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Molecular detection and genotype distribution of Enterocytozoon bieneusi in farmed silver foxes (Vulpes vulpes) and arctic foxes (Vulpes lagopus) in Shandong Province, eastern China

  • Yuan-Yuan Ma
  • Yang Zou
  • Ye-Ting Ma
  • Lan-Bi Nie
  • Shi-Chen Xie
  • Wei Cong
  • Qian-Ming Xu
  • Xing-Quan ZhuEmail author
Genetics, Evolution, and Phylogeny - Short Communication
  • 17 Downloads

Abstract

Enterocytozoon bieneusi is an opportunistic enteric pathogen which can infect a wide range of animal species and humans. It is the most diagnosed species of Microsporidia in humans and has an impact on public health. Many infected animals including foxes may be a potential source for transmitting E. bieneusi to humans. However, limited information is available on the E. bieneusi prevalence and genotypes in farmed foxes in China. Therefore, in the present study, 344 fresh fecal samples were collected from farmed foxes (Vulpes vulpes and Vulpes lagopus) in Shandong Province, and the prevalence and genotypes of E. bieneusi were examined based on sequence analysis of the ribosomal internal transcribed spacer (ITS) region. The overall E. bieneusi prevalence was 9% (31/344); of them, 6.5% (9/138) in farmed silver foxes (V. vulpes) and 10.7% (22/206) in farmed arctic foxes (V. lagopus). Moreover, four known (Hum-q1, NCF2, HND-1, and Type IV) and two novel E. bieneusi genotypes (SDF1 and SDF2) were identified in farmed foxes in the present study. All of the E. bieneusi genotypes belonged to the zoonotic group based on phylogenetic analysis. In addition, 2, 4, 0, and 11 samples were successfully amplified at MS1, MS3, MS4, and MS7 loci, respectively. The present study reveals E. bieneusi prevalence and genotype distribution in farmed foxes in Shandong Province and enlarged the host and geographic information of E. bieneusi in China.

Keywords

Enterocytozoon bieneusi Farmed foxes Prevalence Genotypes Shandong Province China 

Notes

Funding information

Project support was provided by the Agricultural Science and Technology Innovation Program (ASTIP) (Grant No. CAAS-ASTIP-2016-LVRI-03) and The Elite Program of Chinese Academy of Agricultural Sciences.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This study was reviewed and approved by the Animal Administration and Ethics Committee of Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences. All fecal samples were collected from the farmed foxes after the permission of the farm owners or managers, and all procedures were performed strictly in accordance with the requirements of Animal Ethics Procedures and Guidelines of the People’s Republic of China.

