Limitations of molecular biological techniques for assessing the virological safety of foods

Journal of Food Protection

Volumn 62, Issue 6, 1999, Pages 691-697

  Richards, Gary P ^a  

^a DELAWARE STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; FOOD SAFETY; FOULING CONTROL; HEPATITIS A VIRUS; MICROBIAL CONTAMINATION; MOLECULAR BIOLOGY; NORWALK GASTROENTERITIS VIRUS; POLYMERASE CHAIN REACTION; ROTAVIRUS; SNOW MOUNTAIN VIRUS; VIRUS DETECTION;

HEPATITIS A VIRUS; NORWALK VIRUS; POLIOVIRUS; ROTAVIRUS; SNOW MOUNTAIN VIRUS;

EID: 0033152734     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-62.6.691     Document Type: Review

References (95)

1. Arnal, C., J. M. Crance, G. Gantzer, L. Schwartzbrod, R. Deloince, and S. Billaudel. 1998. Persistence of infectious hepatitis A virus and its genome in artificial seawater. Zentralbl. Hyg. Umweltmed. 201:279-284.
2. Atmar, R. L., T. G. Metcalf, F. H. Neill, and M. K. Estes. 1993. Detection of enteric viruses in oysters by using the polymerase chain reaction. Appl. Environ. Microbiol. 59:631-635.
3. Atmar, R. L., F. H. Neill, J. L. Romalde, F. Le Guyader, C. W. Woodley, T. G. Metcalf, and M. K. Estes. 1995. Detection of Norwalk virus and hepatitis A virus in shellfish tissues with the PCR. Appl. Environ. Microbiol. 61:3014-3018.
4. Atmar, R. L., F. H. Neill, C. M. Woodley, R. Manger, G. S. Fout, W. Burkhardt, L. Leja, E. R. McGovern, F. Le Guyader, T. G. Metcalf, and M. K. Estes. 1996. Collaborative evaluation of a method for the detection of Norwalk virus in shellfish tissues by PCR. Appl. Environ. Microbiol. 62:254-258.
5. Bean, N. H., P. M. Griffin, J. S. Goulding, and C. B. Ivey. 1990. Foodborne disease outbreaks, 5-year summary, 1982-1987. J. Food Prot. 53:711-728.
6. Beaulieux, F., D. M. See, I. Leparc-Goffart, M. Aymard, and B. Lina. 1997. Use of magnetic beads versus guanidinium thiocyanale-phenol-chloroform RNA extraction followed by polymerase chain reaction for the rapid, sensitive detection of enterovirus RNA. Res. Virol. 148:11-15.
7. Bemiss, J. A., M. M. Logan, J. D. Sample, and G. P. Richards. 1989. A method for the enumeration of poliovirus in selected molluscan shellfish. J. Virol. Methods 26:209-217.
8. Bouchriti, N., and S. M. Goyal. 1993. Methods for the concentration and detection of human enteric viruses in shellfish: a review. New Microbiol. 16:105.
9. Bryan, F. L. 1980. Foodborne diseases in the United States associated with meat and poultry. J. Food Prot. 43:140-150.
10. Centers for Disease Control. 1987. Outbreaks of viral gastroenteritis - Pennsylvania and Delaware. Morbid. Mortal. Weekly Rep. 36: 709-711.
11. 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. 17:945-948.
12. Centers for Disease Control. 1995. Multistate outbreak of viral gastroenteritis associated with consumption of oysters - Apalachicola Bay, Florida, December 1994-January 1995. Morbid. Mortal. Weekly Rep. 44:37-39.
13. Chenal, V., and R. Griffais. 1994. Chemiluminescent and colorimetric detection of a fluorescein-labeled probe and a digoxigenin-labeled probe after a single hybridization step. Mol. Cell. Probes 8:401-407.
14. Cromeans, T. L., O. V. Nainan, and H. S. Margolis. 1997. Detection of hepatitis A virus RNA in oyster meat. Appl. Environ. Microbiol. 63:2460-2463.
