States of Brandenburg and Saxony-Anhalt: seroprevalence and genotypes. Veterinary Parasitology 185, 7885. doi: 10.1016/j.vetpar.2011.10.030.CrossRefGoogle ScholarPubMed
Howe, D. K. and Sibley, L. D. (1995). Toxoplasma gondii comprises three clonal lineages: correlation of parasite genotype with human disease. Journal of Infectious Diseases 172, 15611566.CrossRefGoogle ScholarPubMed
Howe, D. K., Honore, S., Derouin, F. and Sibley, L. D. (1997). Determination of genotypes of Toxoplasma gondii strains isolated from patients with toxoplasmosis. Journal of Clinical Microbiology 35, 14111414.CrossRefGoogle ScholarPubMed
Hurtado, A., Aduriz, G., Moreno, B., Barandika, J. and Garcia-Perez, A. L. (2001). Single tube nested PCR for the detection of Toxoplasma gondii in fetal tissues from naturally aborted ewes. Veterinary Parasitology 102, 1727. doi: S0304-4017(01)00526-X.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Dunachie, J. F., Siim, J. C. and Work, K. (1969). Life cycle of Toxoplasma gondii. British Medical Journal 4, 806.CrossRefGoogle ScholarPubMed
Hutchison, W. M., Dunachie, J. F., Work, K. and Siim, J. C. (1971). The life cycle of the coccidian parasite, Toxoplasma gondii, in the domestic cat. Transactions of the Royal Society of Tropical Medicine and Hygiene 65, 380399.CrossRefGoogle ScholarPubMed
Innes, E. A. (1997). Toxoplasmosis: comparative species susceptibility and host immune response. Comparative Immunology, Microbiology and Infectious Disease 20, 131138. doi: S0147957196000380.CrossRefGoogle ScholarPubMed
Katzer, F., Brulisauer, F., Collantes-Fernandez, E., Bartley, P. M., Burrells, A., Gunn, G., Maley, S. W., Cousens, C. and Innes, E. A. (2011). Increased Toxoplasma gondii positivity relative to age in 125 Scottish sheep flocks; evidence of frequent acquired infection. Veterinary Research 42, 121. doi: 10.1186/1297-9716-42-121.CrossRefGoogle ScholarPubMed
Khan, A., Su, C., German, M., Storch, G. A., Clifford, D. B. and Sibley, L. D. (2005). Genotyping of Toxoplasma gondii strains from immunocompromised patients reveals high prevalence of type I strains. Journal of Clinical Microbiology 43, 58815887. doi: 10.1128/JCM.43.12.5881-5887.2005.CrossRefGoogle ScholarPubMed
Khan, A., Dubey, J. P., Su, C., Ajioka, J. W., Rosenthal, B. M. and Sibley, L. D. (2011). Genetic analyses of atypical Toxoplasma gondii strains reveal a fourth clonal lineage in North America. International Journal for Parasitology 41, 645655. doi: S0020-7519(11)00046-4 [pii]10.1016/j.ijpara.2011.01.005.CrossRefGoogle ScholarPubMed
Lindstrom, I., Sundar, N., Lindh, J., Kironde, F., Kabasa, J. D., Kwok, O. C., Dubey, J. P. and Smith, J. E. (2008). Isolation and genotyping of Toxoplasma gondii from Ugandan chickens reveals frequent multiple infections. Parasitology 135, 3945. doi: 10.1017/S0031182007003654.CrossRefGoogle ScholarPubMed
Miller, M. A., Grigg, M. E., Kreuder, C., James, E. R., Melli, A. C., Crosbie, P. R., Jessup, D. A., Boothroyd, J. C., Brownstein, D. and Conrad, P. A. (2004). An unusual genotype of Toxoplasma gondii is common in California sea otters (Enhydra lutris nereis) and is a cause of mortality. International Journal for Parasitology 34, 275284. doi: 10.1016/j.ijpara.2003.12.008.CrossRefGoogle ScholarPubMed
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, 227234. doi: 10.1016/j.vetpar.2007.02.017.CrossRefGoogle Scholar
Opsteegh, M., Langelaar, M., Sprong, H., den Hartog, L., De Craeye, S., Bokken, G., Ajzenberg, D., Kijlstra, A. and van der Giessen, J. (2010). Direct detection and genotyping of Toxoplasma gondii in meat samples using magnetic capture and PCR. International Journal of Food Microbiology 139, 193201. doi: 10.1016/j.ijfoodmicro.2010.02.027.CrossRefGoogle ScholarPubMed
Parameswaran, N., Thompson, R. C., Sundar, N., Pan, S., Johnson, M., Smith, N. C. and Grigg, M. E. (2010). Non-archetypal Type II-like and atypical strains of Toxoplasma gondii infecting marsupials of Australia. International Journal for Parasitology 40, 635640. doi: 10.1016/j.ijpara.2010.02.008.CrossRefGoogle ScholarPubMed
Prestrud, K. W., Åsbakk, K., Mørk, T., Fuglei, E., Tryland, M. and Su, C. (2008). Direct high-resolution genotyping of Toxoplasma gondii in arctic foxes (Vulpes lagopus) in the remote arctic Svalbard archipelago reveals widespread clonal Type II lineage. Veterinary Parasitology 158, 121128.CrossRefGoogle ScholarPubMed
Su, C., Zhang, X. and Dubey, J. P. (2006). Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. International Journal for Parasitology 36, 841848.CrossRefGoogle ScholarPubMed
Sundar, N., Cole, R. A., Thomas, N. J., Majumdar, D., Dubey, J. P. and Su, C. (2008). Genetic diversity among sea otter isolates of Toxoplasma gondii. Veterinary Parasitology 151, 125132. doi: 10.1016/j.vetpar.2007.11.012.CrossRefGoogle ScholarPubMed
Tenter, A. M., Heckeroth, A. R. and Weiss, L. M. (2000). Toxoplasma gondii: from animals to humans. International Journal for Parasitology 30, 12171258. doi: S0020-7519(00)00124-7.CrossRefGoogle ScholarPubMed
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, 11171123. doi: 10.1017/S0031182011000904.CrossRefGoogle Scholar
Waap, H., Vilares, A., Rebelo, E., Gomes, S. and Angelo, H. (2008). Epidemiological and genetic characterization of Toxoplasma gondii in urban pigeons from the area of Lisbon (Portugal). Veterinary Parasitology 157, 306309. doi: 10.1016/j.vetpar.2008.07.017.CrossRefGoogle ScholarPubMed
Webster, J. P. (1994). Prevalence and transmission of Toxoplasma gondii in wild brown rats, Rattus norvegicus. Parasitology 108, 407411.CrossRefGoogle ScholarPubMed