Parasites, Hosts and Diseases

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

DOI QR Code

Simultaneous Molecular Detection of Cryptosporidium and Cyclospora from Raw Vegetables in Korea

  • Sim, Seobo (Department of Environmental and Tropical Medicine & International Healthcare Research Institute, Konkuk University School of Medicine) ;
  • Won, Jua (Department of Environmental and Tropical Medicine & International Healthcare Research Institute, Konkuk University School of Medicine) ;
  • Kim, Jae-Whan (Department of Environmental and Tropical Medicine & International Healthcare Research Institute, Konkuk University School of Medicine) ;
  • Kim, Kyungjin (Department of Environmental and Tropical Medicine & International Healthcare Research Institute, Konkuk University School of Medicine) ;
  • Park, Woo-Yoon (Department of Radiation Oncology, College of Medicine, Chungbuk National University) ;
  • Yu, Jae-Ran (Department of Environmental and Tropical Medicine & International Healthcare Research Institute, Konkuk University School of Medicine)
  • Received : 2017.01.14
  • Accepted : 2017.03.19
  • Published : 2017.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Cryptosporidium and Cyclospora are well-known coccidian protozoa that can cause waterborne and food-borne diarrheal illnesses. There have been a few reports regarding contamination in different vegetables with Cryptosporidium, but no data are available regarding the sources of Cyclospora infections in Korea. In the present study, we collected 6 kinds of vegetables (perilla leaves, winter-grown cabbages, chives, sprouts, blueberries, and cherry tomatoes) from July 2014 to June 2015, and investigated contamination by these 2 protozoa using multiplex quantitative real-time PCR. Among 404 vegetables, Cryptosporidium and Cyclospora were detected in 31 (7.7%) and 5 (1.2%) samples, respectively. In addition, Cryptosporidium was isolated from all 6 kinds of vegetables, whereas Cyclospora was detected in 4 kinds of vegetables (except perilla leaves and chives). Cryptosporidium (17.8%) and Cyclospora (2.9%) had the highest detection rates in chives and winter-grown cabbages, respectively. Cryptosporidium was detected all year long; however, Cyclospora was detected only from October to January. In 2 samples (sprout and blueberry), both Cryptosporidium and Cyclospora were detected. Further investigations using TaqI restriction enzyme fragmentation and nested PCR confirmed Cryptosporidium parvum and Cyclospora cayetanensis, respectively. In conclusion, we detected C. cayetanensis in vegetables for the first time in Korea. This suggests that screening should be employed to prevent these protozoal infections in Korea.