15. De Leon, R., S. M. Matsui, R. S. Baric, J. E. Hermann, N. R. Blacklow, H. B. Greenberg, and M. D. Sobsey. 1992. Detection of Norwalk virus in stool specimens by reverse transcriptase-polymerase chain reaction and nonradioactive oligoprobes. J. Clin. Microbiol. 30:3151-3157.
16. Demeke, T., and R. P. Adams. 1992. The effects of plant polysaccharides and buffer additives on PCR. Biotechniques 12:332-333.
17. Deng, M. Y., and D. O. Cliver. 1992. Inactivation of poliovirus type I in mixed human and swine wastes and by bacteria from swine manure. Appl. Environ. Microbiol. 58:2016-2021.
18. Deng. M. Y., and D. O. Cliver. 1995. Persistence of inoculated hepatitis A virus in mixed human and animal wastes. Appl. Environ. Microbiol. 61:87-91.
19. Deng, M. Y., and D. O. Cliver. 1995. Antiviral effects of bacteria isolated from manure. Microbial Ecol. 30:43-54.
20. Deng, M. Y., S. P. Day, and D. O. Cliver. 1994. Detection of hepatitis A virus in environmental samples by antigen-capture PCR. Appl. Environ. Microbiol. 60:1927-1933.
21. De Sena, J., and D. L. Jarvis. 1981. Modification of the poliovirus capsid by ultraviolet light. Can. J. Microbiol. 27:1185-1193.
22. Dix, A. B., and L.-A. Jaykus. 1998. Virion concentration method for the detection of human enteric viruses in extracts of hard-shelled clams. J. Food Prot. 61:458-465.
23. Dowell, S. F., C. Groves, K. B. Kirkland, H. G. Cicirello, T. Ando, Q. Jin, J. R. Gentsch, S. S. Monroe, C. D. Humphrey, and C. Slemp. 1995. A multistate outbreak of oyster-associated gastroenteritis: implications for interstate tracing of contaminated shellfish. J. Infect. Dis. 171:1497-1503.
24. Egger, D., L. Pasamontes, M. Ostermayer, and K. Bienz. 1995. Reverse transcription multiplex PCR for differentiation between polioand enteroviruses from clinical and environmental samples. J. Clin. Microbiol. 33:1442-1447.
25. Fineschi, N., V. Pellegrini, A. J. Zuckerman, and F. Cavalieri. 1992. Assessment of inactivation of hepatitis A vaccine by compound PCR. J. Virol. Methods 39:157-163.
26. Fleissner, M. L., J. E. Herrmann, J. W. Booth, N. R. Blacklow, and N. A. Nowak. 1989. Role of Norwalk virus in two foodborne outbreaks of gastroenteritis: definitive virus association. Am. J. Epidemiol. 129:165-172.
27. Fujioka, R. S., P. C. Loh, and L. S. Lau. 1980. Survival of human enteroviruses in the Hawaiian ocean environment: evidence for virus-inactivating microorganisms. Appl. Environ. Microbiol. 39: 1105-1110.
28. Goswami, B. B., W. H. Koch, and T. A. Cebula. 1993. Detection of hepatitis A virus in Mercenaria mercenaria by coupled reverse transcription and polymerase chain reaction. Appl. Environ. Microbiol. 59:2756-2770.
29. Gray, S. F., and M. R. Evans. 1993. Dose-response in an outbreak of non-bacterial food poisoning traced to a mixed seafood cocktail. Epidemiol. Infect. 110:583-590.
30. Griffin, M. R., J. J. Surowiec, D. I. McCloskey, B. Capuano, B. Pierzynski, M. Quinn, R. Wojnarski, W. E. Parkin, H. Greenberg, and G. W. Gary. 1982. Foodborne Norwalk virus. Am. J. Epidemiol. 115:178-184.
