Abstract
The human health impact of foodborne viral infections can be substantial. General difficulties in recovering and identifying viruses from foods and clinical specimens collected during foodborne outbreaks grossly underestimate the true role of viruses as foodborne pathogens, reinforcing the need for proper inactivation of viruses before the food is consumed. Along with Hepatitis A virus (HAV), human noroviruses (HuNoV) have now emerged as the most frequent cause of foodborne outbreaks of acute non-bacterial gastroenteritis. The other foodborne pathogen of emerging concern is hepatitis E virus. This chapter focuses on the testing and application of microbicidal chemicals (disinfectants and hand hygiene agents) to inactivate viruses on inanimate and animate food contact surfaces as well as for the decontamination of foods consumed raw or with minimal processing.
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References
Abad FX, Pinto RM, Bosch A (1997) Disinfection of human enteric viruses on fomites. FEMS Microbiol Lett 156:107–111
Ansari SA, Sattar SA (2002) The need and methods for assessing the activity of topical agents against viruses. In: Paulson D (ed) Handbook of topical antimicrobials: industrial applications in consumer products and pharmaceuticals. Marcel Dekker, New York, pp 411–445
Ansari SA, Sattar SA, Springthorpe VS, Wells GA, Tostowaryk W (1988) Rotavirus survival on human hands and transfer of infectious virus to animate and non-porous inanimate surfaces. J Clin Microbiol 26:1513–1518
Ansari SA, Sattar SA, Springthorpe VS, Wells GA, Tostowaryk W (1989) In vivo protocol for testing efficacy of hand-washing agents against viruses and bacteria: Experiments with rotavirus and Escherichia coli. Appl Environ Microbiol 55:3113–3118
Ansari SA, Springthorpe VS, Sattar SA (1991) Comparison of cloth-, paper- and warm air-drying in eliminating viruses and bacteria from washed hands. Am J Infect Control 19:243–249
Bae JY, Lee JS, Shin MH, Lee SH, Hwang IG (2011) Effect of wash treatments on reducing human norovirus on iceberg lettuce and perilla leaf. J Food Prot 74:1908–1911
Baert L, Uyttendaele M, Stals A, Van Coillie E, Dierick K, Debevere J, Botteldoorn N (2009a) Review article; reported foodborne outbreaks due to noroviruses in Belgium: the link between food and patient investigations in an international context. Epidemiol Infect 137:316–325
Baert L, Vandekinderen I, Devlieghere F, Van Coillie E, Debevere J, Uyttendaele M (2009b) Efficacy of sodium hypochlorite and peroxyacetic acid to reduce murine norovirus 1, B40-8, Listeria monocytogenes, and Escherichia coli O157:H7 on shredded iceberg lettuce and in residual wash water. J Food Prot 72:1047–1054
Bentley K, Dove BK, Parks SR, Walker JT, Bennett AM (2012) Hydrogen peroxide vapour decontamination of surfaces artificially contaminated with norovirus surrogate feline calicivirus. J Hosp Infect 80:116–121
Beuchat LR (2001) Surface decontamination of fruit and vegetables eaten raw: a review. Document No. WHO/FSF/FOS/98.2, World Health Organization, Geneva
Bidawid S (2013) Preventing and controlling viral contamination of fresh produce. In: Cook N (ed) Viruses in food and water: risks, surveillance and control. Woodhead Publishing Ltd., Cambridge, pp 261–273
Bidawid S, Farber JM, Sattar SA (2000) Contamination of foods by food handlers: experiments on hepatitis A virus transfer to food and its interruption. Appl Environ Microbiol 66:2759–2763
Bidawid S, Malik N, Adegbunrin O, Sattar SA, Farber JM (2003) A feline kidney cell line-based plaque assay for feline calicivirus, a surrogate for Norwalk virus. J Virol Methods 107:163–167
