Abstract
Background
Enterocytozoon bieneusi is a common species of microsporidia that not only influences human health but also threatens animal productive performance and value. However, there have been no systematic studies of the prevalence of E. bieneusi in sheep in China.
Results
A total of 953 fecal specimens were collected from sheep from 11 provinces across five regions of China and analyzed for E. bieneusi by nested PCR targeting the ribosomal internal transcribed spacer (ITS). Enterocytozoon bieneusi infections were detected in four regions, with an overall infection rate of 20.4% (194/953). The highest infection rate was detected in pre-weaned lambs (25.0%), followed by post-weaned lambs (22.2%) and adult sheep (14.6%). Enterocytozoon bieneusi was found in nine of the 11 tested provinces, with infection rates between 2.9–51.7%. Eleven genotypes were identified based on ITS analysis, including seven known genotypes (BEB6, CHG1, CHG3, CHS7, CHS8, COS-I and NESH5) and four novel genotypes (CHHLJS1, CHHLJS2, CHNXS1 and CHXJS1). All 11 genotypes were clustered into group 2, and the zoonotic genotype BEB6 was the dominant genotype (n = 129, 66.5%) in sheep.
Conclusion
The prevalence of E. bieneusi was studied in five regions representing most areas where sheep are bred in China. This is the first report of E. bieneusi infection in sheep for seven Chinese provinces. Geographical differences were detected in the distribution of E. bieneusi genotypes, but no differences were found among sheep in different age groups. The zoonotic genotype BEB6 was the dominant genotype, indicating that sheep are a potential source of zoonotic microsporidiosis in China. These results improve our knowledge of the epidemiology of E. bieneusi in sheep in China.
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Background
Microsporidia are obligate intracellular eukaryotic parasites with a wide range of hosts that includes arthropods, birds, mammals and humans [1, 2]. To date, more than 1300 microsporidian species belonging to 150 genera have been reported [3], including at least 14 microsporidian species belonging to eight families that have been reported to infect humans. The most common species, Enterocytozoon bieneusi [4, 8, 9]. When analyzed in combination with phylogeny, these genotypes can be grouped into several genetically isolated clusters [10]. Group 1 includes zoonotic genotypes that have been reported in humans and animals [11]. Groups 2 to 9 have mainly been reported in animals and wastewater [11, 31], golden takins [32], deer [20], sika deer [20] and alpacas [33]. In addition, this genotype has also been found in humans [36], as well as in urban wastewater [37, 37, 41]. In the present study, BEB6 was the most prevalent genotype, indicating that sheep may be a source of E. bieneusi contamination in wastewater. However, whether E. bieneusi is present in wastewater near farms in these areas is unclear, and more studies are required to further understand the transmission of E. bieneusi between sheep and water.
Conclusions
In this study, we assessed the prevalence and genetic diversity of E. bieneusi in sheep from 11 provinces across five regions of China. E. bieneusi was found in nine provinces, suggesting that E. bieneusi is widespread in sheep in China. The overall infection rate was 20.4%, and the highest infection rate was detected in pre-weaned lambs. At the province level, the prevalence in different age groups also differed. Eleven genotypes were detected in sheep in this study, including four novel genotypes. The zoonotic genotype BEB6 was the dominant genotype and may pose a potential threat to humans. We also observed geographical differences in the genotypic features of E. bieneusi in sheep, but no differences were found in genotypes among the different age groups. This study covered most areas of China where sheep are bred, and for seven of the provinces this is the first report of E. bieneusi. Therefore, this study increases our understanding of the prevalence and genotypic characterization of E. bieneusi in sheep in China.
Abbreviations
- ITS:
-
Internal transcribed spacer
- PCR:
-
Polymerase chain reaction
- SSU rRNA:
-
Small subunit ribosomal RNA
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Acknowledgements
We thank Guodong Mu at Jilin Center for Animal Disease Control and Prevention, Haining Zhou at Ningxia Center for Animal Disease Control and Prevention, Wei Zhu at Tengzhou Animal Husbandry and Veterinary Technology Service Center, and Yibin Hu at Bei**g Centre Polytron Technologies Inc. for their help with sample collection. We also thank International Science Editing for editing this manuscript.
Funding
This study was supported in part by The National Key Research and Development Programme of China (grant no. 2018YFD0502305), National Risk Assessment Project for Quality and Safety of Agricultural Products (grant no. GJFP201800703), Shanghai Agriculture Applied Technology Development Program, China (grant no. G20180110), Technical Standard Programme of Shanghai Science and Technology Commission (grant no. 16DZ0501900) and The Key Technology R & D Programme of Ningxia Hui Autonomous Region, China (grant no. 201601).
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The datasets supporting the conclusions in this article are included within the article. Sequences were submitted to the GenBank database under the accession numbers MH432644-MH432647.
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ZC designed the study and revised the manuscript. HY, RM and LC performed the experiments and drafted the manuscript. YH and RA participated in sample collection. YZ, HJ and XZ participated in DNA extraction and PCR amplification. XW and XH participated in data analysis. All authors read and approved the final manuscript.
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Faecal samples were collected from sheep farms with the consent of farm owners. All experiments were authorised by the Animal Ethics Committee of the Shanghai Veterinary Research Institute and approved by the Animal Care and Use Committee of the Chinese Academy of Agricultural Sciences. The Animal Ethics Committee approval number was Shvri-sh-2013020042. During the whole experimental process, all laboratory work on the study specimens were covered under the Animal Experimental Protocol of Shanghai Veterinary Research Institute (201008): “Use of animal samples for the determination of zoonotic pathogen”.
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Yang, H., Mi, R., Cheng, L. et al. Prevalence and genetic diversity of Enterocytozoon bieneusi in sheep in China. Parasites Vectors 11, 587 (2018). https://doi.org/10.1186/s13071-018-3178-9
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DOI: https://doi.org/10.1186/s13071-018-3178-9