Food and Environmental Virology

, Volume 10, Issue 3, pp 253–262 | Cite as

Persistence of Hepatitis A Virus in Fresh Produce and Production Environments, and the Effect of Disinfection Procedures: A Review

  • N. Cook
  • I. Bertrand
  • C. Gantzer
  • R. M. Pinto
  • A. Bosch
Review Paper


Although information is limited, it is evident that prolonged persistence of infectious Hepatitis A virus (HAV) is a factor in the transmission of the virus via fresh produce. Consequently, data on persistence of the virus on produce, and in environments relevant to production, such as soils, water and surfaces, are required to fully understand the dynamics of transmission of HAV via foods. Furthermore, information on effective disinfection procedures is necessary to implement effective post-harvest control measures. This review summarises current information on HAV persistence in fresh produce and on relevant disinfection procedures. On vegetables, HAV can remain infectious for several days; on frozen berries, it can persist for several months. HAV can remain infectious on surfaces for months, depending on temperature and relative humidity, and can survive desiccation. It can survive for several hours on hands. Washing hands can remove the virus, but further data are required on the appropriate procedure. Chlorination is effective in water, but not when HAV is associated with foodstuffs. Bleach and other sodium hypochlorite disinfectants at high concentrations can reduce HAV on surfaces, but are not suitable for use on fresh produce. There is only limited information on the effects of heating regimes used in the food industry on HAV. HAV is resistant to mild pasteurisation. Some food components, e.g. fats and sugars, can increase the virus’ resistance to higher temperatures. HAV is completely eliminated by boiling. Quantitative prevalence data are needed to allow the setting of appropriate disinfection log reduction targets for fresh produce.


Hepatitis A virus Persistence Removal Food Water Surfaces 



This work was funded by the United Kingdom Food Standards Agency (Project FS101074). The authors thank Jonathan Stein and Karyn Pinnock for assistance with literature acquisition.


