Shellfish-Associated Viral Disease Outbreaks

  • Gary P. Richards
Part of the Food Microbiology and Food Safety book series (FMFS)

4.0. Summary

Numerous outbreaks of shellfish-borne enteric virus illness have been reported worldwide. Most notable among the outbreaks are those involving norovirus illness and hepatitis A. Lessons learned from outbreak investigations indicate that most outbreaks are preventable. Anthropogenic sources of contamination will continue to invade shellfish growing waters, and shellfish, by their very nature, will continue to bioconcentrate these contaminants, including enteric viruses. There is no quick fix for enteric virus contamination of shellfish; however, vigilance on behalf of the industry, regulatory agencies, and the consumer could substantially reduce the incidence of illness. Enhanced monitoring in all areas of shellfish production, harvesting, distribution, and processing would help to reduce viral illnesses. Pollution abatement and improved hygienic practices on behalf of the industry and consumers are needed. New processing and analytical technologies, such as high hydrostatic pressure processing and molecular biological assays, will enhance shellfish safety and continue to provide new avenues to protect the consumer and the industry. Better reporting and epidemiological follow-up of outbreaks are keys to the development of interventions against the foodborne transmission of viral infections.


Fecal Coliform Much Probable Number Enteric Virus Norwalk Virus Sanitation Program 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

