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Cryptosporidium spp., Giardia intestinalis, and Enterocytozoon bieneusi in Captive Non-Human Primates in Qinling Mountains

  • Du, Shuai-Zhi (College of Veterinary Medicine, Northwest A&F University) ;
  • Zhao, Guang-Hui (College of Veterinary Medicine, Northwest A&F University) ;
  • Shao, Jun-Feng (Xi'an Qinling Wildlife Park) ;
  • Fang, Yan-Qin (College of Veterinary Medicine, Northwest A&F University) ;
  • Tian, Ge-Ru (College of Veterinary Medicine, Northwest A&F University) ;
  • Zhang, Long-Xian (College of Animal Science and Veterinary Medicine, Henan Agricultural University) ;
  • Wang, Rong-Jun (College of Animal Science and Veterinary Medicine, Henan Agricultural University) ;
  • Wang, Hai-Yan (College of Animal Science and Veterinary Medicine, Henan Agricultural University) ;
  • Qi, Meng (College of Animal Science and Veterinary Medicine, Henan Agricultural University) ;
  • Yu, San-Ke (College of Veterinary Medicine, Northwest A&F University)
  • 투고 : 2015.02.05
  • 심사 : 2015.07.05
  • 발행 : 2015.08.31

초록

Non-human primates (NHPs) are confirmed as reservoirs of Cryptosporidium spp., Giardia intestinalis, and Enterocytozoon bieneusi. In this study, 197 fresh fecal samples from 8 NHP species in Qinling Mountains, northwestern China, were collected and examined using multilocus sequence typing (MLST) method. The results showed that 35 (17.8%) samples were positive for tested parasites, including Cryptosporidium spp. (3.0%), G. intestinalis (2.0%), and E. bieneusi (12.7%). Cryptosporidium spp. were detected in 6 fecal samples of Macaca mulatta, and were identified as C. parvum (n=1) and C. andersoni (n=5). Subtyping analysis showed Cryptosporidium spp. belonged to the C. andersoni MLST subtype (A4, A4, A4, and A1) and C. parvum 60 kDa glycoprotein (gp60) subtype IId A15G2R1. G. intestinalis assemblage E was detected in 3 M. mulatta and 1 Saimiri sciureus. Intra-variations were observed at the triose phosphate isomerase (tpi), beta giardin (bg), and glutamate dehydrogenase (gdh) loci, with 3, 1, and 2 new subtypes found in respective locus. E. bieneusi was found in Cercopithecus neglectus (25.0%), Papio hamadrayas (16.7%), M. mulatta (16.3%), S. sciureus (10%), and Rhinopithecus roxellana (9.5%), with 5 ribosomal internal transcribed spacer (ITS) genotypes: 2 known genotypes (D and BEB6) and 3 novel genotypes (MH, XH, and BSH). These findings indicated the presence of zoonotic potential of Cryptosporidium spp. and E. bieneusi in NHPs in Qinling Mountains. This is the first report of C. andersoni in NHPs. The present study provided basic information for control of cryptosporidiosis, giardiasis, and microsporidiosis in human and animals in this area.

