Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-23T13:01:33.926Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular detection and characterization of piroplasms infecting cervids and chamois in Northern Spain

Published online by Cambridge University Press:  01 November 2006

J. GARCÍA-SANMARTÍN ,
O. AURTENETXE ,
M. BARRAL ,
I. MARCO ,
S. LAVIN ,
A. L. GARCÍA-PÉREZ  and
A. HURTADO
J. GARCÍA-SANMARTÍN
Affiliation:
Department of Animal Health, NEIKER – Instituto Vasco de Investigación y Desarrollo Agrario, Berreaga 1, 48160 Derio, Bizkaia, Spain
O. AURTENETXE
Affiliation:
Department of Animal Health, NEIKER – Instituto Vasco de Investigación y Desarrollo Agrario, Berreaga 1, 48160 Derio, Bizkaia, Spain
M. BARRAL
Affiliation:
Department of Animal Health, NEIKER – Instituto Vasco de Investigación y Desarrollo Agrario, Berreaga 1, 48160 Derio, Bizkaia, Spain
I. MARCO
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Facultat de Veterinária, Universitat Autonoma de Barcelona, 08193 Bellaterra, Spain
S. LAVIN
Affiliation:
Servei d'Ecopatologia de Fauna Salvatge, Facultat de Veterinária, Universitat Autonoma de Barcelona, 08193 Bellaterra, Spain
A. L. GARCÍA-PÉREZ
Affiliation:
Department of Animal Health, NEIKER – Instituto Vasco de Investigación y Desarrollo Agrario, Berreaga 1, 48160 Derio, Bizkaia, Spain
A. HURTADO
Affiliation:
Department of Animal Health, NEIKER – Instituto Vasco de Investigación y Desarrollo Agrario, Berreaga 1, 48160 Derio, Bizkaia, Spain
Get access Rights & Permissions [Opens in a new window]

Abstract

Wildlife can act as reservoir of different tick-borne pathogens of veterinary and zoonotic importance. To investigate the role of wild ruminants as reservoir of piroplasm infection, 28 red deer, 69 roe deer and 38 chamois from Northern Spain were examined by reverse line blot (RLB) hybridization. The survey detected a prevalence of 85·7% in red deer, 62·3% in roe deer and 28·9% in chamois. Four different piroplasms were identified: Theileria sp. OT3 (previously described in sheep) as the most prevalent (85·7% in red deer, 46·4% in roe deer and 26·3% in chamois); Theileria sp. 3185/02 (previously described in a red deer in Central Spain) more abundant in red deer (53·6%) than in roe deer (10·1%) but absent from chamois; Babesia divergens detected in 6 roe deer; Theileria ovis present in 1 chamois. Mixed infections (Theileria sp. OT3 and Theileria sp. 3185/02) were only found in red and roe deer. Sequencing analysis of the 18S rRNA gene confirmed the RLB results and showed 99·7% identity between Theileria sp. 3185/02 and T. capreoli, suggesting that they are the same species. Tick distribution and contact of wild ruminants with domestic animals are discussed in terms of piroplasm infection. The results suggest that a considerable number of wildlife ruminants are asymptomatic carriers that may serve as reservoirs of the infection posing a serious concern in terms of piroplasmosis control.

Keywords

Theileria spp.Babesia divergenspiroplasmosisPCRreverse line blot hybridizationtick-borne diseaseswildlifedeerchamois
Type
Research Article
Information
Parasitology , Volume 134 , Issue 3 , March 2007 , pp. 391 - 398
Copyright
© 2006 Cambridge University Press

