The influence of temperature, pH, and water immersion on the high hydrostatic pressure inactivation of GI.1 and GII.4 human noroviruses

International Journal of Food Microbiology

Volumn 167, Issue 2, 2013, Pages 138-143

  Li, Xinhui ^a   Chen, Haiqiang ^a   Kingsley, David H ^b  

^a UNIVERSITY OF DELAWARE   (United States)

^b DELAWARE STATE UNIVERSITY   (United States)

Author keywords

Blueberries; Human norovirus; Hydrostatic pressure; PGM binding assay; PH; Temperature

Indexed keywords

PORCINE GASTRIC MUCIN; STOMACH MUCIN; UNCLASSIFIED DRUG; WATER;

ARTICLE; BLUEBERRY; CONJUGATION; CONTROLLED STUDY; FOOD INDUSTRY; FOOD PROCESSING; HYDROSTATIC PRESSURE; MAGNET; MAGNETIC BEAD; NONHUMAN; NOROVIRUS; PH; PROTEIN BINDING; REDUCTION; RISK ASSESSMENT; TEMPERATURE; VIRUS DETECTION; VIRUS INACTIVATION; VIRUS LOAD; VIRUS STRAIN; WATER IMMERSION;

NOROVIRUS; SUS; VACCINIUM;

BLUEBERRIES; HUMAN NOROVIRUS; HYDROSTATIC PRESSURE; PGM BINDING ASSAY; PH; TEMPERATURE;

ANIMALS; BLUEBERRY PLANT; FOOD CONTAMINATION; GASTRIC MUCINS; HUMANS; HYDROGEN-ION CONCENTRATION; HYDROSTATIC PRESSURE; NOROVIRUS; SWINE; TEMPERATURE; WATER;

EID: 84885774770     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2013.08.020     Document Type: Article

References (35)

