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Prevalence and genotypes of Enterocytozoon bieneusi in sika deer in Jilin province, Northeastern China

  • Xiao-Xuan Zhang , Wei Cong , Guo-Hua Liu , Xiao-Ting Ni , Jian-Gang Ma , Wen-Bin Zheng , Quan Zhao and Xing-Quan Zhu EMAIL logo
Published/Copyright: March 30, 2016
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Abstract

Enterocytozoon bieneusi is one of the most important zoonotic pathogen that can infect almost all animals, including humans. However, little information is available regarding prevalence and genotypes of E. bieneusi in sika deer. In the present study, the prevalence of E. bieneusi infection in sika deer in Jilin province, Northeastern China was examined using PCR amplification of the internal transcribed spacer (ITS) region of the ribosomal RNA (rRNA) gene. 23 (7.06%) of 326 samples were tested E. bieneusi-positive, and the risk factor significantly associated with E. bieneusi prevalence was the age of sika deer. Sequence analysis of the ITS rRNA gene suggested that 8 genotypes of E. bieneusi were found in this study, with five known genotypes, namely J (n = 11), BEB6 (n = 4), EbpC (n = 1), CHN-DC1 (n = 1), KIN-1 (n = 1) and three novel genotypes, namely JLD-1 (n = 2), JLD-2 (n = 2) and JLD-3 (n = 1). Phylogenetic analysis indicated that genotypes CHN-DC-1, KIN-1, EbpC, JLD-2 and JLD-3 fell into group 1, while other three genotypes (genotypes J, BEB6 and JLD-1) were clustered into group 2 (so-called bovine-specific groups). These findings indicated the presence of zoonotic E. bieneusi in Jilin province, Northeastern China. Effective strategies should be performed to control E. bieneusi infection in sika deer, other animals and humans.


Xiao-Xuan Zhang and Wei Cong contributed equally to this work and should be consider as first co-authors


Acknowledgments

Project support was provided by National Key Project of Scientific and Technical Supporting Program (Grant No. 2012BAD12B07) and the Science Fund for Creative Research Groups of Gansu Province (Grant No. 1210RJIA006).

Reference

Desportes I., Le Charpentier Y., Galian A., Bernard F., Cochand-Priollet B., Lavergne A., Ravisse P., Modigliani R. 1985. Occurrence of a new microsporidan: Enterocytozoon bieneusi n.g., n. sp., in the enterocytes of a human patient with AIDS. The Journal of Protozoology, 32, 250–254 Didier E.S., Weiss L.M. 2006. Microsporidiosis: current status. Current Opinion in Infectious Diseases, 19, 485–49210.1111/j.1550-7408.1985.tb03046.xSearch in Google Scholar

Didier E.S., Weiss L.M. 2006. Microsporidiosis: current status. Current Opinion in Infectious Diseases, 19, 485–49210.1097/01.qco.0000244055.46382.23Search in Google Scholar

Ghosh K., Weiss L.M. 2009. Molecular diagnostic tests for microsporidia. Interdisciplinary Perspectives on Infectious Diseases, 2009, 926521. DOI: 10.1155/2009/92652110.1155/2009/926521">10.1155/2009/926521Search in Google Scholar

Jiang Y., Tao W., Wan Q., Li Q., Yang Y., Lin Y., Zhang S., Li W. 2015. Zoonotic and potentially host-adapted Enterocytozoon bieneusi genotypes in sheep and cattle in Northeast China and an increasing concern about the zoonotic importance of previously considered ruminant-adapted genotypes. Applied and Environmental Microbiology, 81, 3326–3335. DOI: 10.1128/ AEM.00328-1510.1128/ AEM.00328-15">10.1128/ AEM.00328-15Search in Google Scholar

Karim M.R., Wang R., He X., Zhang L., Li J., Rume F.I., Dong H., Qi M., Jian F., Zhang S., Sun M., Yang G., Zou F., Ning C., Xiao L. 2014a. Multilocus sequence typing of Enterocytozoon bieneusi in nonhuman primates in China. Veterinary Parasitology, 200, 13–23. DOI: 10.1016/j.vetpar.201310.1016/j.vetpar.2013">10.1016/j.vetpar.2013Search in Google Scholar

Karim M.R., Wang R., Dong H., Zhang L., Li J., Zhang S., Rume F.I., Qi M., Jian F., Sun M., Yang G., Zou F., Ning C., Xiao L. 2014b. Genetic polymorphism and zoonotic potential of Enterocytozoon bieneusi from nonhuman primates in China. Applied and Environmental Microbiology, 80, 1893–1898. DOI: 10.1128/AEM.03845-1310.1128/AEM.03845-13">10.1128/AEM.03845-13Search in Google Scholar

