Adhesion of human pathogenic enteric viruses and surrogate viruses to inert and vegetal food surfaces

Food Microbiology

Volumn 32, Issue 1, 2012, Pages 48-56

  Deboosere, Nathalie ^a   Pinon, Anthony ^a   Caudrelier, Yvette ^a   Delobel, Alexandre ^a   Merle, Ghislaine ^b   Perelle, Sylvie ^b   Temmam, Sarah ^c   Loutreul, Julie ^c   Morin, Thierry ^c   Estienney, Marie ^d   Belliot, Gael ^d   Pothier, Pierre ^d   Gantzer, Christophe ^e   Vialette, Michèle ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

^b French Agency for Food   (France)

^c ADRIA Normandie   (France)

^d DIJON UNIVERSITY HOSPITAL   (France)

^e Laboratoire de Chimie Physique et Microbiologie pour l'Environnement   (France)

Author keywords

Adhesion; Agri food contact surfaces; Bacteriophages; Enteric viruses; Food surfaces

Indexed keywords

STAINLESS STEEL;

ANIMAL; ARTICLE; BACTERIOPHAGE; CALICIVIRUS INFECTION; CELL LINE; COMPARATIVE STUDY; FOOD CONTAMINATION; FRUIT; GENETICS; HEPATITIS A; HEPATITIS A VIRUS; HUMAN; ISOLATION AND PURIFICATION; NOROVIRUS; PHYSIOLOGY; VEGETABLE; VIROLOGY;

ANIMALS; BACTERIOPHAGES; CALICIVIRIDAE INFECTIONS; CELL LINE; FOOD CONTAMINATION; FRUIT; HEPATITIS A; HEPATITIS A VIRUS; HUMANS; NOROVIRUS; STAINLESS STEEL; VEGETABLES;

BOVINE ENTEROVIRUS; FRAGARIA X ANANASSA; HEPATITIS A VIRUS; LACTUCA; RUBUS GLAUCUS;

EID: 84864329288     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2012.04.007     Document Type: Article

References (51)