  1. Abad, F. X., Pinto, R. M., & Bosch, A. (1994). Persistence of enteric viruses on environmental fomites. Applied & Environmental Microbiology, 60, 3704–3710.Google Scholar
  2. Abad, F. X., Pinto, R. M., & Bosch, A. (1997). Disinfection of human enteric viruses on fomites. FEMS Microbiology Letters, 156, 107–111.CrossRefPubMedGoogle Scholar
  3. Abad, F. X., Villena, C., Guix, S., Caballero, S., Pinto, R. M., & Bosch, A. (2001). Potential role of fomites in the vehicular transmission of human astroviruses. Applied & Environmental Microbiology, 67, 3904–3907.CrossRefGoogle Scholar
  4. Bae, J. E., Kim, J., Ahn, J., Choi, D. M., Jeong, H. S., Lee, D. H., & Kim, I. S. (2010). Virus inactivation processes for the manufacture of human acellular dermal matrix. Korean Journal of Microbiology & Biotechnology, 38, 168–176.Google Scholar
  5. Bertrand, I., Schijven, J. F., Sánchez, G., Wyn-Jones, P., Ottoson, J., Morin, T., Muscillo, M., Verani, M., Nasser, A., de Roda Husman, A. M., Myrmel, M., Sellwood, J., Cook, N., & Gantzer, C. (2012). The impact of temperature on the inactivation of enteric viruses in food and water: A review. Journal of Applied Microbiology, 112, 1059–1074.CrossRefPubMedGoogle Scholar
  6. Bidawid, S., Farber, J., & Sattar, S. (2001). Persistence of hepatitis A virus on modified atmosphere-packaged (MAP) lettuce. Food Microbiology, 18, 95–102.CrossRefGoogle Scholar
  7. Biziagos, E., Passagot, J., Crance, J., & Deloince, R. (1988). Long-term persistence of hepatitis A virus and poliovirus type 1 in mineral water. Applied and Environmental Microbiology, 54, 2705–2710.PubMedPubMedCentralGoogle Scholar
  8. Blanc, R., & Nasser, A. (1996). Effect of effluent quality and temperature on the persistence of viruses in soil. Water Science and Technology, 33, 237–242.CrossRefGoogle Scholar
  9. Bosch, A. (1995). The persistence of enteric viruses in the water environment. Microbiologia, 11, 393–396.PubMedGoogle Scholar
  10. Bozkurt, H., Ye, X., Harte, F., D’Souza, D. H., & Davidson, P. M. (2015). Thermal inactivation kinetics of hepatitis A virus in spinach. International Journal of Food Microbiology, 193, 147–151.CrossRefPubMedGoogle Scholar
  11. Butot, S., Putallaz, T., Amoroso, R., & Sanchez, G. (2009). Inactivation of enteric viruses in minimally processed berries and herbs. Applied & Environmental Microbiology, 75, 4155–4161.CrossRefGoogle Scholar
  12. Butot, S., Putallaz, T., & Sanchez, G. (2008). Effects of sanitation, freezing and frozen storage on enteric viruses in berries and herbs. International Journal of Food Microbiology, 126, 30–35.CrossRefPubMedGoogle Scholar
  13. CAC. (2012). Guidelines on the application of general principles of food hygiene to the control of viruses in food. CAC/GL, 79:-2012. Rome: Codex Alimentarius Commission.Google Scholar
  14. Casteel, M., Schmidt, C., & Sobsey, M. (2008). Chlorine disinfection of produce to inactivate hepatitis A virus and coliphage MS2. International Journal of Food Microbiology, 125, 267–273.CrossRefPubMedGoogle Scholar
  15. Collier, M. G., Khudyakov, Y. E., Selvage, D., Adams-Cameron, M., Epson, E., Cronquist, A., Jervis, R. H., Lamba, K., Kimura, A. C., Sowadsky, R., Hassan, R., Park, S. Y., Garza, E., Elliott, A. J., Rotstein, D. S., Beal, J., Kuntz, T., Lance, S. E., Dreisch, R., Wise, M. E., Nelson, N. P., Suryaprasad, A., Drobeniuc, J., Holmberg, S. D., Xu, F., & Hepatitis A Outbreak Investigation Team (2014). Outbreak of hepatitis A in the USA associated with frozen pomegranate arils imported from Turkey: An epidemiological case study. The Lancet Infectious Diseases, 14(10), 976–981.CrossRefPubMedGoogle Scholar
