Molecular detection of piroplasms in haematophagus flies in the Nakhon Pathom and Kanchanaburi Provinces, Thailand
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Published:
Aug 21, 2018
Keywords:
Haematophagus flies Theileria spp Babesia spp. Thailand
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Abstract
Theileria spp. and Babesia spp are tick-borne protozoan parasites that infect a wide range of domestic and wild animals. In this study, the haematophagus flies (Stomoxys and tabanids) from Kanchanaburi and Nakhon Pathom Provinces, Thailand were investigated for the presence of piroplasm DNA. All specimens were morphologically identified. The piroplasms in the insect specimens were first screened by PCR using Babesia and Theleria 18S rRNA gene and species-specific sequences based on B. bovis spherical body protein 2, B. bigemina rhoptry-associated protein 1a and Theileria spp. Sequencing was used to confirm the identity of all amplicons. In total, 68 blood sucking insects were morphologically identified as Tabanus spp. (79.41%), Stomoxys spp. (13.24%), Haematobosca spp. (5.88%) and Chrysops spp. (1.47%). PCR results showed only 2 samples were positive for Theileria spp. while all specimens were negative for Babesia spp. Based on sequence and phylogenetic analysis, Theileria spp. 18S rRNA sequences were classified into T. ovis and T. sinensis which share high identity and similarity with isolates from other countries. In this study, we describe for the first time the detection of T. sinensis in tabanid fly. We therefore recommend further investigations to confirm the biting files as a biological or mechanical vector of theses pathogens, particularly Tabanus spp, which should be regarded as a potential vector for transmission of Theileria among domestic animals in Thailand.
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Jirapattharasate, C., Changbunjong, T., Sedwisai, P., & Weluwanarak, T. (2018). Molecular detection of piroplasms in haematophagus flies in the Nakhon Pathom and Kanchanaburi Provinces, Thailand. Veterinary Integrative Sciences, 16(2), 123–133. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/141619
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References
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Cao, S., Zhang, S., Jia, L., Xue, S., Yu, L., Kamyingkird, K., Moumouni, P.F., Moussa, A.A., Zhou, M., Zhang, Y., Terkawi, M.A., Masatani, T.,Nishikawa, Y., Xuan, X., 2013. Molecular detection of Theileria species in sheep from northern China. J. Vet. Med. Sci. 75, 1227-1230.
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Georges, K., Loria, G.R., Riili, S., Greco, A., Caracappa, S., Jongejan, F.,Sparagano, O., 2001. Detection of haemoparasites in cattle by reverse line blot hybridization with a note on the distribution of ticks in Sicily. Vet. Parasitol. 99, 273–286.
Hammer, J.F., Jenkins, C., Bogema, D., Emery, D., 2016. Mechanical transfer of Theileria orientalis: possible roles of biting arthropods, colostrum and husbandry practices in disease transmission. Parasit Vector. 9: 34.
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Jirapattharasate, C., Adjou Moumouni, P.F., Cao, S., Iguchi, A., Liu, M., Wang, G., Zhou, M., Vudriko, P., Efstratiou, A., Changbunjong, T., Sungpradit, S., Ratanakorn, P., Moonarmart, W., Sedwisai, P., Weluwanarak, T, Wongsawang, W., Suzuki, H., Xuan, X., 2017. Molecular detection and genetic diversity of bovine Babesia spp., Theileria orientalis, and Anaplasma marginale in beef cattle in Thailand. Parasitol. Res. 116, 751-762.
Kaewhom, P and Thitasarn, W., 2017. The prevalence of Theileria spp. of goat in Watthana Nakhon District, Sa Kaeo Province. Journal of Mahanakorn Veterinary Medicine. 12, 57-66. (In Thai)
Kamau, J., de Vos, A.J., 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. Parasit Vector. 4, 22.
Lee, S.H., Kim, K.T., Kwon, O.D., Ock, Y., Kim, T., Choi, D., Kwak, D., 2016. Novel detection of Coxiella spp., Theileria luwenshuni, and T. ovis endosymbionts in deer keds (Lipoptena fortisetosa). PLos ONE, DOI: 10.1371/journal.pone.0156727
Liu, J., Guan, G., Liu, Z., Liu, A., Ma, M., Bai, Q, Yin, H., Luo J., 2012. Additional data for a new Theileria sp. from China based on the sequences of ribosomal RNA internal transcribed spacers. Exp. Parasitol. 133, 217-221.
Mans, B.J., Pienaar, R., Latif, A.A., 2015. A review of Theileria diagnostics and epidemiology. Int J Parasitol Parasites Wildl. 4, 104-118.
Mehlhorn, H., Schein, E., 1985. The piroplasms: Life cycle and sexual stages. Advances in Parasitology APL, 23, 4th edition. Academic Press, pp. 38-105.
Mukhebi, A.W., Perry, B.D., Kruska, R., 1992. Estimated economics of theileriosis control in Africa. Prev. Vet. Med. 12, 78-85.
Phasuk, J., Sa-nguansab, S., Pinyopanuwat, N., Chimnoi, W., Jittapalapong, S., 2010. Diversity and seasonal abundance of blood-sucking flies in dairy farms in Amphur Muaklek of Saraburi province. Proceedings of 48th Kasetsart University Annual Conference: Veterinary Medicine, 128-137.
