Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Cryptosporidium suis Infection in Post-Weaned and Adult Pigs in Shaanxi Province, Northwestern China

  • Lin, Qing (College of Veterinary Medicine, Northwest A&F University) ;
  • Wang, Xing-Ye (College of Veterinary Medicine, Northwest A&F University) ;
  • Chen, Jian-Wen (College of Veterinary Medicine, Gansu Agriculture University) ;
  • Ding, Ling (College of Veterinary Medicine, Northwest A&F University) ;
  • Zhao, Guang-Hui (College of Veterinary Medicine, Northwest A&F University)
  • Received : 2014.10.02
  • Accepted : 2014.11.27
  • Published : 2015.02.28
Download PDF
⟨ Previous Next ⟩

Abstract

Cryptosporidium spp., ubiquitous enteric parasitic protozoa of vertebrates, recently emerged as an important cause of economic loss and zoonosis. The present study aimed to determine the distribution and species of Cryptosporidium in post-weaned and adult pigs in Shaanxi province, northwestern China. A total of 1,337 fresh fecal samples of post-weaned and adult pigs were collected by sterile disposable gloves from 8 areas of Shaanxi province. The samples were examined by Sheather's sugar flotation technique and microscopy at${\times}400$ magnification for Cryptosporidium infection, and the species in positive samples was further identified by PCR amplification of the small subunit (SSU) rRNA gene. A total of 44 fecal samples were successfully amplified by the nested PCR of the partial SSU rRNA, with overall prevalence of 3.3%. The average prevalence of Cryptosporidium infection in each pig farms ranged from 0 to 14.4%. Species identification by sequencing of SSU rRNA gene revealed that 42 (3.1%) samples were Cryptosporidium suis and 2 (0.15%) were Cryptosporidium scrofarum. C. suis had the highest prevalence (7.5%) in growers and the lowest in breeding pigs (0.97%). C. suis was the predominant species in pre-weaned and adult pigs, while C. scrofarum infected pigs older than 3 months only. A season-related difference of C. suis was observed in this study, with the highest prevalence in autumn (5.5%) and the lowest (1.7%) in winter. The present study provided basic information for control of Cryptosporidium infection in pigs and assessment of zoonotic transmission of pigs in Shaanxi province, China.