1. AFNOR NF EN 14675 - Essai quantitatif de suspension pour l'évaluation de l'activité virucide des antiseptiques et des désinfectants chimiques utilisés dans le domaine vétérinaire 2006, National Organization for Standardization.
2. Ballester N., Fontaine J., Margolin A. Occurrence and correlations between coliphages and anthropogenic viruses in the Massachusetts Bay using enrichment and ICC-nPCR. J. Water Health 2005, 3(1):59-68.
3. Belliot G., Lavaux A., Souihel D., Agnello D., Pothier P. Use of murine norovirus as a surrogate to evaluate resistance of human norovirus to disinfectants. Appl. Environ. Microbiol. 2008, 74(10):3315-3318.
4. Bidawid S., Farber J.M., Sattar S.A. Contamination of foods by food handlers: experiments on hepatitis A virus transfer to food and its interruption. Appl. Environ. Microbiol. 2000, 66(7):2759-2763.
5. Bustin S., Benes V., Garson J., Hellemans J., Huggett J., Kubista M., Mueller R., Nolan T., Pfaffl M., Shipley G., Vandesompele J., Wittwer C. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 2009, 55(4):611-622.
6. Butot S., Putallaz T., Sánchez G. Procedure for rapid concentration and detection of enteric viruses from berries and vegetables. Appl. Environ. Microbiol. 2007, 73(1):186-192.
7. Cannon J., Papafragkou E., Park G., Osborne J., Jaykus L., Vinjé J. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J. Food Prot. 2006, 69(11):2761-2765.
8. CDC Surveillance for foodborne disease outbreaks - United States, 2007. MMWR 2010, 59(31):973-979.
9. Costafreda M.I., Bosch A., Pintó R. 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. 2006, 72(6):3846-3855.
10. Croci L., Dubois E., Cook N., de Medici D., Schultz A.C., China B., Rutjes S.A., Hoorfar J., Van der Poel W.H.M. Current methods for extraction and concentration of enteric viruses from fresh fruit and vegetables: towards international standards. Food Anal. Methods 2008, 1:73-84. 10.1007/s12161-008-9025-4.
11. Cromeans T., Sobsey M.D., Fields H.A. Development of a plaque assay for a cytopathic, rapidly replicating isolate of hepatitis A virus. J. Med. Virol. 1987, 22(1):45-56.
12. D'Souza D.H., Sair A., Williams K., Papafragkou E., Jean J., Moore C., Jaykus L. Persistence of caliciviruses on environmental surfaces and their transfer to food. Int. J. Food Microbiol. 2006, 108(1):84-91.
13. D'Souza D.H., Su X. Efficacy of chemical treatments against Murine Norovirus, Feline Calicivirus, and MS2 Bacteriophage. Foodborne Pathogens Dis. 2010, 7(3):319-326.
14. da Silva A., Le Saux J., Parnaudeau S., Pommepuy M., Elimelech M., Le Guyader F. Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Appl. Environ. Microbiol. 2007, 73(24):7891-7897.
15. Deboosere N., Legeay O., Caudrelier Y., Lange M. Modelling effect of physical and chemical parameters on heat inactivation kinetics of hepatitis A virus in a fruit model system. Int. J. Food Microbiol. 2004, 93(1):73-85.
16. Doré W., Henshilwood K., Lees D. Evaluation of F-specific RNA bacteriophage as a candidate human enteric virus indicator for bivalve molluscan shellfish. Appl. Environ. Microbiol. 2000, 66(4):1280-1285.
17. Dubois E., Hennechart C., Merle G., Burger C., Hmila N., Ruelle S., Perelle S., Ferré V. 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. 2007, 117:141-149.
18. EFSA Food-Borne Outbreaks in the European Union in 2007 2009.
19. EFSA Scientific opinion on an update on the present knowledge on the occurrence and control of foodborne viruses. EFSA J. 2011, 9(7):2190.
20. EPI. University of Florida, Batz, M.B., Hoffmann, S., Morris, J.G., 2011. Ranking the Risks: The 10 Pathogen-Food Combinations with the Greatest Burden on Public Health.
21. Fino V., Kniel K. Comparative recovery of foodborne viruses from fresh produce. Foodborne Pathog. Dis. 2008, 5(6):819-825.
22. Flannery J., Keaveney S., Doré W. Use of FRNA bacteriophages to indicate the risk of norovirus contamination in Irish oysters. J. Food Prot. 2009, 72(11):2358-2362.
23. Flehmig B. Hepatitis A-virus in cell culture: I. propagation of different hepatitis A-virus isolates in a fetal rhesus monkey kidney cell line (Frhk-4). Med. Microbiol. Immunol. 1980, 168(4):239-248.
24. Furuse K., Hirashima A., Harigai H., Ando A., Watanabe K., Kurosawa K., Inokuchi Y., Watanabe I. Grouping of RNA coliphages based on analysis of the sizes of their RNAs and proteins. Virology 1979, 97(2):328-341.
25. Girard M., Ngazoa S., Mattison K., Jean J. Attachment of noroviruses to stainless steel and their inactivation, using household disinfectants. J. Food Prot. 2010, 73(2):400-404.
26. Gulati B., Allwood P., Hedberg C., Goyal S. Efficacy of commonly used disinfectants for the inactivation of calicivirus on strawberry, lettuce, and a food-contact surface. J. Food Prot. 2001, 64(9):1430-1434.