5.0. References

  1. Ang, L. H., 1998, An outbreak of viral gastroenteritis associated with eating raw oysters. Commun. Dis. Public Health 1:38–40.Google Scholar
  2. Anon., 1991, Council Directive 91/492/EEC. Laying down the health conditions for the production and placing on the market of live bivalve mollusks. Official J. Eur. Comm. L268:1–14Google Scholar
  3. Anon., 1999, National Shellfish Sanitation Program Model Ordinance IV. Shellstock growing areas. Department of Health and Human Services, U.S. Food and Drug Administration, Washington, DC.Google Scholar
  4. Appleton, H., and Pereira, M. S., 1977, A possible virus aetiology in outbreaks of foodpoisoning from cockles. Lancet 1(8015):780–781.CrossRefGoogle Scholar
  5. Arankalle, V. A., Chadha, M. S., Tsarev, S. A., Emerson, S. U., Risbud, A. R., Banerjee, K., and Purcell, R. H., 1994, Seroepidemiology of water-borne hepatitis in India and evidence for a third enterically-transmitted hepatitis agent. Proc. Natl. Acad. Sci. U. S. A. 91:3428–3432.CrossRefGoogle Scholar
  6. Ayers, P. A., 1991, The status of shellfish depuration in Australia and South-east Asia, in: Molluscan Shellfish Depuration (W. S. Otwell, G. E. Rodrick, and R. E. Martin, eds.), CRC Press, Boca Raton, FL, pp. 287–321.Google Scholar
  7. Balayan, M. S., 1997, Epidemiology of hepatitis E virus infection. J Viral Hepat 4:155–65.CrossRefGoogle Scholar
  8. Berg, D. E., Kohn, M. A., Farley, T. A., and McFarland, L. M., 2000, Multi-state outbreaks of acute gastroenteritis traced to fecal-contaminated oysters harvested in Louisiana. J. Infect. Dis. 181(Suppl. 2):S381–386.CrossRefGoogle Scholar
  9. Bosch, A., Sanchez, G., Le Guyader, F., Vanaclocha, H., Haugarreau, L., and Pinto, R. M., 2001, Human enteric viruses in Coquina clams associated with a large hepatitis A outbreak. Water Sci. Technol. 43:61–65.Google Scholar
  10. Cacopardo, B., Russo, R., Preiser, W., Benanti, F., Brancati, F., and Nunnari, A., 1997, Acute hepatitis E in Catania (eastern Sicily) 1980–1994. The role of hepatitis E virus. Infection 25:313–316.CrossRefGoogle Scholar
  11. Caredda, F., Antinori, S. R.T., Pastecchia, C., Zavaglia, C., and Moroni, M., 1985, Clinical features of sporadic non-A, non-B hepatitis possibly associated with faecaloral spread. Lancet 2:444–445.CrossRefGoogle Scholar
  12. Centers for Disease Control, 1982, Enteric illness associated with raw clam consumption—New York. Morbid. Mortal. Weekly Rep. 31:449–450.Google Scholar
  13. Centers for Disease Control, 1993, Multistate outbreak of viral gastroenteritis related to consumption of oysters—Louisiana, Maryland, Mississippi and North Carolina, 1993, Morbid. Mortal. Weekly Rep. 42:945–948.Google Scholar
  14. Clayson, E. T., Shrestha, M. P., Vaughn, D.W., Snitbhan, R., Shrestha, K. B., Longer, C. F., and Innis, B. L., 1997, Rates of hepatitis E virus infection and disease among adolescents and adults in Kathmandu, Nepal. J. Infect. Dis. 176:763–766.CrossRefGoogle Scholar
  15. Conaty, S., Bird, P., Bell, G., Kraa, E., Grohmann, G., and McAnulty, J. M., 2000, Hepatitis A in New South Wales, Australia from consumption of oysters: the first reported outbreak. Epidemiol. Infect. 124:121–130.CrossRefGoogle Scholar
  16. Cooksley, W. G., 2000, What did we learn from the Shanghai hepatitis A epidemic? J. Viral Hepat. 7(Suppl. 1):1–3.CrossRefGoogle Scholar
  17. Desenclos, J. C., Klontz, K. C., Wilder, M. H., Nainan, O.V., Margolis, H. S., and Gunn, R. A., 1991, A multistate outbreak of hepatitis A caused by the consumption of raw oysters. Am. J. Public Health 81:1268–1272.Google Scholar
  18. Food and Drug Administration, 1983, England Shellfish Program Review. U.S. Food and Drug Administration, U.S. Public Health Service, Washington, DC.Google Scholar
  19. Frost, H.W., 1925, Report of committee on the sanitary control of the shellfish industry in the United States. Public Health Rep., 53(Suppl.):1–17.Google Scholar
  20. Fujiyama, S., Akahoshi, M., Sagara, K., Sato, T., and Tsurusaki, R., 1985, An epidemic of hepatitis A related to ingestion of raw oysters. Gastroenterol. Jpn. 20:6–13.Google Scholar
  21. Furuta, T., Akiyama, M., Kato, Y., and Nishio, O., 2003, A food poisoning outbreak caused by purple Washington clams contaminated with norovirus (Norwalk-like virus) and hepatitis A virus. Kansenshogaku Zasshi 77:89–94.Google Scholar