Keywords

References

  1. Mac Kenzie WR, Hoxie NJ, Proctor ME, Gradus MS, Blair KA, Peterson DE, Kazmierczak JJ, Addiss DG, Fox KR, Rose JB, Davis JP. A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. N Engl J Med 1994; 331: 161-167. https://doi.org/10.1056/NEJM199407213310304
  2. Baldursson S, Karanis P. Waterborne transmission of protozoan parasites: review of worldwide outbreaks - an update 2004-2010. Water Res 2011; 45: 6603-6614. https://doi.org/10.1016/j.watres.2011.10.013
  3. Smith HV, Rose JB. Waterborne cryptosporidiosis: current status. Parasitol Today 1998; 14: 14-22. https://doi.org/10.1016/S0169-4758(97)01150-2
  4. Agholi M, Shahabadi SN, Motazedian MH, Hatam GR. Prevalence of enteric protozoan oocysts with special reference to Sarcocystis cruzi among fecal samples of diarrheic immunodeficient patients in Iran. Korean J Parasitol 2016; 54: 339-344. https://doi.org/10.3347/kjp.2016.54.3.339
  5. Ortega YR, Sterling CR, Gilman RH. Cyclospora cayetanensis. Adv Parasitol 1998; 40: 399-418. https://doi.org/10.1016/S0065-308X(08)60128-1
  6. Chacin-Bonilla L. Epidemiology of Cyclospora cayetanensis: a review focusing in endemic areas. Acta Trop 2010; 115: 181-193. https://doi.org/10.1016/j.actatropica.2010.04.001
  7. Abdel-Hafeez EH, Ahmad AK, Ali BA, Moslam FA. Opportunistic parasites among immunosuppressed children in Minia District, Egypt. Korean J Parasitol 2012; 50: 57-62. https://doi.org/10.3347/kjp.2012.50.1.57
  8. Fayer R. Cryptosporidium: a water-borne zoonotic parasite. Vet Parasitol 2004; 126: 37-56. https://doi.org/10.1016/j.vetpar.2004.09.004
  9. Putignani L, Menichella D. Global distribution, public health and clinical impact of the protozoan pathogen Cryptosporidium. Interdiscip Perspect Infect Dis 2010; 2010: 753512.
  10. Herwaldt BL, Ackers ML. An outbreak in 1996 of cyclosporiasis associated with imported raspberries. The Cyclospora Working Group. N Engl J Med 1997; 336: 1548-1556. https://doi.org/10.1056/NEJM199705293362202
  11. Mansfield LS, Gajadhar AA. Cyclospora cayetanensis, a food- and waterborne coccidian parasite. Vet Parasitol 2004; 126: 73-90. https://doi.org/10.1016/j.vetpar.2004.09.011
  12. Moon S, Kwak W, Lee S, Kim W, Oh J, Youn SK. Epidemiological characteristics of the first water-borne outbreak of cryptosporidiosis in Seoul, Korea. J Korean Med Sci 2013; 28: 983-989. https://doi.org/10.3346/jkms.2013.28.7.983
  13. Hong S, Kim K, Yoon S, Park WY, Sim S, Yu JR. Detection of Cryptosporidium parvum in environmental soil and vegetables. J Korean Med Sci 2014; 29: 1367-1371. https://doi.org/10.3346/jkms.2014.29.10.1367
  14. Yu JR, Sohn WM. A case of human cyclosporiasis causing traveler's diarrhea after visiting Indonesia. J Korean Med Sci 2003; 18: 738-741. https://doi.org/10.3346/jkms.2003.18.5.738
  15. Lee SU, Joung M, Ahn MH, Huh S, Song H, Park WY, Yu JR. CP2 gene as a useful viability marker for Cryptosporidium parvum. Parasitol Res 2008; 102: 381-387. https://doi.org/10.1007/s00436-007-0772-8
  16. Kitajima M, Haramoto E, Iker BC, Gerba CP. Occurrence of Cryptosporidium, Giardia, and Cyclospora in influent and effluent water at wastewater treatment plants in Arizona. Sci Total Environ 2014; 484: 129-136. https://doi.org/10.1016/j.scitotenv.2014.03.036
  17. Orlandi PA, Lampel KA. Extraction-free, filter-based template preparation for rapid and sensitive PCR detection of pathogenic parasitic protozoa. J Clin Microbiol 2000; 38: 2271-2277.
  18. Yoo JH. Emerging infectious disease by industrialization and technology. Korean J Infect Dis 1999; 31: 65-78.
  19. Robertson LJ, Chalmers RM. Foodborne cryptosporidiosis: is there really more in Nordic countries? Trends Parasitol 2013; 29: 3-9. https://doi.org/10.1016/j.pt.2012.10.003
  20. Ortega YR, Sanchez R. Update on Cyclospora cayetanensis, a food-borne and waterborne parasite. Clin Microbiol Rev 2010; 23: 218-234. https://doi.org/10.1128/CMR.00026-09
  21. Orlandi PA, Chu D-M, Bier JW, Jackson GJ. Parasites and the food supply. Food Technol 2002; 56: 72-81.
  22. Herman KM, Hall AJ, Gould LH. Outbreaks attributed to fresh leafy vegetables, United States, 1973-2012. Epidemiol Infect 2015; 143: 3011-3021. https://doi.org/10.1017/S0950268815000047
  23. Bhandari D, Tandukar S, Parajuli H, Thapa P, Chaudhary P, Shrestha D, Shah PK, Sherchan JB, Sherchand JB. Cyclospora infection among school children in Kathmandu, Nepal: prevalence and associated risk factors. Trop Med Health 2015; 43: 211-216. https://doi.org/10.2149/tmh.2015-25
  24. Kimura K, Rai SK, Rai G, Insisiengmay S, Kawabata M, Karanis P, Uga S. Study on Cyclospora cayetanensis associated with diarrheal disease in Nepal and Loa PDR. Southeast Asian J Trop Med Public Health 2005; 36: 1371-1376.
  25. Kaminsky RG, Lagos J, Raudales Santos G, Urrutia S. Marked seasonality of Cyclospora cayetanensis infections: ten-year observation of hospital cases, Honduras. BMC Infect Dis 2010; 16: 66.
  26. Eberhard ML, Nace EK, Freeman AR, Streit TG, da Silva AJ, Lammie PJ. Cyclospora cayetanensis infections in Haiti: a common occurrence in the absence of watery diarrhea. Am J Trop Med Hyg 1999; 60: 584-586. https://doi.org/10.4269/ajtmh.1999.60.584
  27. Giangaspero A, Marangi M, Koehler AV, Papini R, Normanno G, Lacasella V, Lonigro A, Gasser RB. Molecular detection of Cyclospora in water, soil, vegetables and humans in southern Italy signals a need for improved monitoring by health authorities. Int J Food Microbiol 2015; 211: 95-100. https://doi.org/10.1016/j.ijfoodmicro.2015.07.002
  28. Lee MY, Cho EJ, Lee JH, Han SH, Park YS. A survey of Cryptosporidium oocysts in water supplies during a 10-year period (2000-2009) in Seoul. Korean J Parasitol 2010; 48: 219-224. https://doi.org/10.3347/kjp.2010.48.3.219
  29. Yu JR, Seo M. Infection status of pigs with Cryptosporidium parvum. Korean J Parasitol 2004; 42: 45-47. https://doi.org/10.3347/kjp.2004.42.1.45
  30. Yu JR, Lee JK, Seo M, Kim SI, Sohn WM, Huh S, Choi HY, Kim TS. Prevalence of cryptosporidiosis among the villagers and domestic animals in several rural areas of Korea. Korean J Parasitol 2004; 42: 1-6. https://doi.org/10.3347/kjp.2004.42.1.1