  16. Cook, N., Knight, A. K., & Richards, G. P. (2016). Persistence and elimination of human norovirus in food and on food contact surfaces: A critical review. Journal of Food Protection, 79, 1273–1294.CrossRefPubMedGoogle Scholar
  17. Croci, L., De Medici, D., Scalfaro, C., Fiore, A., & Toti, L. (2002). The persistence of hepatitis A virus in fresh produce. International Journal of Food Microbiology, 73, 29–34.CrossRefPubMedGoogle Scholar
  18. D’Andrea, L., Perez-Rodriguez, F. J., Costafreda, M. I., Beguiristain, N., Fuentes, C., Aymerich, T., Guix, S., Bosch, A., & Pinto, R. M. (2014). Molecular basis of the behavior of hepatitis a virus exposed to high hydrostatic pressure. Applied and Environmental Microbiology, 80, 6499–6505.CrossRefPubMedPubMedCentralGoogle Scholar
  19. de Paula, V. S., Gaspar, A., & Villar, L. (2010). Optimization of methods for detecting hepatitis A virus in food. Food and Environmental Virology, 2, 47–52.CrossRefGoogle Scholar
  20. Deboosere, N., Legeay, O., Caudrelier, Y., & Lange, M. (2004). Modelling effect of physical and chemical parameters on heat inactivation kinetics of hepatitis A virus in a fruit model system. International Journal of Food Microbiology, 93, 73–85.CrossRefPubMedGoogle Scholar
  21. Deboosere, N., Pinon, A., Delobel, A., Temmam, S., Morin, T., Merle, G., Blaise-Boisseau, S., Perelle, S., & Vialette, M. (2010). A predictive microbiology approach for thermal inactivation of hepatitis A virus in acidified berries. Food Microbiology, 27, 962–967.CrossRefPubMedGoogle Scholar
  22. Deng, M. Y., & Cliver, D. O. (1995). Persistence of inoculated hepatitis A virus in mixed human and animal wastes. Applied & Environmental Microbiology, 61, 87–91.Google Scholar
  23. Dentinger, C. M., Bower, W. A., Nainan, O. V., Cotter, S. M., Myers, G., Dubusky, L. M., Fowler, S., Salehi, E. D., & Bell, B. P. (2001). An outbreak of hepatitis A associated with green onions. The Journal of Infectious Diseases, 183, 1273–1276.CrossRefPubMedGoogle Scholar
  24. Fino, V. R., & Kniel, K. E. (2008). UV light inactivation of hepatitis A virus, Aichi virus, and feline calicivirus on strawberries, green onions, and lettuce. Journal of Food Protection, 71, 908–913.CrossRefPubMedGoogle Scholar
  25. Fiore, A. E. (2004). Hepatitis A transmitted by food. Clinical Infectious Diseases, 38, 705–715.CrossRefPubMedGoogle Scholar
  26. 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. International Journal of Food Microbiology, 151, 98–104.CrossRefPubMedGoogle Scholar
  27. Gerba, C. P., & Kennedy, D. (2007). Enteric virus persistence during household laundering and impact of disinfection with sodium hypochlorite. Applied & Environmental Microbiology, 73, 4425–4428.CrossRefGoogle Scholar
  28. Gerba, C. P., Pepper, I. L., & Whitehead, L. F. III (2002). A risk assessment of emerging pathogens of concern in the land application of biosolids. Water Science and Technology, 46, 225–230.CrossRefPubMedGoogle Scholar
  29. Hirneisen, K. A., & Kniel, K. E. (2013). Inactivation of internalised and surface contaminated enteric viruses in green onions. International Journal of Food Microbiology, 166, 201–206.CrossRefPubMedGoogle Scholar
  30. Hutin, Y. J. F., Pool, V., Cramer, E. H., Nainan, O. V., Weth, J., Williams, I. T., Goldstein, S. T., Gensheimer, K. F., Pell, B. P., Shapiro, C. N., Alter, M. J., & Margolis, S. (1999). A multistate, foodborne outbreak of hepatitis A. New England Journal of Medicine, 340, 595–602.CrossRefPubMedGoogle Scholar
  31. Jean, J., Morales-Rayas, R., Anoman, M.-N., & Lamhoujeb, S. (2011). Inactivation of hepatitis A virus and norovirus surrogate in suspension and on food-contact surfaces using pulsed UV light (pulsed light inactivation of food-borne viruses). Food Microbiology, 28, 568–572.CrossRefPubMedGoogle Scholar
