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Acta Parasitologica

, Volume 64, Issue 1, pp 44–50 | Cite as

Detection and Genotyping Study of Enterocytozoon bieneusi in Sheep and Goats in East-central China

  • Wen-chao Li
  • Kai Wang
  • You-fang GuEmail author
Original Paper
  • 34 Downloads

Abstract

Background

Enterocytozoon bieneusi, the dominant zoonotic species of microsporidia, has been reported in various animals and humans. However, relatively little information is available concerning the worldwide prevalence and genotypes of E. bieneusi in ruminants, such as sheep and goats. The present study was conducted to evaluate the prevalence and genetic characteristics of E. bieneusi in sheep and goats in east-central China.

Methods

Fresh fecal samples from 832 sheep and 781 goats were evaluated for the presence of E. bieneusi using PCR and sequencing of the ribosomal internal transcribed spacer.

Results

28 sheep specimens (3.4%) and 32 goat specimens (4.1%) were positive for E. bieneusi. A total of 12 ITS genotypes were identified, including 7 known genotypes (COS-I, OEB1, BEB6, CHG1, CHG3, COS-II, and CHC8) and 5 novel genotypes (named AHS1, AHS2, JSS1, AHG1, and AHG2). The dominant genotypes in sheep and goats were BEB6 and CHG3, respectively. Phylogenetic analysis revealed that all genotypes obtained in this study belonged to the so-called “cattle-specific” Group 2.

Conclusions

These findings show a relatively low occurrence and genetic diversity of E. bieneusi in sheep and goats in east-central China. Further studies are required to elucidate the role of sheep and goats in the epidemiology of microsporidia.

Keywords

Enterocytozoon bieneusi Genotype Sheep Goat China 

Notes

Acknowledgements

We would like to thank all of the staff in the sampled sheep and goat farms for their assistance with this study. This study was supported by the Modern Cattle and Goat Industrial Technology System Program of Anhui Province, Anhui Provincial Natural Science Foundation (1808085MC84), the Key Program of Anhui Science and Technology University (No. ZRC2016478) and the Key Discipline Construction Program of University of Science and Technology of Anhui (AKZDXK2015A04).

