Chapter 23 : Norovirus, Hepatitis A Virus, and Indicator Microorganisms in Shellfish, Soft Fruits, and Water

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Zoom in

Norovirus, Hepatitis A Virus, and Indicator Microorganisms in Shellfish, Soft Fruits, and Water, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817121/9781555815424_Chap23-1.gif /docserver/preview/fulltext/10.1128/9781555817121/9781555815424_Chap23-2.gif


Viruses such as hepatitis A virus (HAV), noroviruses (NoV), sapoviruses, enteroviruses, astroviruses, adenoviruses, rotaviruses, and hepatitis E virus have all been implicated in food- and/or water-borne outbreaks of illness. This chapter deals with NoV and HAV detection in bivalve mollusks, soft fruits, and water. For bivalve mollusks, fecal indicators are measured either in the shellfish themselves or in their growing waters. When virus detection procedures are mentioned, the recurrent issue of detecting infectious or physical particles comes into discussion. Whenever possible, infectious assays coupled with identification methods are preferred for direct assessment of human health risk. Nucleic acid amplification techniques are currently the most widely used methods for detection of viruses in food and water and also enable investigators to gather information on the virus genotypes occurring in the environment and in food products, thus providing the most relevant epidemiological information, particularly important for the implementation and follow-up of vaccination programs in the human population.

