Parasitology Research

, Volume 116, Issue 2, pp 751–762 | Cite as

Molecular detection and genetic diversity of bovine Babesia spp., Theileria orientalis, and Anaplasma marginale in beef cattle in Thailand

  • Charoonluk Jirapattharasate
  • Paul Franck Adjou Moumouni
  • Shinuo Cao
  • Aiko Iguchi
  • Mingming Liu
  • Guanbo Wang
  • Mo Zhou
  • Patrick Vudriko
  • Artemis Efstratiou
  • Tanasak Changbunjong
  • Sivapong Sungpradit
  • Parntep Ratanakorn
  • Walasinee Moonarmart
  • Poonyapat Sedwisai
  • Thekhawet Weluwanarak
  • Witsanu Wongsawang
  • Hiroshi Suzuki
  • Xuenan Xuan
Original Paper
First Online:
Received:
Accepted:

Abstract

Babesia spp., Theileria orientalis, and Anaplasma marginale are significant tick-borne pathogens that affect the health and productivity of cattle in tropical and subtropical areas. In this study, we used PCR to detect the presence of Babesia bovis, Babesia bigemina, and T. orientalis in 279 beef cattle from Western Thailand and A. marginale in 608 beef cattle from the north, northeastern, and western regions. The PCRs were performed using species-specific primers based on the B. bovis spherical body protein 2 (BboSBP2), B. bigemina rhoptry-associated protein 1a (BbiRAP-1a), T. orientalis major piroplasm surface protein (ToMPSP), and A. marginale major surface protein 4 (AmMSP4) genes. To determine the genetic diversity of the above parasites, amplicons of B. bovis and B. bigemina ITS1-5.8s rRNA gene-ITS2 regions (B. bovis ITS, B. bigemina ITS), ToMPSP, and AmMSP4 genes were sequenced for phylogenetic analysis. PCR results revealed that the prevalence of B. bovis, B. bigemina, T. orientalis, and A. marginale in the Western region was 11.1, 12.5, 7.8, and 39.1 %, respectively. Coinfections of two or three parasites were observed in 17.9 % of the animals sampled. The study revealed that the prevalence of A. marginale in the western region was higher than in the north and northeastern regions (7 %). Sequence analysis showed the BboSBP2 gene to be more conserved than B. bovis ITS in the different isolates and, similarly, the BbiRAP-1a was more conserved than B. bigemina ITS. In the phylogenetic analysis, T. orientalis MPSP sequences were classified into types 3, 5, and 7 as previously reported. A. marginale MSP4 gene sequences shared high identity and similarity with each other and clustered with isolates from other countries. This study provides information on the prevalence and genetic diversity of tick-borne pathogens in beef cattle and highlights the need for effective strategies to control these pathogens in Thailand.

Keywords

Babesia spp. Theileria orientalis Anaplasma marginale Phylogenetic tree Beef cattle Thailand 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgements

This study was financially supported by Grants in Aid for Scientific Research from Ministry of Education, Culture, Sports, Science and Technology (MEXT) (26304036), Japan and Faculty of Veterinary Medicine, Mahidol University (0517.131/0001). The authors would like to appreciate the contribution of the field veterinarians, farmer, and staff of Monitoring and Surveillance Center for Zoonotic Disease in Wildlife and Exotic Animals (MoZWE), Chiangrai, Payao, Mae Hong Sorn, Kanchanaburi Provincial Livestock Office, Bureau of Biotechnology in Livestock Production and Khon Kaen Artificial Insemination and Biotechnology Center.