References

  1. 1.
    Abu Samra N., Thompson P.N., Jori F., Zhang H., Xiao L. 2012. Enterocytozoon bieneusi at the wildlife/livestock interface of the Kruger National Park, South Africa.Veterinary Parasitology,190, 587-590.  https://doi.org/10.1016/j.vetpar.2012.06.031 CrossRefGoogle Scholar
  2. 2.
    Al-Herrawy A.Z., Gad M.A. 2016.Microsporidial spores in fecal samples of some domesticated animals living in giza, Egypt. Iranian Journal of Parasitology,11,195-203Google Scholar
  3. 3.
    Fayer R., Santin M., Trout J.M.2007. Enterocytozoon bieneusi in mature dairy cattle on farms in the eastern United States. Parasitology Research,102,15–20.  https://doi.org/10.1007/s00436-007-0746-x CrossRefGoogle Scholar
  4. 4.
    Fiuza V.R., Lopes C.W., Cosendey R.I., de Oliveira F.C., Fayer R., Santín M. 2016.Zoonotic Enterocytozoon bieneusi genotypes found in brazilian sheep. Research in Veterinary Science,107,196-201. https://doi.org/10.1016/j.rvsc.2016.06.006 CrossRefGoogle Scholar
  5. 5.
    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. Frontiers in Microbiology,8,879.  https://doi.org/10.3389/fmicb.2017.00879 CrossRefGoogle Scholar
  6. 6.
    Hu S., Liu Z., Yan F., Zhang Z., Zhang G., Zhang L., Jian F., Zhang S., Ning C., Wang R. 2017. Zoonotic and host-adapted genotypes of Cryptosporidium spp., Giardia duodenalis and Enterocytozoon bieneusi in dairy cattle in Hebei and Tianjin, China. Veterinary Parasitology, 248:68-73.  https://doi.org/10.1016/j.vetpar.2017.10.024 CrossRefGoogle Scholar
  7. 7.
    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.  https://doi.org/10.1128/aem.01928-15 CrossRefGoogle Scholar
  8. 8.
    Karim M.R., Dong H., Li T., Yu F., Li D., Zhang L., Li J., Wang R., Li S., Li X., Rume F.I., Ning C. 2015.Predomination and new genotypes of Enterocytozoon bieneusi in captive nonhuman primates in zoos in China: high genetic diversity and zoonotic significance. PLoS One, 10,e0117991. https://doi.org/10.1371/journal.pone.0117991 CrossRefGoogle Scholar
  9. 9.
    Keeling P.J., Fast N.M. 2002.Microsporidia: biology and evolution of highly reduced intracellular parasites. Annual Review Microbiology 56:93–116.  https://doi.org/10.1146/annurev.micro.56. 012302.160854CrossRefGoogle Scholar
  10. 10.
    Keeling P. 2009. Five questions about microsporidia. PLoS Pathog,5:e1000489.  https://doi.org/10.1371/journal.ppat.1000489 CrossRefGoogle Scholar
  11. 11.
    Li W., Li Y., Li W., Yang J., Song M., Diao R., Jia H., Lu Y., Zheng J., Zhang X., Xiao L. 2014.Genotypes of Enterocytozoon bieneusi in livestock in China: high prevalence and zoonotic potential. PLoS One. 9,e97623.  https://doi.org/10.1371/journal.pone.0097623 CrossRefGoogle Scholar
  12. 12.
    Li N., Xiao L.H., Wang L., Zhao S.M., Zhao X.K., Duan L.P., Guo M., Liu L., Feng Y.,2012.Molecular surveillance of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi by genotyping and subtyping parasites in wastewater. PLoS Neglected Tropical Diseases,6,e18099.  https://doi.org/10.1371/journal.pntd.0001809 Google Scholar
  13. 13.
    Li W.C., Wang K., Gu Y. 2018. Occurrence of Blastocystis sp. and Pentatrichomonas hominis insheep and goats in China.Parasite & Vectors, 11,93.  https://doi.org/10.1186/s13071-018-2671-5 CrossRefGoogle Scholar
  14. 14.
    Li W, Song Y, Zhong Z, Huang X, Wang C, Li C, Yang H, Liu H, Ren Z, Lan J, Wu K, Peng G.2017.Population genetics of Enterocytozoon bieneusi in captive giant pandas of China. Parasite & Vectors, 10,499. https://doi.org/10.1186/s13071-017-2459-z
  15. 15.
    Lores B., del Aguila C., Arias C. 2002. Enterocytozoon bieneusi (microsporidia) in faecal samples from domestic animals from Galicia, Spain. Memórias do Instituto Oswaldo Cruz,97,941–945.CrossRefGoogle Scholar
  16. 16.
