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Monitoring of norovirus and indicator microorganisms from agricultural products and environmental samples in Korea

한국에서의 농산물 및 환경시료에서 노로바이러스와 위생지표세균의 모니터링

  • Kang, Ji Hyun (Department of Food Science and Biotechnology, Chungbuk National University) ;
  • Shim, Hye Mee (Department of Food Science and Biotechnology, Chungbuk National University) ;
  • Kim, Kwang Yup (Department of Food Science and Biotechnology, Chungbuk National University)
  • 강지현 (충북대학교 식품생명공학과) ;
  • 심혜미 (충북대학교 식품생명공학과) ;
  • 김광엽 (충북대학교 식품생명공학과)
  • Received : 2016.09.22
  • Accepted : 2016.11.14
  • Published : 2017.04.30

Abstract

Norovirus causes frequent epidemic viral gastroenteritis in Korea. The team for the control of noroviral foodborne outbreaks (NOROTECL) executed a project to trace the cause of norovirus contamination in agricultural products and environmental samples to reduce norovirus outbreaks in Korea. Between January and November in 2015, the contaminations by norovirus and indicator microorganisms such as coliforms, Escherichia coil and male specific coliphage (MSC) were examined in 80 agricultural products, 80 soil samples, 78 human feces samples, 3 animal feces samples, 80 agricultural water samples and 80 river water samples. Semi-nested PCR and DNA sequencing revealed 18 genogroup I and 3 genogroup II noroviruses in a total of 18 samples. These noroviruses were validated by real-time (RT)-PCR analysis. For indicator microorganisms, coliform and E. coli were respectively detected in agricultural products (68, 1%), soils (88, 7%), human feces (44, 12.8%), animal feces (67, 67%), agricultural waters (74, 30%) and river waters (96, 51%). The MSC results revealed 14 positive samples.

