Molecular characterization of Cryptosporidium spp. in minks (Neovison vison), blue foxes (Vulpes lagopus), and raccoon dogs (Nyctereutes procyonoides) in farms from Xinjiang, Northwest China

Abstract

The objective of this study was to determine the infection rate and genetic diversity of Cryptosporidium spp. in minks, foxes, and raccoon dogs, farmed in the Xinjiang Uygur Autonomous Region, Northwest China. Fresh fecal specimens were collected from individual cages of farmed minks (n = 214), blue foxes (n = 35), and raccoon dogs (n = 39) and examined using nested PCR based on the Cryptosporidium spp. small subunit rRNA gene. Cryptosporidium spp. was detected in 35 cages (12.2%, 35/288), with a higher infection rate detected in raccoon dogs (20.5%) compared with minks (12.1%) and blue foxes (2.9%). Sequence analysis showed that Cryptosporidium canis was the only species identified in blue foxes and raccoon dogs, while in the 26 Cryptosporidium-positive mink specimens, Cryptosporidium mink genotype (n = 17), C. canis (n = 7), and Cryptosporidium parvum (n = 2) were identified. Further analysis based on the 60-kDa glycoprotein (gp60) gene determined that both C. parvum isolates belonged to the subtype IIdA15G1, while eight of the 17 Cryptosporidium mink genotype isolates were a novel subtype that we have named XeA5G1. To the best of our knowledge, this is the first report of C. parvum subtype IIdA15G1 infection in minks. Since all the Cryptosporidium species/genotypes identified in minks, foxes, and raccoon dogs from Xinjiang have been previously found in humans, our results suggest that these fur animals may play a role in the transmission of zoonotic Cryptosporidium.

This is a preview of subscription content, access via your institution.

Fig. 1

References

  1. Alves M, Xiao L, Sulaiman I, Lal AA, Matos O, Antunes F (2003) Subgenotype analysis of Cryptosporidium isolates from humans, cattle, and zoo ruminants in Portugal. J Clin Microbiol 41(6):2744–2747. https://doi.org/10.1128/jcm.41.6.2744-2747.2003

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  2. Cacciò S, Widmer G (2014) Cryptosporidium: parasite and disease. Springer-Verlag, Wien

    Book  Google Scholar 

  3. Fayer R (2010) Taxonomy and species delimitation in Cryptosporidium. Exp Parasitol 124(1):90–97. https://doi.org/10.1016/j.exppara.2009.03.005

    Article  PubMed  Google Scholar 

  4. Feng Y, Xiao L (2017) Molecular epidemiology of cryptosporidiosis in China. Front Microbiol 8:1701. https://doi.org/10.3389/fmicb.2017.01701

    Article  PubMed  PubMed Central  Google Scholar 

  5. Feng Y, Alderisio KA, Yang W, Blancero LA, Kuhne WG, Nadareski CA, Reid M, Xiao L (2007) Cryptosporidium genotypes in wildlife from a New York watershed. Appl Environ Microbiol 73(20):6475–6483. https://doi.org/10.1128/AEM.01034-07

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  6. Feng Y, Ryan UM, Xiao L (2018) Genetic diversity and population structure of Cryptosporidium. Trends Parasitol 34(11):997–1011. https://doi.org/10.1016/j.pt.2018.07.009

    CAS  Article  Google Scholar 

  7. Gomez-Couso H, Mendez-Hermida F, Ares-Mazas E (2007) First report of Cryptosporidium parvum ‘ferret’ genotype in American mink (Mustela vison Shreber 1777). Parasitol Res 100(4):877–879. https://doi.org/10.1007/s00436-006-0338-1

    CAS  Article  PubMed  Google Scholar 

  8. Jiang J, Alderisio KA, Xiao L (2005) Distribution of Cryptosporidium genotypes in storm event water samples from three watersheds in New York. Appl Environ Microbiol 71(8):4446–4454. https://doi.org/10.1128/AEM.71.8.4446-4454.2005

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Kellnerova K, Holubova N, Jandova A, Vejcik A, McEvoy J, Sak B, Kvac M (2017) First description of Cryptosporidium ubiquitum XIIa subtype family in farmed fur animals. Eur J Protistol 59:108–113. https://doi.org/10.1016/j.ejop.2017.03.007

    Article  PubMed  Google Scholar 

  10. Lv C, Zhang L, Wang R, Jian F, Zhang S, Ning C, Wang H, Feng C, Wang X, Ren X, Qi M, Xiao L (2009) Cryptosporidium spp. in wild, laboratory, and pet rodents in China: prevalence and molecular characterization. Appl Environ Microbiol 75(24):7692–7699. https://doi.org/10.1128/AEM.01386-09

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Mateo M, de Mingo MH, de Lucio A, Morales L, Balseiro A, Espi A, Barral M, Lima Barbero JF, Habela MA, Fernandez-Garcia JL, Bernal RC, Koster PC, Cardona GA, Carmena D (2017) Occurrence and molecular genotyping of Giardia duodenalis and Cryptosporidium spp. in wild mesocarnivores in Spain. Vet Parasitol 235:86–93. https://doi.org/10.1016/j.vetpar.2017.01.016

    Article  PubMed  Google Scholar 

  12. Matsubayashi M, Abe N, Takami K, Kimata I, Iseki M, Nakanishi T, Tani H, Sasai K, Baba E (2004) First record of Cryptosporidium infection in a raccoon dog (Nyctereutes procyonoides viverrinus). Vet Parasitol 120(3):171–175. https://doi.org/10.1016/j.vetpar.2004.01.007