Karim M.R., Dong H., Yu F., Jian, F., Zhang L., Wang R., Zhang S., Rume F.I., Ning C., Xiao L. 2014c. Genetic diversity in Enterocytozoon bieneusi isolates from dogs and cats in China: host specificity and public health implications. Journal of Clinical Microbiology, 52, 3297–3302. DOI: 10.1128/ JCM.01352-1410.1128/ JCM.01352-14">10.1128/ JCM.01352-14Search in Google Scholar

Karim M.R., Yu F., Li J., Li J., Zhang L., Wang R., Rume F.I., Jian F., Zhang S., Ning C. 2014d. First molecular characterization of enteric protozoa and the human pathogenic microsporidian, Enterocytozoon bieneusi, in captive snakes in China. Parasitology Research, 113, 3041–3048. DOI: 10.1007/s00436014-3967-910.1007/s00436-014-3967-9">10.1007/s00436-014-3967-9Search in Google Scholar

Li W., Li Y., Song M., Lu Y., Yang J., Tao W., Jiang Y., Wan Q., Zhang S., Xiao L. 2015. Prevalence and genetic characteristics of Cryptosporidium, Enterocytozoon bieneusi and Giardia duodenalis in cats and dogs in Heilongjiang province, China. Veterinary Parasitology, 208, 125–134. DOI: 10.1016/ j.vetpar.2015.01.01410.1016/ j.vetpar.2015.01.014">10.1016/ j.vetpar.2015.01.014Search in Google Scholar

Li W., Li Y., Li W., Yang J., Song M., Diao R., Jia H., Lu Y., Zheng J., Zhang X., Xiao L. 2014a. Genotypes of Enterocytozoon bieneusi in livestock in China: high prevalence and zoonotic potential. PLoS One, 9, e97623. DOI: 10.1371/journal. pone.0097623.10.1371/journal. pone.0097623">10.1371/journal. pone.0097623Search in Google Scholar

Li W., Diao R., Yang J., Xiao L., Lu Y., Li Y., Song M. 2014b. High diversity of human-pathogenic Enterocytozoon bieneusi genotypes in swine in northeast China. Parasitology Research, 113, 1147–1153. DOI: 10.1007/s00436-014-3752-910.1007/s00436-014-3752-9">10.1007/s00436-014-3752-9Search in Google Scholar

Li W., Cama V., Feng Y., Gilman R.H., Bern C., Zhang X., Xiao L. 2012a. Population genetic analysis of Enterocytozoon bieneusi in humans. International Journal for Parasitology, 42, 287–293. DOI: 10.1016/j.ijpara.2012.01.00310.1016/j.ijpara.2012.01.003">10.1016/j.ijpara.2012.01.003Search in Google Scholar

Li N., Xiao L., Wang L., Zhao S., Zhao X., Duan L., Guo M., Liu L., Feng Y. 2012b Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Neglected Tropical Diseases, 6, e1809. DOI: 10.1371/ journal.pntd.000180910.1371/ journal.pntd.0001809">10.1371/ journal.pntd.0001809Search in Google Scholar

Ma J., Li P., Zhao X., Xu H., Wu W., Wang Y., Guo Y., Wang L., Feng Y., Xiao L. 2015a. Occurrence and molecular characterization of Cryptosporidium spp. and Enterocytozoon bieneusi in dairy cattle, beef cattle and water buffaloes in China. Veterinary Parasitology, 207, 220–227. DOI: 10.1016/j.vetpar.2014.10.01110.1016/j.vetpar.2014.10.011">10.1016/j.vetpar.2014.10.011Search in Google Scholar

Ma J., Cai J., Ma J., Feng Y., Xiao L. 2015b. Enterocytozoon bieneusi genotypes in yaks (Bos grunniens) and their public health potential. The Journal of Eukaryotic Microbiology, 62, 21–25. DOI: 10.1111/jeu.12141.10.1111/jeu.12141">10.1111/jeu.12141Search in Google Scholar

Matos O., Lobo M.L., Xiao L. 2012. Epidemiology of Enterocytozoon bieneusi Infection in Humans. Journal of Parasitology Research, 2012, 981424. DOI: 10.1155/2012/98142410.1155/2012/981424">10.1155/2012/981424Search in Google Scholar