Bidawid S, Malik N, Adegbunrin O, Sattar SA, Farber JM (2004) Norovirus cross-contamination during food handling and interruption of virus transfer by hand antisepsis: experiments with feline calicivirus as a surrogate. J Food Protect 67:103–109
Bosch A, Bidawid S, Le Guyader S, Lees D, Jaykus LA (2011) Norovirus, hepatitis A virus, and indicator microorganisms in shellfish, soft fruits and water. In: Hoorfar J (ed) Rapid detection, characterization and enumeration of foodborne pathogens. ASM Press, Washington, pp 333–347
Bresee JS, Widdowson MA, Monroe SS, Glass RI (2002) Foodborne viral gastroenteritis: challenges and opportunities. Clin Infect Dis 35:748–753
Butot S, Putallaz T, Sánchez G (2008) Effects of sanitation, freezing and frozen storage on enteric viruses in berries and herbs. Int J Food Microbiol 126:30–35
Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinjé J (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
Casteel MJ, Schmidt CE, Sobsey MD (2008) Chlorine disinfection of produce to inactivate hepatitis A virus and coliphage MS2. Int J Food Microbiol 125:267–273
Casteel MJ, Schmidt CE, Sobsey MD (2009) Chlorine inactivation of coliphage MS2 on strawberries by industrial-scale water washing units. J Water Health 7:244–250
D’Souza DH, Su X (2010) Efficacy of chemical treatments against murine norovirus, feline calicivirus, and MS2 bacteriophage. Foodborne Pathog Dis 7:319–326
D’Souza DH, Sair A, Williams K, Papafragkou E, Jean J, Moore C, Jaykus L (2006) Persistence of caliciviruses on environmental surfaces and their transfer to food. Int J Food Microbiol 108:84–91
Doultree JC, Druce JD, Birch CJ, Bowden DS, Marshall JA (1999) Inactivation of feline calicivirus - a Norwalk virus surrogate. J Hosp Infect 41:51–57
U.S. Environmental Protection Agency (2012) Product performance test guidelines OCSPP 810.2200: disinfectants for use on hard surfaces - efficacy data recommendations. http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPPT-2009-0150-0021. Accessed on 29 July 2015
Escudero BI, Rawsthorne H, Gensel C, Jaykus LA (2012) Persistence and transferability of noroviruses on and between common surfaces and foods. J Food Prot 75:927–935
Feliciano L, Li J, Lee J, Pascall MA (2012) Efficacies of sodium hypochlorite and quaternary ammonium sanitizers for reduction of norovirus and selected bacteria during ware-washing operations. PLoS One 7, e50273
Fraisse A, Temmam S, Deboosere N, Guillier L, Delobel A, Maris P, Vialette M, Morin T, Perelle S (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
Girard M, Ngazoa S, Mattison K, Jean J (2010) Attachment of noroviruses to stainless steel and their inactivation, using household disinfectants. J Food Prot 73:400–404
Glass RI, Parashar UD, Estes MK (2009) Norovirus gastroenteritis. N Engl J Med 361:1776–1785
Gulati BR, Allwood PB, Hedberg CW, Goyal SM (2001) Efficacy of commonly used disinfectants for the inactivation of calicivirus on strawberry, lettuce, and a food-contact surface. J Food Prot 64:1430–1434
Health Canada (2007) Guidance document on disinfectant drugs. http://hc-sc.gc.ca/dhp-mps/alt_formats/hpfb-dgpsa/pdf/prodpharma/disinf_desinf-eng.pdf. Accessed on 05 Dec 2013
Health Canada (2009) Guidance document on human-use antiseptic drugs. http://www.hc-sc.gc.ca/dhp-mps/alt_formats/pdf/prodpharma/applic-demande/guide-ld/antiseptic_guide_ld-eng.pdf. Accessed on 5 Dec 2013
Hirneisen KA, Markland SM, Kniel KE (2011) Ozone inactivation of norovirus surrogates on fresh produce. J Food Prot 74:836–839
ASTM International (2010) Standard test method for determining the virus-eliminating effectiveness of hygienic handwash and handrub agents using the fingerpads of adults. Document #E1838. ASTM, West Conshohocken
