Comparative Virucidal Efficacy of Seven Disinfectants Against Murine Norovirus and Feline Calicivirus, Surrogates of Human Norovirus

Food and Environmental Virology

Volumn 8, Issue 1, 2016, Pages 1-12

  Zonta, William ^a   Mauroy, Axel ^a   Farnir, Frederic ^a   Thiry, Etienne ^a  

^a UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Disinfection; Feline calicivirus; Food contact surfaces; Foodborne viruses; Murine norovirus; Norovirus

Indexed keywords

ALCOHOL; ALDEHYDE; BIGUANIDE; DISINFECTANT AGENT; HALOGEN; HYDROGEN PEROXIDE; OXIDIZING AGENT; PERACETIC ACID; QUATERNARY AMMONIUM DERIVATIVE;

ANTIVIRAL ACTIVITY; ARTICLE; CELL LINE RAW 264.7; CELL METABOLISM; CELL VIABILITY; CONTROLLED STUDY; DISINFECTION; FELINE CALICIVIRUS; FOOD; NONHUMAN; NOROVIRUS; PRIORITY JOURNAL; VIRUS GENOME; VIRUS INFECTIVITY; ANIMAL; CAT; CHEMISTRY; COMPARATIVE STUDY; DRUG EFFECTS; FOOD CONTAMINATION; HUMAN; MOUSE; PHYSIOLOGY; PREVENTION AND CONTROL; VIRUS INACTIVATION;

ANIMALS; CALICIVIRUS, FELINE; CATS; DISINFECTANTS; DISINFECTION; FOOD CONTAMINATION; HUMANS; MICE; NOROVIRUS; VIRUS INACTIVATION;

EID: 84958042307     PISSN: 18670334     EISSN: 18670342     Source Type: Journal    
DOI: 10.1007/s12560-015-9216-2     Document Type: Article

References (78)

