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Molecular detection of Babesia spp. and other haemoparasitic infections of cattle in Maputo Province, Mozambique

Published online by Cambridge University Press:  04 February 2010

TIAGO M. MARTINS ,
LUÍS NEVES ,
OLÍVIA C. PEDRO ,
JOSÉ M. FAFETINE ,
VIRGÍLIO E. DO ROSÁRIO  and
ANA DOMINGOS
TIAGO M. MARTINS*
Affiliation:
Unidade de Tecnologias de Proteínas e Anticorpos Monoclonais, Instituto de Higiene e Medicina Tropical, Estrada do Paço do Lumiar 22, 1649-038 Lisboa, Portugal Centro de Malária e Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Rua da Junqueira 96, 1349-008Lisboa, Portugal
LUÍS NEVES
Affiliation:
Centro de Biotecnologia, Universidade Eduardo Mondlane, Av. de Moçambique km 1.5, Maputo, Mozambique
OLÍVIA C. PEDRO
Affiliation:
Centro de Biotecnologia, Universidade Eduardo Mondlane, Av. de Moçambique km 1.5, Maputo, Mozambique Faculdade de Veterinária, Universidade Eduardo Mondlane, Av. de Moçambique km 1.5, Maputo, Mozambique
JOSÉ M. FAFETINE
Affiliation:
Centro de Biotecnologia, Universidade Eduardo Mondlane, Av. de Moçambique km 1.5, Maputo, Mozambique Faculdade de Veterinária, Universidade Eduardo Mondlane, Av. de Moçambique km 1.5, Maputo, Mozambique
VIRGÍLIO E. DO ROSÁRIO
Affiliation:
Centro de Malária e Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Rua da Junqueira 96, 1349-008Lisboa, Portugal
ANA DOMINGOS
Affiliation:
Unidade de Tecnologias de Proteínas e Anticorpos Monoclonais, Instituto de Higiene e Medicina Tropical, Estrada do Paço do Lumiar 22, 1649-038 Lisboa, Portugal Centro de Malária e Doenças Tropicais, Instituto de Higiene e Medicina Tropical, Rua da Junqueira 96, 1349-008Lisboa, Portugal
*
*Corresponding author: Unidade de Tecnologias de Proteínas e Anticorpos Monoclonais, Instituto de Higiene e Medicina Tropical, Estrada do Paço do Lumiar 22, 1649-038Lisboa, Portugal. Tel: +351 210924712. Fax: +351 217163636. E-mail: tmlmartins@gmail.com
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Summary

Molecular detection of Babesia species in apparently healthy cattle within an endemic region was carried out in order to determine the prevalence of carriers and the geographical distribution of Babesia bigemina and Babesia bovis in Maputo Province, Mozambique. Samples from 477 animals at 5 localities were analysed using 2 techniques, the semi-nested hot-start PCR and the reverse line blot (RLB) assay. With the semi-nested hot-start PCR, detection of B. bigemina ranged between 30% and 89%, and of B. bovis between 27% and 83%. The RLB assay was comparatively less sensitive in this study and detection of B. bovis ranged from 0% to 17%, and B. bigemina was not detected at all by this technique. Analysis of new sequences of the 18S rRNA gene revealed that the current B. bigemina RLB probe is not specific for the identification of isolates in Mozambique. The RLB assay, however, resulted in the detection of 8 other haemoparasite species belonging to the genera Babesia, Theileria, Anaplasma and Ehrlichia. 18S rRNA gene sequences from the Theileria spp. were identified, and a phylogenic tree constructed with these sequences yielded a heterogeneous T. mutans-like group. In conclusion, infection with B. bigemina and B. bovis is endemic in Maputo Province, but rates of transmission vary. Furthermore, mixed infections with the haemoparasites responsible for several tick-borne diseases in cattle are common in Mozambique.