31. Gross, T. P., J. G. Conde, G. W. Gary, D. Harting, D. Goeller, and E. Israel. 1989. An outbreak of acute infectious nonbacterial gastroenteritis in a high school in Maryland. Public Health Rep. 104:164-169.
32. Guest, C., K. C. Spitalny, H. P. Madore, K. Pray, R. Dolin, J. E. Hermann, and N. R. Blacklow. 1987. Foodborne Snow Mountain agent gastroenteritis in a school cafeteria. Pediatrics 79:559-563.
33. Hafliger, D., M. Gilgen, J. Luthy, and P. Hubner. 1997. Seminested RT-PCR systems for small round structured viruses and detection of enteric viruses in seafoods. Int. J. Food. Microbiol. 37:27-36.
34. Halliday, M. L., L. Y. Kang, T. K. Zhou, M. D. Hu, Q. C. Pan, T. Y. Fu, Y. S. Huang, and S. L. Hu. 1991. An epidemic of hepatitis A attributable to the ingestion of raw clams in Shanghai, China. J. Infect. Dis. 164:852-859.
35. Hermann, J. E., and D. O. Cliver. 1968. Methods for detecting food-borne enteroviruses. Appl. Microbiol. 16:1564-1569.
36. Herwaldt, B. L., J. F. Lew, C. L. Moe, D. C. Lewis, C. D. Humphrey, S. S. Monroe, E. W. Pon, and R. I. Glass. 1994. Characterization of a variant strain of Norwalk virus from a food-borne outbreak of gastroenteritis on a cruise ship in Hawaii. J. Clin. Microbiol. 32: 861-866.
37. Hilfenhaus, J., A. Groner, T. Nowak, and T Weimer. 1997. Analysis of human plasma products: polymerase chain reaction does not discriminate between live and inactivated viruses. Transfusion 37:935-940.
38. Hill, W. E., S. P. Keasler, M. W. Truckess, P. Feng, C. A. Kaysner, and K. A. Limpel. 1991. Polymerase chain reaction identification of Vibrio vulnificus in artificially contaminated oysters. Appl. Environ. Microbiol. 57:707-711.
39. Iversen, A. M., M. Gill, C. L. R. Bartlett, W. D. Cubitt, and D. A. McSwiggan. 1987. Two outbreaks of foodborne gastroenteritis caused by a small round structured virus: evidence for prolonged infectivity by a food handler. Lancet ii:556-558.
40. Jaykus, L. A., R. De Leon, and M. D. Sobsey. 1995. Development of a molecular method for the detection of enteric viruses in oysters. J. Food Prot. 58:1357-1362.
41. Jaykus, L. A., R. De Leon, and M. D. Sobsey. 1996. A virion concentration method for detection of human enteric viruses in oysters by PCR and oligoprobe hybridization. Appl. Environ. Microbiol. 62: 2074-2080.
42. Khan, A. S., C. L. Moe, R. I. Glass, S. S. Monroe, M. K. Estes, L. E. Chapman, X. Jiang, C. Humphrey, E. Pon, and J. K. Iskander. 1994. Norwalk virus-associated gastroenteritis traced to ice consumption aboard a cruise ship in Hawaii: comparison and application of molecular method-based assays. J. Clin. Microbiol. 32:318-322.
43. Knowlton, D. L., and R. L. Ward. 1987. Characterization of virucidal agents in activated sludge. Appl. Environ. Microbiol. 53:621-626.
44. Kobayashi, S., T. Morishita, T. Yamashita, K. Sakae, O. Nishio, T. Miyake, Y. Ishihara, and S. Isomura. 1991. A large outbreak of gastroenteritis associated with a small round structured virus among school children and teachers in Japan. Epidemiol. Infect. 107:81-86.
45. Koo, D., K. Maloney, and R. Tauxe. 1996. Epidemiology of diarrheal disease outbreaks on cruise ships, 1986 through 1993. JAMA 275: 545-547.