  22. Gerba, C. P., and Goyal, S. M., 1978, Detection and occurrence of enteric viruses in shellfish: a review. J. Food Prot. 41:743–754.Google Scholar
  23. Glass, R. I., Bresee, J., Jiang, B., Gentsch, J., Ando, T., Fankhauser, R., Noel, J., Parashar, U., Rosen, B., and Monroe, S. S., 2001, Gastroenteritis viruses: an overview. Novartis Found. Symp. 238:5–19.CrossRefGoogle Scholar
  24. Graham, D.Y., Jiang, X., Tanaka, T., Opekum, A. R., Madore, H. P., and Estes, M. K., 1994, Norwalk virus infection of volunteers: new insights based on improved assays. J. Infect. Dis. 170:34–43.Google Scholar
  25. Gray, S. F., and Evans, M. R., 1993, Dose-response in an outbreak of non-bacterial food poisoning traced to a mixed seafood cocktail. Epidemiol. Infect. 110:583–590.Google Scholar
  26. Grohmann, G. S., Greenberg, H. B., Welch, B. M., and Murphy, A. M., 1980, Oysterassociated gastroenteritis in Australia: the detection of Norwalk virus and its anti-body by immune electron microscopy and radioimmunoassay. J. Med. Virol. 6:11–19.Google Scholar
  27. Grohmann, G. S., Murphy, A. M., Christopher, P. J., Auty, E., and Greenberg, H. B., 1981, Norwalk virus gastroenteritis in volunteers consuming depurated oysters. Aust. J. Exp. Biol. Med. Sci. 59:219–228.Google Scholar
  28. Gunn, R. A., Janowski, H. T., Lieb, S., Prather, E. C., and Greenberg, H. B., 1982, Norwalk virus gastroenteritis following raw oyster consumption. Am. J. Epidemiol. 115:348–351.Google Scholar
  29. Halliday, M. L., Kang, L.Y., Zhou, T. K., Hu, M. D., Pan, Q. C., Fu, T.Y., Huang, Y. S., and Hu, S. L., 1991, An epidemic of hepatitis A attributable to the ingestion of raw clams in Shanghai, China. J. Infect. Dis. 164:852–859.Google Scholar
  30. Haruki, K., Seto, Y., Murakami, T., and Kimura, T., 1991, Pattern of shedding small, round-structured virus particles in stools of patients of outbreaks of food-poisoning from raw oysters. Microbiol. Immunol. 35:83–86.Google Scholar
  31. Iversen, A. M., Gill, M., Bartlett, C. L., Cubitt, W. D., and McSwiggan, D. A., 1987, Two outbreaks of foodborne gastroenteritis caused by a small round structured virus: evidence for prolonged infectivity in a food handler. Lancet 2(8558): 556–558.CrossRefGoogle Scholar
  32. Kingsley, D. H., Hoover, D. G., Papafragkou, E., and Richards, G. P., 2002a, Inactivation of hepatitis A virus and a calicivirus by high hydrostatic pressure. J. Food Prot. 65:1605–1609.Google Scholar
  33. Kingsley, D. H., Meade, G. K., and Richards, G. P., 2002b, Detection of both hepatitis A virus and Norwalk-like virus in imported clams associated with food-borne illness. Appl. Environ. Microbiol. 68:3914–3918.CrossRefGoogle Scholar
  34. Kingsley, D. H., and Richards, G. P., 2003, Persistence of hepatitis A virus in oysters. J. Food Prot. 66:331–334.Google Scholar
  35. Kirkland, K. B., Meriwether, R. A., Leiss, J. K., and Mac Kenzie, W. R., 1996, Steaming oysters does not prevent Norwalk-like gastroenteritis. Public Health Rep. 111:527–530.Google Scholar
  36. Kiyosawa, K., Gibo, Y., Sodeyama, T., Furuta, K., Imai, H., Yoda, H., Koike, Y., Yoshizawa, K., and Furuta, S., 1987, Possible infectious causes in 651 patients with acute viral hepatitis during a 10-year period (1976–1985). Liver 7:163–168.Google Scholar
  37. Kohn, M. A., Farley, T. A., Ando, T., Curtis, M., Wilson, S. A., Jin, Q., Monroe, S. S., Baron, R. C., McFarland, L. M., and Glass, R. I., 1995, An outbreak of Norwalk virus gastroenteritis associated with eating raw oysters. Implications for maintaining safe oyster beds. JAMA 273:1492.CrossRefGoogle Scholar
  38. Konno, T., Chimoto, T., Taneichi, K., Deno, M., Yoshizaya, T., Kimura, O., Sibaki, H., Konno, M., and Kojima, H., 1983, Oyster-associated hepatitis A. Hokkaido Igaku Zasshi 58:553–555.Google Scholar
  39. Leoni, E., Bevini, C., Degli Esposti, S., and Graziano, A., 1998, An outbreak of intrafamiliar hepatitis A associated with clam consumption: epidemic transmission to a school community. Eur. J. Epidemiol. 14:187–192.CrossRefGoogle Scholar
  40. Linco, S. J., and Grohmann, G. S. 1980, The Darwin outbreak of oyster-associated viral gastroenteritis. Med. J. Aust. 1:211–213.Google Scholar
