First Detection and Genotyping of Enterocytozoon Bieneusi in Pet Golden Hamsters (Mesocricetus Auratus) and Siberian Hamsters (Phodopus Sungorus) in China

Overview

Journal Parasite

Specialty Parasitology

Date 2022 Mar 22

PMID 35315766

Authors

Chaochao Lv

Jingsong Wang

Chen Li

Min Zhang

Weifeng Qian

Affiliations

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Abstract

Enterocytozoon bieneusi, a common opportunistic pathogen, has been detected in humans and a wide range of animals worldwide. However, no information on the prevalence and molecular characterization of E. bieneusi in hamsters is available worldwide. In this study, fecal specimens were collected from 175 golden hamsters and 175 Siberian hamsters purchased from pet shops in three provinces of China. The average infection rate of E. bieneusi was 12.0% (42/350), with 14.9% (26/175) in pet golden hamsters and 9.1% (16/175) in pet Siberian hamsters. Four genotypes were identified in pet golden hamsters, including three known genotypes (D, Henan-II, and SHW5) and one novel genotype (named Ebph1). Five genotypes were found in pet Siberian hamsters, including one known genotype (D) and four novel genotypes (named Ebph2 to Ebph5). Genotypes D and Ebph2 were the dominant genotype in pet golden hamsters (23/26, 88.5%) and Siberian hamsters (9/16, 56.3%), respectively. Phylogenetic analysis showed that the E. bieneusi isolates clustered into two groups: Group 1 (D, Henan-II, SHW5, and Ebph1) and Group 3 (Ebph2 to Ebph5). To the best of our knowledge, this is the first report of E. bieneusi infection in golden hamsters and Siberian hamsters worldwide. The identification of four genotypes belonging to Group 1 of high zoonotic potential suggests that pet hamsters especially golden hamsters can be potential sources of human microsporidiosis.

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References

Deng L, Li W, Yu X, Gong C, Liu X, Zhong Z . First Report of the Human-Pathogenic Enterocytozoon bieneusi from Red-Bellied Tree Squirrels (Callosciurus erythraeus) in Sichuan, China. PLoS One. 2016; 11(9):e0163605. PMC: 5040432. DOI: 10.1371/journal.pone.0163605. View

Yu F, Cao Y, Wang H, Liu Q, Zhao A, Qi M . Host-adaptation of the rare Enterocytozoon bieneusi genotype CHN4 in Myocastor coypus (Rodentia: Echimyidae) in China. Parasit Vectors. 2020; 13(1):578. PMC: 7667729. DOI: 10.1186/s13071-020-04436-0. View

Wang J, Lv C, Zhao D, Zhu R, Li C, Qian W . First detection and genotyping of Enterocytozoon bieneusi in pet fancy rats (Rattus norvegicus) and guinea pigs (Cavia porcellus) in China. Parasite. 2020; 27:21. PMC: 7133117. DOI: 10.1051/parasite/2020019. View

Jiang W, Roellig D, Li N, Wang L, Guo Y, Feng Y . Contribution of hospitals to the occurrence of enteric protists in urban wastewater. Parasitol Res. 2020; 119(9):3033-3040. DOI: 10.1007/s00436-020-06834-w. View

Ben Ayed L, Yang W, Widmer G, Cama V, Ortega Y, Xiao L . Survey and genetic characterization of wastewater in Tunisia for Cryptosporidium spp., Giardia duodenalis, Enterocytozoon bieneusi, Cyclospora cayetanensis and Eimeria spp. J Water Health. 2012; 10(3):431-44. DOI: 10.2166/wh.2012.204. View

Buckholt M, Lee J, Tzipori S . Prevalence of Enterocytozoon bieneusi in swine: an 18-month survey at a slaughterhouse in Massachusetts. Appl Environ Microbiol. 2002; 68(5):2595-9. PMC: 127518. DOI: 10.1128/AEM.68.5.2595-2599.2002. View

Ni H, Sun Y, Qin S, Wang Y, Zhao Q, Sun Z . Molecular Detection of spp. and Infection in Wild Rodents From Six Provinces in China. Front Cell Infect Microbiol. 2021; 11:783508. PMC: 8656357. DOI: 10.3389/fcimb.2021.783508. View

