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Defecation of Norovirus from the Oyster Crassostrea gigas by Depuration Following Translocation of the Growing Area

자연정화에 의한 양식굴(Crassostrea gigas) 중 노로바이러스 저감화

Yu, Hongsik;Park, Yong Su;An, Sera;Park, Kunbawui;Shim, Kil Bo;Song, Ki Cheol;Lee, Tae Seek
유홍식;박용수;안세라;박큰바위;심길보;송기철;이태식

  • Received : 2016.02.29
  • Accepted : 2016.03.30
  • Published : 2016.04.30

Abstract

The efficacy of depuration following growing area translocation for the defecation of norovirus was evaluated under experimental conditions using oysters Crassostrea gigas previously subjected to bioaccumulation of this virus at a waste treatment plant discharge site. Three trials were assayed in an open experimental system with a commercial oyster farm located in a shellfish growing area approved by the Korean Shellfish Sanitation Program. Real-time reverse-transcription polymerase chain reaction (RT-PCR) was used to quantify viruses in the digestive glands of oysters. The final viral loads in oysters after 12 days remained under the detection limit (10 copies/g digestive gland) of the real-time RT-PCR. This reduction trend showed two-phase removal kinetics, with an initial slow reduction or slight increase in viruses during the first 2 days of depuration and subsequent stabilization with 0.12 to 2.64 log unit norovirus copies/g digestive gland per 2 days of depuration for the remaining time.