Citation: Bosch A, Bidawid S, Le Guyader F, Lees D, Jaykus L. 2011. Norovirus, Hepatitis A Virus, and Indicator Microorganisms in Shellfish, Soft Fruits, and Water, p 333-347. In Hoorfar J (ed), Rapid Detection, Characterization, and Enumeration of Foodborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555817121.ch23
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Anonymous. 2005. Microbiology of Food and Animal Feeding Stuffs—Horizontal Method for the Enumeration of Beta-Glucuronidase-Positive Escherichia coli. Part 3. Most Probable Number Technique Using 5-Bromo-4-Chloro-3-Indolyl-Beta- d-Glucuronide. ISO/TS16649-16653. International Organization for Standardization, Geneva, Switzerland.
2. Atmar, R. L.,, F. H. Neill,, J. L. Romalde,, F. Le Guyader,, C. M. 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: 30143018.
3. Ayodeji, M.,, M. Kulka,, S. A. Jackson,, I. Patel,, M. Mammel,, T. A. Cebula, and, B. B. Goswami. 2009. A microarray based approach for the identification of common foodborne viruses. Open Virol. J. 3: 720.
4. Baert, L.,, M. Uyttendaele, and, J. Debevere. 2008a. Evaluation of viral extraction methods on a broad range of Ready-To-Eat foods with conventional and real-time RT-PCR for Norovirus GII detection. Int. J. Food Microbiol. 123: 101108.
5. Baert, L.,, C. E. Wobus,, E. Van Coillie,, L. B. Thackray,, J. Debevere, and, M. Uyttendaele. 2008b. Detection of murine norovirus 1 by using plaque assay, transfection assay, and real-time reverse transcription-PCR before and after heat exposure. Appl. Environ. Microbiol. 74: 543546.
6. Bidawid, S.,, J. M. Farber, and, S. A. Sattar. 2000. Rapid concentration of hepatitis A virus (HAV) from lettuce and strawberries. J. Virol. Methods 88: 175185.
7. Boxman, I. L.,, J. J. Tilburg,, N. A. te Loeke,, H. Vennema,, E. de Boer, and, M. Koopmans. 2007. An efficient and rapid method for recovery of norovirus from food associated with outbreaks of gastroenteritis. J. Food Prot. 70: 504508.
8. Butot, S.,, T. Putallaz,, C. Croquet,, G. Lamothe,, R. Meyer,, H. Joosten, and, G. Sanchez. 2007a. Attachment of enteric viruses to bottles. Appl. Environ. Microbiol. 73: 51045110.
9. Butot, S.,, T. Putallaz, and, G. Sanchez. 2007b. Procedure for rapid concentration and detection of enteric viruses from berries and vegetables. Appl. Environ. Microbiol. 73: 186192.
10. Centers for Disease Control and Prevention. 1997. Hepatitis A associated with consumption of frozen strawberries—Michigan, March 1997. MMWR Morb. Mortal. Wkly. Rep. 46: 288295.
11. Costafreda, M. I.,, A. Bosch, and, R. M. Pinto. 2006. Development, evaluation, and standardization of a real-time TaqMan reverse transcription-PCR assay for quantification of hepatitis A virus in clinical and shellfish samples. Appl. Environ. Microbiol. 72: 38463855.
12. Costa-Mattioli, M.,, S. Monpoeho,, E. Nicand,, M. H. Aleman,, S. Billaudel, and, V. Ferre. 2002a. Quantification and duration of viraemia during hepatitis A infection as determined by realtime RT-PCR. J. Viral Hepat. 9: 101106.
13. Costa-Mattioli, M.,, J. Cristina,, H. Romero,, R. Perez-Bercof,, D. Casane,, R. Colina,, L. Garcia,, I. Vega,, G. Glikman,, V. Romanowsky,, A. Castello,, E. Nicand,, M. Gassin,, S. Billaudel, and, V. Ferre. 2002b. Molecular evolution of hepatitis A virus: a new classification based on the complete VP1 protein. J. Virol. 76: 95169525.
14. Croci, L.,, E. Dubois,, N. Cook,, D. de Medici,, A. Schultz,, B. China,, S. Rutjes,, J. Hoorfar, and, W. Van der Poel. 2008. Current methods for extraction and concentration of enteric viruses from fresh fruit and vegetables: towards international standards. Food Anal. Methods 1: 7384.
15. da Silva, A. K.,, J. C. Le Saux,, S. Parnaudeau,, M. Pommepuy,, M. Elimelech, and, F. S. Le Guyader. 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. 73: 78917897.
16. DePaola, A.,, J. L. Jones,, J. Woods,, W. Burkhardt III,, K. R. Calci,, J. A. Krantz,, J. C. Bowers,, K. Kasturi,, R. H. Byars,, E. Jacobs,, D. Williams-Hill, and, K. Nabe. 2010. Bacterial and viral pathogens in live oysters: 2007 United States market survey. Appl. Environ. Microbiol. 76: 27542768.
17. Dore, W. J.,, K. Henshilwood, and, D. N. Lees. 2000. Evaluation of F-specific RNA bacteriophage as a candidate human enteric virus indicator for bivalve molluscan shellfish. Appl. Environ. Microbiol. 66: 12801285.
18. D’Souza, D. H.,, J. Jean, and, L. Jaykus. 2010. Methods for the detection of viral and parasitic protozoan pathogens in food, p. 1–23. In Y. H. Hui (ed.), Handbook of Food Technology and Engineering, vol. 4. CRC-Taylor and Francis, Boca Raton, FL.
19. Dubois, E.,, C. Hennechart,, G. Merle,, C. Burger,, N. Hmila,, S. Ruelle,, S. Perelle, and, V. Ferre. 2007. Detection and quantification by real-time RT-PCR of hepatitis A virus from inoculated tap waters, salad vegetables, and soft fruits: characterization of the method performances. Int. J. Food Microbiol. 117: 141149.
