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Serological and Molecular Detection of Toxoplasma gondii and Babesia microti in the Blood of Rescued Wild Animals in Gangwon-do (Province), Korea

  • Hong, Sung-Hee (Division of Malaria and Parasitc Diseases, Korea National Institute of Health, Korea Center for Disease Control and Prevention) ;
  • Kim, Hee-Jong (Colleage of Veterinary Medicine, Gangwon National University) ;
  • Jeong, Young-Il (Division of Malaria and Parasitc Diseases, Korea National Institute of Health, Korea Center for Disease Control and Prevention) ;
  • Cho, Shin-Hyeong (Division of Malaria and Parasitc Diseases, Korea National Institute of Health, Korea Center for Disease Control and Prevention) ;
  • Lee, Won-Ja (Division of Malaria and Parasitc Diseases, Korea National Institute of Health, Korea Center for Disease Control and Prevention) ;
  • Kim, Jong-Tak (Colleage of Veterinary Medicine, Gangwon National University) ;
  • Lee, Sang-Eun (Division of Malaria and Parasitc Diseases, Korea National Institute of Health, Korea Center for Disease Control and Prevention)
  • Received : 2016.11.16
  • Accepted : 2017.03.18
  • Published : 2017.04.30

Abstract

Infections of Toxoplasma gondii and Babesia microti are reported in many wild animals worldwide, but information on their incidence and molecular detection in Korean wild fields is limited. In this study, the prevalence of T. gondii and B. microti infection in blood samples of 5 animal species (37 Chinese water deer, 23 raccoon dogs, 6 roe deer, 1 wild boar, and 3 Eurasian badgers) was examined during 2008-2009 in Gangwon-do (Province), the Republic of Korea (=Korea) by using serological and molecular tests. The overall seropositivity of T. gondii was 8.6% (6/70); 10.8% in Chinese water deer, 4.3% in raccoon dogs, and 16.7% in roe deer. PCR revealed only 1 case of T. gondii infection in Chinese water deer, and phylogenic analysis showed that the positive isolate was practically identical to the highly pathogenetic strain type I. In B. microti PCR, the positive rate was 5.7% (4/70), including 2 Chinese water deer and 2 Eurasian badgers. Phylogenetic analysis results of 18S rRNA and the ${\beta}$-tubulin gene showed that all positive isolates were US-type B. microti. To our knowledge, this is the first report of B. microti detected in Chinese water deer and Eurasian badger from Korea. These results indicate a potentially high prevalence of T. gondii and B. microti in wild animals of Gangwon-do, Korea. Furthermore, Chinese water deer might act as a reservoir for parasite infections of domestic animals.

