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      Occurrence and potentially zoonotic genotypes of Enterocytozoon bieneusi in wild rhesus macaques ( Macaca mulatta) living in Nanwan Monkey Island, Hainan, China: a public health concern

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          Abstract

          Background

          Enterocytozoon bieneusi, a microsporidian species, is a zoonotic pathogen found in both humans and animals. Here, we determined the prevalence, explored the different genotypes of E. bieneusi in wild rhesus macaques ( Macaca mulatta) (Hainan Island of China), and assessed their zoonotic potential.

          Methods

          We collected 173 fecal specimens from wild rhesus macaques living in Nanwan Monkey Island, Hainan, China. Subsequently, we identified and genotyped E. bieneusi using nested PCR analysis amplification of the internal transcribed spacer region (ITS) of the rRNA gene. Lastly, a neighbor-joining tree was built based on gene sequences from the ITS region of E. bieneusi.

          Results

          Of the 173 specimens from wild rhesus macaques, 26 (15%) were infected with E. bieneusi. We identified six genotypes of E. bieneusi, of which five were known: PigEBITS7 ( n = 20), D ( n = 2), Type IV ( n = 1), Peru6 (n = 1), Henan-III (n = 1), and a novel genotype: HNM-IX ( n = 1). From the phylogenetic analysis, the six genotypes identified here were all clustered into zoonotic group 1.

          Conclusion

          This study is the first report to detect E. bieneusi infection in wild rhesus macaques from Hainan, China. Human-pathogenic genotypes D, Henan-III, Peru6, PigEbITS7, and Type IV in the wild rhesus macaques support these animals infected with E. bieneusi have a public health significance.

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          Most cited references46

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          Host Specificity of Enterocytozoon bieneusi and Public Health Implications

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            Zoonotic Cryptosporidium species and Enterocytozoon bieneusi genotypes in HIV-positive patients on antiretroviral therapy.

            Molecular diagnostic tools have been used increasingly in the characterization of the transmission of cryptosporidiosis and microsporidiosis in developing countries. However, few studies have examined the distribution of Cryptosporidium species and Enterocytozoon bieneusi genotypes in AIDS patients receiving antiretroviral therapy. In the present study, 683 HIV-positive patients in the National Free Antiretroviral Therapy Program in China and 683 matched HIV-negative controls were enrolled. Cryptosporidium species and subtypes and Enterocytozoon bieneusi genotypes were detected and differentiated by PCR and DNA sequencing. The infection rates were 1.5% and 0.15% for Cryptosporidium and 5.7% and 4.2% for E. bieneusi in HIV-positive and HIV-negative participants, respectively. The majority (8/11) of Cryptosporidium cases were infections by zoonotic species, including Cryptosporidium meleagridis (5), Cryptosporidium parvum (2), and Cryptosporidium suis (1). Prevalent E. bieneusi genotypes detected, including EbpC (39), D (12), and type IV (7), were also potentially zoonotic. The common occurrence of EbpC was a feature of E. bieneusi transmission not seen in other areas. Contact with animals was a risk factor for both cryptosporidiosis and microsporidiosis. The results suggest that zoonotic transmission was significant in the epidemiology of both diseases in rural AIDS patients in China.
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              Epidemiology of Enterocytozoon bieneusi Infection in Humans

              A review was conducted to examine published works that focus on the complex epidemiology of Enterocytozoon bieneusi infection in humans. Studies on the prevalence of these emerging microsporidian pathogens in humans, in developed and developing countries, the different clinical spectra of E. bieneusi intestinal infection in children, in different settings, and the risk factors associated with E. bieneusi infection have been reviewed. This paper also analyses the impact of the recent application of PCR-based molecular methods for species-specific identification and genotype differentiation has had in increasing the knowledge of the molecular epidemiology of E. bieneusi in humans. The advances in the epidemiology of E. bieneusi, in the last two decades, emphasize the importance of epidemiological control and prevention of E. bieneusi infections, from both the veterinary and human medical perspectives.
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                Author and article information

                Contributors
                hayidazhaowei@163.com
                zhh931218@163.com
                382771660@qq.com
                18272734493@163.com
                hhc@wmu.edu.cn
                luganghn@163.com
                tanfengsong@163.com
                Journal
                BMC Vet Res
                BMC Vet Res
                BMC Veterinary Research
                BioMed Central (London )
                1746-6148
                9 June 2021
                9 June 2021
                2021
                : 17
                : 213
                Affiliations
                [1 ]GRID grid.443397.e, ISNI 0000 0004 0368 7493, Key Laboratory of Tropical Translational Medicine of Ministry of Education, , Hainan Medical University, ; Haikou, 571199 China
                [2 ]GRID grid.268099.c, ISNI 0000 0001 0348 3990, Department of Parasitology, , Wenzhou Medical University, ; Wenzhou, 325035 Zhejiang China
                [3 ]Qingdao Shinan District Center for Disease Control and Prevention, Qingdao, 266071 Shandong China
                [4 ]GRID grid.443397.e, ISNI 0000 0004 0368 7493, Department of Pathogenic Biology, , Hainan Medical University, ; Haikou, Hainan China
                [5 ]GRID grid.443397.e, ISNI 0000 0004 0368 7493, Hainan Medical University-The University of Hong Kong Joint Laboratory of Tropical Infectious Diseases, Hainan Medical University, ; Haikou, Hainan China
                Article
                2916
                10.1186/s12917-021-02916-8
                8191004
                34107958
                cb6de1b0-bc85-44c3-a731-0eee609abc65
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                History
                : 12 February 2021
                : 21 May 2021
                Categories
                Research
                Custom metadata
                © The Author(s) 2021

                Veterinary medicine
                enterocytozoon bieneusi,rhesus macaques,hainan,zoonotic
                Veterinary medicine
                enterocytozoon bieneusi, rhesus macaques, hainan, zoonotic

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