1. AFNOR. (2007). EN 14476 Antiseptiques et désinfectants chimiques Essai virucide quantitatif de suspension pour les antiseptiques et désinfectants chimiques utilisés en médecine humaine (p. 34). Association Française de Normalisation.
2. Atmar, R. L. (2010). Noroviruses: State of the Art. Food and Environmental Virology,2(3), 117–126.
3. Atmar, R. L., Opekun, A. R., Gilger, M. A., Estes, M. K., Crawford, S. E., Neill, F. H., et al. (2014). Determination of the 50 % human infectious dose for norwalk virus. Journal of Infectious Diseases,209(7), 1016–1022.
4. Baert, L., Uyttendaele, M., Stals, A., van Coillie, E., Dierick, K., Debevere, J., et al. (2009a). Reported foodborne outbreaks due to noroviruses in Belgium: The link between food and patient investigations in an international context. Epidemiology and Infection,137(3), 316–325.
5. Baert, L., Vandekinderen, I., Devlieghere, F., Van, E. C., Debevere, J., & Uyttendaele, M. (2009b). Efficacy of sodium hypochlorite and peroxyacetic acid to reduce murine norovirus 1, B40-8, Listeria monocytogenes, and Escherichia coli 0157:H7 on shredded iceberg lettuce and in residual wash water. Journal of Food Protection,72(5), 1047–1054.
6. Belliot, G., Lavaux, A., Souihel, D., Agnello, D., & Pothier, P. (2008). Use of murine norovirus as a surrogate to evaluate resistance of human norovirus to disinfectants. Applied and Environmental Microbiology,74(10), 3315–3318.
7. Bellou, M., Kokkinos, P., & Vantarakis, A. (2013). Shellfish-borne viral outbreaks: A systematic review. Food and Environmental Virology,5(1), 13–23.
8. Bidawid, S., Malik, N., Adegbunrin, O., Sattar, S. A., & Farber, J. M. (2003). A feline kidney cell line-based plaque assay for feline calicivirus, a surrogate for Norwalk virus. Journal of Virological Methods,107(2), 163–167.
9. Bresee, J. S., Widdowson, M. A., Monroe, S. S., & Glass, R. I. (2002). Foodborne viral gastroenteritis: Challenges and opportunities. Clinical Infectious Diseases,35(6), 748–753.
10. Cannon, J. L., Papafragkou, E., Park, G. W., Osborne, J., Jaykus, L. A., & Vinjé, J. (2006). Surrogates for the study, of norovirus stability and inactivation in the environment: A comparison of murine norovirus and feline calicivirus. Journal of Food Protection,69(11), 2761–2765.
11. Chambon, M., Bailly, J. L., & Peigue-Lafeuille, H. (1992). Activity of glutaraldehyde at low concentrations against capsid proteins of poliovirus type 1 and echovirus type 25. Applied and Environmental Microbiology,58(11), 3517–3521.
12. Clarke, I. N., & Lambden, P. R. (2000). Organization and expression of calicivirus genes. Journal of Infectious Diseases,181(Suppl 2), S309–S316.
13. Codex Alimentarius. (2012). CAC/GL 79-2012 guidelines on the application of general principles of food hygiene to the control of viruses in food. Codex Committee on Food Hygiene, 13.
14. Crandell, R. A., Fabricant, C. G., & Nelson Rees, W. A. (1973). Development, characterization, and viral susceptibility of a feline (Felis catus) renal cell line (CRFK). In Vitro,9(3), 176–185.
15. Cromeans, T., Park, G. W., Costantini, V., Lee, D., Wang, Q., Farkas, T., et al. (2014). Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Applied and Environmental Microbiology,80(18), 5743–5751. doi:10.1128/aem.01532-14.
16. De Wit, M. A. S., Koopmans, M. P. G., Kortbeek, L. M., Wannet, W. J. B., Vinjé, J., Van Leusden, F., et al. (2001). Sensor, a population-based cohort study on gastroenteritis in the Netherlands: Incidence and etiology. American Journal of Epidemiology,154(7), 666–674.
17. Doré, B., Keaveney, S., Flannery, J., & Rajko-Nenow, P. (2010). Management of health risks associated with oysters harvested from a norovirus contaminated area, Ireland, February-March 2010. Eurosurveillance,15(19), 1–4.
18. Doultree, J. C., Druce, J. D., Birch, C. J., Bowden, D. S., & Marshall, J. A. (1999). Inactivation of feline calicivirus, a Norwalk virus surrogate. Journal of Hospital Infection,41(1), 51–57.
