1932

Abstract

Foodborne outbreaks of viral origin have become increasingly a serious public health concern. High-pressure processing (HPP), a nonthermal technology, has come to the forefront for food processing given its minimal effects on food quality. Recent studies have revealed encouraging results for the inactivation of several human viruses by HPP. This review provides comprehensive information on the use of HPP to eliminate viruses in model systems and foods. We address the influences of various parameters, including pressure level, holding time, pH, temperature, and food matrix on the efficacy of pressure inactivation of viruses, as well as insight into the mechanisms for inactivation of enveloped and nonenveloped viruses. HPP is a promising technology for mitigating virus contamination of foods, thus it is essential to identify the optimal parameters for enhancing virus inactivation while ensuring sensory and nutritional quality retention of foods.

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2015-04-10
2024-03-28
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Literature Cited

  1. Atreya CD. 2004. Major foodborne illness causing viruses and current status of vaccines against the diseases. Foodborne Pathog. Dis. 1:89–96 [Google Scholar]
  2. Baert L, Debevere J, Uyttendaele M. 2009. The efficacy of preservation methods to inactivate foodborne viruses. Int. J. Food Microbiol. 131:83–94 [Google Scholar]
  3. Balasubramaniam VM, Farkas D, Turek EJ. 2008. Preserving foods through high-pressure processing. Food Technol. 62:32–38 [Google Scholar]
  4. Balny C, Masson P, Heremans K. 2002. High pressure effects on biological macromolecules: from structural changes to alteration of cellular processes. Biochim. Biophys. Acta 1595:3–10 [Google Scholar]
  5. Barry-Murphy KGJ, Brown DWG, Cheesbrough JS, Hoffman PN. 2000. Norwalk-like viruses—investigation of patterns of environmental contamination on a hospital ward and evaluation of decontamination procedures Presented at Public Health Leadersh. Soc. Annu. Sci. Conf., 25th, New Orleans, La.
  6. Basset JGA, Macheboeuf M, Manil P. 1938. Action of high pressure on plant viruses. Proc. Soc. Exp. Biol. Med. 38:248–51 [Google Scholar]
  7. 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. 66:2759–63 [Google Scholar]
  8. Buckow R, Isbarn S, Knorr D, Heinz V, Lehmacher A. 2008. Predictive model for inactivation of feline calicivirus, a norovirus surrogate, by heat and high hydrostatic pressure. Appl. Environ. Microbiol. 74:1030–38 [Google Scholar]
  9. Calci KR, Meade GK, Tezloff RC, Kingsley DH. 2005. High-pressure inactivation of hepatitis A virus within oysters. Appl. Environ. Microbiol. 71:339–43 [Google Scholar]
  10. 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. 69:2761–65 [Google Scholar]
  11. Cascarino J. 2007. Inactivation of viruses by high hydrostatic pressure in ready-to-eat food products MS thesis., Univ. Del., Newark, Del.
  12. Centers for Disease Control and Prevention 2003. Norovirus activity—United States, 2002. MMWR Weekly Jan. 24. http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5203a1.htm
  13. Centers for Disease Control and Prevention 2011. Updated norovirus outbreak management and disease prevention guidelines. MMWR Weekly Mar. 4. http://www.cdc.gov/mmwr/preview/mmwrhtml/rr6003a1.htm
  14. Cheetham S, Souza M, Meulia T, Grimes S, Han MG, Saif LJ. 2006. Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J. Virol. 80:2110372–81 [Google Scholar]
