Virus inactivation on hard surfaces or in suspension by chemical disinfectants: Systematic review and meta-analysis of norovirus surrogates

Journal of Food Protection

Volumn 76, Issue 6, 2013, Pages 1006-1016

  Hoelzer, K ^a   Fanaselle, W ^a   Pouillot, R ^a   Van Doren, J M ^a   Dennis, S ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISINFECTANT AGENT;

ANIMAL; CALICIVIRUS INFECTION; CAT; COLIPHAGE; DISINFECTION; DRUG EFFECT; EQUIPMENT CONTAMINATION; GENETICS; HEPATITIS A VIRUS; HUMAN; META ANALYSIS; MOUSE; NOROVIRUS; REVIEW; SIGNAL NOISE RATIO; SUSPENSION; VESIVIRUS; VIROLOGY; VIRUS INACTIVATION;

ANIMALS; CALICIVIRIDAE INFECTIONS; CALICIVIRUS, FELINE; CATS; DISINFECTANTS; DISINFECTION; EQUIPMENT CONTAMINATION; HEPATITIS A VIRUS; HUMANS; LEVIVIRUS; MICE; NOROVIRUS; SIGNAL-TO-NOISE RATIO; SUSPENSIONS; VIRUS INACTIVATION;

FELINE CALICIVIRUS; HEPATITIS A VIRUS; MURINE NOROVIRUS 1; NOROVIRUS; VESIVIRUS;

EID: 84878825426     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-12-438     Document Type: Review

References (56)