Keywords

Norovirus;Crassostrea gigas;Oyster;Translocation;Depuration

References

  1. Butt AA, Aldridge KE and Sanders CV. 2004. Infections related to the ingestion of seafood. Part I: viral and bacterial infections. Lancet Infect Dis 4, 201-212. http://dx.doi.org/10.1016/S1473-3099(04)00969-7. https://doi.org/10.1016/S1473-3099(04)00969-7
  2. Dore B, Keaveney1 S, Flannery1 J and Rajko-Nenow1 P. 2010. Management of health risks associated with oysters harvested from a norovirus contaminated area, Ireland, February–March 2010. Euro Surveill 15, 1-4.
  3. Chalmers JWT and McMillan JH. 1995. An outbreak of viral gastroenteritis associated with adequately prepared oysters. Epidemiol Infect 115, 163-167. http://dx.doi.org/10.1017/S095026 8800058222. https://doi.org/10.1017/S0950268800058222
  4. DAF. 2011. Health protocol for the translocation and movement of live bivalve molluscus. Retrieve form https://www.daf.qld.gov.au/fisheries/aquaculture/management-and-policies/fampr003-move ment-of-live-bivalve-molluscs on January 2016.
  5. Da Silva AK, Le Saux JC, Parnaudeau S, Pommepuy M, Eimelech M and Le Guyader FS. 2007. Evaluation of removal of noroviruses during wastewater treatment, using real time reverse transcription-PCR: different behaviors of genogroups I and II. Appl Environ Microbiol 24, 7891-7897. http://dx.doi.org/10.1128/AEM.01428-07. https://doi.org/10.1128/AEM.01428-07
  6. European Commission. 2004. Regulation (EC) no 854/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. L226. Off J Eur Communities, 83-127.
  7. Iwai M, Hasegawa S, Obara M, Nakamura K, Horimoto E, Takizawa T, Kurata T, Sogen S and Shiraki K. 2009. Continuous presence of noroviruses and sapoviruses in raw sewage reflects infections among inhabitants of Toyoma, Japan(2006 to 2008). Appl Environ Microbiol 75, 1264-1270. http://dx.doi.org/10.1128/AEM.01166-08. https://doi.org/10.1128/AEM.01166-08
  8. Jothikumar N, Lowther JA, Henshilwood K, Lees DN, Hill VR and Vinj J. 2005. Rapid and sensitive detection of noroviruses by using TaqMan-based one-step reverse transcription-PCR assays and application to naturally contaminated shellfish samples. Appl Environ Microbiol 71, 1870-1875. http://dx.doi.org /doi/10.1128/AEM.71.4.1870-1875.2005. https://doi.org/10.1128/AEM.71.4.1870-1875.2005
  9. Lees DN. 2000. Viruses and bivalve shellfish. Int J Food Microbiol 59, 81-116. http://dx.doi.org/ 10.1016/S0168-1605(00)00248-8. https://doi.org/10.1016/S0168-1605(00)00248-8
  10. Kroneman A, Verhoef L, Harris J, Vennema H, Duzier E, van Duynhoven Y, Gray J, Iturriza M, Böttiger B, Falkenhorst G, Johnsen C, von Bonsdorff CH,Maunula L, Kuusi M, Pothier P, Gallay A, Schreier E, Höhne M, Koch J, Szücs G, Reuter G, Krisztalovics K, Lynch M, McKeown P, Foley B, Coughlan S, Ruggeri FM, Di Bartolo I, Vainio K, Isakbaeva E, Poljsak-Prijatelj M, Grom AH, Mijovski JZ, Bosch A, Buesa J, Fauquier AS, Hernandéz-Pezzi G, Hedlund KO and Koopmans M. 2008. Analysis of integrated virological and epidemiological reports of norovirus outbreaks collected within the foodborne viruses in Europe Network from 1 July 2001 to 30 June 2006. J Clinical Microbiol 46, 2959-2965. http://dx.doi.org/10.1128/JCM.00499-08. https://doi.org/10.1128/JCM.00499-08
  11. Le Guyader FS, Loisy F, Atmar RL, Hutson AM, Estes MK, Ruvoen-Clouet N, Pommepuy M and Le Pendu J. 2006. Norwalk virus-specific binding to oyster digestive tissues. Emerg Infect Dis 12, 931-936. http://dx.doi.org/10.3201/eid1206.051519. https://doi.org/10.3201/eid1206.051519
  12. Le Guyader FS, Neil FH, Dubois E, Bon F, Loisy F, Kohli E, Pommepuy M and Atmar RL. 2003. A semiquantitative approach to estimate Norwalk-like virus contamination of oysters implicated in an outbreak. Int J Food Microbiol 87, 107-112. http://dx.doi.org/10.1016/S0168-1605(03)00058-8. https://doi.org/10.1016/S0168-1605(03)00058-8
  13. Maalouf H, Schaeffer J, Parnaudeau S, Le Pendu J, Atmar RL, Crawford SE and Le Guyader FS. 2011. Strain-dependent norovirus bioaccumulation in oysters. Appl Environ Microbiol 77, 3189-3196. http://dx.doi.org/10.1128/AEM.03010-10. https://doi.org/10.1128/AEM.03010-10
  14. Maalouf H, Zakhour M, Le Pendu J, Le Saux JC, Atmar RL and Le Guyader FS. 2010. Norovirus genogroup I and II ligands in oysters: tissue distribution and seasonal variations. Appl Environ Microbiol 76, 5621-5630. http://dx.doi.org/10.1128/AEM.00148-10. https://doi.org/10.1128/AEM.00148-10
  15. McMenemy P. 2014. Depuration dynamics of norovirus in oysters. Ph.D. Thesis, University of Stirling, Stirling, U.K.