References

  1. AbouLaila M, Yokoyama N, Igarashi I (2010) Development and evaluation of a nested PCR based on spherical body protein 2 gene for the diagnosis of Babesia bovis infection. Vet Parasitol 169:45–50CrossRefPubMedGoogle Scholar
  2. Altangerel K, Lan DTB, Long PT, Ueno A, Li Y, Luo Y, Macedo AC, Matsumoto K, Inokuma H, Kawazu S, Igarachi I, Xuan X, Yokoyama N (2011a) Molecular epidemiological survey of Theileria orientalis in Thua Thien Hue province, Vietnam. J Vet Med Sci 73:701–705CrossRefGoogle Scholar
  3. Altangerel K, Sivakumar T, Inpankaew T, Jittapalapong S, Terkawi MA, Ueno A, Xuan X, Igarachi I, Yokoyama N (2011b) Molecular prevalence of different genotypes of Theileria orientalis detected from cattle and water buffaloes in Thailand. J Parasitol 97:1075–1079CrossRefPubMedGoogle Scholar
  4. Altay K, Aydin MF, Dumanli N, Aktas M (2008) Molecular detection of Theileria and Babesia infections in cattle. Vet Parsitol 158:295–301CrossRefGoogle Scholar
  5. Aparna M, Ravindran R, Vimalkumar MB, Lakshmanan B, Rameshkumar P, Kumar KG, Kumar A, Promod K, Ajithkumar S, Ravishankar C, Devada K, Subramanian H, George JA, Ghosh S (2011) Molecular characterization of Theileria orientalis causing fatal infection in crossbred adult bovines of South India. Parasitol Int 60:524–529CrossRefPubMedGoogle Scholar
  6. Aubry A, Geale DW (2011) A review of bovine anaplasmosis. Transbound Emerg Dis 58:1–30CrossRefPubMedGoogle Scholar
  7. Bock R, Jackson L, de Vos A, Jorgensen W (2004) Babesiosis of cattle. Parasitology 129(Suppl):247–269CrossRefGoogle Scholar
  8. Bostrom B, Wolf C, Greene C, Peterson DS (2008) Sequence conservation in the rRNA first internal transcribed spacer region of Babesia gibsoni genotype Asia isolates. Vet Parasitol 152:152–157CrossRefPubMedGoogle Scholar
  9. Cao S, Aboge GO, Terkawi MA, Yu L, Kamyingkird K, Luo Y, Li Y, Goo YK, Yamagishi J, Nishikawa Y, Yokoyama N, Suzuki H, Igarashi I, Maeda R, Inpankaew T, Jittapalapong S, Xuan X (2012) Molecular detection and identification of Babesia bovis and Babesia bigemina in cattle in northern Thailand. Parasitol Res 111:1259–1266CrossRefPubMedGoogle Scholar
  10. Chanbunjong T, Buddhirongawatr R, Suwanpakdee S, Yongyuttawichai P, Cheewajorn P, Jangjaras J, Sangloung C, Ratanakorn P (2009) A survey of ectoparasitic arthropods on domestic animals in Tak province, Thailand. Southeast Asian J Trop Med Public Health 40:435–442Google Scholar
  11. De la Fuente J, Lew A, Lutz H, Meli ML, Hofmann-Lehmann R, Shkap V, Molad T, Mangold AJ, Almazán C, Naranjo V, Gortázar C, Torina A, Caracappa S, García-Pérez AL, Barral M, Oporto B, Ceci L, Carelli G, Blouin EF, Kocan KM (2005) Genetic diversity of Anaplasma species major surface protein and implications for anaplasmosis serodiagnosis and vaccine development. Anim Health Res Rev 6:75–89CrossRefPubMedGoogle Scholar
  12. Everitt JI, Shadduck JA, Steinkamp C, Clabaugh G (1986) Experimental Babesia bovis infection in Holstein calves. Vet Pathol 23:556–562CrossRefPubMedGoogle Scholar
  13. Fujisaki K (1992) A review of the taxonomy of Theileria sergenti/buffeli/orientalis group parasites in cattle. J Protozool Res 2:87–96Google Scholar
  14. Hammer JF, Jenkins C, Bogema D, Emery D (2016) Mechanical transfer of Theileria orientalis: possible roles of biting arthropods, colostrum and husbandry practices in disease transmission. Parasite Vector 9:34CrossRefGoogle Scholar
  15. Hofmann-Lehmann R, Meli ML, Dreher UM, Gönczi E, Deplazes P, Braun U, Engels M, Schüpbach J, Jörger K, Thoma R, Griot C, Stärk KD, Willi B, Schmidt J, Kocan KM, Lutz H (2004) Concurrent infections with vector-borne pathogens associated with fatal hemolytic anemia in a cattle herd in Switzerland. J Clin Microbiol 42:3775–3780CrossRefPubMedPubMedCentralGoogle Scholar
  16. Humphry RW, Cameron GJ, Gunn GJ (2004) A practical approach to calculate sample size for herd prevalence surveys. Prev Vet Med 14:173–188CrossRefGoogle Scholar