Phasuk, J., Prabaripai, A., Chareonviriyaphap, T., 2013. Seasonality and daily flight activity of stable flies (Diptera: Muscidae) on dairy farms in Saraburi Province, Thailand. Parasaite. 20, 17.
Sivakumar, T., Hayashida, K., Sugimoto, C., Yokoyama, N., 2014. Evolution and genetic diversity of Theileria. Infect. Genet. Evol. 27, 250-263.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetic analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729.
Terkawi, M.A., Huyen, N.X., Cao, S., Inpankaew, T., Maklon, K., Aboulaila, M., Ueno, A., Goo, Y.K., 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, 201-207.
Tumrasvin, W. and Shinonaga, S., 1978. Studies on medically important flies in Thailnd. V. On 32 species belonging to the subfamilies Muscinae and Stomoxyinae including the taxonomic keys (Diptera: Muscidae). Bull Tokyo Med Dent Univ. 25, 201-227.
Tumrasvin, W., 1989. Tabanus species and their distribution in Thailand (Diptera: Tabanidae). Southeast Asian J. Trop. Med. Public Health. 20, 319-323.
Tunnakundacha, S., Desquesnes, M., Masmeatathip, R., 2017. Comparison of Vavoua, Malaise and Nzi traps with and without attractants for trapping of Stomoxys spp. (Diptera: Muscidae) and tabanids (Diptera: Tabanidae) on cattle farms. Agriculture and Natural Resources. 51, 319-323.
Uilenberg, G., 1995. International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Vet Parasitol. 57, 19-41.
Watts, J.G., Playford, M.C., Hickey, K.L., 2016. Theileria orientalis: a review. N Z Vet J. 64, 3-9.
Zumpt, F., 1973. Stomoxyine biting flies of the world. Gustav Fisher Verlag, pp. 175.
Altangerel, K., Sivakumar, T., Inpankaew, T., Jittapalapong, S., Terkawi, M.A.,Ueno, A., Xuan, X., Igarachi, I., Yokoyama, N., 2011. Molecular prevalence of different genotypes of Theileria orientalis detected from cattle and water buffaloes in Thailand. J Parasitol. 97, 1075-1079.
Bai, Q., Liu, G.Y., Yin, H., Zhao, Q.Z., Liu, D.K., Ren, J.X., Li, X., 2002. Theileria sinensis nov: study on molecular taxonomy. Acta. Anim. Husb. Vet. Sci. 33, 185-190.
Baldacchino, F., Muenworn, V., Desquesnes, M., Desoli, F., Charoenviriyaphap,T., Duvallet G., 2013. Transmission of pathogens by Stomoxys flies (Diptera, Muscidae): a review. Parasite. 20, 26.
Bock, R., Jackson, L., de Vos, A., Jorgensen, W., 2004. Babesiosis of cattle. Parasitology. 129 (Suppl), 247-269.
Cao, S., Zhang, S., Jia, L., Xue, S., Yu, L., Kamyingkird, K., Moumouni, P.F., Moussa, A.A., Zhou, M., Zhang, Y., Terkawi, M.A., Masatani, T.,Nishikawa, Y., Xuan, X., 2013. Molecular detection of Theileria species in sheep from northern China. J. Vet. Med. Sci. 75, 1227-1230.
Changbunjong, T., Sungpradit, S., Kanthasaewee, O., Sedwisai, P., Tangsudjai,S., Ruangsittichai, J., 2016. Molecular detection of Theileria and Babesia in a diversity of Stomoxyini flies (Diptera: Muscidae) from Khao Yai National Park, Thailand. Thai. J. Vet. Med. 46, 227-234.
Changbunjong, T., Sedwisai, P., Weluwanarak, T., Nitiyamatawat, E.,Sariwongchan, R., Chareonviriyaphap T., 2018. Species diversity and abundance of Tabanus spp. (Diptera: Tabanidae) in different habitats of Thailand. J. Asia Pac. Entomol. 21, 134-139.
Everitt, J.I., Shadduck, J.A., Steinkamp, C., Clabaugh, G., 1986. Experimental Babesia bovis infections in Holstein Calves. Vet. Pathol. 23, 556-562.
Fernández de Marco, M., Brugman, V.M., Hernández-Triana, L.M., Thorne,L., Phipps, L.P., Nikolov, N.I., Fooks, A.R., Johnson, N., 2016. Detection of Theileria orientalis in mosquito blood meals in the United Kingdom. Vet. Parasitol. 229, 31-36.
Fujisaki, K., Kamio, T., Kawazu, S., Shimizu, S., Shimura, K., 1993. Theileria sergenti: experimental transmission by the long-nosed cattle louse, Linognathus vituli. Ann. Trop. Med. Parasitol. 87, 217-218.
Georges, K., Loria, G.R., Riili, S., Greco, A., Caracappa, S., Jongejan, F.,Sparagano, O., 2001. Detection of haemoparasites in cattle by reverse line blot hybridization with a note on the distribution of ticks in Sicily. Vet. Parasitol. 99, 273–286.