1. Abad, F. X., R. M. Pinto, and A. Bosch. 1997. Disinfection of human enteric viruses on fomites. FEMS Microbiol. Lett. 156:107-111.
2. Ali, Y., M. J. Dolan, E. J. Fendler, and E. L. Larson. 2000. Alcohols, p. 229-254. In S. S. Block (ed.), Disinfection, sterilization, and preservation, 5th ed. Lippincott Williams & Wilkins, Philadelphia.
3. Belliot, G., A. Lavaux, D. Souihel, D. Agnello, and P. Pothier. 2008. Use of murine norovirus as a surrogate to evaluate resistance of human norovirus to disinfectants. Appl. Environ. Microbiol. 74: 3315-3318.
4. Bender, R., C. Bunce, M. Clarke, S. Gates, S. Lange, N. L. Pace, and K. Thorlund. 2008. Attention should be given to multiplicity issues in systematic reviews. J. Clin. Epidemiol. 61:857-865.
5. Borenstein, M., L. V. Hedges, J. P. T. Higgins, and H. R. Rothstein. 2009. Introduction to meta-analysis. John Wiley & Sons, Chichester, UK.
6. Cannon, J. L., E. Papafragkou, G. W. Park, J. Osborne, L. A. Jaykus, and J. Vinje. 2006. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J. Food Prot. 69:2761-2765.
7. Carrillo-Tripp, M., C. M. Shepherd, I. A. Borelli, S. Venkataraman, G. Lander, P. Natarajan, J. E. Johnson, C. L. Brooks III, and V. S. Reddy. 2009. VIPERdb2: an enhanced and web API enabled relational database for structural virology. Nucleic Acids Res. 37: D436-D442.
8. Centers for Disease Control and Prevention, Healthcare Infection Control Practices Advisory Committee. 2008. Guideline for disinfection and sterilization in healthcare facilities. Available at: http://www.cdc.gov/hicpac/Disinfection- Sterilization/acknowledg.html. Accessed September 2012.
9. Centers for Disease Control and Prevention, National Center for Immunization and. Respiratory Diseases, Division of Viral Diseases. 2011. Updated norovirus outbreak management and disease prevention guidelines. Morb. Mortal. Wkly. Rep. Recomm. Rep. 60:1-18. Available at: http://www.cdc.gov/mmwr/ preview/mmwrhtml/rr6003a1.htm. Accessed September 2012.
10. Cliver, D. O. 2009. Capsid and infectivity in virus detection. Food Environ. Virol. 1:123-128.
11. Davis, R., S. Zivanovic, D. H. D'Souza, and P. M. Davidson. 2012. Effectiveness of chitosan on the inactivation of enteric viral surrogates. Food Microbiol. 32:57-62.
12. D'Souza, D. H., and X. Su. 2010. Efficacy of chemical treatments against murine norovirus, feline calicivirus, and MS2 bacteriophage. Foodborne Pathog. Dis. 7:319-326.
13. D'Souza, D. H., X. Su, and F. Harte. 2011. Comparison of reduction in foodborne viral surrogates by high pressure homogenization. J. Food Prot. 74:1840-1846.
14. European Food Safety Authority. 2008. Assessment of the possible effect of the four antimicrobial treatment substances on the emergence of antimicrobial resistance. Scientific opinion of the Panel on Biological Hazards. EFSA J. 659:1-26.
15. Flint, S. J., L. W. Enquist, V. R. Racaniello, and A. M. Skalka. 2004. Principles of virology. ASM Press, Washington, DC.
16. Foster, G. A., and C. H. Goldsmith. 2006. Problems commonly associated with forest plots addressed using high resolution graphics in SAS®, paper 139-31. In K. J. LeBouton (ed.), Proceedings of the SAS Users Group International 31, San Francisco, 26 to 29 March 2006.
17. Fraisse, A., S. Temmam, N. Deboosere, L. Guillier, A. Delobel, P. Maris, M. Vialette, T. Morin, and S. Perelle. 2011. Comparison of chlorine and peroxyacetic-based disinfectant to inactivate feline calicivirus, murine norovirus and hepatitis A virus on lettuce. Int. J. Food Microbiol. 151:98-104.
18. Guerrero, C. A., and L. P. Moreno. 2012. Rotavirus receptor proteins Hsc70 and integrin alphabeta3 are located in the lipid microdomains of animal intestinal cells. Acta Virol. 56:63-70.
19. Hollinger, F. B., and J. R. Ticehurst. 1996. Hepatitis A virus, p. 735-790. In B. N. Fields, D. M. Knipe, P. M. Howley, R. M. Chanock, T. P. Monath, J. L. Melnick, B. Roizman, and S. E. Straus (ed.), Fields virology. Lippincott-Raven, Philadelphia.
20. Katpally, U., and T. J. Smith. 2010. The caliciviruses. Curr. Top. Microbiol. Immunol. 343:23-41.
21. Kim, S. W., S. B. Baek, J. H. Ha, M. H. Lee, C. Choi, and S. D. Ha. 2012. Chlorine treatment to inactivate norovirus on food contact surfaces. J. Food Prot. 75:184-188.
22. King, A. M. Q., M. J. Adams, E. B. Carstens, and E. J. Lefkowitz (ed.). 2012. Virus taxonomy: ninth report of the International Committee on Taxonomy of Viruses. Elsevier, San Diego, CA. Available at: http://ictvonline.org/index. asp?bhcp=1. Accessed September 2012.
23. Kong, M., X. G. Chen, K. Xing, and H. J. Park. 2010. Antimicrobial properties of chitosan and mode of action: a state of the art review. Int. J. Food Microbiol. 144:51-63.
24. MacCannell, T., C. A. Umscheid, R. K. Agarwal, I. Lee, G. Kuntz, K. B. Stevenson, and the Healthcare Infection Control Practices Advisory Committee. 2011. Guideline for the prevention and control of norovirus gastroenteritis outbreaks in healthcare settings. Infect. Control Hosp. Epidemiol. 32:939-969. Available at: http://www.cdc.gov/hicpac/pdf/norovirus/Norovirus-Guideline-2011. pdf./Accessed September 2012.
25. Macinga, D. R., S. A. Sattar, L. A. Jaykus, and J. W. Arbogast. 2008. Improved inactivation of nonenveloped enteric viruses and their surrogates by a novel alcohol-based hand sanitizer. Appl. Environ. Microbiol. 74:5047-5052.
26. Matthews, J. E., B. W. Dickey, R. D. Miller, J. R. Felzer, B. P. Dawson, A. S. Lee, J. J. Rocks, J. Kiel, J. S. Montes, C. L. Moe, J. N. Eisenberg, and J. S. Leon. 2012. The epidemiology of published norovirus outbreaks: a review of risk factors associated with attack rate and genogroup. Epidemiol. Infect. 140:1161-1172.