  32. Jean, J., Vachon, J. F., Moroni, O., Darveau, A., Kukavica-Ibrulj, I., & Fliss, I. (2003). Effectiveness of commercial disinfectants for inactivating hepatitis A virus on agri-food surfaces. Journal of Food Protection, 66, 115–119.CrossRefPubMedGoogle Scholar
  33. Kim, S. J., Si, J., Lee, J. E., & Ko, G. (2012). Temperature and humidity influences on inactivation kinetics of enteric viruses on surfaces. Environmental Science and Technology, 46, 13303–13310.CrossRefPubMedGoogle Scholar
  34. Kingsley, D. H., Guan, D., & Hoover, D. G. (2005). Pressure inactivation of hepatitis A virus in strawberry puree and sliced green onions. Journal of Food Protection, 68, 1748–1751.CrossRefPubMedGoogle Scholar
  35. Kokkinos, P., Bouwknegt, M., Verhaelen, K., Willems, K., Moloney, R., de Roda Husman, A. M., D’Agostino, M., Cook, N., & Vantarakis, A. (2015). Virological fit-for-purpose risk assessment in a leafy green production Enterprise. Food Control, 51, 333–339.CrossRefGoogle Scholar
  36. Kokkinos, P., Kozyra, I., Lazic, S., Bouwknegt, M., Rutjes, S., Willems, K., Moloney, R., de Roda Husman, A. M., Kaupke, A., Legaki, E., D’Agostino, M., Cook, N., Rzeżutka, A., Petrovic, T., & Vantarakis, A. (2012). Harmonised investigation of occurrence of human enteric viruses in the leafy green vegetables supply chain in three European countries. Food and Environmental Virology, 4, 179–191.CrossRefPubMedGoogle Scholar
  37. Kokkinos, P., Kozyra, I., Lazic, S., Söderberg, K., Vasickova, P., Bouwknegt, M., Rutjes, S., Willems, K., Moloney, R., de Roda Husman, A. M., Kaupke, A., Legaki, E., D’Agostino, M., Cook, N., von Bonsdorff, C.-H., Rzeżutka, A., Petrovic, T., Maunula, K., Pavlik, I., & Vantarakis, A. (2017). Virological quality of irrigation water in leafy green vegetables and berry fruits production chains. Food and Environmental Virology, 9, 72–78.CrossRefPubMedGoogle Scholar
  38. Kramer, A., Galabov, A. S., Sattar, S. A., Doehner, L., Pivert, A., Payan, C., Wolff, M. H., Yilmaz, A., & Steinmann, J. (2006). Virucidal activity of a new hand disinfectant with reduced ethanol content: Comparison with other alcohol-based formulations. Journal of Hospital Infection, 62, 98–106.CrossRefPubMedGoogle Scholar
  39. Laird, D. T., Sun, Y., Reineke, K. F., & Shieh, Y. C. (2011). Effective hepatitis A virus inactivation during low-heat dehydration of contaminated green onions. Food Microbiology, 28, 998–1002.CrossRefPubMedGoogle Scholar
  40. Lee, S. J., Si, J., Yun, H. S., & Ko, G. (2015). Effect of temperature and relative humidity on the survival of foodborne viruses during food storage. Applied and Environmental Microbiology, 81, 2075–2081.CrossRefPubMedPubMedCentralGoogle Scholar
  41. Li, J. W., Xin, Z. T., Wang, X. W., Zheng, J. L., & Chao, F. H. (2002). Mechanisms of inactivation of hepatitis A virus by chlorine. Applied and Environmental Microbiology, 68, 4951–4955.CrossRefPubMedPubMedCentralGoogle Scholar
  42. Lu, Y., Joerger, R., & Wu, C. (2011). Study of the chemical composition and antimicrobial activities of ethanolic extracts from roots of Scutellaria baicalensis Georgi. Journal of Agricultural and Food Chemistry, 59, 10934–10942.CrossRefPubMedGoogle Scholar
  43. Martin, H., Soumet, C., Fresnel, R., Morin, T., Lamaudière, S., Le Sauvage, A. L., Deleurme, K., & Maris, P. J. (2013). Comparison of the virucidal efficiency of peracetic acid, potassium monopersulfate and sodium hypochlorite on hepatitis A and enteric cytopathogenic bovine orphan virus. Applied Microbiology, 115, 955–968.Google Scholar
  44. Mbithi, J. N., Springthorpe, V. S., Boulet, J. R., & Satter, S. A. (1992). Persistence of hepatitis A virus on human hands and its transfer on contact with animate and inanimate surfaces. Journal of Clinical Microbiology, 30, 757–763.PubMedPubMedCentralGoogle Scholar