  17. Ibrahim HM, Adjou Moumouni PF, Mohammed-Geba K, Sheir SK, Hashem ISX, Cao S, Terkawi MA, Kamyingkird K, Nishikawa Y, Suzuki H, Xuan X (2013) Molecular and serological prevalence of Babesia bigemina and Babesia bovis in cattle and water buffalos under small-scale dairy farming in Beheira and Faiyum Provinces, Egypt. Vet Parasitol 198:187–192CrossRefPubMedGoogle Scholar
  18. Jirapattharasate C, Adjou Moumouni PF, Cao S, Iguchi A, Liu M, Wang G, Zhou M, Vudriko P, Changbunjong T, Sungpradit S, Ratanakorn P, Moonarmart W, Sedwisai P, Weluwanarak T, Wongsawang W, Suzuki H, Xuan X (2016) Molecular epidemiology of bovine Babesia spp. and Theileria orientalis parasites in beef cattle from northern and northeastern Thailand. Parasitol Int 65:62–69CrossRefPubMedGoogle Scholar
  19. Kamau J, de Vos AJ, Platford M, Salim B, Kinyajui P, Sugimoto C (2011) Emergence of new types of Theileria orientalis in Australian cattle and possible cause of theileriosis outbreaks. Parasite Vector 4:22CrossRefGoogle Scholar
  20. Kocan KM, de la Fuente J, Blouin EF, Coetzee JF, Ewing SA (2010) The natural history of Anaplasma marginale. Vet Parasitol 167:95–107CrossRefPubMedGoogle Scholar
  21. Liu Z, Ma M, Wang Z, Peng Y, Li Y, Guan G, Luo J, Yin H (2012) Molecular survey and genetic identification of Anaplasma species in goats from central and south China. Appl Environ Microbiol 78:464–470CrossRefPubMedPubMedCentralGoogle Scholar
  22. McFadden AMJ, Rawdon TG, Meyer J, Makin J, Morley CM, Clough RR, Tham K, Müllner P, Geysen D (2011) An outbreak of haemolytic anaemia associated with infection of Theileria orientalis in naïve cattle. N Z Vet J 59:79–85CrossRefPubMedGoogle Scholar
  23. Mukhebi AW, Perry BD, Kruska R (1992) Estimated economics of theileriosis control in Africa. Prev Vet Med 12:78–85CrossRefGoogle Scholar
  24. Nagano D, Sivakumar T, De Macedo AC, Inpankaew T, Alhassan A, Igarashi I, Yokoyama N (2013) The genetic diversity of merozoite surface antigen (MSA-1) among Babesia bovis detected from cattle populations in Thailand, Brazil and Ghana. J Vet Med Sci 75:1463–1470CrossRefPubMedPubMedCentralGoogle Scholar
  25. Niu Q, Luo J, Guan G, Liu Z, Ma M, Liu A, Gao J, Ren Q, Li Y, Qiu J, Yin H (2009) Differentiation of two ovine Babesia based on the ribosomal DNA internal transcribed spacer (ITS) sequences. Exp Parasitol 121:64–68CrossRefPubMedGoogle Scholar
  26. Oliveira-Sequeira TCG, Oliveira MCS, Araujo JP, Amarante AFT (2005) PCR-based detection of Babesia bovis and Babesia bigemina in their natural host Boophilus microplus and cattle. Int J Parasitol 35:105–111CrossRefPubMedGoogle Scholar
  27. Ota N, Mizuno D, Kuboki N, Igarashi I, Nakamura Y, Yamashina H, Hanzaike T, Fujii K, Ones S, Hata H, Kondo S, Matsui S, Koga M, Matsumoto K, Inokuma H, Yokoyama N (2009) Epidemiological survey of Theileria orientalis infection in grazing cattle in the eastern part of Hokkaido, Japan. J Vet Med Sci 71:937–944CrossRefPubMedGoogle Scholar
  28. Palmer GH, Rurangirwa ER, McElwain TF (2001) Strain composition of the Ehrlichia Anaplasma marginale within persistently infected cattle, a mammalian reservoir for tick transmission. J Clin Microbiol 39:631–635CrossRefPubMedPubMedCentralGoogle Scholar
  29. Perera PK, Gasser RB, Anderson GA, Jeffers M, Bell CM, Jabbar A (2013) Epidemiological survey following oriental theileriosis outbreaks in Victoria, Australia, on selected cattle farms. Vet Parasitol 197:509–521CrossRefPubMedGoogle Scholar
  30. Richey EJ, Palmer GH (1990) Bovine anaplasmosis. Compend Contin Educ Pract Vet 12:1661–1668Google Scholar
  31. Saetiew N, Simking P, Saengow S, Kurajog B, Yimming B, Saeng-chuto K, Chimnoi W, Kengradomkil C, Yangtara S, Suksai S, Thaprathom N, Seneemanoma C, Penghirun K, Desquesnes M, Herder S, Morand S, Jittapalapong S (2014) Seasonal effect on Anaplasma marginale infections of beef cattle in previously flooding areas. Proceeding of 52nd Kasetsart University Annual Conference: Animal, Veterinary Medicine (Suppl): 267–277Google Scholar