20. El Senousy, W. M.,, S. Guix,, I. Abid,, R. M. Pinto, and, A. Bosch. 2007. Removal of astrovirus from water and sewage treatment plants, evaluated by a competitive reverse transcription-PCR. Appl. Environ. Microbiol. 73: 164167.
21. Endley, S.,, L. Lu,, E. Vega,, M. E. Hume, and, S. D. Pillai. 2003. Male-specific coliphages as an additional fecal contamination indicator for screening fresh carrots. J. Food Prot. 66: 8893.
22. Fukuda, S.,, S. Takao,, M. Kuwayama,, Y. Shimazu, and, K. Miyazaki. 2006. Rapid detection of norovirus from fecal specimens by real-time reverse transcription-loop-mediated isothermal amplification assay. J. Clin. Microbiol. 44: 13761381.
23. Gajardo, R.,, R. M. Pinto, and, A. Bosch. 1995. Polymerase chain-reaction amplification and typing of rotavirus in environmental samples. Water Sci. Technol. 31: 371374.
24. Gaulin, C. D.,, D. Ramsay,, P. Cardinal, and, M. A. D’Halevyn. 1999. Epidemic of gastroenteritis of viral origin associated with eating imported raspberries. Can. J. Public Health 90: 3740.
25. Hu, Y.,, and I. Arsov. 2009. Nested real-time PCR for hepatitis A detection. Lett. Appl. Microbiol. 49: 615619.
26. Jean, J.,, D. H. D’Souza, and, L. A. Jaykus. 2004. Multiplex nucleic acid sequence-based amplification for simultaneous detection of several enteric viruses in model ready-to-eat foods. Appl. Environ. Microbiol. 70: 66036610.
27. Jothikumar, N.,, T. L. Cromeans,, M. D. Sobsey, and, B. H. Robertson. 2005a. Development and evaluation of a broadly reactive TaqMan assay for rapid detection of hepatitis A virus. Appl. Environ. Microbiol. 71: 33593363.
28. Jothikumar, N.,, J. A. Lowther,, K. Henshilwood,, D. N. Lees,, V. R. Hill, and, J. Vinje. 2005b. 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: 18701875.
29. Kageyama, T.,, S. Kojima,, M. Shinohara,, K. Uchida,, S. Fukushi,, F. B. Hoshino,, N. Takeda, and, K. Katayama. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 41: 15481557.
30. Kiulia, N. M.,, R. Netshikweta,, N. A. Page,, W. B. van Zyl,, M. M. Kiraithe,, A. Nyachieo,, J. M. Mwenda, and, M. B. Taylor. 2010. The detection of enteric viruses in selected urban and rural river water and sewage in Kenya, with special reference to rotaviruses. J. Appl. Microbiol. 109: 818828.
31. Konduru, K.,, and G. Kaplan. 2006. Stable growth of wild-type hepatitis A virus in cell culture. J. Virol. 80: 13521360.
32. Lees, D. 2000. Viruses and bivalve shellfish. Int. J. Food Microbiol. 59: 81116.
33. Lees, D. N. 2010. International standardisation of a method for detection of human pathogenic viruses in molluscan shellfish. Food Environ. Virol. 2: 146155.
34. Le Guyader, F. S.,, J. C. Le Saux,, K. Ambert-Balay,, J. Krol,, O. Serais,, S. Parnaudeau,, H. Giraudon,, G. Delmas,, M. Pommepuy,, P. Pothier, and, R. L. Atmar. 2008. Aichi virus, norovirus, astrovirus, enterovirus, and rotavirus involved in clinical cases from a French oyster-related gastroenteritis outbreak. J. Clin. Microbiol. 46: 40114017.
35. Le Guyader, F. S.,, S. Parnaudeau,, J. Schaeffer,, A. Bosch,, F. Loisy,, M. Pommepuy, and, R. L. Atmar. 2009. Detection and quantification of noroviruses in shellfish. Appl. Environ. Microbiol. 75: 618624.
36. 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: 19831988.
37. Loisy, F.,, R. L. Atmar,, P. Guillon,, P. Le Cann,, M. Pommepuy, and, F. S. Le Guyader. 2005. Real-time RT-PCR for norovirus screening in shellfish. J. Virol. Methods 123: 17.
38. Lopman, B.,, H. Vennema,, E. Kohli,, P. Pothier,, A. Sanchez,, A. Negredo,, J. Buesa,, E. Schreier,, M. Reacher,, D. Brown,, J. Gray,, M. Iturriza,, C. Gallimore,, B. Bottiger,, K. O. Hedlund,, M. Torven,, C. H. von Bonsdorff,, L. Maunula,, M. Poljsak-Prijatelj,, J. Zimsek,, G. Reuter,, G. Szucs,, B. Melegh,, L. Svennson,, Y. van Duijnhoven, and, M. Koopmans. 2004. Increase in viral gastroenteritis outbreaks in Europe and epidemic spread of new norovirus variant. Lancet 363: 682688.
39. Love, D. C.,, M. J. Casteel,, J. S. Meschke, and, M. D. Sobsey. 2008. Methods for recovery of hepatitis A virus (HAV) and other viruses from processed foods and detection of HAV by nested RT-PCR and TaqMan RT-PCR. Int. J. Food Microbiol. 126: 221226.
40. Lowther, J. A.,, J. M. Avant,, K. Gizynski,, R. E. Rangdale, and, D. N. Lees. 2010. Comparison between quantitative real-time reverse transcription PCR results for norovirus in oysters and self-reported gastroenteric illness in restaurant customers. J. Food Prot. 73: 305311.
41. Lynch, M.,, J. Painter,, R. Woodruff, and, C. Braden. 2006. Surveillance for foodborne-disease outbreaks—United States, 1998–2002. MMWR Surveill. Summ. 55: 142.
42. Morales-Rayas, R.,, P. F. Wolffs, and, M. W. Griffiths. 2010. Simultaneous separation and detection of hepatitis A virus and norovirus in produce. Int. J. Food Microbiol. 139: 4855.
43. Nenonen, N. P.,, C. Hannoun,, M. B. Olsson, and, T. Bergstrom. 2009. Molecular analysis of an oyster-related norovirus outbreak. J. Clin. Virol. 45: 105108.
44. Pagotto, F.,, N. Corneau,, K. Mattison, and, S. Bidawid. 2008. Development of a DNA microarray for the simultaneous detection and genotyping of noroviruses. J. Food Prot. 71: 14341441.