46. Kostenbader, K. D., Jr., and D. O. Cliver. 1972. Polyelectrolyte flocculation as an aid to recovery of enteroviruses from oysters. Appl. Microbiol. 24:540-543.
47. Kuritsky, J. N., M. T. Osterholm, H. B. Greenberg, J. A. Korlath, J. R. Godes, C. W. Hedberg, J. C. Forfang, A. Z. Kapikian, J. C. McCullough, and K. E. White. 1984. Norwalk gastroenteritis: a community outbreak associated with bakery product consumption. Ann. Intern. Med. 100:519-521.
48. Lees, D. N., K. Henshilwood, and W. J. Dore. 1994. Development of a method for detection of enteroviruses in shellfish by PCR with poliovirus as a model. Appl. Environ. Microbiol. 60:2999-3005.
49. Lees, D. N., K. Henshilwood, J. Green, C. I. Gallimore, and D. W. Brown. 1995. Detection of small round structured viruses in shellfish by reverse transcription-PCR. Appl. Environ. Microbiol. 61:4418-4424.
50. Le Gall-Recule, G., and V. Jestin. 1995. Production of digoxigeninlabeled DNA probe for detection of Muscovy duck parvovirus. Mol. Cell. Probes 9:39-44.
51. Le Guyader, F., E. Dubois, D. Menard, and M. Pommepuy. 1994. Detection of hepatitis A virus, rotavirus, and enterovirus in naturally contaminated shellfish and sediment by reverse transcription-seminested PCR. Appl. Environ. Microbiol. 60:3665-3671.
52. Le Guyader, F., F. H. Neill, M. K. Estes, S. S. Monroe, T. Ando, and R. L. Atmar. 1996. Detection and analysis of a small round-structured virus strain in oysters implicated in an outbreak of acute gastroenteritis. Appl. Environ. Microbiol. 62:4268-4272.
53. Le Guyader, F., V. Aparie-Marchais, J. Brillet, and S. Billaudel. 1993. Use of genomic probes to detect hepatitis A virus and enterovirus RNAs in wild shellfish and relationship of viral contamination to bacterial contamination. Appl. Environ. Microbiol. 59:3963-3968.
54. Lewis, G. D., and T. G. Metcalf. 1988. Polyethylene glycol precipitation for recovery of pathogenic viruses, including hepatitis A virus and human rotavirus, from oyster, water, and sediment samples. Appl. Environ. Microbiol. 54:1983-1988.
55. Lieb, S., R. A. Gunn, R. Medina, N. Singh, R. D. May, H. T. Janowski, and W. E. Woodward. 1985. Norwalk virus gastroenteritis. An outbreak associated with a cafeteria at a college. Am. J. Epidemiol. 121:259-268.
56. Limsawat, S., and S. Ohgaki. 1997. Fate of liberated viral RNA in wastewater determined by PCR. Appl. Environ. Microbiol. 63:2932-2933.
57. Lo, S. V., A. M. Connolly, S. R. Palmer, D. Wright, P. D. Thomas, and D. Johnson. 1994. The role of the pre-symptomatic food handler in a common source outbreak of food-borne SRSV gastroenteritis in a group of hospitals. Epidemiol. Infect. 113:513-521.
58. Lopez-Sabater, E. L., M. Y. Deng, and D. O. Cliver. 1997. Magnetic immunoseparation PCR assay (MIPA) for detection of hepatitis A virus (HAV) in American oyster (Crassostrea virginica). Lett. Appl. Microbiol. 24:101-104.
59. Ma, J. F., T. M. Straub, I. L. Pepper, and C. P. Gerba. 1994. Cell culture and PCR determination of poliovirus inactivation by disinfectants. Appl. Environ. Microbiol. 60:4203-4206.
60. MacDonald, K. L., and P. M. Griffin. 1986. Foodborne disease outbreaks, annual summary, 1982. Morbid. Mortal. Weekly Rep. 35: 7SS-16SS.