  16. Nappier SP, Graczyk TK, Tamang L and Schwab KJ. 2010. Colocalized Crassostrea virginica and Crassostrea ariakensis Oysters differ in bioaccumulation, retention and depuration of microbial indicators and human enteropathogens. J Appl Microbiol 108, 736-744. http://dx.doi.org/10.1111/ j.1365-2672.2009.04480.x. https://doi.org/10.1111/j.1365-2672.2009.04480.x
  17. Mcleod C, Hay B, Grant C, Greening G and Day D. 2009a. Localization of norovirus and poliovirus in Pacific oysters. J Appl Microbiol 106, 1220-1230. http://dx.doi.org/10.1111/j.1365-2672.2008.04091.x. https://doi.org/10.1111/j.1365-2672.2008.04091.x
  18. Mcleod C, Hay B, Grant C, Greening G and Day D. 2009b. Inactivation and elimination of human enteric viruses by Pacific oysters. J Appl Microbiol 107, 1809-1818. http://dx.doi.org/10.1111/ j.1365-2672.2009.04373.x. https://doi.org/10.1111/j.1365-2672.2009.04373.x
  19. Nappier SP, Graczyk TK and Schwab KJ. 2008. Bioaccumulation, retention, and depuration of enteric viruses by Crassostrea virginica and Crassostrea ariakensis oysters. Appl Environ Microbiol 74, 6825-6831. http://dx.doi.org/10.1128/AEM.01000-08. https://doi.org/10.1128/AEM.01000-08
  20. Oh EG, Yoo HD, Yu HS, Ha KS, Shin SB, Lee TS, Lee HJ, Kim JH and Son KT. 2012. Removal of fecal indicator bacteria from bivalves under natural and electrolyzed water. Korean J Fish Aquat Sci 45, 11-16. http://dx.doi.org/10.5657/KFAS.2012.0011. https://doi.org/10.5657/KFAS.2012.0011
  21. Pint RM, Costafreda MI and Bosch A. 2009. Risk assessment in shellfish-borne outbreaks of hepatitis A. Appl Environ Microbiol 75, 7350-7355. http://dx.doi.org/10.1128/AEM.01177-09. https://doi.org/10.1128/AEM.01177-09
  22. Polo D, Álvarez C, Longa A and Romalde JL. 2014a. Depuration effectiveness for hepatitis A virus removal from mussels(Mytilus galloprovincialis). Int J Food Microbiol 180, 24-29. http://dx.doi. org/10.1016/j.ijfoodmicro.2014.04.001. https://doi.org/10.1016/j.ijfoodmicro.2014.04.001
  23. Polo D, Álvarez C, Vilariño ML, Longa A and Romalde JL. 2014b. Depuration kinetics of hepatitis A virus in clams. Food Microbiol 39, 103-107. http://dx.doi.org/10.1016/j.fm.2013.11.011. https://doi.org/10.1016/j.fm.2013.11.011
  24. Scallan E, Hoekstra RM, Angulo FJ and Tauxe RV. 2011. Foodborne llness acquired in the United States—Major pathogens. Emerg Infect Dis 17, 7-15. http://dx.doi.org/10.3201/eid1701.P11101. https://doi.org/10.3201/eid1701.P11101
  25. Polo D, Vilariño ML, Manso CF and Romalde JL. 2010. Imported mollusks and dissemination of human enteric viruses. Emerg Infect Dis 16, 1036-1038. http://dx.doi.org/10.3201/eid1606. 091748. https://doi.org/10.3201/eid1606.091748
  26. Provost K, Ozbay G, Anderson R, Richards GP and Kingsley DH. 2011. Hemocytes are sites of enteric virus persistence within oysters. Appl Environ Microbiol 77, 8360-8369. http://dx.doi.org/10.1128/AEM.06887-11. https://doi.org/10.1128/AEM.06887-11
  27. Richards GP, McLeod C and Le Guyader FS. 2010. Processing strategies to inactivate viruses in shellfish. Food Environ Virol 2, 183-193. http://dx.doi.org/10.1007/s12560-010-9045-2. https://doi.org/10.1007/s12560-010-9045-2
  28. Shin SB, Oh EG, Lee HJ, Kim YK, Lee TS and Kim JH. 2014. Norovirus quantification in oysters Crassostrea gigas collected from Tongyeoung, Korea. Korean J Fish Aquat Sci 47, 501-507. http://dx.doi.org/10.5657/KFAS.2014.0501. https://doi.org/10.5657/KFAS.2014.0501
  29. Steel RGD and Torrie JH. 1980. Principle and procedure of statistics; a biometrical approach (2nd ed.). Mitchell GJ and Mitchell JH, eds. MacGraw-Hill Book Company, New York, U.S.A., 121-165.
  30. Tian P, Bates AH, Jensen HM and Mandrell RE. 2006. Norovirus binds to blood group A-like antigens in oyster gastrointestinal cells. Lett Appl Microbiol 43, 645-651. http://dx.doi.org/ 10.1111/j.1472-765X.2006.02010.x. https://doi.org/10.1111/j.1472-765X.2006.02010.x
  31. Ueki Y, Shoji M, Suto A, Tanabe T, Okimura Y, Kikuchi Y, Saito N, Sano D and Omura T. 2007. Persistence of caliciviruses in artificially contaminated oysters during depuration. Appl Environ Microbiol 73, 5698-5701. http://dx.doi.org/10.1128/AEM.00290-07. https://doi.org/10.1128/AEM.00290-07
  32. US FDA (Food and Drug Adminstration). 2013. National Shellfish Sanitation Program, Guide for the Control of Molluscan Shellfish, Model ordinance. Retrieved from http://www.fda.gov/Food/Food Safety/Product-Specific Information/Seafood/Federal State Programs/National Shellfish Sanitation Program/default.htm on January 18, 2016.
  33. Wang D, Wu Q, Kou X, Yao L and Zhang J. 2008. Distribution of norovirus in oyster tissues. J Appl Microbiol 105, 1966-1972. http://dx.doi.org/10.1111/j.1365-2672.2008.03970.x. https://doi.org/10.1111/j.1365-2672.2008.03970.x