Li N, Xiao L, Wang L, Zhao S, Zhao X, Duan L . Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Negl Trop Dis. 2012; 6(9):e1809. PMC: 3435239. DOI: 10.1371/journal.pntd.0001809. View

Li J, Jiang Y, Wang W, Chao L, Jia Y, Yuan Y . Molecular identification and genotyping of Enterocytozoon bieneusi in experimental rats in China. Exp Parasitol. 2020; 210:107850. DOI: 10.1016/j.exppara.2020.107850. View

10.

Guo Y, Alderisio K, Yang W, Cama V, Feng Y, Xiao L . Host specificity and source of Enterocytozoon bieneusi genotypes in a drinking source watershed. Appl Environ Microbiol. 2013; 80(1):218-25. PMC: 3911003. DOI: 10.1128/AEM.02997-13. View

11.

Didier E, Weiss L . Microsporidiosis: current status. Curr Opin Infect Dis. 2006; 19(5):485-92. PMC: 3109650. DOI: 10.1097/01.qco.0000244055.46382.23. View

12.

Deng L, Chai Y, Luo R, Yang L, Yao J, Zhong Z . Occurrence and genetic characteristics of Cryptosporidium spp. and Enterocytozoon bieneusi in pet red squirrels (Sciurus vulgaris) in China. Sci Rep. 2020; 10(1):1026. PMC: 6978461. DOI: 10.1038/s41598-020-57896-w. View

13.

Qi M, Luo N, Wang H, Yu F, Wang R, Huang J . Zoonotic Cryptosporidium spp. and Enterocytozoon bieneusi in pet chinchillas (Chinchilla lanigera) in China. Parasitol Int. 2015; 64(5):339-41. DOI: 10.1016/j.parint.2015.05.007. View

14.

Yu F, Qi M, Zhao Z, Lv C, Wang Y, Wang R . The Potential Role of Synanthropic Rodents and Flies in the Transmission of Enterocytozoon bieneusi on a Dairy Cattle farm in China. J Eukaryot Microbiol. 2018; 66(3):435-441. DOI: 10.1111/jeu.12687. View

15.

Ryan U, Feng Y, Fayer R, Xiao L . Taxonomy and molecular epidemiology of Cryptosporidium and Giardia - a 50 year perspective (1971-2021). Int J Parasitol. 2021; 51(13-14):1099-1119. DOI: 10.1016/j.ijpara.2021.08.007. View

16.

Cama V, Pearson J, Cabrera L, Pacheco L, Gilman R, Meyer S . Transmission of Enterocytozoon bieneusi between a child and guinea pigs. J Clin Microbiol. 2007; 45(8):2708-10. PMC: 1951230. DOI: 10.1128/JCM.00725-07. View

17.

Santin M, Fayer R . Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J Eukaryot Microbiol. 2009; 56(1):34-8. DOI: 10.1111/j.1550-7408.2008.00380.x. View

18.

Wang H, Liu Q, Jiang X, Zhang Y, Zhao A, Cui Z . Dominance of zoonotic genotype D of Enterocytozoon bieneusi in bamboo rats (Rhizomys sinensis). Infect Genet Evol. 2019; 73:113-118. DOI: 10.1016/j.meegid.2019.04.025. View

19.

Meerburg B, Singleton G, Kijlstra A . Rodent-borne diseases and their risks for public health. Crit Rev Microbiol. 2009; 35(3):221-70. DOI: 10.1080/10408410902989837. View

20.

Masuda A, Wada M, Saho H, Tokunaga K, Kikuchi Y, Yamasaki F . Prevalence and Molecular Characterization of the Zoonotic Enteric Protozoans spp., Enterocytozoon bieneusi, and from Pallas's Squirrels (Callosciurus erythraeus) in Kanagawa Prefecture, Japan. Microbiol Spectr. 2021; 9(3):e0099021. PMC: 8567245. DOI: 10.1128/Spectrum.00990-21. View