Cited by

  1. Genotyping genetically heterogeneousCyclospora cayetanensisinfections to complement epidemiological case linkage vol.146, pp.10, 2017, https://doi.org/10.1017/s0031182019000581
  2. Cyclospora cayetanensis and Cyclosporiasis: An Update vol.7, pp.9, 2019, https://doi.org/10.3390/microorganisms7090317
  3. Status of common parasitic diseases in Korea in 2019 vol.62, pp.8, 2017, https://doi.org/10.5124/jkma.2019.62.8.437
  4. Cryptosporidium spp., prevalence, molecular characterisation and socio-demographic risk factors among immigrants in Qatar vol.13, pp.10, 2019, https://doi.org/10.1371/journal.pntd.0007750
  5. Molecular Prevalence and Genotypes of Cryptosporidium parvum and Giardia duodenalis in Patients with Acute Diarrhea in Korea, 2013-2016 vol.57, pp.5, 2019, https://doi.org/10.3347/kjp.2019.57.5.531
  6. A Molecular Tool for Rapid Detection and Traceability of Cyclospora cayetanensis in Fresh Berries and Berry Farm Soils vol.9, pp.3, 2017, https://doi.org/10.3390/foods9030261
  7. Detection of Cryptosporidium oocysts and Giardia cysts in vegetables from street markets from the Qinghai Tibetan Plateau Area in China vol.119, pp.6, 2017, https://doi.org/10.1007/s00436-020-06661-z
  8. Prevalence of Cryptosporidium and Giardia in vegetables in Iran: a nineteen-years meta-analysis review vol.18, pp.2, 2017, https://doi.org/10.1007/s40201-020-00493-w
  9. Detection of human intestinal protozoan parasites in vegetables and fruits: a review vol.13, pp.1, 2017, https://doi.org/10.1186/s13071-020-04255-3
  10. Diverse Genotypes and Species of Cryptosporidium in Wild Rodent Species from the West Coast of the USA and Implications for Raw Produce Safety and Microbial Water Quality vol.9, pp.4, 2017, https://doi.org/10.3390/microorganisms9040867
  11. Detection of Cyclospora cayetanensis , Echinococcus multilocularis , Toxocara spp. and microsporidia in fresh produce using molecular methods: – A review vol.23, pp.None, 2017, https://doi.org/10.1016/j.fawpar.2021.e00124
  12. Causes of acute gastroenteritis in Korean children between 2004 and 2019 vol.64, pp.6, 2021, https://doi.org/10.3345/cep.2020.01256