  15. Chen H, Hoover DG, Kingsley DH. 2005. Temperature and treatment time influence high hydrostatic pressure inactivation of feline calicivirus, a norovirus surrogate. J. Food Prot. 68:2389–94 [Google Scholar]
  16. Chen ZM, Tian SM, Ruan KC. 2001. A vaccine to coxsackievirus prepared by high pressure. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 33:128–30 [Google Scholar]
  17. Cruz-Romero M, Smiddy M, Hill C, Kerry JP, Kelly AL. 2004. Effects of high pressure treatment on physicochemical characteristics of fresh oysters (Crassostrea gigas). Innov. Food Sci. Emerg. Technol. 5:161–69 [Google Scholar]
  18. Da Poian AT, Carneiro FA, Stauffer F. 2009. Viral inactivation based on inhibition of membrane fusion: understanding the role of histidine protonation to develop new viral vaccines. Protein Pept. Lett. 16:779–85 [Google Scholar]
  19. Dancho BA, Chen H, Kingsley DH. 2012. Discrimination between infectious and non-infectious human norovirus using porcine gastric mucin. Int. J. Food Microbiol. 155:222–26 [Google Scholar]
  20. Dicaprio E, Ma Y, Purgianto A, Hughes J, Li J. 2012. Internalization and dissemination of human norovirus and animal caliciviruses in hydroponically grown romaine lettuce. Appl. Environ. Microbiol. 78:6143–52 [Google Scholar]
  21. Farkas DF, Hoover DG. 2000. High pressure processing. J. Food Sci. 65:47–64 [Google Scholar]
  22. Farkas J. 1998. Irradiation as a method for decontaminating food—a review. Int. J. Food Microbiol. 44:189–204 [Google Scholar]
  23. Farr D. 1990. High pressure technology in the food industry. Trends Food Sci. Technol. 1:14–16 [Google Scholar]
  24. Feng K, Divers E, Ma Y, Li J. 2011. Inactivation of a human norovirus surrogate, human norovirus virus-like particles, and vesicular stomatitis virus by gamma irradiation. Appl. Environ. Microbiol. 77:3507–17 [Google Scholar]
  25. Fino VR, Kniel KE. 2008. UV light inactivation of hepatitis A virus, Aichi virus, and feline calicivirus on strawberries, green onions, and lettuce. J. Food Prot. 71:908–13 [Google Scholar]
  26. Freitas MS, Da Poian AT, Barth OM, Rebello MA, Silva JL, Gaspar LP. 2006. The fusogenic state of Mayaro virus induced by low pH and by hydrostatic pressure. Cell Biochem. Biophys. 44:325–35 [Google Scholar]
  27. Gaspar LP, Mendes YS, Yamamura AMY, Almeida LFC, Caride E. et al. 2008. Pressure-inactivated yellow fever 17DD virus: implications for vaccine development. J. Virol. Methods 150:57–62 [Google Scholar]
  28. Giddings NJ, Allard HA, Hite BH. 1929. Inactivation of the tobacco mosaic virus by high pressure. Phytopathology 19:749–50 [Google Scholar]
  29. Gogal RM, Kerr R, Kingsley DH, Granata LA, LeRoith T. et al. 2011. High hydrostatic pressure processing of murine norovirus 1-contaminated oysters inhibits oral infection in STAT-1(−/−)-deficient female mice. J. Food Prot. 74:209–14 [Google Scholar]
  30. Green J, Wright PA, Gallimore CI, Mitchell O, Morgan-Capner P, Brown DWG. 1998. The role of environmental contamination with small round structured viruses in a hospital outbreak investigated by reverse-transcriptase polymerase chain reaction assay. J. Hosp. Infect. 39:39–45 [Google Scholar]
  31. Gross M, Jaenicke R. 1994. Proteins under pressure. The influence of high hydrostatic pressure on structure, function and assembly of proteins and protein complexes. Eur. J. Biochem. 221:617–30 [Google Scholar]
  32. Grove SF, Forsyth S, Wan J, Coventry J, Cole M. et al. 2008. Inactivation of hepatitis A virus, poliovirus and a norovirus surrogate by high pressure processing. Innov. Food Sci. Emerg. Technol. 9:206–10 [Google Scholar]
