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Detection of Babesia DNA in blood and spleen samples from Eurasian badgers (Meles meles) in Scotland

Published online by Cambridge University Press:  08 May 2017

PAUL M. BARTLEY*
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, EH26 0PZ, Scotland, UK
CARI WILSON
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, EH26 0PZ, Scotland, UK
ELISABETH A. INNES
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, EH26 0PZ, Scotland, UK
FRANK KATZER
Affiliation:
Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, EH26 0PZ, Scotland, UK
*
*Corresponding author: Moredun Research Institute, Pentlands Science Park, Bush Loan, Penicuik, EH26 0PZ, Scotland, UK. E-mail: Paul.bartley@moredun.ac.uk

Summary

Babesia are intraerythrocytic parasites of importance worldwide within the fields of human and veterinary medicine, as some Babesia sp., including Babesia microti are potentially zoonotic and can cause fatal disease in both humans and animals. The aims of this study were to use a nested PCR (amplifying the 18S rRNA gene) to determine the presence and species of Babesia parasite DNA found in blood (n = 47) and spleen (n = 47) samples collected from Eurasian badgers (Meles meles) in Scotland. The results showed 28/47 (59·6%) blood and 14/47 (29·8%) spleen samples tested positive for the presence of Babesia DNA. Initial sequence analysis of the Babesia DNA identified three distinct sequence types (submitted to GenBank KX528553, KX528554 and KX528555), which demonstrated ⩾99% identity to Babesia sp. parasites previously identified in badgers in Spain (KT223484 and KT223485). Phylogenetic analysis showed that the three isolates are closely related to Babesia annae, B. microti and other Piroplasmida species found in wildlife. Further sequence analysis of the samples demonstrated that the badgers were routinely infected with more than one parasite isolate and there was also evidence of genetic recombination between the Babesia parasite isolates (submitted to GenBank KY250472 – KY250477)

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

Anisimova, M. and Gascuel, O. (2006). Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Systematic Biology 55, 539552.Google Scholar
Baneth, G., Florin-Christensen, M., Cardoso, L. and Schnittger, L. (2015). Reclassification of Theileria annae as Babesia vulpes sp. Nov. Parasites & Vectors 8, 207.Google Scholar
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.Google Scholar
Bartley, P. M., Hamilton, C., Wilson, C., Innes, E. A. and Katzer, F. (2016). Detection of Babesia annae DNA in lung exudate samples from Red foxes (Vulpes vulpes) in Great Britain. Parasites & Vectors 9, 84.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, 17681776.Google Scholar
Criado-Fornelio, A., Martinez-Marcos, A., Buling-Sarana, A. and Barba-Carretero, J. C. (2003). Molecular studies on Babesia, Theileria and Hepatozoon in southern Europe – Part I. Epizootiological aspects. Veterinary Parasitology 113, 189201.Google Scholar
Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., Dufayard, J. F., Guindon, S., Lefort, V., Lescot, M., Claverie, J. M. and Gascuel, O. (2008). Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research 36, W465W469.Google Scholar
Gimenez, C., Casado, N., Criado-Fornelio, A., de Miguel, F. A. and Dominguez-Penafiel, G. (2009). A molecular survey of Piroplasmida and Hepatozoon isolated from domestic and wild animals in Burgos (northern Spain). Veterinary Parasitology 162, 147150.CrossRefGoogle ScholarPubMed
Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W. and Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3·0. Systematic Biology 59, 307321.Google Scholar
Healing, T. D. (1981). Infections with blood parasites in the small British rodents Apodemus sylvaticus, Clethrionomys glareolus and Microtus agrestis . Parasitology 83, 179189.CrossRefGoogle ScholarPubMed
Homer, M. J., Aguilar-Delfin, I., Telford, S. R. III, Krause, P. J. and Persing, D. H. (2000). Babesiosis. Clinical Microbiology Reviews 13, 451469.Google Scholar
Jameson, L. J. and Medlock, J. M. (2011). Tick surveillance in Great Britain. Vector Borne and Zoonotic Diseases 11, 403–12.Google Scholar
Judge, J., Wilson, G. J., Macarthur, R., Delahay, R. J. and McDonald, R. A. (2014). Density and abundance of badger social groups in England and Wales in 2011–2013. International Journal of Scientific Reports 4, 3809.CrossRefGoogle ScholarPubMed
Katzer, F., Canton, G., Burrells, A., Palarea-Albaladejo, J., Horton, B., Bartley, P. M., Pang, Y., Chianini, F., Innes, E. A. and Benavides, J. (2014). Immunization of lambs with the S48 strain of Toxoplasma gondii reduces tissue cyst burden following oral challenge with a complete strain of the parasite. Veterinary Parasitology 205, 4656.Google Scholar
Liesner, J. M., Krucken, J., Schaper, R., Pachnicke, S., Kohn, B., Muller, E., Schulze, C. and von Samson-Himmelstjerna, G. (2016). Vector-borne pathogens in dogs and red foxes from the federal state of Brandenburg, Germany. Veterinary Parasitology 224, 4451.Google Scholar
Liyanagunawardena, N., Sivakumar, T., Kothalawala, H., Silva, S. S., Battsetseg, B., Lan, D. T., Inoue, N., Igarashi, I. and Yokoyama, N. (2016). Type-specific PCR assays for Babesia bovis msa-1 genotypes in Asia: revisiting the genetic diversity in Sri Lanka, Mongolia, and Vietnam. Infection Genetics and Evolution 37, 6469.Google Scholar
Millan, J., Proboste, T., Fernandez de Mera, I. G., Chirife, A. D., de la Fuente, J. and Altet, L. (2015). Molecular detection of vector-borne pathogens in wild and domestic carnivores and their ticks at the human-wildlife interface. Ticks and Tick Borne Diseases 7, 284290.Google Scholar
Peirce, M. A. and Neal, C. (1974). Piroplasmosis in British badgers (Meles meles). Veterinary Record 94, 493494.Google Scholar
Rainey, E., Butler, A., Bierman, S. and Roberts, A. M. I. (2009) Scottish Badger Distribution Survey 2006–2009: estimating the distribution and density of badger main setts in Scotland. Report prepared by Scottish Badgers and Biomathematics and Statistics Scotland.Google Scholar
Robertson, A., McDonald, R. A., Delahay, R. J., Kelly, S. D. and Bearhop, S. (2014). Individual foraging specialisation in a social mammal: the European badger (Meles meles). Oecologia 176, 409421.Google Scholar
Simpson, V. R., Panciera, R. J., Hargreaves, J., McGarry, J. W., Scholes, S. F., Bown, K. J. and Birtles, R. J. (2005). Myocarditis and myositis due to infection with Hepatozoon species in pine martens (Martes martes) in Scotland. Veterinary Record 156, 442446.Google Scholar
Simsek, S., Dumanli, N. and Koroglu, E. (2003). Piroplasmosis in a badger from Turkey. Veterinary Record 153, 372.Google Scholar
Yokoyama, N., Sivakumar, T., Tuvshintulga, B., Hayashida, K., Igarashi, I., Inoue, N., Long, P. T. and Lan, D. T. (2015). Genetic variations in merozoite surface antigen genes of Babesia bovis detected in Vietnamese cattle and water buffaloes. Infection Genetics and Evolution 30, 288295.Google Scholar
Young, A., Marquez-Grant, N., Stillman, R., Smith, M. J. and Korstjens, A. H. (2015). An investigation of red fox (Vulpes vulpes) and Eurasian badger (Meles meles) scavenging, scattering, and removal of deer remains: forensic implications and applications. Journal of Forensic Science 60(Suppl 1), S3955.Google Scholar