    Article  PubMed  Google Scholar 

  13. Nagano Y, Finn MB, Lowery CJ, Murphy T, Moriarty J, Power E, Toolan D, O'Loughlin A, Watabe M, McCorry KA, Crothers E, Dooley JS, Rao JR, Rooney PJ, Millar BC, Matsuda M, Elborn JS, Moore JE (2007) Occurrence of Cryptosporidium parvum and bacterial pathogens in faecal material in the red fox (Vulpes vulpes) population. Vet Res Commun 31(5):559–564. https://doi.org/10.1007/s11259-007-3519-1

    CAS  Article  PubMed  Google Scholar 

  14. Papanikolopoulou V, Baroudi D, Guo Y, Wang Y, Papadopoulos E, Lafi SQ, Abd El-Tawab MM, Diakou A, Giadinis ND, Feng Y, Xiao L (2018) Genotypes and subtypes of Cryptosporidium spp. in diarrheic lambs and goat kids in northern Greece. Parasitol Int 67(4):472–475. https://doi.org/10.1016/j.parint.2018.04.007

    Article  PubMed  Google Scholar 

  15. Quilez J, Torres E, Chalmers RM, Hadfield SJ, Del Cacho E, Sanchez-Acedo C (2008) Cryptosporidium genotypes and subtypes in lambs and goat kids in Spain. Appl Environ Microbiol 74(19):6026–6031. https://doi.org/10.1128/AEM.00606-08

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  16. Stuart P, Golden O, Zintl A, de Waal T, Mulcahy G, McCarthy E, Lawton C (2013) A coprological survey of parasites of wild carnivores in Ireland. Parasitol Res 112(10):3587–3593. https://doi.org/10.1007/s00436-013-3544-7

    Article  PubMed  Google Scholar 

  17. Wang R, Zhang L, Feng Y, Ning C, Jian F, Xiao L, Zhao J, Wang Y (2008) Molecular characterization of a new genotype of Cryptosporidium from American minks (Mustela vison) in China. Vet Parasitol 154(1–2):162–166. https://doi.org/10.1016/j.vetpar.2007.12.038

    CAS  Article  PubMed  Google Scholar 

  18. Xiao L, Sulaiman IM, Ryan UM, Zhou L, Atwill ER, Tischler ML, Zhang X, Fayer R, Lal AA (2002) Host adaptation and host-parasite co-evolution in Cryptosporidium: implications for taxonomy and public health. Int J Parasitol 32(14):1773–1785

    Article  Google Scholar 

  19. Yang Z, Zhao W, Wang J, Ren G, Zhang W, Liu A (2018) Molecular detection and genetic characterizations of Cryptosporidium spp. in farmed foxes, minks, and raccoon dogs in northeastern China. Parasitol Res 117(1):169–175. https://doi.org/10.1007/s00436-017-5686-5

    Article  PubMed  Google Scholar 

  20. Zhang S, Tao W, Liu C, Jiang Y, Wan Q, Li Q, Yang H, Lin Y, Li W (2016a) First report of Cryptosporidium canis in foxes (Vulpes vulpes) and raccoon dogs (Nyctereutes procyonoides) and identification of several novel subtype families for Cryptosporidium mink genotype in minks (Mustela vison) in China. Infect Genet Evol 41:21–25. https://doi.org/10.1016/j.meegid.2016.03.016

    Article  PubMed  Google Scholar 

  21. Zhang XX, Cong W, Ma JG, Lou ZL, Zheng WB, Zhao Q, Zhu XQ (2016b) First report of Cryptosporidium canis in farmed Arctic foxes (Vulpes lagopus) in China. Parasit Vectors 9:126. https://doi.org/10.1186/s13071-016-1396-6

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Zhou L, Fayer R, Trout JM, Ryan UM, Schaefer FW 3rd, Xiao L (2004) Genotypes of Cryptosporidium species infecting fur-bearing mammals differ from those of species infecting humans. Appl Environ Microbiol 70(12):7574–7577. https://doi.org/10.1128/AEM.70.12.7574-7577.2004

    CAS  Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We thank Gemma Richards, PhD, from the Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac), for editing the English text of a draft of this manuscript.

We also thank MogoEdit, China (http://www.mogoedit.com), for polishing the revised manuscript.

Funding

This study was supported by the National Natural Science Foundation of China (31702227) and the Program for Young and Middle-aged Leading Science, Technology, and Innovation of Xinjiang Production & Construction Group (2018CB034). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Meng Qi.

Ethics declarations

Appropriate permission was obtained from the farm managers prior to fecal specimen collection, and no specific permits were required for the described field studies. The protocol was reviewed and approved by the Ethics Committee of Tarim University.

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Section Editor: Yaoyu Feng

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Qian, W., Zhang, Y., Jiang, Y. et al. Molecular characterization of Cryptosporidium spp. in minks (Neovison vison), blue foxes (Vulpes lagopus), and raccoon dogs (Nyctereutes procyonoides) in farms from Xinjiang, Northwest China. Parasitol Res 119, 3923–3927 (2020). https://doi.org/10.1007/s00436-020-06909-8

Download citation

Keywords

  • Cryptosporidium
  • Zoonotic
  • Subtyping
  • Mink
  • Fox
  • Raccoon dog
  • China