61. Metcalf, T. G., E. Moulton, and D. Eckerson. 1980. Improved method and test strategy for recovery of enteric viruses from shellfish. Appl. Environ. Microbiol. 39:141-152.
62. Murao, M. 1991. Food-borne outbreak of gastroenteritis caused by small round structured virus. 2. An outbreak associated with bakery product consumption. Kansenshogaku Zasshi. 65:1600-1605.
63. Ojeh, C. K., T. M. Cusack, and R. H. Yolken. 1995. Evaluation of the effects of disinfectants on rotavirus RNA and infectivity by the polymerase chain reaction and cell-culture methods. Mol. Cell. Probes 9:341-346.
64. Patterson, W., P. Haswell, P. T. Fryers, and J. Green. 1997. Outbreak of small round structured virus gastroenteritis arose after kitchen assistant vomited. Commun. Dis. Rep. CDC Rev. 7:R101-R103.
65. Patti, A. M., A. L. Santi, R. Gabrieli, S. Fiamma, M. Cauletti, and A. Pana. 1987. Hepatitis A virus and poliovirus inactivation in estuarine water. Water Res. 21:1335-1338.
66. Portnoy, B. L., P. A. Mackowiak, C. T. Caraway, T. W. Walker, T. W. McKinley, and C. A. Klein. 1975. Oyster-associated hepatitis failure of shellfish certification program to prevent outbreaks. JAMA 233:1065-1068.
67. Reid, J. A., E. O. Caul, D. G. White, and S. R. Palmer. 1988. Role of infected food handler in hotel outbreak of Norwalk-like viral gastroenteritis: implications for control. Lancet ii:321-323.
68. Reynolds, K. A., C. P. Gerba, and I. L. Pepper. 1996. Detection of infectious enteroviruses by an integrated cell culture-PCR procedure. Appl. Environ. Microbiol. 62:1424-1427.
69. Richards, G. P. 1985. Outbreaks of shellfish-associated enteric virus illness in the United States: requisite for development of viral guidelines. J. Food. Prot. 48:815-823.
70. Richards, G. P. 1987. Shellfish-associated enteric virus illness in the United States, 1934-1984. Estuaries 10:84-85.
71. Richards, G. P. 1988. Microbial purification of shellfish: a review of depuration and relaying. J. Food Prot. 51:218-251.
72. Richards, G. P. 1991. Shellfish depuration, p. 395-428. In D. A. Ward and C. Hackney (ed.), Microbiology of marine food products. Van Nostrand Reinhold Co., New York.
73. Richards, G. P., D. Goldmintz, D. L. Green, and J. A. Babinchak. 1982. Rapid methods for extraction and concentration of poliovirus from oyster tissues. J. Virol. Methods 5:285-291.
74. Riordan, T., J. Craske, J. L. Roberts, and A. Curry. 1984. Food borne infection by a Norwalk like virus (small round structured virus). J. Clin. Pathol. 37:817-820.
75. Rodgers, F. G., P. Hufton, E. Kurzawska, C. Molloy, and S. Morgan. 1985. Morphological response of human enteroviruses to ultra-violet radiation, heat and disinfectants. J. Med. Microbiol. 20:123-130.
76. Romalde, J. L. 1996. New molecular methods for the detection of hepatitis A and Norwalk viruses in shellfish. Microbiologia 12:547-556.
77. Sadovski, A. Y., B. Fattal, D. Goldberg, E. Katzenelson, and H. I. Shuval. 1978. High levels of microbial contamination of vegetables irrigated with wastewater by the drip method. Appl. Environ. Microbiol. 36:824-830.
78. Schwab, K. J., M. K. Estes, F. H. Neill, and R. L. Atmar. 1997. Use of heat release and an internal RNA standard control in reverse transcription-PCR detection of Norwalk virus from stool samples. J. Clin. Microbiol. 35:511-514.