  33. Grove SF, Lee A, Lewis T, Stewart CM, Chen HQ, Hoover DG. 2006. Inactivation of foodborne viruses of significance by high pressure and other processes. J. Food Prot. 69:957–68 [Google Scholar]
  34. He H, Adams RM, Farkas DF, Morrissey MT. 2002. Use of high-pressure processing for oyster shucking and shelf-life extension. J. Food Sci. 67:640–45 [Google Scholar]
  35. Hirneisen KA, Kniel KE. 2013. Inactivation of internalized and surface contaminated enteric viruses in green onions. Int. J. Food Microbiol. 166:201–6 [Google Scholar]
  36. Hoover DG. 1993. Pressure effects on biological systems. Food Technol. 47:150–55 [Google Scholar]
  37. Hoover DG, Metrick C, Papineau AM, Farkas DF, Knorr D. 1989. Biological effects of high hydrostatic pressure on food microorganisms. Food Technol. 43:99–107 [Google Scholar]
  38. Isbarn S, Buckow R, Himmelreich A, Lehmacher A, Heinz V. 2007. Inactivation of avian influenza virus by heat and high hydrostatic pressure. J. Food Prot. 70:667–73 [Google Scholar]
  39. Ishimaru D, Sa-Carvalho D, Silva JL. 2004. Pressure-inactivated FMDV: a potential vaccine. Vaccine 22:2334–39 [Google Scholar]
  40. Jay JM. 1992. Radiation preservation of foods and nature of microbial radiation resistance. Modern Food Microbiology JM Jay 290–313 New York: Springer [Google Scholar]
  41. Jean J, Morales-Rayas R, Anoman MN, 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 Microbiol. 28:568–72 [Google Scholar]
  42. Jurkiewicz E, Billasboas M, Silva JL, Weber G, Hunsmann G, Clegg RM. 1995. Inactivation of simian immunodeficiency virus by hydrostatic pressure. Proc. Natl. Acad. Sci. USA 92:6935–37 [Google Scholar]
  43. Kingsley DH, Chen HQ. 2008. Aqueous matrix compositions and pH influence feline calicivirus inactivation by high pressure processing. J. Food Prot. 71:1598–603 [Google Scholar]
  44. Kingsley DH, Chen HQ. 2009. Influence of pH, salt, and temperature on pressure inactivation of hepatitis A virus. Int. J. Food Microbiol. 130:61–64 [Google Scholar]
  45. Kingsley DH, Chen HQ, Hoover DG. 2004. Inactivation of selected picornaviruses by high hydrostatic pressure. Virus Res. 102:221–24 [Google Scholar]
  46. Kingsley DH, Guan DS, Hoover DG. 2005. Pressure inactivation of hepatitis A virus in strawberry puree and sliced green onions. J. Food Prot. 68:1748–51 [Google Scholar]
  47. Kingsley DH, Guan DS, Hoover DG, Chen HQ. 2006. Inactivation of hepatitis A virus by high-pressure processing: the role of temperature and pressure oscillation. J. Food Prot. 69:2454–59 [Google Scholar]
  48. Kingsley DH, Hollinian DR, Calci KR, Chen HQ, Flick GJ. 2007. Inactivation of a norovirus by high-pressure processing. Appl. Environ. Microbiol. 73:581–85 [Google Scholar]
  49. Kingsley DH, Hoover DG, Papafragkou E, Richards GP. 2002. Inactivation of hepatitis A virus and a calicivirus by high hydrostatic pressure. J. Food Prot. 65:1605–9 [Google Scholar]
  50. Knoerzer K, Buckow R, Versteeg C. 2010. Adiabatic compression heating coefficients for high-pressure processing—a study of some insulating polymer materials. J. Food Eng. 98:110–19 [Google Scholar]
  51. Koopmans M, Duizer E. 2004. Foodborne viruses: an emerging problem. Int. J. Food Microbiol. 90:23–41 [Google Scholar]
  52. Koopmans M, von Bonsdorff CH, Vinje J, de Medici D, Monroe S. 2002. Foodborne viruses. FEMS Microbiol. Rev. 26:187–205 [Google Scholar]
  53. Lee J, Zoh KD, Ko G. 2008. Inactivation and UV disinfection of murine norovirus with TiO2 under various environmental conditions. Appl. Environ. Microbiol. 74:2111–17 [Google Scholar]
  54. Leon JS, Kingsley DH, Montes JS, Richards GP, Lyon GM. et al. 2011. Randomized, double-blinded clinical trial for human norovirus inactivation in oysters by high hydrostatic pressure processing. Appl. Environ. Microbiol. 77:5476–82 [Google Scholar]