19. D’Souza, D. H., Sair, A., Williams, K., Papafragkou, E., Jean, J., Moore, C., et al. (2006). Persistence of caliciviruses on environmental surfaces and their transfer to food. International Journal of Food Microbiology,108(1), 84–91.
20. D’Souza, D. H., & Su, X. (2010). Efficacy of chemical treatments against murine norovirus, feline calicivirus, and MS2 bacteriophage. Foodborne Pathogens and Disease,7(3), 319–326.
21. Duizer, E., Bijkerk, P., Rockx, B., De Groot, A., Twisk, F., & Koopmans, M. (2004a). Inactivation of caliciviruses. Applied and Environmental Microbiology,70(8), 4538–4543.
22. Duizer, E., Schwab, K. J., Neill, F. H., Atmar, R. L., Koopmans, M. P. G., & Estes, M. K. (2004b). Laboratory efforts to cultivate noroviruses. Journal of General Virology,85(1), 79–87.
23. EFSA & ECDC. (2011). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2009. EFSA Journal 2011, 9(3), 378.
24. EFSA, & ECDC. (2012). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2010. EFSA Journal 2012, 10(3), 442.
25. EFSA & ECDC. (2013). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2011. EFSA Journal 2013, 11(4), 250.
26. FAO/WHO. (2008). Viruses in food: Scientific advice to support risk management activities. Microbiological risk assessment series 13, meeting report. Geneva: World Health Organization.
27. Fraisse, A., Temmam, S., Deboosere, N., Guillier, L., Delobel, A., Maris, P., et al. (2011). Comparison of chlorine and peroxyacetic-based disinfectant to inactivate Feline calicivirus, Murine norovirus and Hepatitis A virus on lettuce. International Journal of Food Microbiology,151(1), 98–104.
28. Girard, M., Ngazoa, S., Mattison, K., & Jean, J. (2010). Attachment of noroviruses to stainless steel and their inactivation, using household disinfectants. Journal of Food Protection,73(2), 400–404.
29. Glass, R. I., Parashar, U. D., & Estes, M. K. (2009). Norovirus gastroenteritis. New England Journal of Medicine,361(18), 1776–1785.
30. Green, K. Y. (2007). Caliciviridae: The Noroviruses. In D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman, et al. (Eds.), Fields virology (5th ed., pp. 949–979). Philadelphia: Lippincott Williams & Wilkins.
31. Green, K. Y. (2013). Caliciviridae: The noroviruses. In D. M. Knipe, P. M. Howley, J. I. Cohen, D. E. Griffin, R. A. Lamb, M. A. Martin, et al. (Eds.), Fields virology (6th ed., pp. 583–609). Philadelphia: Lippincott Williams & Wilkins.
32. Green, K. Y., Ando, T., Balayan, M. S., Berke, T., Clarke, I. N., Estes, M. K., et al. (2000). Taxonomy of the caliciviruses. Journal of Infectious Diseases,181(Suppl 2), S322–S330.
33. Guix, S., Asanaka, M., Katayama, K., Crawford, S. E., Neill, F. H., Atmar, R. L., et al. (2007). Norwalk virus RNA is infectious in mammalian cells. Journal of Virology,81(22), 12238–12248.
34. Gulati, B. R., Allwood, P. B., Hedberg, C. W., & Goyal, S. M. (2001). Efficacy of commonly used disinfectants for the inactivation of calicivirus on strawberry, lettuce, and a food-contact surface. Journal of Food Protection,64(9), 1430–1434.
35. Hall, A. J., Wikswo, M. E., Manikonda, K., Roberts, V. A., Yoder, J. S., & Hannah Gould, L. (2013). Acute gastroenteritis surveillance through the national outbreak reporting system, United States. Emerging Infectious Diseases,19(8), 1308–1309.
36. Hall, A. J., Wikswo, M. E., Pringle, K., Gould, L. H., & Parashar, U. D. (2014). Vital signs: Foodborne norovirus outbreaks—United States, 2009–2012. Morbidity and Mortality Weekly Report,63(22), 491–495.
37. Hannah Gould, L., Mungai, E. A., Johnson, S. D., Richardson, L. C., Williams, I. T., Griffin, P. M., et al. (2013). Surveillance for foodborne disease outbreaks—United States, 2009–2010. Morbidity and Mortality Weekly Report,62(3), 41–47.