Keywords

References

  1. Chomel BB, Belotto A, Meslin FX. Wildlife, exotic pets, and emerging zoonoses. Emerg Infect Dis 2007; 13: 6-11. https://doi.org/10.3201/eid1301.060480
  2. Mackenstedt U, Jenkins D, Romig T. The role of wildlife in the transmission of parasitic zoonoses in peri-urban and urban areas. Int J Parasitol Parasites Wildl 2015; 4: 71-79. https://doi.org/10.1016/j.ijppaw.2015.01.006
  3. Cutler SJ, Fooks AR, van der Poel WH. Public health threat of new, reemerging, and neglected zoonoses in the industrialized world. Emerg Infect Dis 2010; 16: 1-7. https://doi.org/10.3201/eid1601.081467
  4. Fevre EM, Bronsvoort BM, Hamilton KA, Cleaveland S. Animal movements and the spread of infectious diseases. Trends Microbiol 2006; 14: 125-131. https://doi.org/10.1016/j.tim.2006.01.004
  5. Youn HJ. Review of Zoonotic Parasites in Medical and Veterinary Fields in the Republic of Korea. Korean J Parasitol 2009; 47: 133-141. https://doi.org/10.3347/kjp.2009.47.S.S133
  6. Kang SW, Doan HT, Noh JH, Choe SE, Yoo MS, Kim YH, Reddy KE, Nguyen TT, Van, Quyen D, Nguyen LT, Kweon CH, Jung SC. Seroprevalence of Toxoplasma gondi and Trichinella spiralis infections in wild boars (Sus scrofa) in Korea. Parasitol Int 2013; 62: 583-585. https://doi.org/10.1016/j.parint.2013.08.015
  7. Han JI, Lee SJ, Jang HJ, and Na KJ. Asymptomatic Babesia microti-like parasite infection in wild raccoon dogs (Nyctereutes procyonoides) in South Korea. J Wildl Dis 2010; 46: 632-635. https://doi.org/10.7589/0090-3558-46.2.632
  8. Dubey JP, Jones JL. Toxoplasma gondii infection in humans and animals in the United States. Int J Parasitol 2008; 38: 1257-1278. https://doi.org/10.1016/j.ijpara.2008.03.007
  9. Kjemtrup AM, Conrad PA. Human babesiosis: an emerging tick-borne disease. Int J Parasitol 2000; 30: 1323-1337. https://doi.org/10.1016/S0020-7519(00)00137-5
  10. Jeong W, Yoon H, Kim YK, Moon OK, Kim DS An DJ. Prevalence of Antibodies to Toxoplasma gondii in South Korean Wild Boar (Sus scrofa coreanus). J Wildl Dis 2014; 50: 902-905. https://doi.org/10.7589/2013-03-077
  11. Zamoto A, Tsuji M, Wei Q, Cho SH, Shin EH, Kim TS, Leonova GN, Hagiwara K, Asakawa M, Kariwa H, Takashima I, Ishihara C. Epizootiologic survey for Babesia microti among small wild mammals in Northeastern Eurasia and a geographic diversity in the $\ss$-tubulin gene sequences. J Vet Med Sci 2004; 66: 785-792. https://doi.org/10.1292/jvms.66.785
  12. Hong SH, Lee SE, Jeong YI, Kim HC, Chong ST, Klein TA, Song JW, Gu SH, Cho SH, Lee WJ. Prevalence and molecular characterizations of Toxoplasma gondii and Babesia microti from small mammals captured in Gyeonggi and Gangwon Provinces, Republic of Korea. Vet Parasitol 2014; 205: 512-517. https://doi.org/10.1016/j.vetpar.2014.07.032
  13. Choi WY, Nam HW, Kwak NH, Huh W, Kim YR, Kang MW, Cho SY, Dubey JP. Foodborne outbreaks of human toxoplasmosis. J Infect Dis 1997; 175: 1280-1282. https://doi.org/10.1086/593702
  14. Morzaria S, Katende J, Kairo A, Nene V, Musoke A. New methods for the diagnosis of Babesia bigemina infection. Mem Inst Oswaldo Cruz 1992; 87 (Suppl): 201-205.
  15. Kawabuchi T, Tsuji M, Sado A, Matoba Y, Asakawa M, Ishihara C. Babesia microti-like parasites detected in feral raccoons (Procyon lotor) captured in Hokkaido, Japan. J Vet Med Sci 2005; 67: 825-827. https://doi.org/10.1292/jvms.67.825
  16. Chen J, Li ZY, Zhou DH, Liu GH, Zhu XQ. Genetic diversity among Toxoplasma gondii strains from different hosts and geographical regions revealed by sequence analysis of GRA5 gene. Parasit Vectors 2012; 5: 279. https://doi.org/10.1186/1756-3305-5-279