  55. Li X, Ye M, Neetoo H, Golovan S, Chen H. 2013. Pressure inactivation of Tulane virus, a candidate surrogate for human norovirus and its potential application in food industry. Int. J. Food Microbiol. 162:37–42 [Google Scholar]
  56. Lopez-Caballero ME, Perez-Mateos M, Montero P, Borderias AJ. 2000. Oyster preservation by high-pressure treatment. J. Food Prot. 63:196–201 [Google Scholar]
  57. Lou F, Huang P, Neetoo H, Gurtler JB, Niemira BA. et al. 2012. High-pressure inactivation of human norovirus virus-like particles provides evidence that the capsid of human norovirus is highly pressure resistant. Appl. Environ. Microbiol. 78:5320–27 [Google Scholar]
  58. Lou F, Neetoo H, Chen H, Li J. 2011a. Inactivation of a human norovirus surrogate by high-pressure processing: effectiveness, mechanism, and potential application in the fresh produce industry. Appl. Environ. Microbiol. 77:1862–71 [Google Scholar]
  59. Lou F, Neetoo H, Li J, Chen H. 2011b. Lack of correlation between virus barosensitivity and the presence of a viral envelope during inactivation of human rotavirus, vesicular stomatitis virus, and avian metapneumovirus by high-pressure processing. Appl. Environ. Microbiol. 77:8538–47 [Google Scholar]
  60. Murchie LW, Cruz-Romero M, Kerry JP, Linton M, Patterson MF. et al. 2005. High pressure processing of shellfish: a review of microbiological and other quality aspects. Innovat. Food Sci. Emerg. Tech. 6:257–70 [Google Scholar]
  61. Murchie LW, Kelly AL, Wiley M, Adair BM, Patterson M. 2007. Inactivation of a calicivirus and enterovirus in shellfish by high pressure. Innovat. Food Sci. Emerg. Tech. 8:213–17 [Google Scholar]
  62. Nakagami T, Shigehisa T, Ohmori T, Taji S, Hase A. et al. 1992. Inactivation of herpes viruses by high hydrostatic pressure. J. Virol. Methods 38:255–61 [Google Scholar]
  63. Neetoo H, Chen HQ. 2011. Individual and combined application of dry heat with high hydrostatic pressure to inactivate Salmonella and Escherichia coli O157:H7 on alfalfa seeds. Food Microbiol. 28:119–27 [Google Scholar]
  64. Oliveira AC, Ishimaru D, Goncalves RB, Smith TJ, Mason P. et al. 1999. Low temperature and pressure stability of picornaviruses: implications for virus uncoating. Biophys. J. 76:1270–79 [Google Scholar]
  65. Perche PY, Clery C, Bouloy M, Burckhart MF. 1997. Study of inactivation and immunogenicity of rift valley fever virus type clone 13 treated by high hydrostatic pressure. Am. J. Trop. Med. Hyg. 57:457 [Google Scholar]
  66. Pontes L, Fornells LA, Giongo V, Araujo JRV, Sepulveda A. et al. 1997. Pressure inactivation of animal viruses: potential biotechnological applications. High Pressure Research in Biosciences and Biotechnology K Heremans 91–94 Leuven, Belg: Leuven Univ. Press [Google Scholar]
  67. Praveen C, Dancho BA, Kingsley DH, Calci KR, Meade GK. et al. 2013. Susceptibility of murine norovirus and hepatitis A virus to electron beam irradiation in oysters and quantifying the reduction in potential infection risks. Appl. Environ. Microbiol. 79:3796–801 [Google Scholar]
  68. Rastogi NK, Raghavarao KSMS, Balasubramaniam VM, Niranjan K, Knorr D. 2007. Opportunities and challenges in high pressure processing of foods. Crit. Rev. Food Sci. Nutr. 47:69–112 [Google Scholar]
  69. Rawsthorne H, Phister TG, Jaykus LA. 2009. Development of a fluorescent in situ method for visualization of enteric viruses. Appl. Environ. Microbiol. 75:7822–27 [Google Scholar]