Keywords

norovirus;male-specific coliphage;semi-nested PCR;real-time RT-PCR

References

  1. Emerging Infectious Diseases. Norovirus and foodborne disease, United States, 1991-2000. Available form: www.cdc.gov/eid. Accessed Jan. 2005;11(1):95-102. https://doi.org/10.3201/eid1101.040426
  2. Ho ZJM, Vithia G, Ng CG, Maurer-Stroh S, Tan CM, Loh J, Lin TPR, Lee JMV. Emergence of norovirus GI.2 outbreaks in military camps in Singapore. Int. J. Infect Dis. 31: 21-30 (2015)
  3. Green J, Henshilwood K, Gallimore CI, Brown DWG, Lees DN. A nested reverse transcriptase PCR assay for detection of small roundstructured viruses in environmentally contaminated molluscan shellfish. Appl. Environ. Microbiol. 64: 858-863 (1998)
  4. Brugha R, Vipond IB, Evans MR, Sandifer QD, Roberts RJ, Salmon RL, Caul EO, Mukerjee A. A community outbreak of food-borne small round-structured virus gastroenteritis caused by a contaminated water supply. Epidemiol. Infect. 122: 145-154 (1999) https://doi.org/10.1017/S0950268898001885
  5. Fankhauser RL, Monroe SS, Noel JS, Humphrey CD, Bresee JS, Parashar UD, Ando T, Glass RI. Epidemiologic and molecular trends of "Norwalk-like viruses" associated with outbreaks of gastroenteritis in the United State. J. Infect. Dis. 186: 1-7 (2002) https://doi.org/10.1086/341085
  6. Glass RI, Noel J, Ando T, Fankhauser R, Belliot G, Mounts A, Parashar UD, Bresee JS, Monroe SS. The epidemiology of enteric caliciviruses from humans: A reassessment using new diagnostics. J. Infect. Dis. 181: 254-261 (2000) https://doi.org/10.1086/315588
  7. Shin SB, Oh EG, Lee HJ, Kim YK, Lee TS, Kim JH. Norovirus quantification in oysters crassostrea gigas collected from Tongyeoung, Korea. Korean J. Fish Aquat. Sci. 47: 501-507 (2014)
  8. Vinje J, Green J, Lewis DC, Gallimore CI, Brown DWG, Koopmans MPG. Genetic polymorphism across regions of the three open reading frames of "Norwalk-like viruses". Arch. Virol. 145: 223-241 (2000) https://doi.org/10.1007/s007050050020
  9. Paik SY. Research on the contamination levels of norovirus in food catering facilities. National Institute of Food and Drug Safety Evaluation, Osong, Korea. pp. 1-150 (2009)
  10. Wollants E, Coster SD, Van Ranst MV, Maes P. A decade of norovirus genetic diversity in Belgium. Infect. Genet. Evol. 30: 37-44 (2015) https://doi.org/10.1016/j.meegid.2014.12.001
  11. Kageyama T, Shinohara M, Uchida K, Fukushi S, Hoshino FB, Kojima S, Takai R, Oka T, Takeda N, Katayama K. Coexistence of multiple genotypes, including newly identified genotypes, in outbreaks of gastroenteritis due to norovirus in Japan. J. Clin. Microbiol. 42: 2988-2995 (2004) https://doi.org/10.1128/JCM.42.7.2988-2995.2004
  12. Kim NH, Park EH, Park YK, Min SK, Jin SH, Park SH. Study on norovirus genotypes in Busan, Korea. J. Life Sci. 21: 845-850(2011) https://doi.org/10.5352/JLS.2011.21.6.845
  13. Shin SB, Oh EG, Yu HS, Lee HJ, Kim JH, Park KBW, Kwon JY, Yun HD, Son KT. Inactivation of a norovirus surrogate (Feline calicivirus) during the ripening of oyster kimch. Korean J. Fish Aquat. Sci. 43: 415-420 (2010)
  14. Kim KY. Research on the contamination levels of norovirus in food catering facilities. National Institute of Food and Drug Safety Evaluation, Osong, Korea. pp. 1-98 (2009)
  15. Ha JH, Lee JS, Joo IS, Lee HJ, Ha SD. Comparison Study on Viabilities of Human Norovirus and Norovirus Surrogates. Safe food, Seoul, Korea. pp. 19-25 (2014)
  16. Gould LH, Walsh KA, Vieira AR, Herman K, Williams IT, Hall AJ, Cole D. Surveillance for foodborne disease outbreaks- United States, 1998-2008. MMWR Morb. Mortal. Wkly. Rep. 62: 1-34 (2013)
  17. Eric CM, Peter KC, Angela WLL, Ann HW, Wilina WLL. Atypical norovirus epidemic in Hong Kong during summer of 2006 caused by a new genogroup II/4 variant. J. Clin. Microbiol. 45: 2205-2011 (2007) https://doi.org/10.1128/JCM.02489-06
  18. Kim BJ. Correlation between norovirus detection and indicator organisms presence in agricultural produce, growing soil, feces, agricultural water, and river water. MS thesis, University of Dongguk, Gyeongju, Korea (2015)
  19. Choi WS. Development of protocol for the detection of foodborne virus in food. National Institute of Food and Drug Safety Evaluation, Osong, Korea. pp. 1-90 (2004)