  32. Saetiew N, Simking P, Inpankaew T, Wongpanit K, Kamyingkird K, Wongnakphet S, Stich RW, Jittapalapong S (2015) Prevalence and genetic diversity of Anaplasma marginale infections in water buffaloes in Northeast Thailand. J Trop Med Parasitol 38:9–16Google Scholar
  33. Simking P, Saengow S, Bangphoomi K, Sarataphan N, Wongnarkpet S, Inpankaew T, Jittapalapong S, Munkhjargal T, Sivakumar T, Yokoyama N, Igarashi I (2013) The molecular prevalence and MSA-2b gene-based genetic diversity of Babesia bovis in daily cattle in Thailand. Vet Parasitol 197:642–648CrossRefPubMedGoogle Scholar
  34. Sivakumar T, Hayashida K, Sugimoto C, Yokoyama N (2014) Evolution and genetic diversity of Theileria. Infect Genet Evol 27:250–263CrossRefPubMedGoogle Scholar
  35. Suarez CE, Noh S (2011) Emerging perspectives in the research of bovine babesiosis and anaplasmosis. Vet Parasitol 180:109–125CrossRefPubMedGoogle Scholar
  36. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetic analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefPubMedPubMedCentralGoogle Scholar
  37. Tananyutthawongese C, Saengsombat K, Sukhumsirichat W, Uthaisang W, Sarataphan N, Chansiri K (1999) Detection of bovine hemoparasite infection using multiplex polymerase chain reaction. Sci Asia 25:85–90CrossRefGoogle Scholar
  38. Terkawi MA, Huyen NX, Cao S, Inpankaew T, Maklon K, Aboulaila M, Ueno A, Goo YK, Yokoyama N, Jittapalapong S, Xuan X, Igarashi I (2011) Molecular and serological prevalence of Babesia bovis and Babesia bigemina in water buffaloes in the northeast region of Thailand. Vet Parasitol 178:201–207CrossRefPubMedGoogle Scholar
  39. Torina A, Agnone A, Blanda V, Alongi A, D’Agostino A, Caracappa S, Marino AM, Di Macro V, de la Fuente J (2012) Development and validation of two PCR tests for the detection of and differentiation between Anaplasma ovis and Anaplasma marginale. Ticks Tick Borne Dis 3:282–286CrossRefGoogle Scholar
  40. Uilenberg G (1995) International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Vet Parasitol 57:19–41CrossRefPubMedGoogle Scholar
  41. Weir W, Karagenc T, Baird M, Tait A, Shiels BR (2010) Evolution and diversity of secretome genes in the apicomplexan parasite Theileria annulata. BMC Genomics 11:11–42CrossRefGoogle Scholar
  42. Ybañez AD, Sivakumar T, Ybañez RHD, Vincoy MRB, Tingson JA, Perez ZO, Gabotero SR, Buchorno LP, Inoue N, Matsumoto K, Inokuma H, Yokoyama N (2013) Molecular survey of bovine vector-borne pathogens in Cebu, Philippines. Vet Parasitol 196:13–20CrossRefPubMedGoogle Scholar
  43. Zhou M, Cao S, Sevinc F, Sevinc M, Ceylan O, Adjou Moumouni PF, Jirapattharasate C, Liu M, Wang G, Iguchi A, Vudriko P, Suzuki H, Xuan X (2016) Molecular detection and genetic identification of Babesia bigemina, Theileria annulata, Theileria orientalis and Anaplasma marginale in Turkey. Ticks Tick Borne Dis 7:126–134CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Charoonluk Jirapattharasate
    • 1
    • 2
  • Paul Franck Adjou Moumouni
    • 1
  • Shinuo Cao
    • 1
  • Aiko Iguchi
    • 1
  • Mingming Liu
    • 1
  • Guanbo Wang
    • 1
  • Mo Zhou
    • 1
  • Patrick Vudriko
    • 1
  • Artemis Efstratiou
    • 1
  • Tanasak Changbunjong
    • 2
  • Sivapong Sungpradit
    • 2
  • Parntep Ratanakorn
    • 3
  • Walasinee Moonarmart
    • 3
  • Poonyapat Sedwisai
    • 4
  • Thekhawet Weluwanarak
    • 4
  • Witsanu Wongsawang
    • 5
  • Hiroshi Suzuki
    • 1
  • Xuenan Xuan
    • 1
  1. 1.National Research Center for Protozoan DiseasesObihiro University of Agriculture and Veterinary MedicineObihiroJapan
  2. 2.Department of Pre-clinic and Applied Animal Science, Faculty of Veterinary ScienceMahidol UniversitySalayaThailand
  3. 3.Department of Clinical Science and Public Health, Faculty of Veterinary ScienceMahidol UniversitySalayaThailand
  4. 4.The Monitoring and Surveillance Center for Zoonotic Diseases in Wildlife and Exotic Animals, Faculty of Veterinary ScienceMahidol UniversitySalayaThailand
  5. 5.Livestock and Wildlife Hospital, Faculty of Veterinary ScienceMahidol UniversityKanchanaburiThailand

Personalised recommendations