Keywords

tick-borne diseasescattleBabesia bigeminaBabesia bovishot-start PCRRLB
Type
Research Article
Information
Parasitology , Volume 137 , Issue 6 , May 2010 , pp. 939 - 946
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Alfredo, A., Jonsson, N., Finch, T., Neves, L., Molloy, J. and Jorgensen, W. (2005). Serological survey of Babesia bovis and Anaplasma marginale in cattle in Tete Province, Mozambique. Tropical Animal Health and Production 37, 121–131. doi: 10.1023/B:TROP.0000048513.80797.97CrossRefGoogle Scholar
Bekker, C. P., de Vos, S., Taoufik, A., Sparagano, O. A. and Jongejan, F. (2002). Simultaneous detection of Anaplasma and Ehrlichia species in ruminants and detection of Ehrlichia ruminantium in Amblyomma variegatum ticks by reverse line blot hybridization. Veterinary Microbiology 89, 223–238. doi: 10.1016/S0378-1135(02)00179-7CrossRefGoogle ScholarPubMed
Birkenheuer, A. J., Levy, M. G. and Breitschwerdt, E. B. (2003). Development and evaluation of a semi-nested PCR for detection and differentiation of Babesia gibsoni (Asian genotype) and B. canis DNA in canine blood samples. Journal of Clinical Microbiology 41, 4172–4177. doi: 10.1128/JCM.41.9.4172-4177.2003CrossRefGoogle Scholar
Bock, R., Jackson, L., de Vos, A. and Jorgensen, W. (2004). Babesiosis of cattle. Parasitology 129 (Suppl.) S247–S269. doi: 10.1017/S0031182004005190CrossRefGoogle ScholarPubMed
Calder, J. A., Reddy, G. R., Chieves, L., Courtney, C. H., Littell, R., Livengood, J. R., Norval, R. A., Smith, C. and Dame, J. B. (1996). Monitoring Babesia bovis infections in cattle by using PCR-based tests. Journal of Clinical Microbiology 34, 2748–2755.CrossRefGoogle ScholarPubMed
Chae, J. S., Allsopp, B. A., Waghela, S. D., Park, J. H., Kakuda, T., Sugimoto, C., Allsopp, M. T., Wagner, G. G. and Holman, P. J. (1999). A study of the systematics of Theileria spp. based upon small-subunit ribosomal RNA gene sequences. Parasitology Research 85, 877–883. doi: 10.1007/s004360050651CrossRefGoogle ScholarPubMed
Christensson, D. A. (1987). Clinical and serological response after experimental inoculation with Babesia divergens of newborn calves with and without maternal antibodies. Acta Veterinaria Scandinavica 28, 381–392.CrossRefGoogle ScholarPubMed
de Matos, C. (2008). Species composition and geographic distribution of ticks infesting cattle, goats and dogs in Maputo Province, Mozambique. M.Sc. (Veterinary Sciences) dissertation, Faculty of Veterinary Science, University of Pretoria.Google Scholar
De Vos, A. J. and Potgieter, F. T. (1994). Bovine babesiosis. In Infectious Diseases of Livestock with Special Reference to Southern Africa (ed. Coetzer, J. A. W., Thomson, G. R. and Tustin, R. C.). Oxford University Press, Cape Town, South Africa.Google Scholar
Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39, 783–791.CrossRefGoogle ScholarPubMed
Figueroa, J. V., Chieves, L. P., Johnson, G. S. and Buening, G. M. (1993). Multiplex polymerase chain reaction based assay for the detection of Babesia bigemina, Babesia bovis and Anaplasma marginale DNA in bovine blood. Veterinary Parasitology 50, 69–81. doi: 10.1016/0304-4017(93)90008-BCrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hilpertshauser, H., Deplazes, P., Schnyder, M., Gern, L. and Mathis, A. (2006). Babesia spp. identified by PCR in ticks collected from domestic and wild ruminants in southern Switzerland. Applied and Environmental Microbiology 72, 6503–6507. doi: 10.1128/AEM.00823-06CrossRefGoogle ScholarPubMed
Mahoney, D. F. and Ross, D. R. (1972). Epizootiological factors in the control of bovine babesiosis. Australian Veterinary Journal 37, 44–47.CrossRefGoogle Scholar
Mamman, M., Aliu, Y. O., and Peregrine, A. S. (1993). Comparative pharmacokinetics of diminazene in noninfected Boran (Bos indicus) cattle and Boran cattle infected with Trypanosoma congolense. Antimicrobial Agents and Chemotherapy 37, 1050–1055.CrossRefGoogle ScholarPubMed
Martins, T. M., Pedro, O. C., Caldeira, R. A., do Rosário, V. E., Neves, L. and Domingos, A. (2008). Detection of bovine babesiosis in Mozambique by a novel seminested hot-start PCR method. Veterinary Parasitology 153, 225–230. doi: 10.1016/j.vetpar.2008.01.037CrossRefGoogle ScholarPubMed
Molano, M., Meijer, C. J. L. M., Morré, S. A., Pol, R. and van den Brule, A. J. C. (2004). Combination of PCR targeting the VD2 of omp1 and reverse line blot analysis for typing of urogenital Chlamydia trachomatis serovars in cervical scrape specimens. Journal of Clinical Microbiology 42, 2935–2939. doi: 10.1128/JCM.42.7.2935-2939.2004CrossRefGoogle ScholarPubMed
Nijhof, A. M., Penzhorn, B. L., Lynen, G., Mollel, J. O., Morkel, P., Bekker, C. P., Jongejan, F. (2003). Babesia bicornis sp. nov. and Theileria bicornis sp. nov.: tick-borne parasites associated with mortality in the black rhinoceros (Diceros bicornis). Journal of Clinical Microbiology 41, 2249–2254. doi: 10.1128/JCM.41.5.2249–2254.2003CrossRefGoogle ScholarPubMed
Nindl, I., Köhler, A., Gottschling, M., Forschner, T., Lehmanna, M., Meijer, C. J. L. M., Snijders, P. J. F. and Stockfleth, E. (2007). Extension of the typing in a general-primer-PCR reverse-line-blotting system to detect all 25 cutaneous beta human papillomaviruses. Journal of Virological Methods 146, 1–4. doi: 10.1016/j.jviromet.2007.05.022CrossRefGoogle Scholar
Nyangiwe, N. and Horak, I. G. (2007). The species composition and seasonal abundance of free-living ticks on Döhne Sourveld and Eastern Province Thornveld. Ikhala, Research Bulletin of the Eastern Cape Department of Agriculture 2, 1–6.Google Scholar
Oura, C. A. L., Bishop, R. P., Wampande, E. M., Lubega, G. W. and Tait, A. (2004). Application of a reverse line blot assay to the study of haemoparasites in cattle in Uganda. International Journal for Parasitology 34, 603–613. doi: 10.1016/j.ijpara.2003.12.012CrossRefGoogle Scholar
Petrigh, R., Ruybal, P., Thompson, C., Neumann, R., Moretta, R., Wilkowsky, S., Draghi, G., Echaide, I., de Echaide, S. T. and Farber, M. (2008). Improved molecular tools for detection of Babesia bigemina. Annals of the New York Academy of Sciences 1149, 155–157. doi: 10.1196/annals.1428.038CrossRefGoogle ScholarPubMed
Salih, D. A., El Hussein, A. M., Seitzer, U. and Ahmed, J. S. (2007). Epidemiological studies on tick-borne diseases of cattle in Central Equatoria State, Southern Sudan. Parasitology Research 101, 1035–1044. doi: 10.1007/s00436-007-0583-yCrossRefGoogle ScholarPubMed
Schouls, L. M., van de Pol, I., Rijpkema, S. G. and Schot, C. S. (1999). Detection and identification of Ehrlichia, Borrelia burgdorferi Sensu Lato, and Bartonella species in Dutch Ixodes ricinus ticks. Journal of Clinical Microbiology 37, 2215–2222.CrossRefGoogle ScholarPubMed
Shkap, V., Leibovitz, B., Krigel, Y., Hammerschlag, J., Marcovics, A., Fish, L., Molad, T., Savitsky, I. and Mazuz, M. (2005). Vaccination of older Bos taurus bulls against bovine babesiosis. Veterinary Parasitology 129, 235–242. doi: 10.1016/j.vetpar.2005.01.013CrossRefGoogle ScholarPubMed
Sneath, P. H. A. and Sokal, R. R. (1973). Numerical Taxonomy. Freeman, San Francisco, CA, USA.Google Scholar
Sutherst, R. W. and Bourne, A. S. (2006). The effect of desiccation and low temperature on the viability of eggs and emerging larvae of the tick, Rhipicephalus (Boophilus) microplus (Canestrini) (Ixodidae). International Journal for Parasitology 36, 193–200. doi:10.1016/j.ijpara.2005.09.007CrossRefGoogle ScholarPubMed
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 1596–1599. doi: 10.1093/molbev/msm092CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Uilenberg, G. (2006). Babesia – a historical overview. Veterinary Parasitology 138, 3–10. doi: 10.1016/j.vetpar.2006.01.035CrossRefGoogle ScholarPubMed
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.16.4.622-636.2003CrossRefGoogle ScholarPubMed