38. Hirneisen, K. A., Black, E. P., Cascarino, J. L., Fino, V. R., Hoover, D. G., & Kniel, K. E. (2010). Viral inactivation in foods: A review of traditional and novel food-processing technologies. Comprehensive Reviews in Food Science and Food Safety,9(1), 3–20.
39. Hirneisen, K. A., & Kniel, K. E. (2013). Comparing human norovirus surrogates: Murine norovirus and Tulane virus. Journal of Food Protection,76(1), 139–143.
40. Hyde, J. L., Sosnovtsev, S. V., Green, K. Y., Wobus, C., Virgin, H. W., & Mackenzie, J. M. (2009). Mouse norovirus replication is associated with virus-induced vesicle clusters originating from membranes derived from the secretory pathway. Journal of Virology,83(19), 9709–9719.
41. Iwasawa, A., Niwano, Y., Kohno, M., & Ayaki, M. (2012). Virucidal activity of alcohol-based hand rub disinfectants. Biocontrol Science,17(1), 45–49.
42. Jiang, X., Wang, M., Wang, K., & Estes, M. K. (1993). Sequence and genomic organization of Norwalk virus. Virology,195(1), 51–61. doi:10.1006/viro.1993.1345.
43. Jimenez, L., & Chiang, M. (2006). Virucidal activity of a quaternary ammonium compound disinfectant against feline calicivirus: A surrogate for norovirus. American Journal of Infection Control,34(5), 269–273.
44. Jones, M. K., Watanabe, M., Zhu, S., Graves, C. L., Keyes, L. R., Grau, K. R., et al. (2014). Enteric bacteria promote human and mouse norovirus infection of B cells. Science,346(6210), 755–759.
45. Karst, S. M., Wobus, C. E., Lay, M., Davidson, J., & Virgin Iv, H. W. (2003). STAT1-dependent innate immunity to a norwalk-like virus. Science,299(5612), 1575–1578.
46. Kim, S. W., Baek, S. B., Ha, J. H., Lee, M. H., Choi, C., & Ha, S. D. (2012). Chlorine treatment to inactivate norovirus on food contact surfaces. Journal of Food Protection,75(1), 184–188.
47. Kingsley, D. H., Vincent, E. M., Meade, G. K., Watson, C. L., & Fan, X. (2014). Inactivation of human norovirus using chemical sanitizers. International Journal of Food Microbiology,171, 94–99.
48. Kniel, K. E. (2014). The makings of a good human norovirus surrogate. Current Opinion in Virology,4, 85–90. doi:10.1016/j.coviro.2014.01.002.
49. Koopmans, M., & Duizer, E. (2004). Foodborne viruses: An emerging problem. International Journal of Food Microbiology,90(1), 23–41.
50. Kroneman, A., Verhoef, L., Harris, J., Vennema, H., Duizer, E., Van Duynhoven, Y., et al. (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. Journal of Clinical Microbiology,46(9), 2959–2965.
51. Lim, M. Y., Kim, J. M., & Ko, G. (2010). Disinfection kinetics of murine norovirus using chlorine and chlorine dioxide. Water Research,44(10), 3243–3251.
52. Lopman, B. A., Adak, G. K., Reacher, M. H., & Brown, D. W. G. (2003). Two epidemiologic patterns of Norovirus outbreaks: Surveillance in England and Wales, 1992–2000. Emerging Infectious Diseases,9(1), 71–77.
53. Maillard, J. Y. (2001). Virus susceptibility to biocides: An understanding. Reviews in Medical Microbiology,12(2), 63–74.
54. Malik, Y. S., Maherchandani, S., Allwood, P. B., & Goyal, S. M. (2005). Evaluation of animal origin cell cultures for in vitro cultivation of noroviruses. Journal of Applied Research,5(2), 312–317.
55. Malik, Y. S., Maherchandani, S., & Goyal, S. M. (2006). Comparative efficacy of ethanol and isopropanol against feline calicivirus, a norovirus surrogate. American Journal of Infection Control,34(1), 31–35.
56. Mathijs, E., Stals, A., Baert, L., Botteldoorn, N., Denayer, S., Mauroy, A., et al. (2012). A review of known and hypothetical transmission routes for noroviruses. Food and Environmental Virology,4(4), 131–152.
57. Matsuhira, T., Kaji, C., Murakami, S., Maebashi, K., Oka, T., Takeda, N., et al. (2012). Evaluation of four antiseptics using a novel Murine norovirus. Experimental Animals,61(1), 35–40.
58. McDonnell, G., & Russell, A. D. (1999). Antiseptics and disinfectants: Activity, action, and resistance. Clinical Microbiology Reviews,12(1), 147–179.
59. Nuanualsuwan, S., & Cliver, D. O. (2003). Capsid functions of inactivated human picornaviruses and feline calicivirus. Applied and Environmental Microbiology,69(1), 350–357.