  20. Lu QB, Huang DD, Zhao J, Wang HY, Zhang XA, Xu HM, Qu F, Liu W, Cao WC. An increasing prevalence of recombinant GII norovirus in pediatric patients with diarrhea during 2010-2013 in China. Infect. Genet. Evol. 31: 48-52 (2015) https://doi.org/10.1016/j.meegid.2015.01.008
  21. Mathijs E, Denayer S, Palmeira L, Botteldoorn N, Scipioni A, Vanderplasschen A, Dierick K. Novel norovirus recombinants and of GII. 4 sub-lineages associated with outbreaks between 2006 and 2010 in Belgium. Virol. J. 8: 1 (2011) https://doi.org/10.1186/1743-422X-8-1
  22. Hoa-Tran TN, Nakagomi T, Sano D, Sherchand JB, Pandey BD, Cunliffe NA, Nakagomi O. Molecular epidemiology of noroviruses detected in Nepalese children with acute diarrhea between 2005 and 2011: Increase and predominance of minor genotype GII.13. Infect. Genet. Evol. 30: 27-36 (2015) https://doi.org/10.1016/j.meegid.2014.12.003
  23. Shin CS. A study on the technology for enhancing water hygiene in water pipe and supplying. Kwater, Daejeon, Korea. pp. 1-82 (2014)
  24. Jheong WH, Kim JM, Jang SJ, Park JY, Oh JH, Choi HJ, Yang SY, Park SJ, Seo EY. A study on the bacteriophages as indicators of viruses in water environment. National Institute of Environmental Research, Incheon, Korea. pp. 1-98 (2008)
  25. Alderisio KA, Wait DA, Sobsey MD. "Detection and characterization of male-specific RNA coliphages in a New York City reservoir." Watershed Restoration Management New York City Water Supply Studies. JJ McDonnell, DL Leopold, JB Stribling & LR Neville. 133-142 (1996)
  26. Lee HT, Kim HY, Park HJ, Cho YE, Ryu SY, Lee KJ, Jung JS, Ko GP. Evaluation of Influent Water Quality Using Indicator Microorganisms in Lake Shiwha. J. Environ. Health Sci. 34: 86-94 (2008)
  27. Leclerc H, Edberg S, Pierzo V, Delattre JM. Bacteriophages as indicators of enteric viruses and public health risk in groundwaters. J. Appl. Microbiol. 88: 5-21 (2000)
  28. Fonager J, Hindbaek LS, Fischer TK. Rapid emergence and antigenic diversification of the norovirus 2012 Sydney variant in Denmark, October to December, 2012. Euro Surveill. 18: 1-24 (2013)
  29. Ham HJ, Oh SA, Kim CK, Jang JI, Jo SJ, Choi SM. Molecular characteristics of human noroviruses genogroup I and genogroup II detected in acute gastroenteritis patients in Seoul. J. Environ. Health Sci. 38: 57-65 (2012)
  30. Ho ECM, Cheng PKC, Lau AWL, Wong AH, Lim WWL. Atypical norovirus epidemic in Hong Kong during summer of 2006 caused by a new genogroup II/4 variant. J. Clin. Microbiol. 45: 2205-2011 (2007) https://doi.org/10.1128/JCM.02489-06
  31. Hedlund KO, Rubilar-Abreu E, Svensson L. Epidemiology of calicivirus infections in Sweden, 1994-1998. J. Infect. Dis. 181: 275-280 (2000) https://doi.org/10.1086/315585
  32. Kim EJ, Kim MS, Chae YZ, Cheon DS. Prevalence of human noroviruses detected from outbreaks of gastroenteritis patients in Seoul, Korea. Korean J. Microbiol. 48: 102-108 (2012) https://doi.org/10.7845/kjm.2012.48.2.102
  33. Oh SA, Park SH, Ham HJ, Seung HJ, Jang JI, Suh SW, Jo SJ, Choi SM, Jeong HS. Molecular characterization of norovirus and rotavirus in outbreak of acute gastroenteritis in Seoul. J. Bacteriol. 43: 307-316 (2013)
  34. Kim NH, Park EH, Park YK, Min SK, Jin SH, Park SH. Study on Norovirus Genotypes in Busan, Korea. J. Life Sci. 21: 845-850 (2011) https://doi.org/10.5352/JLS.2011.21.6.845
  35. Lopman BA, Adak GK, Reacher MH, Brown DW. Two epidemiologic atterns of norovirus outbreak; surveillance in england and wales, 1992-2000. Emerg. Infect. Dis. 9: 71-77 (2003) https://doi.org/10.3201/eid0901.020175
  36. Hedlund KO, Rubilar-Abreu E, Svensson L. Epidemiology of calicivirus infections in Sweden, 1994-1998. J. Infect. Dis. 181:275-280 (2000) https://doi.org/10.1086/315585
  37. Kim YJ, Lee MG, Kam SK. Characteristics of norovirus occurrence in Jeju. J. Env. Sci. Intern. 23: 219-229 (2014) https://doi.org/10.5322/JESI.2014.23.2.219
  38. Wobus CE, Thackray LB, Virgin HW. Murine norovirus: A model system to study norovirus biology and pathogenesis. J. Virol. 80: 5104-5112 (2006) https://doi.org/10.1128/JVI.02346-05
  39. Moon A, Ahn J, Choi WS. Elution buffers for human enteric viruses in vegetables with applications to norovirus detection. J. Food Hyg. Saf. 28: 1229-1153 (2013)

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