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참고문헌

  1. Xiao L, Fayer R. Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. Int J Parasitol 2008; 38: 1239-1255. https://doi.org/10.1016/j.ijpara.2008.03.006
  2. Thellier M, Breton J. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite 2008; 15: 349-358. https://doi.org/10.1051/parasite/2008153349
  3. Fayer R. Taxonomy and species delimitation in Cryptosporidium. Exp Parasitol 2010; 124: 90-97. https://doi.org/10.1016/j.exppara.2009.03.005
  4. Ryan U, Caccio SM. Zoonotic potential of Giardia. Int J Parasitol 2013; 43: 943-956. https://doi.org/10.1016/j.ijpara.2013.06.001
  5. Xiao L. Molecular epidemiology of cryptosporidiosis: an update. Exp Parasitol 2010; 124: 80-89. https://doi.org/10.1016/j.exppara.2009.03.018
  6. Nizeyi JB, Cranfield MR, Graczyk TK. Cattle near the Bwindi Impenetrable National Park, Uganda, as a reservoir of Cryptosporidium parvum and Giardia duodenalis for local community and free-ranging gorillas. Parasitol Res 2002; 88: 380-385. https://doi.org/10.1007/s00436-001-0543-x
  7. Ye J, Xiao L, Ma J, Guo M, Liu L, Feng Y. Anthroponotic enteric parasites in monkeys in public park, China. Emerg Infect Dis 2012; 18: 1640-1643. https://doi.org/10.3201/eid1810.120653
  8. Ye J, Xiao L, Li J, Huang W, Amer SE, Guo Y, Roellig D, Feng Y. Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China. Parasitol Int 2014; 63: 132-137. https://doi.org/10.1016/j.parint.2013.10.007
  9. Karim MR, Wang R, Dong H, Zhang L, Li J, Zhang S, Rume FI, Qi M, Jian F, Sun M, Yang G, Zou F, Ning C, Xiao L. Genetic polymorphism and zoonotic potential of Enterocytozoon bieneusi from nonhuman primates in China. Appl Environ Microbiol 2014; 80: 1893-1898. https://doi.org/10.1128/AEM.03845-13
  10. Karim MR, Zhang S, Jian F, Li J, Zhou C, Zhang L, Sun M, Yang G, Zou F, Dong H, Li J, Rume FI, Qi M, Wang R, Ning C, Xiao L. Multilocus typing of Cryptosporidium spp, and Giardia duodenalis from non-human primates in China. Int J Parasitol 2014; 18: 1039-1047.
  11. Karim MR, Dong H, Yu F, Jian F, Zhang L, Wang R, Zhang S, Rume FI, Ning C, Xiao L. Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications. J Clin Microbiol 2014; 52: 3297-302. https://doi.org/10.1128/JCM.01352-14
  12. Zhao GH, Ren WX, Gao M, Bian QQ, Hu B, Cong MM, Lin Q, Wang RJ, Qi M, Qi MZ, Zhu XQ, Zhang LX. Genotyping Cryptosporidium andersoni in cattle in Shaanxi Province, Northwestern China. PLoS One 2013; 8: e60112. https://doi.org/10.1371/journal.pone.0060112
  13. Abeywardena H, Jex AR, Koehler AV, Rajapakse RP, Udayawarna K, Haydon SR, Stevens MA, Gasser RB. First molecular characterization of Cryptosporidium and Giardia from bovines (Bos taurus and Bubalus bubalis) in Sri Lanka: unexpected absence of C. parvum from pre-weaned calves. Parasit Vectors 2014; 7: 75. https://doi.org/10.1186/1756-3305-7-75
  14. Legesse M, Erko B. Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia. Exp Parasitol 2004; 90: 231-236.
  15. Li N, Xiao L, Wang L, Zhao S, Zhao X, Duan L, Guo M, Liu L, Feng Y. Molecular surveillance of Cryptosporidium spp, Giardia duodenalis and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Negl Trop Dis 2012; 6: e1809. https://doi.org/10.1371/journal.pntd.0001809
  16. Berrilli F, Prisco C, Friedrich KG, Di Cerbo P, Di Cave D, De Liberato C. Giardia duodenalis assemblages and Entamoeba species infecting non-human primates in an Italian zoological garden: zoonotic potential and management traits. Parasit Vectors 2011; 4: 199. https://doi.org/10.1186/1756-3305-4-199
  17. David EB, Patti M, Coradi ST, Oliveira-Sequeira TC, Ribolla PE, Guimaraes S. Molecular typing of Giardia duodenalis isolates from nonhuman primates housed in a Brazilian zoo. Rev Inst Med Tro SP 2014; 56: 49-54 https://doi.org/10.1590/S0036-46652014000100007