45. Papafragkou, E.,, M. Plante,, K. Mattison,, S. Bidawid,, K. Karthikeyan,, J. M. Farber, and, L. A. Jaykus. 2008. Rapid and sensitive detection of hepatitis A virus in representative food matrices. J. Virol. Methods 147: 177187.
46. Pintó, R. M.,, M. I. Costafreda, and, A. Bosch. 2009. Risk assessment in shellfish-borne outbreaks of hepatitis A. Appl. Environ. Microbiol. 75: 73507355.
47. Ponka, A.,, L. Maunula,, C. H. von Bonsdorff, and, O. Lyytikainen. 1999. An outbreak of calicivirus associated with consumption of frozen raspberries. Epidemiol. Infect. 123: 469474.
48. Robertson, B. H.,, R. W. Jansen,, B. Khanna,, A. Totsuka,, O. V. Nainan,, G. Siegl,, A. Widell,, H. S. Margolis,, S. Isomura,, K. Ito,, T. Ishizu,, Y. Moritsugu, and, S. M. Lemon. 1992. Genetic relatedness of hepatitis A virus strains recovered from different geographical regions. J. Gen. Virol. 73: 13651377.
49. Rutjes, S. A.,, H. H. J. L. van den Berg,, W. J. Lodder, and, A. M. de Roda Husman. 2006. Real-time detection of noroviruses in surface water by use of a broadly reactive nucleic acid sequence-based amplification assay. Appl. Environ. Microbiol. 72: 53495358.
50. Scherer, K.,, D. Mäde,, L. Ellerbroek,, J. Schulenburg,, R. Johne, and, G. Klein. 2009. Application of a swab sampling method for the detection of norovirus and rotavirus to artificially contaminated food and environmental surfaces. Food Environ. Virol. 1: 4249.
51. Shieh, Y. C.,, Y. E. Khudyakov,, G. Xia,, L. M. Ganova-Raeva,, F. M. Khambaty,, J. W. Woods,, J. E. Veazey,, M. L. Motes,, M. B. Glatzer,, S. R. Bialek, and, A. E. Fiore. 2007. Molecular confirmation of oysters as the vector for hepatitis A in a 2005 multistate outbreak. J. Food Prot. 70: 145150.
52. Sobsey, M. D.,, and J. S. Glass. 1980. Poliovirus concentration from tap water with electropositive adsorbent filters. Appl. Environ. Microbiol. 40: 201210.
53. Straub, T. M.,, K. Höner zu Bentrup,, P. O. Orosz-Coghlan,, A. Dohnalkova,, B. K. Mayer,, R. A. Bartholomew,, C. O. Valdez,, C. J. Bruckner,, C. P. Gerba,, M. Abbaszadegan, and, C. A. Nickerson. 2007. In vitro cell culture infectivity assay for human noroviruses. Emerg. Infect. Dis. 13: 396403.
54. Svraka, S.,, E. Duizer,, H. Vennema,, E. de Bruin,, B. van der Veer,, B. Dorresteijn, and, M. Koopmans. 2007. Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. J. Clin. Microbiol. 45: 13891394.
55. Tallo, T.,, H. Norder,, V. Tefanova,, K. Ott,, V. Ustina,, T. Prukk,, O. Solomonova,, J. Schmidt,, K. Zilmer,, L. Priimägi,, T. Krispin, and, L. O. Magnius. 2003. Sequential changes in hepatitis A virus genotype distribution in Estonia during 1994 to 2001. J. Med. Virol. 70: 187193.
56. Terio, V.,, V. Martella,, P. Moschidou,, P. Di Pinto,, G. Tantillo, and, C. Buonavoglia. 2010. Norovirus in retail shellfish. Food Microbiol. 27: 2932.
57. Teunis, P. F.,, C. L. Moe,, P. Liu,, S. E. Miller,, L. Lindesmith,, R. S. Baric,, J. Le Pendu, and, R. L. Calderon. 2008. Norwalk virus: how infectious is it? J. Med. Virol. 80: 14681476.
58. Verhoef, L.,, H. Vennema,, W. van Pelt,, D. Lees,, H. Boshuizen,, K. Henshilwood, and, M. Koopmans. 2010. Use of norovirus genotype profiles to differentiate origins of foodborne outbreaks. Emerg. Infect. Dis. 16: 617624.
59. Vilagines, P.,, B. Sarrette,, G. Husson, and, R. Vilagines. 1993. Glass wool for virus concentration at ambient water pH level. Water Sci. Technol. 27: 34.
60. Villena, C.,, W. M. El-Senousy,, F. X. Abad,, R. M. Pinto, and, A. Bosch. 2003. Group A rotavirus in sewage samples from Barcelona and Cairo: emergence of unusual genotypes. Appl. Environ. Microbiol. 69: 39193923.
61. Vinje, J.,, H. Vennema,, L. Maunula,, C. H. von Bonsdorff,, M. Hoehne,, E. Schreier,, A. Richards,, J. Green,, D. Brown,, S. S. Beard,, S. S. Monroe,, E. de Bruin,, L. Svensson, and, M. P. Koopmans. 2003. International collaborative study to compare reverse transcriptase PCR assays for detection and genotyping of noroviruses. J. Clin. Microbiol. 41: 14231433.
62. Westrell, T.,, V. Dusch,, S. Ethelberg,, J. Harris,, M. Hjertqvist,, S. N. Jourdan-da,, A. Koller,, A. Lenglet,, M. Lisby, and, L. Vold. 2010. Norovirus outbreaks linked to oyster consumption in the United Kingdom, Norway, France, Sweden and Denmark, 2010. Euro Surveill. 15 (12): 19524.
63. Wheeler, C.,, T. M. Vogt,, G. L. Armstrong,, G. Vaughan,, A. Weltman,, O. V. Nainan,, V. Dato,, G. L. Xia,, K. Waller,, J. Amon,, T. M. Lee,, A. Highbaugh-Battle,, C. Hembree,, S. Evenson,, M. A. Ruta,, I. T. Williams,, A. E. Fiore, and, B. P. Bell. 2005. An outbreak of hepatitis A associated with green onions. N. Engl. J. Med. 353: 890897.
64. World Health Organization. 2004. Guidelines for Drinking-Water Quality, 3rd ed., vol. 1. Recommendations. World Health Organization, Geneva, Switzerland.
65. Wyn-Jones, P. 2007. The detection of waterborne viruses, p. 177–204. In A. Bosch (ed.), Human Viruses in Water, vol. 17. Elsevier, Amsterdam, The Netherlands.