  70. Roberts P, Hope A. 2003. Virus inactivation by high intensity broad spectrum pulsed light. J. Virol. Methods 110:61–65 [Google Scholar]
  71. Ronnqvist M, Mikkela A, Tuominen P, Salo S, Maunula L. 2014. Ultraviolet light inactivation of murine norovirus and human norovirus GII: PCR may overestimate the persistence of noroviruses even when combined with pre-PCR treatments. Food Environ. Virol. 6:48–57 [Google Scholar]
  72. Rzezutka A, Cook N. 2004. Survival of human enteric viruses in the environment and food. FEMS Microbiol. Rev. 28:441–53 [Google Scholar]
  73. Sánchez G, Aznar R, Martinez A, Rodrigo D. 2011. Inactivation of human and murine norovirus by high-pressure processing. Foodborne Pathog. Dis. 8:249–53 [Google Scholar]
  74. Sanglay GC, Li J, Uribe RM, Lee K. 2011. Electron-beam inactivation of a norovirus surrogate in fresh produce and model systems. J. Food Prot. 74:1155–60 [Google Scholar]
  75. Santos JLR, Bispo JAC, Landini GF, Bonafe CFS. 2004. Proton dependence of tobacco mosaic virus dissociation by pressure. Biophys. Chem. 111:53–61 [Google Scholar]
  76. Schultz AC, Uhrbrand K, Norrung B, Dalsgaard A. 2012. Inactivation of norovirus surrogates on surfaces and raspberries by steam-ultrasound treatment. J. Food Prot. 75:376–81 [Google Scholar]
  77. Sharma M, Shearerb AEH, Hooverb DG, Liua MN, Solomona MB. et al. 2008. Comparison of hydrostatic and hydrodynamic pressure to inactivate foodborne viruses. Innov. Food Sci. Emerg. Technol. 9:418–22 [Google Scholar]
  78. Silva JL, Luan P, Glaser M, Voss EW, Weber G. 1992. Effects of hydrostatic pressure on a membrane-enveloped virus—high immunogenicity of the pressure-inactivated virus. J. Virol. 66:2111–17 [Google Scholar]
  79. Su X, Zivanovic S, D'Souza DH. 2010. Inactivation of human enteric virus surrogates by high-intensity ultrasound. Foodborne Pathog. Dis. 7:1055–61 [Google Scholar]
  80. Tang Q, Li D, Xu J, Wang J, Zhao Y. et al. 2010. Mechanism of inactivation of murine norovirus-1 by high pressure processing. Int. J. Food Microbiol. 137:186–89 [Google Scholar]
  81. Thurston-Enriquez JA, Haas CN, Jacangelo J, Riley K, Gerba CP. 2003. Inactivation of feline calicivirus and adenovirus type 40 by UV radiation. Appl. Environ. Microbiol. 69:577–82 [Google Scholar]
  82. Tian SM, Ruan KC, Qian JF, Shao GQ, Balny C. 2000. Effects of hydrostatic pressure on the structure and biological activity of infectious bursal disease virus. Eur. J. Biochem. 267:4486–94 [Google Scholar]
  83. Ting E. 2008. Compression heating and temperature control in high pressure processing. High Pressure Processing of Foods CJ Doona, FE Feeherry 227–35 Oxford, UK: IFT Press, Blackwell Publ. [Google Scholar]
  84. Urbanucci A, Myrmel M, Berg I, von Bonsdorff CH, Maunula L. 2009. Potential internalisation of caliciviruses in lettuce. Int. J. Food Microbiol. 135:175–78 [Google Scholar]
  85. Wei J, Jin Y, Sims T, Kniel KE. 2010. Manure- and biosolids-resident murine norovirus 1 attachment to and internalization by romaine lettuce. Appl. Environ. Microbiol. 76:578–83 [Google Scholar]
  86. Wilkinson N, Kurdziel AS, Langton S, Needs E, Cook N. 2001. Resistance of poliovirus to inactivation by high hydrostatic pressures. Innov. Food Sci. Emerg. Technol. 2:95–98 [Google Scholar]
  87. Wobus CE, Thackray LB, Virgin HW. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80:5104–12 [Google Scholar]
  88. Ye M, Li X, Kingsley DH, Jiang X, Chen H. 2014. Inactivation of human norovirus in contaminated oysters and clams by high hydrostatic pressure. Appl. Environ. Microbiol. 80:2248–53 [Google Scholar]
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