  17. Su C, Zhang X, Dubey JP. Genotyping of Toxoplasma gondii by multilocus PCR-RFLP markers: a high resolution and simple method for identification of parasites. Int J Parasitol 2006; 36: 841-848. https://doi.org/10.1016/j.ijpara.2006.03.003
  18. Tsuji M, Zamoto A, Kawabuchi T, Kataoka T, Nakajima R, Asakawa M, Ishihara C. Babesia microti-like parasites detected in Eurasian red squirrels (Sciurus vulgaris orientis) in Hokkaido, Japan. J Vet Med Sci 2006; 68: 643-646. https://doi.org/10.1292/jvms.68.643
  19. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4: 406-425.
  20. Kumar S, Nei M, Dudley J, Tamura K. MEGA: A biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 2008; 9: 299-306. https://doi.org/10.1093/bib/bbn017
  21. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39: 783-791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x
  22. Sibley LD, Boothroyd JC. Virulent strains of Toxoplasma gondii comprise a single clonal lineage. Nature 1992; 359: 82-85. https://doi.org/10.1038/359082a0
  23. Berger-Schoch AE, Herrmann DC, Schares G, Muller N, Bernet D, Gottstein B, Frey CF. Prevalence and genotypes of Toxoplasma gondii in feline faeces (oocysts) and meat from sheep, cattle and pigs in Switzerland. Vet Parasitol 2011; 177: 290-297. https://doi.org/10.1016/j.vetpar.2010.11.046
  24. De Craeye S, Speybroeck N, Ajzenberg D, Darde ML, Collinet F, Tavernier P, Van Gucht S, Dorny P, Dierick K. Toxoplasma gondii and Neospora caninum in wildlife: common parasites in Belgian foxes and Cervidae? Vet Parasitol 2011; 178: 64-69. https://doi.org/10.1016/j.vetpar.2010.12.016
  25. Hong SH, Jeong YI, Kim JY, Cho SH, Lee WJ, Lee SE. Prevalence of Toxoplasma gondii infection in household cats in Korea and risk factors. Korean J Parasitol 2013; 51: 357-361. https://doi.org/10.3347/kjp.2013.51.3.357
  26. Jung BY, Gebeyehu EB, Lee SH, Seo MG, Byun JW, Oem JK, Kim HY, Kwak D. Detection and determination of Toxoplasma gondii seroprevalence in native Korean goats (Capra hircus coreanae). Vector Borne Zoonotic Dis 2014; 14: 374-377. https://doi.org/10.1089/vbz.2013.1452
  27. Lee SE, Hong SH, Jeong YI, Lee JH, Yoo SJ, Lim HS, Lee WJ, Cho SH. Cross-sectional analysis of the seropositivity and risk factors of Toxoplasma gondii infection among veterinarians, in relation to their public professional activities. Vet Parasitol 2014; 203: 29-34. https://doi.org/10.1016/j.vetpar.2014.01.001
  28. Dubey JP. Review of "Toxoplasmosis of Animals and Humans (Second Edition)" by J.P. Dubey. Parasit Vectors 2010; 3: 112. https://doi.org/10.1186/1756-3305-3-112
  29. Ross RD, Stec LA, Werner JC, Blumenkranz MS, Glazer L, Williams GA. Presumed acquired ocular toxoplasmosis in deer hunters. Retina 2001; 21: 226-229. https://doi.org/10.1097/00006982-200106000-00005
  30. Telford SR 3rd1, Mather TN, Adler GH, Spielman A. Short-tailed shrews as reservoirs of the agents of lyme disease and human babesiosis. J Parasitol 1990; 76: 681-683.
  31. Spielman A, Etkind P, Piesman J, Ruebush TK 2nd, Juranek DD, Jacobs MS. Reservoir hosts of human babesiosis on Nantucket Island. Am J Trop Med Hyg 1981; 30: 560-565. https://doi.org/10.4269/ajtmh.1981.30.560
  32. Birkenheuer AJ, Marr HS, Hladio N, Acton AE. Molecular evidence of prevalent dual piroplasma infections in North American raccoons (Procyon lotor). Parasitology 2008; 135: 33-37.
  33. Birkenheuer AJ, Horney B, Bailey M, Scott M, Sherbert B, Catto V, Marr HS, Camacho AT, Ballman AE. Babesia microti-like infections are prevalent in North American foxes. Vet Parasitol 2010; 172: 179-182. https://doi.org/10.1016/j.vetpar.2010.05.020

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