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

Barandika, J. F., Berriatua, E., Barral, M., Juste, R. A., Anda, P. and Garcia-Perez, A. L. ( 2006). Risk factors associated with ixodid tick species distributions in the Basque region in Spain. Medical and Veterinary Entomology 20, 177–188. doi: 10.1111/j.1365-2915.2006.00619.x.CrossRefGoogle Scholar
Chae, J. S., Waghela, S. D., Craig, T. M., Kocan, A. A., Wagner, G. G. and Holman, P. J. ( 1999). Two Theileria cervi SSU RRNA gene sequence types found in isolates from white-tailed deer and elk in North America. Journal of Wildlife Diseases 35, 458–465.CrossRefGoogle Scholar
Conrad, P. A., Kjemtrup, A. M., Carreno, R. A., Thomford, J., Wainwright, K., Eberhard, M., Quick, R., Telford, I., Sr. and Herwaldt, B. L. ( 2006). Description of Babesia duncani n.sp. (Apicomplexa: Babesiidae) from humans and its differentiation from other piroplasms. International Journal for Parasitology 36, 779–789.Google Scholar
Duh, D., Petrovec, M. and Avsic-Zupanc, T. ( 2005 a). Molecular characterization of human pathogen Babesia EU1 in Ixodes ricinus ticks from Slovenia. The Journal of Parasitology 91, 463–465.Google Scholar
Duh, D., Petrovec, M., Bidovec, A. and Avsic-Zupanc, T. ( 2005 b). Cervids as Babesiae hosts, Slovenia. Emerging Infectious Diseases 11, 1121–1123.Google Scholar
Ferrer, D. and Castella, J. ( 1999). Seroprevalence of Theileria ovis in small ruminants in north-east Spain determined by the indirect fluorescent antibody test. The Veterinary Record 145, 346–347.CrossRefGoogle Scholar
Ferrer, D., Castella, J., Gutierrez, J. F., Lavin, S. and Marco, I. ( 1998 a). Seroprevalence of Babesia ovis in mouflon sheep in Spain. Journal of Wildlife Diseases 34, 637–639.Google Scholar
Ferrer, D., Castella, J., Gutierrez, J. F., Lavin, S. and Marco, I. ( 1998 b). Seroprevalence of Babesia ovis in Spanish ibex (Capra pyrenaica) in Catalonia, northeastern Spain. Veterinary Parasitology 75, 93–98. doi: 10.1016/S0304-4017(97)00199-4.CrossRefGoogle Scholar
Garcia-Sanmartin, J., Nagore, D., Garcia-Perez, A. L., Juste, R. A. and Hurtado, A. ( 2006). Molecular diagnosis of Theileria and Babesia species infecting cattle in Northern Spain using reverse line blot macroarrays. BMC Veterinary Research 2, 16. doi: 10.1186/1746-6148-2-16.CrossRefGoogle Scholar
Gil-Collado, J., Guillén-Llera, J. L. and Zapatero-Ramos, L. M. ( 1979). Claves para la identificación de los Ixodoidea españoles (adultos). Revista Ibérica de Parasitología 39, 107–111.Google Scholar
Goethert, H. K. and Telford, S. R., III ( 2003). Enzootic transmission of Babesia divergens among cottontail rabbits on Nantucket Island, Massachusetts. The American Journal of Tropical Medicine and Hygiene 69, 455–460.Google Scholar
Gray, J. S., Murphy, T. M., Taylor, S. M., Blewett, D. A. and Harrington, R. ( 1990). Comparative morphological and cross transmission studies with bovine and deer babesias in Ireland. Preventive Veterinary Medicine 9, 185–193. doi: 10.1016/0167-5877(90)90065-P.CrossRefGoogle Scholar
Gray, J. S., Murphy, T. M., Waldrup, K. A., Wagner, G. G., Blewett, D. A. and Harrington, R. ( 1991). Comparative studies of Babesia spp. from white-tailed and sika deer. Journal of Wildlife Diseases 27, 86–91.Google Scholar
Gubbels, J. M., de Vos, A. P., van der Weide, M., Viseras, J., Schouls, L. M., de Vries, E. and Jongejan, F. ( 1999). Simultaneous detection of bovine Theileria and Babesia species by reverse line blot hybridization. Journal of Clinical Microbiology 37, 1782–1789.Google Scholar
Herwaldt, B. L., Caccio, S., Gherlinzoni, F., Aspock, H., Slemenda, S. B., Piccaluga, P., Martinelli, G., Edelhofer, R., Hollenstein, U., Poletti, G., Pampiglione, S., Loschenberger, K., Tura, S. and Pieniazek, N. J. ( 2003). Molecular characterization of a non-Babesia divergens organism causing zoonotic babesiosis in Europe. Emerging Infectious Diseases 9, 942–948.CrossRefGoogle Scholar
Hofle, U., Vicente, J., Nagore, D., Hurtado, A., Pena, A., De La Fuente, J. and Gortazar, C. ( 2004). The risks of translocating wildlife. Pathogenic infection with Theileria sp. and Elaeophora elaphi in an imported red deer. Veterinary Parasitology 126, 387–395. doi: 10.1016/S0304-4017(04)00416-9.CrossRefGoogle Scholar
Holman, P. J., Bendele, K. G., Schoelkopf, L., Jones-Witthuhn, R. L. and Jones, S. O. ( 2003). Ribosomal RNA analysis of Babesia odocoilei isolates from farmed reindeer (Rangifer tarandus tarandus) and elk (Cervus elaphus canadensis) in Wisconsin. Parasitology Research 91, 378–383. doi: 10.1007/s00436-003-0984-5.CrossRefGoogle Scholar