1. Carter M.J. Enterically infecting viruses: pathogenicity, transmission and significance for food and waterborne infection. J. Appl. Microbiol. 2005, 98:1354-1380.
2. Chen H., Hoover D.G., Kingsley D.H. Temperature and treatment time influence high hydrostatic pressure inactivation of feline calicivirus, a norovirus surrogate. J. Food Prot. 2005, 68:2389-2394.
3. Cotterelle B., Drougard C., Rolland J., Becamel M., Boudon M., Pinede S., Traore O., Balay K., Pothier P., Espie E. Outbreak of norovirus infection associated with the consumption of frozen raspberries, France, March 2005. Euro surveillance:bulletin europeen sur les maladies transmissibles=European Communicable Disease Bulletin 2005, 10:E050428.1. (Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2690).
4. Dancho B.A., Chen H., Kingsley D.H. Discrimination between infectious and non-infectious human norovirus using porcine gastric mucin. Int. J. Food Microbiol. 2012, 155:222-226.
5. Desai R., Hembree C.D., Handel A., Matthews J.E., Dickey B.W., McDonald S., Hall A.J., Parashar U.D., Leon J.S., Lopman B. Severe outcomes are associated with genogroup 2 genotype 4 norovirus outbreaks: a systematic literature review. Clin. Infect. Dis. 2012, 55:189-193.
6. Diez-Valcarce M., Kovac K., Raspor P., Rodríguez-Lázaro D., Hernández M. Virus genome quantification does not predict norovirus infectivity after application of food inactivation processing technologies. Food Environ. Virol. 2011, 3:141-146.
7. Donaldson E.F., Lindesmith L.C., Lobue A.D., Baric R.S. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol. Rev. 2008, 225:190-211.
8. Duizer E., Schwab K.J., Neill F.H., Atmar R.L., Koopmans M.P., Estes M.K. Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 2004, 85:79-87.
9. Falkenhorst G., Krusell L., Lisby M., Madsen S.B., Bottiger B., Molbak K. Imported frozen raspberries cause a series of norovirus outbreaks in Denmark, 2005. Euro surveillance: bulletin europeen sur les maladies transmissibles=European Communicable Disease Bulletin 2005, 10:E050922.2. (Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2795).
10. Herbst-Kralovetz M.M., Radtke A.L., Lay M.K., Hjelm B.E., Bolick A.N., Sarker S.S., Atmar R.L., Kingsley D.H., Arntzen C.J., Estes M.K., Nickerson C.A. Lack of norovirus replication and histo-blood group antigen expression in 3-D intestinal epithelial cell cultures. Emerg. Infect. Dis. 2013, 19:431-438.
11. Huang Y., Ye M., Chen H. Inactivation of Escherichia coli O157:H7 and Salmonella spp. in strawberry puree by high hydrostatic pressure with/without subsequent frozen storage. Int. J. Food Microbiol. 2013, 160:337-343.
12. Kingsley D.H. High pressure processing and its application to the challenge of virus-contaminated foods. Food Environ. Virol. 2013, 5:1-12.
13. Kingsley D.H., Chen H. Aqueous matrix compositions and pH influence feline calicivirus inactivation by high pressure processing. J. Food Prot. 2008, 71:1598-1603.
14. Kingsley D.H., Chen H., Hoover D.G. Inactivation of selected picornaviruses by high hydrostatic pressure. Virus Res. 2004, 102:221-224.
15. Kingsley D.H., Holliman D.R., Calci K.R., Chen H., Flick G.J. Inactivation of a norovirus by high pressure processing. Appl. Environ. Microbiol. 2007, 73:581-585.
16. Knorr D., Heinz V., Buckow R. High pressure application for food biopolymers. Biochim. Biophys. Acta 2006, 1764:619-631.
17. Kovač K., Diez-Valcarce M., Hernandez M., Raspor P., Rodríguez-Lázaro D. High hydrostatic pressure as emergent technology for the elimination of foodborne viruses. Trends Food Sci. Technol. 2010, 21:558-568.
18. Kovač K., Diez-Valcarce M., Raspor P., Hernandez M., Rodríguez-Lázaro D. Effect of high hydrostatic pressure processing on norovirus infectivity and genome stability in strawberry puree and mineral water. Int. J. Food Microbiol. 2012, 152:35-39.
19. Le Guyader F.S., Mittelholzer C., Haugarreau L., Hedlund K.O., Alsterlund R., Pommepuy M., Svensson L. Detection of noroviruses in raspberries associated with a gastroenteritis outbreak. Int. J. Food Microbiol. 2004, 97:179-186.
20. Leon J.S., Kingsley D.H., Montes J.S., Richards G.P., Lyon G.M., Abdulhafid G.M., Seitz S.R., Fernandez M.L., Teunis P.F., Flick G.J., Moe C.L. Randomized, double-blinded clinical trial for human norovirus inactivation in oysters by high hydrostatic pressure processing. Appl. Environ. Microbiol. 2011, 77:5476-5482.
21. Li J., Predmore A., Divers E., Lou F. New interventions against human norovirus: progress, opportunities, and challenges. Annu. Rev. Food Sci. Tech. 2012, 3:331-352.
22. Li X., Ye M., Neetoo H., Golovan S., Chen H. Pressure inactivation of Tulane virus, a candidate surrogate for human norovirus and its potential application in food industry. Int. J. Food Microbiol. 2013, 162:37-42.
23. Lou F., Neetoo H., Chen H., Li J. Inactivation of a human norovirus surrogate by high-pressure processing: effectiveness, mechanism, and potential application in the fresh produce industry. Appl. Environ. Microbiol. 2011, 77:1862-1871.
24. Lysen M., Thorhagen M., Brytting M., Hjertqvist M., Andersson Y., Hedlund K.O. Genetic diversity among food-borne and waterborne norovirus strains causing outbreaks in Sweden. J. Clin. Microbiol. 2009, 47:2411-2418.
25. Marionneau S., Ruvoen N., Le Moullac-Vaidye B., Clement M., Cailleau-Thomas A., Ruiz-Palacois G., Huang P., Jiang X., Le Pendu J. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 2002, 122:1967-1977.
26. Pan L., Zhang Q., Li X., Tian P. Detection of human norovirus in cherry tomatoes, blueberries and vegetable salad by using a receptor-binding capture and magnetic sequestration (RBCMS) method. Food Microbiol. 2012, 30:420-426.
27. Potera C. Pesticide spraying may spread norovirus. Environ. Heal. Perspect. 2013, 121:148.
28. Rodriguez-Lazaro D., Cook N., Ruggeri F.M., Sellwood J., Nasser A., Nascimento M.S., D'Agostino M., Santos R., Saiz J.C., Rzezutka A., Bosch A., Girones R., Carducci A., Muscillo M., Kovac K., Diez-Valcarce M., Vantarakis A., von Bonsdorff C.H., de Roda Husman A.M., Hernandez M., van der Poel W.H. Virus hazards from food, water and other contaminated environments. FEMS Microbiol. Rev. 2012, 36:786-814.
29. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.A., Roy S.L., Jones J.L., Griffin P.M. Foodborne illness acquired in the United States - major pathogens. Emerg. Infect. Dis. 2011, 17:7-15.
30. Stals A., Baert L., Botteldoorn N., Werbrouck H., Herman L., Uyttendaele M., Van Coillie E. Multiplex real-time RT-PCR for simultaneous detection of GI/GII noroviruses and murine norovirus 1. J. Virol. Methods 2009, 161:247-253.
31. Tian P., Jiang X., Zhong W., Jensen H.M., Brandl M., Bates A.H., Engelbrektson A.L., Mandrell R. Binding of recombinant norovirus like particle to histo-blood group antigen on cells in the lumen of pig duodenum. Res. Vet. Sci. 2007, 83:410-418.
32. Tian P., Engelbrektson A., Mandrell R. Two-log increase in sensitivity for detection of norovirus in complex samples by concentration with porcine gastric mucin conjugated to magnetic beads. Appl. Environ. Microbiol. 2008, 74:4271-4276.
33. Tian P., Yang D., Jiang X., Zhong W., Cannon J.L., Burkhardt W., Woods J.W., Hartman G., Lindesmith L., Baric R.S., Mandrell R. Specificity and kinetics of norovirus binding to magnetic bead-conjugated histo-blood group antigens. J. Appl. Microbiol. 2010, 109:1753-1762.
34. Tian P., Yang D., Mandrell R. A simple method to recover Norovirus from fresh produce with large sample size by using histo-blood group antigen-conjugated to magnetic beads in a recirculating affinity magnetic separation system (RCAMS). Int. J. Food Microbiol. 2011, 147:223-227.
35. Tian P., Yang D., Pan L., Mandrell R. Application of a receptor-binding capture quantitative reverse transcription-PCR assay to concentrate human norovirus from sewage and to study the distribution and stability of the virus. Appl. Environ. Microbiol. 2012, 78:429-436.