Generic image for table

Summary of the principles of virus concentration, purification, and RNA extraction from soft fruits

Citation: Bosch A, Bidawid S, Le Guyader F, Lees D, Jaykus L. 2011. Norovirus, Hepatitis A Virus, and Indicator Microorganisms in Shellfish, Soft Fruits, and Water, p 333-347. In Hoorfar J (ed), Rapid Detection, Characterization, and Enumeration of Foodborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555817121.ch23
Generic image for table

Summary of candidate methodological approaches to the detection of virus contamination in soft fruits

Citation: Bosch A, Bidawid S, Le Guyader F, Lees D, Jaykus L. 2011. Norovirus, Hepatitis A Virus, and Indicator Microorganisms in Shellfish, Soft Fruits, and Water, p 333-347. In Hoorfar J (ed), Rapid Detection, Characterization, and Enumeration of Foodborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555817121.ch23
Generic image for table

Procedures for the concentration of viruses from water samples

Citation: Bosch A, Bidawid S, Le Guyader F, Lees D, Jaykus L. 2011. Norovirus, Hepatitis A Virus, and Indicator Microorganisms in Shellfish, Soft Fruits, and Water, p 333-347. In Hoorfar J (ed), Rapid Detection, Characterization, and Enumeration of Foodborne Pathogens. ASM Press, Washington, DC. doi: 10.1128/9781555817121.ch23

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error