Holman, P. J., Madeley, J., Craig, T. M., Allsopp, B. A., Allsopp, M. T., Petrini, K. R., Waghela, S. D. and Wagner, G. G. ( 2000). Antigenic, phenotypic and molecular characterization confirms Babesia odocoilei isolated from three cervids. Journal of Wildlife Diseases 36, 518–530.CrossRefGoogle Scholar
Holman, P. J., Swift, P. K., Frey, R. E., Bennett, J., Cruz, D. and Wagner, G. G. ( 2002). Genotypically unique Babesia spp. isolated from reindeer (Rangifer tarandus tarandus) in the United States. Parasitology Research 88, 405–411. doi: 10.1007/s00436-001-0576-1.CrossRefGoogle Scholar
Hurtado, A., Aduriz, G., Gomez, N., Oporto, B., Juste, R. A., Lavin, S., Lopez-Olvera, J. R. and Marco, I. ( 2004). Molecular identification of a new pestivirus associated with increased mortality in the Pyrenean Chamois (Rupicapra pyrenaica pyrenaica) in Spain. Journal of Wildlife Diseases 40, 796–800.CrossRefGoogle Scholar
Inokuma, H., Tsuji, M., Kim, S. J., Fujimoto, T., Nagata, M., Hosoi, E., Arai, S., Ishihara, C. and Okuda, M. ( 2004). Phylogenetic analysis of Theileria sp. from sika deer, Cervus nippon, in Japan. Veterinary Parasitology 120, 339–345. doi: 10.1016/j.vetpar.2004.01.011.CrossRefGoogle Scholar
Kjemtrup, A. M. and Conrad, P. A. ( 2000). Human babesiosis: an emerging tick-borne disease. International Journal for Parasitology 30, 1323–1337. doi: 10.1016/S0020-7519(00)00137-5.CrossRefGoogle Scholar
Langton, C., Gray, J. S., Waters, P. F. and Holman, P. J. ( 2003). Naturally acquired babesiosis in a reindeer (Rangifer tarandus tarandus) herd in Great Britain. Parasitology Research 89, 194–198. doi: 10.1007/s00436-002-0737-x.CrossRefGoogle Scholar
Manilla G. ( 1998). Fauna D'Italia: Acari, Ixodida, 1st Edn. Edizioni Calderini, Bologna.
Marco, I., Velarde, R., Castella, J., Ferrer, D. and Lavin, S. ( 2000). Presumptive Babesia ovis infection in a spanish ibex (Capra pyrenaica). Veterinary Parasitology 87, 217–221. doi: 10.1016/S0304-4017(99)00170-3.CrossRefGoogle Scholar
Nagore, D., Garcia-Sanmartin, J., Garcia-Perez, A. L., Juste, R. A. and Hurtado, A. ( 2004 a). Detection and identification of equine Theileria and Babesia species by reverse line blotting: epidemiological survey and phylogenetic analysis. Veterinary Parasitology 123, 41–54. doi: 10.1016/j.vetpar.2004.04.010.CrossRefGoogle Scholar
Nagore, D., Garcia-Sanmartin, J., Garcia-Perez, A. L., Juste, R. A. and Hurtado, A. ( 2004 b). Identification, genetic diversity and prevalence of Theileria and Babesia species in a sheep population from Northern Spain. International Journal for Parasitology 34, 1059–1067. doi: 10.1016/j.ijpara.2004.05.008.CrossRefGoogle Scholar
Persing, D. H., Herwaldt, B. L., Glaser, C., Lane, R. S., Thomford, J. W., Mathiesen, D., Krause, P. J., Phillip, D. F. and Conrad, P. A. ( 1995). Infection with a babesia-like organism in northern California. The New England Journal of Medicine 332, 298–303. doi: 10.1056/NEJM199502023320504.CrossRefGoogle Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. ( 1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle Scholar
Waldrup, K. A., Moritz, J., Bagget, D., Magyar, S. and Wagner, G. G. ( 1992). Monthly incidence of Theileria cervi and seroconversion to Babesia odocoilei in white-tailed deer (Odocoileus virginianus) in Texas. Journal of Wildlife Diseases 28, 457–459.CrossRefGoogle Scholar
Yabsley, M. J., Davidson, W. R., Stallknecht, D. E., Varela, A. S., Swift, P. K., Devos, J. C. and Dubay, S. A. ( 2005). Evidence of tick-borne organisms in mule deer (Odocoileus hemionus) from the Western United States. Vector Borne and Zoonotic Diseases 5, 351–362. doi: 10.1089/vbz.2005.5.351.CrossRefGoogle Scholar
Yabsley, M. J., Quick, T. C. and Little, S. E. ( 2005). Theileriosis in a white-tailed deer (Odocoileus virginianus) fawn. Journal of Wildlife Diseases 41, 806–809.CrossRefGoogle Scholar
Zintl, A., Gray, J. S., Skerrett, H. E. and Mulcahy, G. ( 2005). Possible mechanisms underlying age-related resistance to bovine babesiosis. Parasite Immunology 27, 115–120. doi: 10.1111/j.1365-3024.2005.00748.x.CrossRefGoogle Scholar
Zintl, A., Mulcahy, G., Skerrett, H. E., Taylor, S. M. and Gray, J. S. ( 2003). Babesia divergens, a bovine blood parasite of veterinary and zoonotic importance. Clinical Microbiology Reviews 16, 622–636. doi: 10.1128/CMR.16.4.622-636.2003.CrossRefGoogle Scholar