60. O’Brien, R. T., & Newman, J. (1979). Structural and compositional changes associated with chlorine inactivation of polioviruses. Applied and Environmental Microbiology,38(6), 1034–1039.
61. Park, G. W., Barclay, L., MacInga, D., Charbonneau, D., Pettigrew, C. A., & Vinjé, J. (2010). Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus, and GII.4 norovirus. Journal of Food Protection,73(12), 2232–2238.
62. Park, G. W., & Sobsey, M. D. (2011). Simultaneous comparison of murine norovirus, feline calicivirus, coliphage MS2, and GII.4 norovirus to evaluate the efficacy of sodium hypochlorite against human norovirus on a fecally soiled stainless steel surface. Foodborne Pathogens and Disease,8(9), 1005–1010.
63. Patel, M. M., Widdowson, M. A., Glass, R. I., Akazawa, K., Vinjé, J., & Parashar, U. D. (2008). Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerging Infectious Diseases,14(8), 1224–1231.
64. Radford, A. D., Coyne, K. P., Dawson, S., Porter, C. J., & Gaskell, R. M. (2007). Feline calicivirus. Veterinary Research,38(2), 319–335.
65. Ramani, S., Atmar, R. L., & Estes, M. K. (2014). Epidemiology of human noroviruses and updates on vaccine development. Current Opinion in Gastroenterology,30(1), 25–33.
66. Rodriguez-Lazaro, D., Cook, N., Ruggeri, F. M., Sellwood, J., Nasser, A., Nascimento, M. S., et al. (2012). Virus hazards from food, water and other contaminated environments. FEMS Microbiology Reviews,36(4), 786–814.
67. Scallan, E., Hoekstra, R. M., Angulo, F. J., Tauxe, R. V., Widdowson, M. A., Roy, S. L., et al. (2011). Foodborne illness acquired in the United States—major pathogens. Emerging Infectious Diseases,17(1), 7–15.
68. Seymour, I. J., & Appleton, H. (2001). Foodborne viruses and fresh produce. Journal of Applied Microbiology,91(5), 759–773.
69. Siebenga, J. J., Vennema, H., Duizer, E., & Koopmans, M. P. G. (2007). Gastroenteritis caused by norovirus GGII.4, the Netherlands, 1994–2005. Emerging Infectious Diseases,13(1), 144–146.
70. Slomka, M. J., & Appleton, H. (1998). Feline calicivirus as a model system for heat inactivation studies of small round structured viruses in shellfish. Epidemiology and Infection,121(2), 401–407.
71. Su, X., & D’Souza, D. H. (2012). Inactivation of human norovirus surrogates by benzalkonium chloride, potassium peroxymonosulfate, tannic acid, and gallic acid. Foodborne Pathogens and Disease,9(9), 829–834.
72. Teunis, P. F. M., Moe, C. L., Liu, P., Miller, S. E., Lindesmith, L., Baric, R. S., et al. (2008). Norwalk virus: How infectious is it? Journal of Medical Virology,80(8), 1468–1476.
73. Tuan Zainazor, C., Noor Hidayah, M. S., Chai, L. C., Tunung, R., Mohamad Ghazali, F., & Son, R. (2010). The scenario of norovirus contamination in food and food handlers. Journal of Microbiology and Biotechnology,20(2), 229–237.
74. Tung, G., Macinga, D., Arbogast, J., & Jaykus, L. A. (2013). Efficacy of commonly used disinfectants for inactivation of human noroviruses and their surrogates. Journal of Food Protection,76(7), 1210–1217.
75. Vimont, A., Fliss, I., & Jean, J. (2015). Study of the virucidal potential of organic peroxyacids against norovirus on food-contact surfaces. Food and Environmental Virology,7(1), 49–57.
76. Whitehead, K., & McCue, K. A. (2010). Virucidal efficacy of disinfectant actives against feline calicivirus, a surrogate for norovirus, in a short contact time. American Journal of Infection Control,38(1), 26–30.
77. Wobus, C. E., Thackray, L. B., & Virgin Iv, H. W. (2006). Murine norovirus: A model system to study norovirus biology and pathogenesis. Journal of Virology,80(11), 5104–5112.
78. Wutzler, P., & Sauerbrei, A. (2000). Virucidal efficacy of a combination of 0.2 % peracetic acid and 80 % (v/v) ethanol (PAA-ethanol) as a potential hand disinfectant. Journal of Hospital Infection,46(4), 304–308.