27. Havelaar A.H., van O.M., Drost Y.C. F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water. Appl. Environ. Microbiol. 1993, 59(9):2956-2962.
28. ISO 10705-1 Qualité de l'eau - Détection et dénombrement des bactériophages 1995.
29. Jean J., Vachon J., Moroni O., Darveau A., Kukavica-Ibrulj I.I.F. Effectiveness of commercial disinfectants for inactivating hepatitis A virus on agri-food surfaces. J. Food Prot. 2003, 66(1):115-119.
30. Jimenez L., Chiang M. Virucidal activity of a quaternary ammonium compound disinfectant against feline calicivirus: a surrogate for norovirus. Am. J. Infect. Control 2006, 34(5):269-273.
31. Jiménez-Clavero M., Escribano-Romero E., Mansilla C., Gómez N., Córdoba L., Roblas N., Ponz F., Ley V., Sáiz J. Survey of bovine enterovirus in biological and environmental samples by a highly sensitive real-time reverse transcription-PCR. Appl. Environ. Microbiol. 2005, 71(7):3536-3543.
32. Kageyama T., Kojima S., Shinohara M., Uchida K., Fukushi S., Hoshino F.B., Takeda N., Katayama K. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 2003, 41(4):1548-1557.
33. Karst S., Wobus C., Lay M., Davidson J., Virgin H. STAT1-dependent innate immunity to a Norwalk-like virus. Science 2003, 299(5612):1575-1578.
34. Kramer A., Schwebke I., Kampf G. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 2006, 6:130. 10.1186/1471-2334-6-130.
35. Kukavica-Ibrulj I., Darveau A., Jean J., Fliss I. Hepatitis A virus attachment to agri-food surfaces using immunological, virological and thermodynamic assays. J. Appl. Microbiol. 2004, 97(5):923-934.
36. Kurdziel A., Wilkinson N., Langton S., Cook N. Survival of poliovirus on soft fruit and salad vegetables. J. Food Prot. 2001, 64(5):706-709.
37. Langlet J., Gaboriaud F., Duval J., Gantzer C. Aggregation and surface properties of F-specific RNA phages: implication for membrane filtration processes. Water Res. 2008, 42(10-11):2769-2777.
38. Langlet J., Gaboriaud F., Gantzer C., Duval J. Impact of chemical and structural anisotropy on the electrophoretic mobility of spherical soft multilayer particles: the case of bacteriophage MS2. Biophys. J. 2008, 94(8):3293-3312.
39. Le Guyader F., Parnaudeau S., Schaeffer J., Bosch A., Loisy F., Pommepuy M., Atmar R. Detection and quantification of noroviruses in shellfish. Appl. Environ. Microbiol. 2009, 75(3):618-624.
40. Lemon S.M., Murphy P.C., Shields P.A., Ping L.H., Feinstone S.M., Cromeans T., Jansen R.W. Antigenic and genetic variation in cytopathic hepatitis A virus variants arising during persistent infection: evidence for genetic recombination. J. Virol. 1991, 65(4):2056-2065.
41. Loisy F., Atmar R., Guillon P., Le Cann P., Pommepuy M., Le Guyader F. Real-time RT-PCR for norovirus screening in shellfish. J. Virol. Methods 2005, 123(1):1-7.
42. Malik Y., Goyal S. Virucidal efficacy of sodium bicarbonate on a food contact surface against feline calicivirus, a norovirus surrogate. Int. J. Food Microbiol. 2006, 109(1-2):160-163.
43. Mbithi J., Springthorpe V., Sattar S. Effect of relative humidity and air temperature on survival of hepatitis A virus on environmental surfaces. Appl. Environ. Microbiol. 1991, 57(5):1394-1399.
44. Mbithi J., Springthorpe V., Boulet J., Sattar S. Survival of hepatitis A virus on human hands and its transfer on contact with animate and inanimate surfaces. J. Clin. Microbiol. 1992, 30(4):757-763.
45. Ogorzaly L., Gantzer C. Development of real-time RT-PCR methods for specific detection of F-specific RNA bacteriophage genogroups: application to urban raw wastewater. J. Virol. Methods 2006, 138:131-139.
46. Rolfe K., Parmar S., Mururi D., Wreghitt T., Jalal H., Zhang H., Curran M. An internally controlled, one-step, real-time RT-PCR assay for norovirus detection and genogrouping. J. Clin. Virol. 2007, 39(4):318-321.
47. Svraka S., Duizer E., Vennema H., de Bruin E., van der Veer B., Dorresteijn B., Koopmans M. Etiological role of viruses in outbreaks of acute gastroenteritis in The Netherlands from 1994 through 2005. J. Clin. Microbiol. 2007, 45(5):1389-1394.
48. Vega E., Smith J., Garland J., Matos A., Pillaii S. Variability of virus attachment patterns to butterhead lettuce. J. Food Prot. 2005, 68(10):2112-2117.
49. Vega E., Garland J., Pillai S. Electrostatic forces control nonspecific virus attachment to lettuce. J. Food Prot. 2008, 71(3):522-529.
50. WHO Viruses in Food: Scientific Advice to Support Risk Management Activities 2008.
51. Wobus C.E., Karst S.M., Thackray L.B., Chang K.O., Sosnovtsev S.V., Belliot G., Krug A., Mackenzie J.M., Green K.Y., Virgin H.W. Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2004, 2:e432.