    Peng X.Q., Tian G.R., Ren G.J., Yu Z.Q., Lok J.B., Zhang L.X., Wang X.T., Song J.K., Zhao G.H.2016.Infection rate of Giardia duodenalis, Cryptosporidium spp. and Enterocytozoon bieneusi in cashmere, dairy and meat goats in China. Infection,Genetics and Evolution,41,26-31.  https://doi.org/10.1016/j.meegid.2016.03.021 CrossRefGoogle Scholar
  17. 17.
    Santin M., Fayer R. 2009. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. The Journal of Eukaryotic Microbiology,l56,34-38.  https://doi.org/10.1111/j.1550-7408.2008.00380.x
  18. 18.
    Santín, M., Fayer, R.2011.Microsporidiosis: Enterocytozoon bieneusi in domesticated and wild animals. Research in Veterinary Science,90, 363–371.  https://doi.org/10.1016/j.rvsc.2010.07.014 CrossRefGoogle Scholar
  19. 19.
    Shi K., Li M., Wang X., Li J., Karim M.R., Wang R., Zhang L., Jian F., Ning C. 2016. Molecular survey of Enterocytozoon bieneusi in sheep and goats in China. Parasite & Vectors, 9:23. https://doi.org/10.1186/s13071-016-1304-0 CrossRefGoogle Scholar
  20. 20.
    Stensvold C.R., Beser J., Ljungstrom B., Troell K., Lebbad M. 2014. Low host-specific Enterocytozoon bieneusi genotype BEB6 is common in Swedish lambs.Veterinary Parasitology,205,371–374. https://doi.org/10.1016/j.vetpar.2014.06.010 CrossRefGoogle Scholar
  21. 21.
    Sulaiman I.M., Fayer R., Lal A.A., Trout J.M., Schaefer F.W., Xiao L. 2003.Molecular characterization of microsporidia indicates that wild mammals harbor host-adapted Enterocytozoon spp. as well as human-pathogenic Enterocytozoon bieneusi. Applied and Environmental Microbiology,69,4495–4501.  https://doi.org/10.1128/aem.69.8.4495-4501.CrossRefGoogle Scholar
  22. 22.
    Xu H., Jin Y., Wu W., Li P., Wang L., Li N., Feng Y., Xiao L.2016.Genotypes of Cryptosporidium spp.,Enterocytozoon bieneusi and Giardia duodenalis in dogs and cats in Shanghai,China. Parasite & Vectors,9,121.  https://doi.org/10.1186/s13071-016-1409-5 CrossRefGoogle Scholar
  23. 23.
    Yang Z.Y., ZhaoW., Shen Y.J., Zhang W.Z., Shi Y., Ren G.X., Yang D., Ling H., Yang F.K., Liu A.Q., Cao J.P. 2016.Subtyping of Cryptosporidium cuniculus and genotyping of Enterocytozoon bieneusi in rabbits in two farms in Heilongjiang Province, China. Parasite,23,52. https://doi.org/10.1051/parasite/2016063 CrossRefGoogle Scholar
  24. 24.
    Ye J, Xiao L,Wang Y, Guo Y, Roellig DM, 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.  https://doi.org/10.1016/j.vetpar.2015.04.011 CrossRefGoogle Scholar
  25. 25.
    Zhang Q., Cai J., Li P., Wang L., Guo Y., Li C., Lei M., Feng Y., Xiao L. 2018. Enterocytozoon bieneusi genotypes in Tibetan sheep and yaks.Parasitology Research, 117,721-727.  https://doi.org/10.1007/s00436-017-5742-1 CrossRefGoogle Scholar
  26. 26.
    Zhang X., Wang Z., Su Y., Liang X., Sun X., Peng S., Lu H., Jiang N., Yin J.,Xiang M., Chen Q. 2011. Identification and genotyping of Enterocytozoon bieneusi in China.Journal of Clinical Microbiology, 49,2006–2008. https://doi.org/10.1128/jcm.00372-11 CrossRefGoogle Scholar
  27. 27.
    Zhang Z., Huang J., Karim M.R., Zhao J., Dong H., Ai W., Li F., Zhang L., Wang R.2015. Zoonotic Enterocytozoon bieneusi genotypes in Pere David’s deer (Elaphurus davidianus) in Henan, China. Experimental Parasitology,155,46–48.  https://doi.org/10.1016/j.exppara.2015.05.008 CrossRefGoogle Scholar
  28. 28.
    Zhao W., Zhang W., Yang D., Zhang L., Wang R., Liu A. 2015.Prevalence of Enterocytozoon bieneusi and genetic diversity of ITS genotypes in sheep and goats in China. Infection,Genetics and Evolution,32,265-70.  https://doi.org/10.1016/j.meegid.2015.03.026 CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019

Authors and Affiliations

  1. 1.College of Animal ScienceAnhui Science and Technology UniversityFengyangPeople’s Republic of China

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