  41. Lopman, B., van Duynhoven, Y., Hanon, F. X., Reacher, M., Koopmans, M., Brown, D., and Consortium on Foodborne Viruses in Europe, 2002, Laboratory capability in Europe for foodborne viruses. Eur. Surveill. 7:61–65.Google Scholar
  42. Lucioni, C., Cipriani, V., Mazzi, S., and Panunzio, M., 1998, Cost of an outbreak of hepatitis A in Puglia, Italy. Pharmacoeconomics 13:257–266.CrossRefGoogle Scholar
  43. Mackowiak, P. A., Caraway, C. T., and Portnoy, B. L., 1976, Oyster-associated hepatitis: lessons from the Louisiana experience. Am. J. Epidemiol. 103:181–191.Google Scholar
  44. Maguire, H., Heptonstall, J., and Begg, N. T., 1992, The epidemiology and control of hepatitis A. Commun. Dis. Rep. CDC Rev. 2:R114–117.Google Scholar
  45. Mast, E. E., and Krawczynski, K., 1996, Hepatitis E: an overview. Annu. Rev. Med. 47:257–266.CrossRefGoogle Scholar
  46. McDonnell, S., Kirkland, K. B., Hlady, W.G., Aristeguieta, C., Hopkins, R. S., Monroe, S. S., and Glass, R. I., 1997, Failure of cooking to prevent shellfish-associated viral gastroenteritis. Arch. Intern. Med. 157:111–116.CrossRefGoogle Scholar
  47. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Chapiro, C., Griffin, P. M., and Tauxe, R. V., 1999, Food-related illness and deaths in the United States. Emerg. Infect. Dis. 5:607–625.CrossRefGoogle Scholar
  48. Mele, A., Rosmini, F., Zampieri, A., and Gill, O. N., 1986, Integrated epidemiological system for acute viral hepatitis in Italy (SEIEVA): description and preliminary results. Eur. J. Epidemiol. 2:300–304.CrossRefGoogle Scholar
  49. Mele, A., Rastelli, M. G., Gill, O. N., di Bisceglie, D., Rosmini, F., Pardelli, G., Valtriani, C., and Patriarchi, P., 1989, Recurrent epidemic hepatitis A associated with raw shellfish, probably controlled through public health measures. Am. J. Epidemiol. 130:540–546.Google Scholar
  50. Mele, A., Stroffolini, T., Palumbo, F., Gallo, G., Ragni, G., Balocchini, E., Tosti, M. E., Corona, R., Marzolini, A., and Moiraghi, A., 1997, Incidence of and risk factors for hepatitis A in Italy: public health indications from a 10-year surveillance. SEIEVA Collaborating Group. J. Hepatol. 26:743–747.CrossRefGoogle Scholar
  51. Morse, D. L., Guzewich, J. J., Hanrahan, J. P., Stricof, R., Shayegani, M., Deibel, R., Grabau, J. C., Nowak, N. A., Herrmann, J. E., Cukor, G., and Blacklow, N. R., 1986, Widespread outbreak of clam-and oyster-associated gastroenteritis. Role of Norwalk virus. N. Engl. J. Med. 314:678–681.CrossRefGoogle Scholar
  52. Murphy, A. M., Grohmann, G. S., Christopher, P. J., Lopez, W. A., Davey, G. R., and Millsom, R. H., 1979, An Australia-wide outbreak of gastroenteritis from oysters caused by Norwalk virus. Med. J. Aust. 2:329–333.Google Scholar
  53. New York State Department of Health, 1983, Clam-associated enteric illness in New York May-September 1982: a preliminary report. New York State Department of Health, Albany, NY, pp. 1–10.Google Scholar
  54. O’Mahony, M.C., Gooch, C. D., Smyth, D. A., Thrussell, A. J., Bartlett, C. L., and Noah, N. D., 1983, Epidemic hepatitis A from cockles. Lancet 1(8323):518–520.CrossRefGoogle Scholar
  55. Otsu, R., 1999, Outbreaks of gastroenteritis caused by SRSVs from 1987 to 1992 in Kyushu, Japan: four outbreaks associated with oyster consumption. Eur. J. Epidemiol. 15:175–180.CrossRefGoogle Scholar
  56. Polakoff, S., 1990, Report of clinical hepatitis A from public health and hospital microbiology laboratories to the PHLS Comunicable Disease Surveillance Centre during the period 1980–1988. J. Infect. 21:111–117.CrossRefGoogle Scholar
  57. Portnoy, B. L., Mackowiak, P. A., Caraway, C. T., Walker, J. A., McKinley, T.W., and Klin, C. A. Jr., 1975, Oyster-associated hepatitis. Failure of shellfish certification program to prevent outbreaks. JAMA 233:1065–1068.CrossRefGoogle Scholar
  58. Richards, G. P., 1985, Outbreaks of enteric virus illness in the United States: requisite for development of viral guidelines. J. Food Prot. 48:815–832.Google Scholar
  59. Richards, G. P., 1987, Shellfish-associated enteric virus illness in the United States, 1934–1984. Estuaries 10:84–85.CrossRefGoogle Scholar