  45. Mbithi, J. N., Springthorpe, V. S., & Sattar, S. A. (1990). Chemical disinfection of hepatitis A virus on environmental surfaces. Applied and Environmental Microbiology, 56, 3601–3604.PubMedPubMedCentralGoogle Scholar
  46. Mbithi, J. N., Springthorpe, V. S., & Sattar, S. A. (1991). Effect of relative humidity and air temperature on persistence of hepatitis A virus on environmental surfaces. Applied and Environmental Microbiology, 57, 1394–1399.PubMedPubMedCentralGoogle Scholar
  47. Mbithi, J. N., Springthorpe, V. S., & Sattar, S. A. (1993). Comparative in vivo efficiencies of hand-washing agents against hepatitis A virus (HM-175) and poliovirus type 1 (Sabin). Applied and Environmental Microbiology, 59, 3463–3469.PubMedPubMedCentralGoogle Scholar
  48. McCaustland, K. A., Bond, W. W., Bradley, D. W., Ebert, J. W., & Maynard, J. E. (1982). Persistence of hepatitis A virus in faeces after drying and storage for 1 month. Journal of Clinical Microbiology, 16, 957–958.PubMedPubMedCentralGoogle Scholar
  49. Millard, J., Appleton, H., & Parry, J. V. (1987). Studies on heat inactivation of hepatitis A virus with special reference to shellfish. Epidemiology and Infection, 98, 397–414.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nguyen-The, C. (2012). Biological hazards in processed fruits and vegetables—risk factors and impact of processing techniques. LWT Food Science and Technology, 49, 172–177.CrossRefGoogle Scholar
  51. Park, S. Y., Kim, A. N., Lee, K. H., & Ha, S. D. (2015) Ultraviolet-C efficacy against a norovirus surrogate and hepatitis A virus on a stainless steel surface. International Journal of Food Microbiology, 211, 73–78.CrossRefPubMedGoogle Scholar
  52. Parry, J. V., & Mortimer, P. P. (1984). The heat sensitivity of hepatitis A virus determined by a simple tissue culture method. Journal of Medical Virology, 14, 277–284.CrossRefPubMedGoogle Scholar
  53. Pintó, R., Costafreda, M., Perez-Rodriguez, F., D’Andrea, L., & Bosch, A. (2010). Hepatitis A virus: State of the art. Food and Environmental Virology, 2, 127–135.CrossRefGoogle Scholar
  54. Randazzo, W., Falcó, I., Aznar, R., & Sánchez, G. (2017). Effect of green tea extract on enteric viruses and its application as natural sanitizer. Food Microbiology, 66, 150–156.CrossRefPubMedGoogle Scholar
  55. Roberts, P., & Hope, A. (2003). Virus inactivation by high intensity broad spectrum pulsed light. Journal of Virological Methods, 110, 61–65.CrossRefPubMedGoogle Scholar
  56. Rzeżutka, A., & Cook, N. (2004). Survival of human enteric viruses in the environment and food. FEMS Microbiology Reviews, 28, 441–453.CrossRefPubMedGoogle Scholar
  57. Sabbah, S., Springthorpe, S., & Sattar, S. A. (2010). Use of a mixture of surrogates for infectious bioagents in a standard approach to assessing disinfection of environmental surfaces. Applied & Environmental Microbiology, 76, 6020–6022.CrossRefGoogle Scholar
  58. Scholz, E., Heinricy, U., & Flehmig, B. (1989). Acid stability of hepatitis A virus. Journal of General Virology, 70, 2481–2486.CrossRefPubMedGoogle Scholar
  59. Sewlikar, S., & D’Souza, D. H. (2017). Survival of hepatitis A virus and Aichi virus in cranberry-based juices at refrigeration (4 °C). Food Microbiology, 62, 251–255.CrossRefPubMedGoogle Scholar
  60. Seymour, I. J., & Appleton, H. (2001). Foodborne viruses and fresh produce. Journal of Applied Microbiology, 91, 759–773.CrossRefPubMedGoogle Scholar
  61. Shieh, Y., Stewart, D., & Laird, D. (2009). Persistence of hepatitis A virus in spinach during low temperature storage. Journal of Food Protection, 72, 2390–2393.CrossRefPubMedGoogle Scholar