ASTM International (2011a) Standard test method to assess the activity of microbicides against viruses in suspension. Document #E1052. ASTM, West Conshohocken
ASTM International (2011b) Standard test method to assess virucidal activity of chemicals intended for disinfection of inanimate, nonporous environmental surfaces. Document #E1053. ASTM, West Conshohocken
ASTM International (2011c) Standard quantitative disk carrier test method for determining the bactericidal, virucidal, fungicidal, mycobactericidal and sporicidal activities of liquid chemical germicides. Document #E2197, ASTM, West Conshohocken
ASTM International (2012) Standard practice for use of gel filtration columns for cytotoxicity reduction and neutralization. Document # E1482. ASTM, West Conshohocken
ASTM International (2013) Standard test method for evaluation of hygienic handwash and handrub formulations for virus-eliminating activity using the entire hand. Document # E2011. ASTM, West Conshohocken
Kim SW, Baek SB, Ha JH, Lee MH, Choi C, Ha SD (2012) Chlorine treatment to inactivate norovirus on food contact surfaces. J Food Prot 75:184–188
Koopmans M, von Bonsdorff CH, Vinje J, de Medici D, Monroe S (2002) Foodborne viruses. FEMS Microbiol Rev 26:187–205
Lages SL, Ramakrishnan MA, Goyal SM (2008) In-vivo efficacy of hand sanitizers against feline calicivirus: a surrogate for norovirus. J Hosp Infect 68:159–163
Lim MY, Kim JM, Ko G (2010) Disinfection kinetics of murine norovirus using chlorine and chlorine dioxide. Water Res 44:3243–3251
Liu P, Yuen Y, Hsiao HM, Jaykus LA, Moe C (2010) Effectiveness of liquid soap and hand sanitizer against Norwalk virus on contaminated hands. Appl Environ Microbiol 76:394–399
Lloyd-Evans N, Springthorpe VS, Sattar SA (1986) Chemical disinfection of human rotavirus-contaminated inanimate surfaces. J Hyg 97:163–173
Maillard J-Y, Sattar SA, Pinto F (2013) Virucidal activity of microbicides. In: Fraise A, Maillard J-Y, Sattar SA (eds) Principles and practice of disinfection, preservation & sterilization, 5th edn. Wiley-Interscience, Oxford, pp 178–207
Mattison K, Karthikeyan K, Abebe M, Malik N, Sattar SA, Farber JM, Bidawid S (2007) Survival of calicivirus in foods and on surfaces: experiments with feline calicivirus as a surrogate for norovirus. J Food Prot 70:500–503
Mbithi JN, Springthorpe VS, Sattar SA (1990) Chemical disinfection of hepatitis A virus on environmental surfaces. Appl Environ Microbiol 56:3601–3604
Mbithi JN, Springthorpe VS, Sattar SA (1991) The effect of relative humidity and air temperature on the survival of hepatitis A virus on environmental surfaces. Appl Environ Microbiol 57:1394–1399
Mbithi JN, Springthorpe VS, Boulet JR, Sattar SA (1992) Survival of hepatitis A virus on human hands and its transfer on contact with animate and inanimate surfaces. J Clin Microbiol 30:757–763
Mbithi JN, Springthorpe VS, Sattar SA (1993) Comparative in vivo efficiency of hand-washing agents against hepatitis A virus (HM-175) & poliovirus type 1 (Sabin). Appl Environ Microbiol 59:3463–3469
Miyashita K, Kang JH, Saga A, Takahashi K, Shimamura T, Yasumoto A, Fukushima H, Sogabe S, Konishi K, Uchida T, Fu**aga A, Matsui T, Sakurai Y, Tsuji K, Maguchi H, Taniguchi M, Abe N, Fazle Akbar SM, Arai M, Mishiro S (2012) Three cases of acute or fulminant hepatitis E caused by ingestion of pork meat and entrails in Hokkaido, Japan: zoonotic food-borne transmission of hepatitis E virus and public health concerns. Hepatol Res 42:870–878
Mundel T, Orenstein WA (2013) No country is safe without global eradication of poliomyelitis. N Engl J Med 369:2045–2046
Organization for Economic Cooperation and Development (OECD) (2013) Guidance document on quantitative methods for evaluating the activity of microbicides used on hard non-porous surfaces. Document # No. 187, JT03342231; ENV/JM/MONO (2013)11. OECD, Paris
Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, Griffin PM (2013) Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998–2008. Emerg Infect Dis 19:407–415
Park GW, Barclay L, Macinga D, Charbonneau D, Pettigrew CA, Vinjé J (2010) Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus, and GII.4 norovirus. J Food Prot 73:2232–2238
Ramia S, Sattar SA (1980) The role of trypsin in plaque formation by simian rotavirus SA-ll. Can J Comp Med 44:433–439
Sair AI, D’Souza DH, Jaykus LA (2002) Human enteric viruses as causes of foodborne disease. Comp Rev Food Sci Technol 1:73–89
Sattar SA (2006) Allen Denver Russell Memorial Lecture. The use of microbiocides in infection control: a critical look at safety, testing & applications. J Appl Microbiol 101:743–753
Sattar SA (2007) Hierarchy of susceptibility of viruses to environmental surface disinfectants: a predictor of activity against new & emerging viral pathogens. J AOAC Int 90:1655–1658
Sattar SA, Ansari SA (2002) The fingerpad protocol to assess hygienic hand antiseptics against viruses. J Virol Methods 103:171–181
Sattar SA, Bidawid S (2001) Environmental considerations in preventing the foodborne spread of hepatitis A. In: Hui YH, Sattar SA, Murrell KD, Nip WK, Stanfield PS (eds) Foodborne disease handbook. Marcel Dekker, New York, pp 205–216
Sattar SA, Springthorpe VS (1996) Transmission of viral infections through animate and inanimate surfaces and infection control through chemical disinfection. In: Hurst CJ (ed) Modeling disease transmission and its prevention by disinfection. Cambridge University Press, New York, pp 224–257
Sattar SA, Springthorpe VS (1999) Viricidal activity of biocides - activity against human viruses. In: Russell AD, Hugo WB, Ayliffe GAJ (eds) Principles and practice of disinfection, preservation and sterilization, 3rd edn. Blackwell, London, pp 168–186
Sattar SA, Springthorpe VS (2001a) Methods for testing the virucidal activity of chemicals. In: Block SS (ed) Disinfection, sterilization and preservation, 5th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1391–1412
Sattar SA, Springthorpe VS (2001b) New methods for efficacy testing of disinfectants and antiseptics. In: Rutala WA (ed) Disinfection, sterilization, and antisepsis: principles and practices in healthcare facilities. Association of Professionals in Infection Control (APIC), Washington, pp 173–186
Sattar SA, Tetro J (2001) Other foodborne viruses. In: Hui YH, Sattar SA, Murrell KD, Nip W-K, Stanfield PS (eds) Foodborne disease handbook. Marcel Dekker, New York, pp 127–136
Sattar SA, Raphael RA, Lochnan H, Springthorpe VS (1983) Rotavirus inactivation by chemical disinfectants and antiseptics used in hospitals. Can J Microbiol 29:1464–1469
Sattar SA, Lloyd-Evans N, Springthorpe VS, Nair RC (1986) Institutional outbreaks of rotavirus diarrhea: potential role of fomites and environmental surfaces as vehicles for virus spread. J Hyg 96:277–289
Sattar SA, Jacobsen H, Rahman H, Rubino J, Cusack T (1994) Interruption of rotavirus spread through chemical disinfection. Infect Control Hosp Epidemiol 15:751–756
Sattar SA, Abebe M, Bueti A, Jampani H, Newman J (2000a) Activity of an alcohol-based hand gel against human adeno-, rhino-, and rotaviruses using the fingerpad method. Infect Control Hosp Epidemiol 21:516–519
Sattar SA, Tetro J, Bidawid S, Farber J (2000b) Foodborne spread of hepatitis A: recent studies on virus survival, transfer and inactivation. Can J Infect Dis 11:159–163
Sattar SA, Springthorpe VS, Tetro J (2001) Rotavirus. In: Hui YH, Sattar SA, Murrell KD, Nip W-K, Stanfield PS (eds) Foodborne disease handbook. Marcel Dekker, Inc., New York, pp 99–125