  60. Richards G. P., 1988, Microbial purification of shellfish: a review of depuration and relaying. J. Food Prot. 51:218–251.Google Scholar
  61. Richards, G. P., 1991, Shellfish depuration, in: Microbiology of Marine Food Products (D. R. Ward and C. R. Hackney, eds.), Van Nostrand Reinhold, New York, pp. 395–428.Google Scholar
  62. Richards, G. P., 1999, Limitations of molecular biological techniques for assessing the virological safety of foods. J. Food Prot. 62:691–697.Google Scholar
  63. Richards, G. P., 2001, Enteric virus contamination of foods through industrial practices: a primer on intervention strategies. J. Indust. Microbiol. Biotechnol. 17:117–125.CrossRefGoogle Scholar
  64. Richards, G. P., 2003, The evolution of molluscan shellfish safety, in: Molluscan Shell-fish Safety (A. Villalba, B. Reguera, J. L. Romalde, and R. Beira, eds.), Conselleria de Pesca e Asuntos Maritimos, Xunta de Galicia and Intergovernmental Oceanographic Commission of UNESCO, Galicia, Spain, pp. 221–245.Google Scholar
  65. Richards, G. P., Watson, M.A., and Kingsley, D. H. 2004, A SYBR green, real-time RTPCR method to detect and quantitate Norwalk virus in stools. J. Virol. Methods 116: 63–70.CrossRefGoogle Scholar
  66. Rippey, S. R., 1994, Infectious diseases associated with molluscan shellfish consumption. Clin. Microbiol. Rev. 7:419–425.Google Scholar
  67. Romalde, J. L., Torrado, I., Ribao, C., and Barja, J. L. 2001, Global market: shellfish imports as a source of reemerging food-borne hepatitis A virus infections in Spain. Int. Microbiol. 4:223–226.CrossRefGoogle Scholar
  68. Sanchez, G., Pinto, R. M., Vanaclocha, H., and Bosch, A., 2002, Molecular characterization of hepatitis A virus isolates from a transcontinental shellfish-borne outbreak. J. Clin. Microbiol. 40:4148–4155.CrossRefGoogle Scholar
  69. Sekine, S., Okada, S., Hayashi, Y., Ando, T., Terayama, T., Yabuuchi, K., Miki, T., and Ohashi, M., 1989, Prevalence of small round structured virus infections in acute gastroenteritis outbreaks in Tokyo. Microbiol. Immunol. 33:207–217.Google Scholar
  70. Simons, G., Greening, G., Gao, W., and Campbell, D., 2001, Raw oyster consumption and outbreaks of viral gastroenteritis in New Zealand: evidence for risk to the public’s health. Aust. N. Z. J. Public Health 25:234–240.Google Scholar
  71. Stafford, R., Strain, D., Heymer, M., Smith, C., Trent, M., and Beard, J., 1997, An outbreak of virus gastroenteritis following consumption of oysters. Commun. Dis. Intell. 21:317–320.Google Scholar
  72. Tang, Y.W., Wang, J. X., Xu, Z.Y., Guo, Y. F., Qian, W. H., and Xu, J. X., 1991, A serologically cofirmed, case-control study, of a large outbreak of hepatitis A in China, associated with consumption of clams. Epidemiol. Infect. 107:651–657.CrossRefGoogle Scholar
  73. Tomar, B. S., 1998, Hepatitis E in India. Zhonghua Min Guo Xiao Er Ke Yi Xue Hui Za Zhi 39:150–156.Google Scholar
  74. Truman, B. I., Madore, H. P., Menegus, M. A., Nitzkin, J. L., and Dolin, R., 1987, Snow Mountain agent gastroenteritis from clams. Am. J. Epidemiol. 126:516–525.Google Scholar
  75. Velazquez, O., Stetler, H. C., Avila, C., Ornelas, G., Alvarez, C., Hadler, S. C., Bradley, D.W., and Sepulveda, J., 1990, Epidemic transmission of enterically transmitted non-A, non-B hepatitis in Mexico, 1986–1987. JAMA 263:3281–3285.CrossRefGoogle Scholar
  76. Wang, J.V., Hu, S. L., Liu, H.Y., Hong, Y. L., Cao, S. Z., and Wu, L. F., 1990, Risk factor analysis of an epidemic of hepatitis A in a factory in Shanghai. Int. J. Epidemiol. 19:435–438.CrossRefGoogle Scholar
  77. White, K. E., Osterholm, M. T., Mariotti, J. A., Korlath, J. A., Lawrence, D. H., Ristinen, T. L., and Greenberg, H. B., 1986, A foodborne outbreak of Norwalk virus gastroenteritis: evidence for post recovery transmission. Am. J. Epidemiol. 124:120–126.Google Scholar
  78. Xu, Z. Y., Li, Z. H., Wang, J. X., Xiao, Z. P., and Dong, D. X., 1992, Ecology and prevention of a shellfish-associated hepatitis A epidemic in Shanghai, China, Vaccine 10(Suppl. 1):S67–68.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2006

Authors and Affiliations

  • Gary P. Richards
    • 1
  1. 1.United States Department of Agriculture—Agricultural Research Service, Microbial Food Safety Research UnitDelaware State UniversityDover

Personalised recommendations