  62. Siegl, G., Weitz, M., & Kronaure, G. (1984). Stability of hepatitis A virus. Intervirology, 22, 218–226.CrossRefPubMedGoogle Scholar
  63. Sobsey, M. D., Shields, P. A., Hauchman, F. S., Davies, A. L., Rullman, V. A., & Bosch, A., Zuckerman, A. J., ed (1988). Persistence and persistence of hepatitis A virus in environmental samples. In Viral hepatitis and liver disease (pp. 121–124). New York: Alan R. Liss, Inc.Google Scholar
  64. Sobsey, M. D., Shields, P. A., Hauchman, F. S., Hazard, R. L., & Caton, L. W. (1986). Persistence and transport of hepatitis A virus in soils, groundwater and wastewater. Water Science and Technology, 10, 97–106.CrossRefGoogle Scholar
  65. Solomon, E. B., Fino, V., Wei, J., & Kniel, K. E. (2009). Comparative susceptibilities of hepatitis A virus, feline calicivirus, bacteriophage MS2 and bacteriophage PhiX-174 to inactivation by quaternary ammonium and oxidative disinfectants. International Journal of Antimicrobial Agents, 33, 288–289.CrossRefPubMedGoogle Scholar
  66. Stine, S., Song, I., Choi, C., & Gerba, C. (2005). Effect of relative humidity on preharvest persistence of bacterial and viral pathogens on the surface of cantaloupe, lettuce, and bell peppers. Journal of Food Protection, 68, 1352–1358.CrossRefPubMedGoogle Scholar
  67. Su, X., & D’Souza, D. H. (2013). Grape seed extract for foodborne virus reduction on produce. Food Microbiology, 34, 1–6.CrossRefPubMedGoogle Scholar
  68. Sun, Y., Laird, D., & Shieh, Y. (2012). Temperature-dependent persistence of hepatitis A virus during storage of contaminated onions. Applied and Environmental Microbiology, 78, 4976–4983.CrossRefPubMedPubMedCentralGoogle Scholar
  69. Takahashi, M., Okakura, Y., Takahashi, H., Imamura, M., Takeuchi, A., Shidara, H., Kuda, T., & Kimura, B. (2017). Heat-denatured lysozyme could be a novel disinfectant for reducing hepatitis A virus and murine norovirus on berry fruit. International Journal of Food Microbiology, 266, 104–108.CrossRefPubMedGoogle Scholar
  70. Terio, V., Bottaro, M., Di Pinto, A., Catella, C., Chironna, M., Bozzo, G., Kingsley, D. H., Bonerba, E., Morea, A., & Martella, V. (2015). Outbreak of hepatitis A in Italy associated with frozen red currants imported from Poland: A case study. Food and Environmental Virology, 7, 305–308.CrossRefPubMedGoogle Scholar
  71. Terpstra, F. G., van den Blink, A. E., Bos, L. M., Boots, A. G. C., Brinkhuis, F. H. M., Gijsen, E., van Remmerden, Y., Schuitemaker, H. & van ‘t Wout, A. B. (2007). Resistance of surface-dried virus to common disinfection procedures. Journal of Hospital Infection, 66, 332–338.CrossRefPubMedGoogle Scholar
  72. Wang, Q., Hirneisen, K. A., Markland, S. M., & Kniel, K. E. (2013). Persistence of murine norovirus, Tulane virus, and hepatitis A virus on alfalfa seeds and sprouts during storage and germination. Applied and Environmental Microbiology, 79, 7021–7027.CrossRefPubMedPubMedCentralGoogle Scholar
  73. Wolff, M. H., Schmitt, J., Rahaus, M., & Koenig, A. (2001). Hepatitis A virus: A test method for virucidal activity. Journal of Hospital Infection, 48, S18–S22.Google Scholar

Copyright information

© Crown 2018

Authors and Affiliations

  • N. Cook
    • 1
    • 2
  • I. Bertrand
    • 3
    • 4
    • 5
  • C. Gantzer
    • 3
    • 4
    • 5
  • R. M. Pinto
    • 6
  • A. Bosch
    • 6
  1. 1.Food and Environment Research AgencyYorkUK
  2. 2.Jorvik Food and Environmental Virology Ltd.YorkUK
  3. 3.Université de Lorraine, LCPME (Laboratoire de Chimie Physique et Microbiologie pour l’Environnement), UMR 7564, Faculté de PharmacieNancyFrance
  4. 4.CNRS, LCPME, UMR 7564NancyFrance
  5. 5.Institut Jean BarriolUniversité de Lorraine, Faculté des Sciences et TechnologiesVandœuvre-lès-NancyFrance
  6. 6.University of BarcelonaBarcelonaSpain

Personalised recommendations