  18. Hogan JN, Miller WA, Cranfield MR, Ramer J, Hassell J, Noheri JB, Conrad PA, Gilardi KV. Giardia in mountain gorillas (Gorilla beringei beringei) forest buffalo (Syncerus caffer) and domestic cattle in Volcanoes National Park Rwanda. J Wild Dis 2014; 50: 21-30. https://doi.org/10.7589/2012-09-229
  19. Sak B, Kvac M, Petrzelkova K, Kvetonova D, Pomajbikova K, Mulama M, Kiyang J, Modry D. Diversity of microsporidia (Fungi: Microsporidia) among captive great apes in European zoos and African sanctuaries: evidence for zoonotic transmission? Folia Parasitol 2011; 58: 81-86. https://doi.org/10.14411/fp.2011.008
  20. Pangasa A, Jex AR, Nolan MJ, Campbell BE, Haydon SR, Stevens MA, Gasser RB. Highly sensitive non-isotopic restriction endonuclease fingerprinting of nucleotide variability in the gp60 gene within Cryptosporidium species genotypes and subgenotypes infective to humans and its implications. Electrophoresis 2010; 31: 1637-1647. https://doi.org/10.1002/elps.200900706
  21. Ajjampur SS, Liakath FB, Kannan A, Rajendran P, Sarkar R, Moses PD, Simon A, Agarwal I, Mathew A, O'Connor R, Ward H, Kang G. Multisite study of cryptosporidiosis in children with diarrhea in India. J Clin Microbiol 2010; 48: 2075-2081. https://doi.org/10.1128/JCM.02509-09
  22. Wang R, Zhang L, Axen C, Bjorkman C, Jian F, Amer S, Liu A, Feng Y, Li G, Lv C, Zhao Z, Qi M, Dong H, Wang H, Sun Y, Ning C, Xiao L. Cryptosporidium parvum IId family: clonal population and dispersal from Western Asia to other geographical regions. Sci Rep 2014; 4: 4208.
  23. Guyot K, Follet-dumoulin A, Lelievre E, Sarfati C, Rabodonirina M, Nevez G, Cailliez JC, Camus D, Dei-Cas E. Molecular characterization of Cryptosporidium isolates obtained from humans in France. J Clin Microbiol 2001; 39: 3472-3480. https://doi.org/10.1128/JCM.39.10.3472-3480.2001
  24. Leoni F, Amar C, Nichols G, Pedraza-Diaz S, Mclauchlin J. Genetic analysis of Cryptosporidium from 2414 humans with diarrhoea in England between 1985 and 2000. J Med Microbiol 2006; 55: 703-707. https://doi.org/10.1099/jmm.0.46251-0
  25. Masuno K, Fukuda Y, Kubo M, Ikarashi R, Kuraishi T, Hattori S, Kimura J, Kai C, Yanai T, Nakai Y. Infectivity of Cryptosporidium andersoni and Cryptosporidium muris to normal and immunosuppressive cynomolgus monkeys. J Vet Med Sci 2014; 76: 169-172. https://doi.org/10.1292/jvms.13-0350
  26. Foronda P, Bargues MD, Abreu-acosta N, Periago MV, Valero MA, Valladares B, Mas-Coma S. Identification of genotypes of Giardia intestinalis of human isolates in Egypt. Parasitol Res 2008; 103: 1177-1181. https://doi.org/10.1007/s00436-008-1113-2
  27. Johnston AR, Gillespie TR, Rwego IB, Mclachlan TL, Kent AD, Goldberg TL. Molecular epidemiology of cross-species Giardia duodenalis transmission in western Uganda. PLoS Negl Trop Dis 2010; 4: e683. https://doi.org/10.1371/journal.pntd.0000683
  28. Zhang X, Wang Z, Su Y, Liang X, Sun X, Peng S, Lu H, Jiang N, Yin J, Xiang M, Chen Q. Identification and genotyping of Enterocytozoon bieneusi in China. J Clin Microbiol 2011; 49: 2006-2008. https://doi.org/10.1128/JCM.00372-11
  29. Li W, Kiulia NM, Mwenda JM, Nyachieo A, Taylor MB, Zhang X, Xiao L. Cyclospora papionis, Cryptosporidium hominis and human-pathogenic Enterocytozoon bieneusi in captive baboons in Kenya. J Clin Microbiol 2011; 49: 4326-4329. https://doi.org/10.1128/JCM.05051-11
  30. Wang H, Zhao G, Chen G, Jian F, Zhang S, Feng C, Wang R, Zhu J, Dong H, Hu A, Wang M, Zhang L. Multilocus genotyping of Giardia duodenalis in dairy cattle in Henan, China. PLoS One 2014; 9: e100453. https://doi.org/10.1371/journal.pone.0100453
  31. Geurden T, Goossens E, Levecke B, Vercammen F, Vercruysse J, Claerebout E. Occurrence and molecular characterization of Cryptosporidium and Giardia in captive wild ruminants in Belgium. J Zoo Wildl Med 2009; 40: 126-130. https://doi.org/10.1638/2008-0152.1

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