79. Sekla, L., W. Stackiw, S. Dzogan, and D. Sargeant. 1989. Foodborne gastroenteritis due to Norwalk virus in a Winnipeg hotel. Can. Med. Assoc. J. 140:1461-1464.
80. Severini, G. M., L. Mestroni, A. Falaschi, F. Camerini, and M. Giacca. 1993 Nested polymerase chain reaction for high-sensitivity detection of enteroviral RNA in biological samples. J. Clin. Microbiol. 31:1345-1349.
81. Sobsey, M. D., R. J. Carrick, and H. R. Jensen. 1975. Improved methods for detecting enteric viruses in oysters. Appl. Environ. Microbiol. 36:121-128.
82. Stafford, R., D. Strain, M. Heymer, C. Smith, M. Trent, and J. Beard. 1997. An outbreak of Norwalk virus gastroenteritis following consumption of oysters. Commun. Dis. Intell. 21:317-320.
83. Stone, T., and I. Durrant. Hybridization of horseradish peroxidaselabeled probes and detection by enhanced chemiluminescence. Mol. Biotechnol. 6:69-73.
84. Tierney, J. T., R. Sullivan, and E. P. Larkin. 1977. Persistence of poliovirus 1 in soil and on vegetables grown in soil previously flooded with inoculated sewage sludge or effluent. Appl. Environ. Microbiol. 33:109-113.
85. Toranzo, A. E., J. L. Barja, and F. M. Hetrick. 1982. Antiviral activity of antibiotic-producing marine bacteria. Can. J. Microbiol. 28: 231-238.
86. Truman, B. I., H. P. Madore, M. A. Menegus, J. L. Nitzkin, and R. Dolin. 1987. Snow Mountain agent gastroenteritis from clams. Am. J. Epidemiol. 126:516-525.
87. Tsai, Y.-L., B. Tran, and C. J. Palmer. 1995. Analysis of viral RNA persistence in seawater by reverse transcriptase-PCR. Appl. Environ. Microbiol. 61:363-366.
88. Ward, B. K., C. M. Chenoweth, and L. G. Irving. 1982. Recovery of viruses from vegetable surfaces. Appl. Environ. Microbiol. 44: 1389-1394.
89. Ward, R. L., D. R. Knowlton, and P. E. Winter. 1986. Mechanism of inactivation of enteric viruses in fresh water. Appl. Environ. Microbiol. 52:450-459.
90. Warner, R. D., R. W. Carr, F. K. McClesky, P. C. Johnson, L. M. Elmer, and V. E. Davison. 1991. A large nontypical outbreak of Norwalk virus. Gastroenteritis associated with exposing celery to nonpotable water and with Citrobacter freundii. Arch. Intern. Med. 151:2419-2424.
91. Whitby, K., and J. A. Garson. 1995. Optimisation and evaluation of a quantitative chemiluminescent polymerase chain reaction assay for hepatitis C virus RNA. J. Virol. Methods 51:75-88.
92. White, K. E., M. T. Osterholm, J. A. Mariotti, J. A. Korlath, D. H. Lawrence, T. L. Ristinen, and H. B. Greenberg. 1986. A foodborne outbreak of Norwalk virus gastroenteritis. Evidence for post-recovery transmission. Am. J. Epidemiol. 124:120-126.
93. Xu, Z. Y., Z. H. Li, J. X. Wang, Z. P. Xiao, and D. X. Dong. 1992. Ecology and prevention of a shellfish-associated hepatitis A epidemic in Shanghai, China. Vaccine 10 Suppl. 1:S67-S68.
94. Yang, F., and X. Xu. 1993. A new method of RNA preparation for detection of hepatitis A virus in environmental samples by the polymerase chain reaction. J. Virol. Methods 43:77-84.
95. Zhou, Y. J., M. K. Estes, X. Jiang, and T. G. Metcalf. 1991. Concentration and detection of hepatitis A virus and rotavirus from shellfish by hybridization tests. Appl. Environ. Microbiol. 57:2963-2968.