27. Mbithi, J. N., V. S. Springthorpe, and S. A. Sattar. 1993. Comparative in vivo efficiencies of hand-washing agents against hepatitis A virus (HM-175) and poliovirus type 1 (Sabin). Appl. Environ. Microbiol. 59:3463-3469.
28. Michen, B., and T. Graule. 2010. Isoelectric points of viruses. J. Appl. Microbiol. 109:388-397.
29. Morton, H. E. 1950. The relationship of concentration and germicidal efficiency of ethyl alcohol. Ann. N. Y. Acad. Sci. 53:191-196.
30. Ossiboff, R. J., and J. S. Parker. 2007. Identification of regions and residues in feline junctional adhesion molecule required for feline calicivirus binding and infection. J. Virol. 81:13608-13621.
31. Park, G. W., L. Barclay, D. Macinga, D. Charbonneau, C. A. Pettigrew, and J. Vinje. 2010. Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus, and GII.4 norovirus. J. Food Prot. 73:2232-2238.
32. Park, G. W., K. G. Linden, and M. D. Sobsey. 2011. Inactivation of murine norovirus, feline calicivirus and echovirus 12 as surrogates for human norovirus (NoV) and coliphage (Fz) MS2 by ultraviolet light (254 nm) and the effect of cell association on UV inactivation. Lett. Appl. Microbiol. 52:162-167.
33. Park, G. W., and M. D. Sobsey. 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 Pathog. Dis. 8:1005-1010.
34. Raafat, D., K. von Bargen, A. Haas, and H. G. Sahl. 2008. Insights into the mode of action of chitosan as an antibacterial compound. Appl. Environ. Microbiol. 74:3764-3773.
35. Rossmann, M. G., Y. He, and R. J. Kuhn. 2002. Picornavirus-receptor interactions. Trends Microbiol. 10:324-331.
36. Said, M. A., T. M. Perl, and C. L. Sears. 2008. Healthcare epidemiology: gastrointestinal flu: norovirus in health care and long-term care facilities. Clin. Infect. Dis. 47:1202-1208.
37. Sattar, S. A., M. Ali, and J. A. Tetro. 2011. In vivo comparison of two human norovirus surrogates for testing ethanol-based handrubs: the mouse chasing the cat! PLoS One 6:e17340.
38. Scallan, E., R. M. Hoekstra, F. J. Angulo, R. V. Tauxe, M. A. Widdowson, S. L. Roy, J. L. Jones, and P. M. Griffin. 2011. Foodborne illness acquired in the United States - major pathogens. Emerg. Infect. Dis. 17:7-15.
39. Schaffer, J. M., and F. W. Tilley. 1927. Further investigations of the relation between the chemical constitution and the germicidal activity of alcohols and phenols. J. Bacteriol. 14:259-273.
40. Solomon, E. B., V. Fino, J. Wei, and K. E. Kniel. 2009. Comparative susceptibilities of hepatitis A virus, feline calicivirus, bacteriophage MS2 and bacteriophage PhiX-174 to inactivation by quaternary ammonium and oxidative disinfectants. Int. J. Antimicrob. Agents 33:288-289.
41. Sterne, J. A., and M. Egger. 2001. Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J. Clin. Epidemiol. 54: 1046-1055.
42. Stuart, A. D., and T. D. Brown. 2006. Entry of feline calicivirus is dependent on clathrin-mediated endocytosis and acidification in endosomes. J. Virol. 80:7500-7509.
43. Su, X., and D. H. D'Souza. 2012. Inactivation of human norovirus surrogates by benzalkonium chloride, potassium peroxymonosulfate, tannic acid, and gallic acid. Foodborne Pathog. Dis. 9:829-834.
44. Su, X., S. Zivanovic, and D. H. D'Souza. 2009. Effect of chitosan on the infectivity of murine norovirus, feline calicivirus, and bacterio-phage MS2. J. Food Prot. 72:2623-2628.
45. Tan, M., and X. Jiang. 2010. Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog. 6:e1000983.
46. Taube, S., J. W. Perry, K. Yetming, S. P. Patel, H. Auble, L. Shu, H. F. Nawar, C. H. Lee, T. D. Connell, J. A. Shayman, and C. E. Wobus. 2009. Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noro-viruses. J. Virol. 83:4092-4101.
47. 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. 80:1468-1476.
48. Thompson, P., J. Lu, and G. G. Kaplan. 1998. The Cys-rich region of hepatitis A virus cellular receptor 1 is required for binding of hepatitis A virus and protective monoclonal antibody 190/4. J. Virol. 72:3751-3761.
49. Tilley, F. W., and J. M. Schaffer. 1926. Relation between the chemical constitution and germicidal activity of the monohydric alcohols and phenols. J. Bacteriol. 12:303-309.
50. Toropova, K., P. G. Stockley, and N. A. Ranson. 2011. Visualising a viral RNA genome poised for release from its receptor complex. J. Mol. Biol. 408:408-419.
51. U.S. Environmental Protection Agency, Antimicrobials Division. [no date]. Initial virucidal effectiveness test: using feline calicivirus as surrogate for norovirus. Available at: http://epa.gov/oppad001/pdf-files/initial-virucidal- test.pdf. Accessed September 2012.
52. U.S. Food and Drug Administration. 2000. Guidance for industry and FDA reviewers: content and format of premarket notification [510(k)] submissions for liquid chemical sterilants/high level disinfectants. Available at: http://www.fda.gov/medicaldevices/deviceregulationandguidance/guidancedocuments/ ucm073773.htm. Accessed September 2012.
53. U.S. Government Printing Office. 1989. Disinfection. 40 CFR 141.72. U.S. Government Printing Office, Washington, DC.
54. van Houwelingen, H. C., L. R. Arends, and T. Stijnen. 2002. Advanced methods in meta-analysis: multivariate approach and metaregression. Stat. Med. 21:589-624.
55. Vashist, S., D. Bailey, A. Putics, and I. Goodfellow. 2009. Model systems for the study of human norovirus biology. Future Virol. 4: 353-367.
56. Whitehead, K., and K. A. McCue. 2010. Virucidal efficacy of disinfectant actives against feline calicivirus, a surrogate for norovirus, in a short contact time. Am. J. Infect. Control 38:26-30.