References

  1. Galván-Díaz AL, Magnet A, Fenoy S, Henriques-Gil N, Haro M, Gordo FP, Millán J, Miró G, del Águila C, Izquierdo F (2014) Microsporidia detection and genotyping study of human pathogenic E. bieneusi in animals from Spain. PLoS One 9:e92289CrossRefGoogle Scholar
  2. Li W, Feng Y, Santin M (2019a) Host specificity of Enterocytozoon bieneusi and public health implications. Trends Parasitol 35:436–451CrossRefGoogle Scholar
  3. Matos O, Lobo ML, Xiao L (2012) Epidemiology of Enterocytozoon bieneusi infection in humans. J Parasitol Res 2012:981424CrossRefGoogle Scholar
  4. Santín M, Calero Bernal R, Carmena D, Mateo M, Balseiro A, Barral M, Lima Barbero JF, Habela MÁ (2018) Molecular characterization of Enterocytozoon bieneusi in wild carnivores in Spain. J Eukaryot Microbiol 65:468–474CrossRefGoogle Scholar
  5. Sulaiman IM, Fayer R, Lal AA, Trout JM, Schaefer FW 3rd, Xiao L (2003) Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Appl Environ Microbiol 69:4495–4501CrossRefGoogle Scholar
  6. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882CrossRefGoogle Scholar
  7. Xu C, Ma X, Zhang H, Zhang XX, Zhao JP, Ba HX, Rui-Du, Xing XM, Wang QK, Zhao Q (2016) Prevalence, risk factors and molecular characterization of Enterocytozoon bieneusi in raccoon dogs (Nyctereutes procyonoides) in five provinces of Northern China. Acta Trop 161:68–72CrossRefGoogle Scholar
  8. Yang Y, Lin Y, Li Q, Zhang S, Tao W, Wan Q, Jiang Y, Li W (2015) Widespread presence of human-pathogenic Enterocytozoon bieneusi genotype D in farmed foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) in China: first identification and zoonotic concern. Parasitol Res 114:4341–4348CrossRefGoogle Scholar
  9. Yue DM, Ma JG, Li FC, Hou JL, Zheng WB, Zhao Q, Zhang XX, Zhu XQ (2017) Occurrence of Enterocytozoon bieneusi in donkeys (Equus asinus) in China: a public health concern. Front Microbiol 8:565CrossRefGoogle Scholar
  10. Zhang X, Cong W, Lou Z, Ma J, Zheng W, Yao Q, Zhao Q, Zhu X (2016) Prevalence, risk factors and multilocus genotyping of Enterocytozoon bieneusi in farmed foxes (Vulpes lagopus), Northern China. Parasit Vectors 9:72CrossRefGoogle Scholar
  11. Zhang Y, Koehler AV, Wang T, Robertson GJ, Bradbury RS, Gasser RB (2018) Enterocytozoon bieneusi genotypes in people with gastrointestinal disorders in Queensland and Western Australia. Infect Genet Evol 65:293–299CrossRefGoogle Scholar
  12. Zhao GH, Du SZ, Wang HB, Hu XF, Deng MJ, Yu SK, Zhang LX, Zhu XQ (2015a) First report of zoonotic Cryptosporidium spp., Giardia intestinalis and Enterocytozoon bieneusi in golden takins (Budorcas taxicolor bedfordi). Infect Genet Evol 34:394–401CrossRefGoogle Scholar
  13. Zhao W, Zhang W, Yang Z, Liu A, Zhang L, Yang F, Wang R, Ling H (2015b) Genotyping of Enterocytozoon bieneusi in farmed blue foxes (Alopex lagopus) and raccoon dogs (Nyctereutes procyonoides) in China. PLoS One 10:e142611Google Scholar
  14. Li W, Feng Y, Zhang L, Xiao L (2019b) Potential impacts of host specificity on zoonotic or interspecies transmission of Enterocytozoon bieneusi. Infect Genet Evol 75:104033CrossRefGoogle Scholar
  15. Li W, Xiao L (2019) Multilocus sequence typing and population genetic analysis of Enterocytozoon bieneusi: host specificity and its impacts on public health. Front Genet 10:30CrossRefGoogle Scholar
  16. Huang J, Zhang Z, Yang Y, Wang R, Zhao J, Jian F, Ning C, Zhang L (2017) New genotypes of Enterocytozoon bieneusi isolated from sika deer and red deer in China. Front Microbiol. 8:879CrossRefGoogle Scholar
  17. Feng Y, Li N, Dearen T, Lobo ML, Matos O, Cama V, Xiao L (2011) Development of a multilocus sequence typing tool for high-resolution genotyping of Enterocytozoon bieneusi. Appl Environ Microbiol 77:4822–4828CrossRefGoogle Scholar
  18. Chen D, Wang SS, Zou Y, Li Z, Xie SC, Shi LQ, Zou FC, Zhu XQ, Yang JF, Zhao GH (2018) Prevalence and multi-locus genotypes of Enterocytozoon bieneusi in black-boned sheep and goats in Yunnan Province, southwestern China. Infect Genet Evol 65:385–391CrossRefGoogle Scholar
  19. Zou Y, Zheng WB, Song HY, Xia CY, Shi B, Liu JZ, Hou JL, Zhu XQ (2019) Prevalence and genetic characterization of Enterocytozoon bieneusi and Giardia duodenalis in Tibetan pigs in Tibet, China. Infect Genet Evol 75:104019CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.College of Animal Science and TechnologyAnhui Agricultural UniversityHefeiPeople’s Republic of China
  2. 2.State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, Lanzhou Veterinary Research InstituteChinese Academy of Agricultural SciencesLanzhouPeople’s Republic of China
  3. 3.Marine CollegeShandong University at WeihaiWeihaiPeople’s Republic of China
  4. 4.Jiangsu Co-innovation Center for the Prevention and Control of Important Animal Infectious Diseases and ZoonosesYangzhou University College of Veterinary MedicineYangzhouPeople’s Republic of China

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