Hammer, J.F., Jenkins, C., Bogema, D., Emery, D., 2016. Mechanical transfer of Theileria orientalis: possible roles of biting arthropods, colostrum and husbandry practices in disease transmission. Parasit Vector. 9: 34.
Hunt, G.J., 1997. Insect DNA extraction protocol. Fingerprinting methods based on arbitrarily primed PCR (ed. by M. R. Micheliand R. Bova), Springer-Verlag, Berlin. pp. 21–24.
Izzo, M.M., Poe, I., Horadagoda, N., de Vos, A.J., House, J.K., 2010. Haemolytic anemia in cattle in NSW associated with Theleria infections. Aust. Vet. J. 88, 45-51.
Jirapattharasate, C., Adjou Moumouni, P.F., Cao, S., Iguchi, A., Liu, M., Wang, G., Zhou, M., Vudriko, P., Efstratiou, A., Changbunjong, T., Sungpradit, S., Ratanakorn, P., Moonarmart, W., Sedwisai, P., Weluwanarak, T, Wongsawang, W., Suzuki, H., Xuan, X., 2017. Molecular detection and genetic diversity of bovine Babesia spp., Theileria orientalis, and Anaplasma marginale in beef cattle in Thailand. Parasitol. Res. 116, 751-762.
Kaewhom, P and Thitasarn, W., 2017. The prevalence of Theileria spp. of goat in Watthana Nakhon District, Sa Kaeo Province. Journal of Mahanakorn Veterinary Medicine. 12, 57-66. (In Thai)
Kamau, J., de Vos, A.J., 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. Parasit Vector. 4, 22.
Lee, S.H., Kim, K.T., Kwon, O.D., Ock, Y., Kim, T., Choi, D., Kwak, D., 2016. Novel detection of Coxiella spp., Theileria luwenshuni, and T. ovis endosymbionts in deer keds (Lipoptena fortisetosa). PLos ONE, DOI: 10.1371/journal.pone.0156727
Liu, J., Guan, G., Liu, Z., Liu, A., Ma, M., Bai, Q, Yin, H., Luo J., 2012. Additional data for a new Theileria sp. from China based on the sequences of ribosomal RNA internal transcribed spacers. Exp. Parasitol. 133, 217-221.
Mans, B.J., Pienaar, R., Latif, A.A., 2015. A review of Theileria diagnostics and epidemiology. Int J Parasitol Parasites Wildl. 4, 104-118.
Mehlhorn, H., Schein, E., 1985. The piroplasms: Life cycle and sexual stages. Advances in Parasitology APL, 23, 4th edition. Academic Press, pp. 38-105.
Mukhebi, A.W., Perry, B.D., Kruska, R., 1992. Estimated economics of theileriosis control in Africa. Prev. Vet. Med. 12, 78-85.
Phasuk, J., Sa-nguansab, S., Pinyopanuwat, N., Chimnoi, W., Jittapalapong, S., 2010. Diversity and seasonal abundance of blood-sucking flies in dairy farms in Amphur Muaklek of Saraburi province. Proceedings of 48th Kasetsart University Annual Conference: Veterinary Medicine, 128-137.
Phasuk, J., Prabaripai, A., Chareonviriyaphap, T., 2013. Seasonality and daily flight activity of stable flies (Diptera: Muscidae) on dairy farms in Saraburi Province, Thailand. Parasaite. 20, 17.
Sivakumar, T., Hayashida, K., Sugimoto, C., Yokoyama, N., 2014. Evolution and genetic diversity of Theileria. Infect. Genet. Evol. 27, 250-263.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetic analysis version 6.0. Mol. Biol. Evol. 30, 2725-2729.
Terkawi, M.A., Huyen, N.X., Cao, S., Inpankaew, T., Maklon, K., Aboulaila, M., Ueno, A., Goo, Y.K., 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, 201-207.
Tumrasvin, W. and Shinonaga, S., 1978. Studies on medically important flies in Thailnd. V. On 32 species belonging to the subfamilies Muscinae and Stomoxyinae including the taxonomic keys (Diptera: Muscidae). Bull Tokyo Med Dent Univ. 25, 201-227.
Tumrasvin, W., 1989. Tabanus species and their distribution in Thailand (Diptera: Tabanidae). Southeast Asian J. Trop. Med. Public Health. 20, 319-323.
Tunnakundacha, S., Desquesnes, M., Masmeatathip, R., 2017. Comparison of Vavoua, Malaise and Nzi traps with and without attractants for trapping of Stomoxys spp. (Diptera: Muscidae) and tabanids (Diptera: Tabanidae) on cattle farms. Agriculture and Natural Resources. 51, 319-323.
Uilenberg, G., 1995. International collaborative research: significance of tick-borne hemoparasitic diseases to world animal health. Vet Parasitol. 57, 19-41.
Watts, J.G., Playford, M.C., Hickey, K.L., 2016. Theileria orientalis: a review. N Z Vet J. 64, 3-9.
Zumpt, F., 1973. Stomoxyine biting flies of the world. Gustav Fisher Verlag, pp. 175.