Keywords

References

  1. Jex AR, Pangasa A, Campbell BE, Whipp M, Hogg G, Sinclair MI, Stevens M, Gasser RB. Classification of Cryptosporidium species from patients with sporadic cryptosporidiosis by use of sequence-based multilocus analysis following mutation scanning. J Clin Microbiol 2008; 46: 2252-2262. https://doi.org/10.1128/JCM.00116-08
  2. Tomazic ML, Maidana J, Dominguez M, Uriarte EL, Galarza R, Garro C, Florin-Christensen M, Schnittger L. Molecular characterization of Cryptosporidium isolates from calves in Argentina. Vet Parasitol 2013; 198: 382-386. https://doi.org/10.1016/j.vetpar.2013.09.022
  3. Xiao L. Molecular epidemiology of Cryptosporidiosis: an update. Exp Parasitol 2010; 124: 80-89. https://doi.org/10.1016/j.exppara.2009.03.018
  4. Leoni F, Amar C, Nichols G, Pedraza-Diaz S, McLauchlin J. Genetic analysis of Cryptosporidium from 2414 humans with diarrhoea in England between 1985 and 2000. J Med Microbiol 2006; 55: 703-707. https://doi.org/10.1099/jmm.0.46251-0
  5. Kvac M, Kestranova M, Pinkova M, Kvetonova D, Kalinova J, Wagnerova P, Kotkova M, Vitovec J, Ditrich O, McEvoy J, Stenger B, Sak B. Cryptosporidium scrofarum n. sp. (Apicomplexa: Cryptosporidiidae) in domestic pigs (Sus scrofa). Vet Parasitol 2013; 191: 218-227. https://doi.org/10.1016/j.vetpar.2012.09.005
  6. Yui T, Nakajima T, Yamamoto N, Kon M, Abe N, Matsubayashi M, Shibahara T. Age-related detection and molecular characterization of Cryptosporidium suis and Cryptosporidium scrofarum in pre- and post-weaned piglets and adult pigs in Japan. Parasitol Res 2014; 113: 359-365. https://doi.org/10.1007/s00436-013-3662-2
  7. Sheoran A, Wiffin A, Widmer G, Singh P, Tzipori S. Infection with Cryptosporidium hominis provides incomplete protection of the host against Cryptosporidium parvum. J Infect Dis 2012; 205: 1019-1023. https://doi.org/10.1093/infdis/jir874
  8. Akiyoshi DE, Dilo J, Pearson C, Chapman S, Tumwine J, Tzipori S. Characterization of Cryptosporidium meleagridis of human origin passaged through different host species. Infect Immun 2003; 71: 1828-1832. https://doi.org/10.1128/IAI.71.4.1828-1832.2003
  9. Darabus G, Olariu R. The homologous and interspecies transmission of Cryptosporidium parvum and Cryptosporidium meleagridis. Pol J Vet Sci 2003; 6: 225-228.
  10. Bouzid M, Hunter PR, Chalmers RM, Tyler KM. Cryptosporidium pathogenicity and virulence. Clin Microbiol Rev 2013; 26: 115-134. https://doi.org/10.1128/CMR.00076-12
  11. Omidian Z, Ebrahimzadeh E, Shahbazi P, Asghari Z, Shayan P. Application of recombinant Cryptosporidium parvum P23 for isolation and prevention. Parasitol Res 2014; 113: 229-237. https://doi.org/10.1007/s00436-013-3648-0
  12. Kvac M, Kvetonova D, Sak B, Ditrich O. Cryptosporidium pig genotype II in immunocompetent man. Emerg Infect Dis 2009; 15: 982-983. https://doi.org/10.3201/eid1506.071621
  13. Xiao L, Bern C, Arrowood M, Sulaiman I, Zhou L, Kawai V, Vivar A, Lal AA, Gilman RH. Identification of the Cryptosporidium pig genotype in a human patient. J Infect Dis 2002; 185: 1846-1848. https://doi.org/10.1086/340841
  14. Qiu SX, Lu QB, Qi M, Zhang XH, Duan ZX, Nin CS, Jian FC, Zhang LX. The prevalence of Cryptosporidium spp. in pigs in Henan province. Chin J Zoonosis 2008; 24: 481-482 (in Chinese).
  15. Zhao C, Li P. Epidemiologic survey of pig cryptosporidiosis in Fengtai county in Anhui province. Chin J Vet Parasitol 2003; 11: 42-44 (in Chinese).
  16. Chen F, Huang K. Prevalence and phylogenetic analysis of Cryptosporidium in pigs in eastern China. Zoonoses Public Health 2007; 54: 393-400. https://doi.org/10.1111/j.1863-2378.2007.01078.x
  17. Xiao L, Singh A, Limor J, Graczyk TK, Gradus S, Lal A. Molecular characterization of Cryptosporidium oocysts in samples of raw surface water and wastewater. Appl Environ Microbiol 2001; 67: 1097-1101. https://doi.org/10.1128/AEM.67.3.1097-1101.2001
  18. Burland TG. DNASTAR's Lasergene sequence analysis software. Methods Mol Biol 2000; 132: 71-91.
  19. Tamura K, Dudley J, Nei M, Kumar S. MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 2007; 24: 1596-1599. https://doi.org/10.1093/molbev/msm092
  20. Wang R, Qiu S, Jian F, Zhang S, Shen Y, Zhang L, Ning C, Cao J, Qi M, Xiao L. Prevalence and molecular identification of Cryptosporidium spp. in pigs in Henan, China. Parasitol Res 2010; 107: 1489-1494. https://doi.org/10.1007/s00436-010-2024-6
  21. Zhao CC, Li PY. Epidemiologic survey on pig cryptosporidiosis in Fengtai county in Anhui province. Chin J Vet Parasitol 2003; 11: 42-44 (in Chinese).
  22. Ryan UM, Samarasinghe B, Read C, Buddle JR, Robertson ID, Thompson RC. Identification of a novel Cryptosporidium genotype in pigs. Appl Environ Microbiol 2003; 69: 3970-3974. https://doi.org/10.1128/AEM.69.7.3970-3974.2003
  23. Maddox-Hyttel C, Langkjaer RB, Enemark HL, Vigre H. Cryptosporidium and Giardia in different age groups of Danish cattle and pigs-occurrence and management associated risk factors. Vet Parasitol 2006; 141: 48-59. https://doi.org/10.1016/j.vetpar.2006.04.032
  24. Suarez-Luengas L, Clavel A, Quilez J, Goni-Cepero MP, Torres E, Sanchez-Acedo C, del Cacho E. Molecular characterization of Cryptosporidium isolates from pigs in Zaragoza (northeastern Spain). Vet Parasitol 2007; 148: 231-235. https://doi.org/10.1016/j.vetpar.2007.06.022