Sattar SA, Springthorpe VS, Tetro J, Vashon B, Keswick B (2002) Hygienic hand antiseptics: should they not have activity and label claims against viruses? Am J Infect Control 30:355–372
Sattar S, Springthorpe VS, Adegbunrin O, Zafer AA, Busa M (2003) A disc-based quantitative carrier test method to assess the virucidal activity of chemical microbicides. J Virol Methods 112:3–12
Sattar SA, Ali M, Tetro J (2011) In vivo comparison of two human norovirus surrogates for testing ethanol-based handrubs: the mouse chasing the cat! PLoS One 6(2):1–6
Scallan ER, Hoekstra RM, Angulo FJ, Tauxi RV, Widdowson MA, Roy SL, Jones JL, Griffin PM (2011) Foodborne illness acquired in the United States- major pathogens. Emerg Infect Dis 17:7–15
Seo K, Lee JE, Lim MY, Ko G (2012) Effect of temperature, pH, and NaCl on the inactivation kinetics of murine norovirus. J Food Prot 75:533–540
Seymour IJ, Appleton H (2001) Foodborne viruses and fresh produce. J Appl Microbiol 91:759–779
Sharps CP, Kotwal G, Cannon JL (2012) Human norovirus transfer to stainless steel and small fruits during handling. J Food Prot 75:1437–1446
Solomon EB, Fino V, Wei J, Kniel KE (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 33:288–2899
Springthorpe VS, Sattar SA (2003) Quantitative carrier tests to assess the germicidal activities of chemicals: rationales and procedures. Centre for Research on Environmental Microbiology (CREM), University of Ottawa, Ottawa. Available from: QCTmanual@webbertraining.com. ISBN 0-88927-298-0
Springthorpe VS, Sattar SA (2005) Carrier tests to assess microbicidal activities of chemical disinfectants for use on medical devices and environmental surfaces. J AOAC Int 88:182–201
Springthorpe VS, Grenier JL, Lloyd-Evans N, Sattar SA (1986) Chemical disinfection of human rotaviruses; efficacy of commercially available products in suspension test. J Hyg 97:139–161
Stals A, Uyttendaele M, Baert L, Van Coillie E (2013) Norovirus transfer between food contact material. J Food Prot 76:1202–1209
Sutton SVW (1996) Neutralizer evaluations as control experiments for antimicrobial efficacy tests. In: Ascenzi JM (ed) Handbook of disinfectants and antiseptics. Marcel Dekker, New York, pp 43–62
Traoré O, Springthorpe VS, Sattar SA (2002) A quantitative study of the survival of two species of Candida on porous and non-porous environmental surfaces and hands. J Appl Microbiol 92:549–555
Tung G, Macinga D, Arbogast J, Jaykus LA (2013) Efficacy of commonly used disinfectants for inactivation of human noroviruses and their surrogates. J Food Prot 76:1210–1217
Verhoef L, Koopmans M, Van Pelt W, Duizer E, Haagsma J, Werber D, Van Asten L, Havelaar A (2013) The estimate of disease burden of norovirus in The Netherlands. Epidemiol Infect 141:496–506
Ward RL, Bernstein DI, Knowlton DR, Sherwood JR, Young EC, Cusack TM, Rubino JR, Schiff GM (1991) Prevention of surface-to-human transmission of rotavirus by treatment with disinfectant spray. J Clin Microbiol 29:1991–1996
Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, Belliot G, Krug A, Mackenzie JM, Green KY, Virgin HW (2004) Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2(12)
Woolwine JD, Gerberding JL (1995) Effect of testing method on apparent activities of antiviral disinfectants and antiseptics. Antimicrob Agents Chemother 39:921–923
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Sattar, S.A., Bidawid, S. (2016). Using Microbicidal Chemicals to Interrupt the Spread of Foodborne Viruses. In: Goyal, S., Cannon, J. (eds) Viruses in Foods. Food Microbiology and Food Safety(). Springer, Cham. https://doi.org/10.1007/978-3-319-30723-7_14
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