Santin M., Fayer R. 2015. Enterocytozoon bieneusi, Giardia, and Cryptosporidium infecting white-tailed deer. The Journal of Eukaryotic Microbiology, 62, 34–43. DOI: 10.1111/jeu.1215510.1111/jeu.12155">10.1111/jeu.12155Search in Google Scholar

Santín M., Fayer R. 2011. Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Research in Veterinary Science, 90, 363–371. DOI: 10.1016/j.rvsc.2010.07.01410.1016/j.rvsc.2010.07.014">10.1016/j.rvsc.2010.07.014Search in Google Scholar

Santín M., Fayer R. 2009. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. The Journal of Eukaryotic Microbiology, 56, 34–38. DOI: 10.1111/j.1550-7408.2008.00380.x10.1111/j.1550-7408.2008.00380.x">10.1111/j.1550-7408.2008.00380.xSearch in Google Scholar

Thellier M., Breton J. 2008. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite, 15, 349–35810.1051/parasite/2008153349Search in Google Scholar PubMed

Wang L., Xiao L., Duan L., Ye J., Guo Y., Guo M., Liu L., Feng Y. 2013a. Concurrent infections of Giardia duodenalis, Enterocytozoon bieneusi, and Clostridium difficile in children during a cryptosporidiosis outbreak in a pediatric hospital in China. PLoS Neglected Tropical Diseases, 7, e2437. DOI: 10. 1371/journal.pntd.000243710. 1371/journal.pntd.0002437">10. 1371/journal.pntd.0002437Search in Google Scholar

Wang L., Zhang H., Zhao X., Zhang L., Zhang G., Guo M., Liu L., Feng Y., Xiao L. 2013b. Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy. Journal of Clinical Microbiology, 51, 557–563. DOI: 10.1128/JCM.02758-1210.1128/JCM.02758-12">10.1128/JCM.02758-12Search in Google Scholar

Ye J., Xiao L., Wang Y., Guo Y., Roellig D.M., Feng Y. 2015. Dominance of Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotype BEB6 in sheep in Inner Mongolia, China. Veterinary Parasitology, 210, 235–239. DOI: 10.1016/ j.vetpar.2015.04.01110.1016/j.vetpar.2015.04.011Search in Google Scholar

Ye J., Xiao L., Li J., Huang W., Amer S.E., Guo Y., Roellig D., Feng Y. 2014. Occurrence of human-pathogenic Enterocytozoon bieneusi, Giardia duodenalis and Cryptosporidium genotypes in laboratory macaques in Guangxi, China. Parasitology International, 63, 132–137. DOI: 10.1016/j.parint.2013.10.00710.1016/j.parint.2013.10.007">10.1016/j.parint.2013.10.007Search in Google Scholar

Ye J., Xiao L., Ma J., Guo M., Liu L., Feng Y. 2012. Anthroponotic enteric parasites in monkeys in public park, China. Emerging Infectious Diseases, 18, 1640–1643. DOI: 10.3201/eid1810. 12065310.3201/eid1810.120653Search in Google Scholar

Zhao W., Zhang W., Wang R., Liu W., Liu A., Yang D., Yang F., Karim M.R., Zhang L. 2014. Enterocytozoon bieneusi in sika deer (Cervus nippon) and red deer (Cervus elaphus): deer specificity and zoonotic potential of ITS genotypes. Parasitology Research, 113, 4243–4250. DOI: 10.1007/s00436014-4100-910.1007/s00436-014-4100-9">10.1007/s00436-014-4100-9Search in Google Scholar

Zhao W., Zhang W., Yang D., Zhang L., Wang R., Liu A. 2015a. Prevalence of Enterocytozoon bieneusi and genetic diversity of ITS genotypes in sheep and goats in China. Infection, Genetics and Evolution, 32, 265–270. DOI: 10.1016/j.meegid. 2015.03.02610.1016/j.meegid. 2015.03.026">10.1016/j.meegid. 2015.03.026Search in Google Scholar

Zhao W., Zhang W., Yang F., Zhang L., Wang R., Cao J., Shen Y., Liu A. 2015b. Enterocytozoon bieneusi in dairy cattle in the Northeast of China: genetic diversity of ITS gene and evaluation of zoonotic transmission potential. The Journal of Eukaryotic Microbiology, 62, 553–60. DOI: 10.1111/jeu.1221010.1111/jeu.12210">10.1111/jeu.12210Search in Google Scholar

Received: 2015-9-23
Revised: 2015-10-9
Accepted: 2015-12-30
Published Online: 2016-3-30
Published in Print: 2016-6-1

© W. StefańskiInstitute of Parasitology, PAS

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