  25. Zintl A, Neville D, Maguire D, Fanning S, Mulcahy G, Smith HV, De Waal T. Prevalence of Cryptosporidium species in intensively farmed pigs in Ireland. Parasitology 2007; 134: 1575-1582.
  26. Nguyen ST, Honma H, Geurden T, Ikarash M, Fukuda Y, Huynh VV, Nguyen DT, Nakai Y. Prevalence and risk factors associated with Cryptosporidium oocyst shedding in pigs in Central Vietnam. Res Vet Sci 2012; 93: 848-852. https://doi.org/10.1016/j.rvsc.2012.01.007
  27. Wieler LH, Ilieff A, Herbst W, Bauer C, Vieler E, Bauerfeind R, Failing K, Klos H, Wengert D, Baljer G, Zahner H. Prevalence of enteropathogens in suckling and weaned piglets with diarrhoea in southern Germany. J Vet Med B Infect Dis Vet Public Health 2001; 48: 151-159. https://doi.org/10.1046/j.1439-0450.2001.00431.x
  28. Roepstorff A, Nansen P. Epidemiology and control of helminth infections in pigs under intensive and non-intensive production systems. Vet Parasitol 1994; 54: 69-85. https://doi.org/10.1016/0304-4017(94)90084-1
  29. Damriyasa IM, Bauer C. Prevalence and age-dependent occurrence of intestinal protozoan infections in suckling piglets. Berl Munch Tierarztl Wochenschr 2006; 119: 287-290.
  30. Zhang W, Yang F, Liu A, Wang R, Zhang L, Shen Y, Cao J, Ling H. Prevalence and genetic characterizations of Cryptosporidium spp. in pre-weaned and post-weaned piglets in Heilongjiang Province, China. PLoS One 2013; 8: e67564. https://doi.org/10.1371/journal.pone.0067564
  31. Morgan UM, Buddle JR, Armson A, Elliot A, Thompson RCA. Molecular and biological characterisation of Cryptosporidium in pigs. Australian Vet J 1999; 77: 44-47. https://doi.org/10.1111/j.1751-0813.1999.tb12428.x
  32. Guselle NJ, Appelbee AJ, Olson ME. Biology of Cryptosporidium parvum in pigs: from weaning to market. Vet Parasitol 2003; 113: 7-18. https://doi.org/10.1016/S0304-4017(03)00039-6
  33. Ryan UM, Monis P, Enemark HL, Sulaiman I, Samarasinghe B, Read C, Buddle R, Robertson I, Zhou L, Thompson RC, Xiao L. Cryptosporidium suis n. sp. (Apicomplexa: Cryptosporidiidae) in pigs (Sus scrofa). J Parasitol 2004; 90: 769-773. https://doi.org/10.1645/GE-202R1
  34. Langkjaer RB, Vigre H, Enemark HL, Maddox-Hyttel C. Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark. Parasitology 2007; 134: 339-350. https://doi.org/10.1017/S0031182006001533
  35. Hsu BM, Wun HY, Hsu CL. Detection and species identification of Cryptosporidium from Taiwan feeding animals. J Parasitol 2008; 94: 252-256. https://doi.org/10.1645/GE-1135.1
  36. Leoni F, Amar C, Nichols G, Pedraza-Diaz S, McLauchlin J. Genetic analysis of Cryptosporidium from 2414 humans with diarrhoea in England between 1985 and 2000. J Med Microbiol 2006 55: 703-707. https://doi.org/10.1099/jmm.0.46251-0
  37. Kvac M, Hanzlikova D, Sak B, Kvetonova D. Prevalence and age-related infection of Cryptosporidium suis, C. muris and Cryptosporidium pig genotype II in pigs on a farm complex in the Czech Republic. Vet Parasitol 2009; 160: 319-322. https://doi.org/10.1016/j.vetpar.2008.11.007
  38. Xiao S, An W, Chen Z, Zhang D, Yu J, Yang M. Occurrences and genotypes of Cryptosporidium oocysts in river network of southern-eastern China. Parasitol Res 2012; 110: 1701-1709. https://doi.org/10.1007/s00436-011-2688-6
  39. Feng Y, Li N, Duan L, Xiao L. Cryptosporidium genotype and subtype distribution in raw wastewater in Shanghai, China: evidence for possible unique Cryptosporidium hominis transmission. J Clin Microbiol 2009; 47: 153-157. https://doi.org/10.1128/JCM.01777-08
  40. Feng Y, Zhao X, Chen J, Jin W, Zhou X, Li N, Wang L, Xiao L. Occurrence, source, and human infection potential of Cryptosporidium and Giardia spp. in source and tap water in Shanghai, China. Appl Environ Microbiol 2011; 77: 3609-3616. https://doi.org/10.1128/AEM.00146-11
  41. Jenikova M, Nemejc K, Sak B, Kvetonova D, Kvac M. New view on the age-specificity of pig Cryptosporidium by species-specific primers for distinguishing Cryptosporidium suis and Cryptosporidium pig genotype II. Vet Parasitol 2011; 176: 120-125. https://doi.org/10.1016/j.vetpar.2010.11.010
  42. Yoshiuchi R, Matsubayashi M, Kimata I, Furuya M, Tani H, Sasai K. Survey and molecular characterization of Cryptosporidium and Giardia spp. in owned companion animal, dogs and cats, in Japan. Vet Parasitol 2010; 174: 313-316. https://doi.org/10.1016/j.vetpar.2010.09.004

Cited by

  1. Molecular Epidemiology of Cryptosporidiosis in China vol.8, pp.None, 2015, https://doi.org/10.3389/fmicb.2017.01701
  2. Presence of zoonotic Cryptosporidium scrofarum , Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotypes in captive Eurasian wild boars ( Sus scrofa ) in China: potential for zoonot vol.10, pp.None, 2017, https://doi.org/10.1186/s13071-016-1942-2
  3. Molecular identification and epidemiological comparison of Cryptosporidium spp. among different pig breeds in Tibet and Henan, China vol.15, pp.None, 2019, https://doi.org/10.1186/s12917-019-1847-3
  4. Prevalence of Cryptosporidium in pigs in China: A systematic review and meta‐analysis vol.68, pp.3, 2015, https://doi.org/10.1111/tbed.13806