Survival of murine norovirus, tulane virus, and hepatitis a virus on alfalfa seeds and sprouts during storage and germination

Applied and Environmental Microbiology

Volumn 79, Issue 22, 2013, Pages 7021-7027

  Wang, Qing ^a   Hirneisen, Kirsten A ^a   Markland, Sarah M ^a   Kniel, Kalmia E ^a  

^a UNIVERSITY OF DELAWARE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALFALFA SEEDS; HEPATITIS A VIRUS; NOROVIRUS; PREVENTION PROCEDURES; STORAGE PERIODS; TESTING TIME;

CULTIVATION; DIGITAL STORAGE; TISSUE CULTURE; VIRUSES;

SEED;

ETIOLOGY; GERMINATION; HERB; INOCULATION; SANITATION; SEED; SURVIVAL; VIRUS;

ALFALFA; ANIMAL; ARTICLE; FOOD CONTAMINATION; FOOD CONTROL; FOOD HANDLING; FOOD POISONING; FOOD STORAGE; GERMINATION; GROWTH, DEVELOPMENT AND AGING; HEPATITIS A VIRUS; ISOLATION AND PURIFICATION; METHODOLOGY; MOUSE; NOROVIRUS; PLANT SEED; VIROLOGY;

ANIMALS; FOOD CONTAMINATION; FOOD HANDLING; FOOD MICROBIOLOGY; FOOD STORAGE; FOODBORNE DISEASES; GERMINATION; HEPATITIS A VIRUS; MEDICAGO SATIVA; MICE; NOROVIRUS; SEEDS;

EID: 84886656513     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01704-13     Document Type: Article

References (58)

1. Schrader WL. 2002. Sprout production in California, publication 8060. University of California Department of Agriculture and Natural Resources, Davis, CA.
2. Erdozain G, Erdozain MS, Powell D. 2011. Sprouts associated outbreaks. Bites, Manhattan, KS.
3. Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C, Wilking H, Deleré Y, an der Heiden M, Adlhoch C, Dreesman J, Ehlers J, Ethelberg S, Faber M, Frank C, Fricke G, Greiner M, Höhle M, Ivarsson S, Jark U, Kirchner M, Koch J, Krause G, Luber P, Rosner B, Stark K, Kühne M. 2011. German outbreak of Escherichia coli O104:H4 associated with sprouts. N. Engl. J. Med. 365:1763-1770.
4. International Food Safety Network. 25 April 2009, posting date. Sprout associated outbreaks in North America, 1990-2009. IFSN, Manhattan, KS. http://foodsafety.ksu.edu/en/article-details.php?a=3&c=10&sc=74&id=865.
5. Itoh Y, Sugita-Konishi Y, Kasuga F, Iwaki M, Hara-Kudo Y, Saito N, Noguchi Y, Konuma H, Kumagai S. 1998. Enterohemorrhagic Escherichia coli O157:H7 present in radish sprouts. Appl. Environ. Microbiol. 64:1532-1535.
6. Castro-Rosas J, Escartín EF. 2000. Survival and growth of Vibrio cholerae O1, Salmonella typhi, and Escherichia coli O157:H7 in alfalfa sprouts. J. Food Sci. 65:162-165.
7. Barak JD, Whitehand LC, Charkowski AO. 2002. Differences in attachment of Salmonella enterica serovars and Escherichia coli O157: H7 to alfalfa sprouts. Appl. Environ. Microbiol. 68:4758-4763.
8. Fransisca L, Feng H. 2012. Effect of surface roughness on inactivation of Escherichia coli O157:H7 87-23 by new organic-acid surfactant combinations on alfalfa, broccoli, and radish seeds. J. Food Prot. 75:261-269.
9. Gorski L, Palumbo JD, Nguyen KD. 2004. Strain-specific differences in the attachment of Listeria monocytogenes to alfalfa sprouts. J. Food Prot. 67:2488-2495.
10. Barak JD, Gorski L, