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Infections by Babesia caballi and Theileria equi in Jordanian equids: epidemiology and genetic diversity

Published online by Cambridge University Press:  15 May 2013

MONEEB A. QABLAN ,
MIROSLAV OBORNÍK ,
KLÁRA J. PETRŽELKOVÁ ,
MICHAL SLOBODA ,
MUSTAFA F. SHUDIEFAT ,
PETR HOŘÍN ,
JULIUS LUKEŠ  and
DAVID MODRÝ
MONEEB A. QABLAN*
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic
MIROSLAV OBORNÍK
Affiliation:
Institute of Parasitology, Biology Centre, and Faculty of Sciences, University of South Bohemia, 370 05 České Budějovice, Czech Republic
KLÁRA J. PETRŽELKOVÁ
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic Institute of Vertebrate Biology, Czech Academy of Sciences, 603 00 Brno, Czech Republic Liberec Zoo, 460 01 Liberec, Czech Republic
MICHAL SLOBODA
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic
MUSTAFA F. SHUDIEFAT
Affiliation:
National Center for Research and Development, Badia Research Program, Amman, Jordan
PETR HOŘÍN
Affiliation:
Institute of Animal Genetics, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic CEITEC – Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic
JULIUS LUKEŠ
Affiliation:
Institute of Parasitology, Biology Centre, and Faculty of Sciences, University of South Bohemia, 370 05 České Budějovice, Czech Republic
DAVID MODRÝ
Affiliation:
Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic Institute of Parasitology, Biology Centre, and Faculty of Sciences, University of South Bohemia, 370 05 České Budějovice, Czech Republic CEITEC – Central European Institute of Technology, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic
*
*Corresponding author: Department of Pathology and Parasitology, Faculty of Veterinary Medicine, University of Veterinary and Pharmaceutical Sciences, 612 42 Brno, Czech Republic. E-mail: moneeb_78@hotmail.com
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Summary

Microscopic diagnosis of equine piroplasmoses, caused by Theileria equi and Babesia caballi, is hindered by low parasitaemia during the latent phase of the infections. However, this constraint can be overcome by the application of PCR followed by sequencing. Out of 288 animals examined, the piroplasmid DNA was detected in 78 (27·1%). Multiplex PCR indicated that T. equi (18·8%) was more prevalent than B. caballi (7·3%), while mixed infections were conspicuously absent. Sequences of 69 PCR amplicons obtained by the ‘catch-all’ PCR were in concordance with those amplified by the multiplex strategy. Computed minimal adequate model analyses for both equine piroplasmid species separately showed a significant effect of host species and age in the case of T. equi, while in the B. caballi infections only the correlation with host sex was significant. Phylogenetic analyses inferred the occurrence of three genotypes of T. equi and B. caballi. Moreover, a novel genotype C of B. caballi was identified. The dendrogram based on obtained sequences of T. equi revealed possible speciation events. The infections with T. equi and B. caballi are enzootic in all ecozones of Jordan and different genotypes circulate wherever dense horse population exists.

Keywords

JordanequineTheileria equiBabesia caballigenetic diversity
Type
Research Article
Information
Parasitology , Volume 140 , Issue 9 , August 2013 , pp. 1096 - 1103
Copyright
Copyright © Cambridge University Press 2013 

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References

REFERENCES

Abutarbush, S. M., Alqawasmeh, D. M., Mukbel, R. M. and Al-Majali, A. M. (2011). Equine babesiosis: seroprevalence, risk factors and comparison of different diagnostic methods in Jordan. Transboundary and Emerging Diseases 59, 72–78.CrossRefGoogle ScholarPubMed
Al-Eisawi, D. M. (1985). Vegetation of Jordan. In Studies in the History and Archaeology of Jordan. I (ed. Hadidi, A.), pp. 45–57. Ministry of Archaeology, Amman, Jordan.Google Scholar
Alhassan, A., Pumidonming, W., Okamura, M., Hirata, H., Battsetseg, B., Fujisaki, K., Yokoyama, N. and Igarashi, I. (2005). Development of a single-round and multiplex PCR method for the simultaneous detection of Babesia caballi and Babesia equi in horse blood. Veterinary Parasitology 129, 43–49.CrossRefGoogle ScholarPubMed
Allsopp, M. T. E. P. and Allsopp, B. A. (2006). Molecular sequence evidence for the reclassification of some Babesia species. Annals of the New York Academy of Sciences 1081, 509–517.CrossRefGoogle ScholarPubMed
Balkaya, I., Utuki, A. E. and Piskin, F. C. (2010). Prevalence of Theileria equi and B. caballi in donkeys from eastern Turkey in winter season. Pakistan Veterinary Journal 30, 245–246.Google Scholar
Bashiruddin, J. B., Cammà, C. and Rebêlo, E. (1999). Molecular detection of Babesia equi and Babesia caballi in horse blood by PCR amplification of part of the 16s rRNA gene. Veterinary Parasitology 84, 75–83.CrossRefGoogle ScholarPubMed
Battsetseg, B., Lucero, S., Xuan, X., Claveria, F. G., Inoue, N., Alhassan, A., Kanno, T., Igarashi, I., Nagasawa, H., Mikami, T. and Fujisaki, K. (2002). Detection of natural infection of Boophilus microplus with Babesia equi and Babesia caballi in Brazilian horses using nested polymerase chain reaction. Veterinary Parasitology 107, 351–357.CrossRefGoogle ScholarPubMed
Bhoora, R., Franssen, L., Oosthuizen, M. C., Guthrie, A. J., Zweygarth, E., Penzhorn, B. L., Jongejan, F. and Collins, N. E. (2009). Sequence heterogeneity in the 18S rRNA gene within Theileria equi and Babesia caballi from horses in South Africa. Veterinary Parasitology 159, 112–120.CrossRefGoogle ScholarPubMed
Boldbaatar, D., Xuan, X., Battsetseg, B., Igarashi, I., Battur, B., Batsukh, Z., Bayambaa, B., and Fujisaki, K. (2005). Epidemiological study of equine piroplasmosis in Mongolia. Veterinary Parasitology 127, 29–32.CrossRefGoogle ScholarPubMed
Brüning, A. (1996). Equine piroplasmosis, an update on diagnosis, treatment and prevention. British Veterinary Journal 152, 139–151.CrossRefGoogle ScholarPubMed
Cacciò, S., Cammà, C., Onuma, M. and Severini, C. (2000). The β-tubulin gene of Babesia and Theileria parasites is an informative marker for species discrimination. International Journal for Parasitology 30, 1181–1185.CrossRefGoogle ScholarPubMed
Chauvin, A., Moreau, E., Bonnet, S., Plantard, O. and Malandrin, L. (2009). Babesia and its host: adaptation to long-lasting interactions as a way to achieve efficient transmission. Veterinary Research 40, 37.CrossRefGoogle ScholarPubMed
Crawley, M. J. (2007). The R Book. John Wiley & Sons, Chichester, UK.CrossRefGoogle 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 II. Phylogenetic analysis and evolutionary history. Veterinary Parasitology 114, 173–194.CrossRefGoogle ScholarPubMed
De Waal, D. T. (1992). Equine piroplasmosis: a review. British Veterinary Journal 148, 6–14.CrossRefGoogle ScholarPubMed
Dos Santos, T. M., Roier, E. C., Santos, H. A., Pires, M. S., Vilela, J. A., Moraes, L. M., Almeida, F. Q., Baldani, C. D., Machado, R. Z. and Massard, C. L. (2011). Factors associated to Theileria equi in equids of two microregions from Rio de Janeiro, Brazil. Brazilian Journal of Veterinary Parasitology 20, 235–241.Google ScholarPubMed
Grandi, G., Molinari, G., Tittarelli, M., Sassera, D. and Kramer, L. H. (2011). Prevalence of Theileria equi and Babesia caballi infection in horses from northern Italy. Vector-Borne Zoonotic Diseases 11, 955–956.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696–704.CrossRefGoogle ScholarPubMed
Hailat, N. Q., Lafi, S. Q., Al-Darraji, A. M. and Al-Ani, F. K. (1997). Equine babesiosis associated with strenuous exercise: clinical and pathological studies in Jordan. Veterinary Parasitology 69, 1–8.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
Hunfeld, K. P., Hildebrandt, A. and Gray, J. S. (2008). Babesiosis: recent insights into an ancient disease. International Journal for Parasitology 38, 1219–1237.CrossRefGoogle ScholarPubMed
Karatepe, B., Karatepe, M., Cakmak, A., Karaer, Z. and Ergun, G. (2009). Investigation of seroprevalence of Theileria equi and Babesia caballi in horses in Nigde province, Turkey. Tropical Animal Health and Production 41, 109–113.CrossRefGoogle Scholar
Kouam, M. K., Kantzoura, V., Gajadhar, A. A., Theis, J. H., Papadopoulos, E. and Theodoropoulos, G. G. (2010 a). Seroprevalence of equine piroplasms and host-related factors associated with infection in Greece. Veterinary Parasitology 169, 273–278.CrossRefGoogle ScholarPubMed
Kouam, M. K., Kantzoura, V., Masouka, P. M., Gajadhar, A. A. and Theodoropoulos, G. (2010 b). Genetic diversity of equine piroplasms in Greece with a note on speciation within Theileria genotypes (T. equi and T. equi-like). Infection, Genetic and Evolution 10, 963–968.CrossRefGoogle Scholar
Kumar, S., Kumar, R., Gupta, A. K. and Dwivedi, S. K. (2008). Passive transfer of Theileria equi antibodies to neonate foals of immune tolerant mares. Veterinary Parasitology 151, 80–85.CrossRefGoogle ScholarPubMed
Lack, J. B., Reichard, M. V. and Van Den Bussche, R. A. (2012). Phylogeny and evolution of the piroplasmida as inferred from 18S rRNA sequences. International Journal for Parasitology 42, 353–363.CrossRefGoogle ScholarPubMed
Lassmann, T. and Sonnhammer, E. L. (2005). Kalign – an accurate and fast multiple sequence alignment algorithm. BMC Bioinformatics 6, 298.CrossRefGoogle ScholarPubMed
Moretti, A., Mangili, V., Salvatori, R., Maresca, C., Scoccia, E., Alessandra, T., Moretta, I., Gabrielli, S., Tampieri, M. P. and Pietrobelli, M. (2010). Prevalence and diagnosis of Babesia and Theileria infections in horses in Italy: a preliminary study. Veterinary Journal 184, 346–350.CrossRefGoogle ScholarPubMed
Nagore, D., García-Sanmartín, J., García-Pérez, A. L., Juste, R. A. and Hurtado, A. (2004). Detection and identification of equine Theileria and Babesia species by reverse line blotting: epidemiological survey and phylogenetic analysis. Veterinary Parasitology 123, 41–45.CrossRefGoogle ScholarPubMed
Pearson, R. A., Nengomasha, E. and Krecek, R. (2000). The challenge in using donkeys for work in Africa. In Donkeys, People and Development, a Resource Book of the Animal Traction Network for Eastern and Southern Africa (ATNESA). (ed. Starkey, P. and Fielding, D.), pp. 194–195. ACP-EUT Technical Center for Agricultural and Rural Cooperation (CTA), Wageningen, the Netherlands.Google Scholar
Qablan, M. A., Kubelová, M., Široký, P., Modrý, M. and Amr, Z. S. (2012 a). Stray dogs of northern Jordan as reservoirs of ticks and tick-borne haemopathogens. Parasitology Research 111, 301–307.CrossRefGoogle Scholar
Qablan, M. A., Sloboda, M., Jirků, M., Oborník, M., Dwairi, S., Amr, Z. S., Hořín, P., Lukeš, J. and Modrý, M. (2012 b). Quest for the piroplasms in camels: identification of Theileria equi and Babesia caballi in Jordanian dromedaries by PCR. Veterinary Parasitology 186, 456–460.CrossRefGoogle ScholarPubMed
Roberts, C. W., Walker, W. and Alexander, J. (2001). Sex-associated hormones and immunity to protozoan parasites. Clinical Microbiology Reviews 14, 476–488.CrossRefGoogle ScholarPubMed
Rüegg, S. R., Torgerson, P., Deplazes, P. and Mathis, A. (2007). Age-dependent dynamics of Theileria equi and Babesia caballi infections in southwest Mongolia based on IFAT and/or PCR prevalence data from domestic horses and ticks. Parasitology 134, 939–947.CrossRefGoogle ScholarPubMed
Salim, B., Bakheit, M. A., Kamau, J., Nakamura, I. and Sugimoto, C. (2010). Nucleotide sequence heterogeneity in the small subunit ribosomal RNA gene Theileria equi from horses in Sudan. Parasitology Research 106, 493–498.CrossRefGoogle ScholarPubMed
Shkap, V., Cohen, I., Leibovitz, B., Savitsky, Pipano E., Avni, G., Shofer, S., Giger, U., Kappmeyer, L. and Knowles, D. (1998). Seroprevalence of Babesia equi among horses in Israel using competitive inhibition ELISA and IFA assays. Veterinary Parasitology 76, 251–259.CrossRefGoogle ScholarPubMed
Schnittger, L., Rodriguez, A. E., Florin-Christensen, M. and Morrison, D. A. (2012). Babesia: a world emerging. Infection, Genetic and Evolution 12, 1788–1809.CrossRefGoogle ScholarPubMed
Sloboda, M., Jirků, M., Lukešová, D., Qablan, M. A., Batsukh, Z., Fiala, I., Hořín, P., Modrý, M. and Lukeš, J. (2011). A survey of piroplasmids in horses and Bactrian camels in North-Eastern Mongolia. Veterinary Parasitology 179, 246–249.CrossRefGoogle ScholarPubMed
Starkey, P. and Starkey, M. (2000). Regional and world trends in donkey populations. In Donkeys, People and Development, a Resource Book of the Animal Traction Network for Eastern and Southern Africa (ATNESA). (ed. Starkey, P. and Fielding, D.), pp. 10–12. ACP-EUT Technical Center for Agricultural and Rural Cooperation (CTA), Wageningen, the Netherlands.Google Scholar
Swofford, D. L. (2002). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0b10 (Alvitec). Sinauer Associates, Sunderland, MA, USA.Google Scholar
Zobba, R., Ardu, M., Niccolini, S., Chessa, B., Manna, L., Cocco, R. and Parpaglia, M. L. P. (2008). Clinical and laboratory findings in equine piroplasmosis. Journal of Equine Veterinary Science 28, 301–308.CrossRefGoogle Scholar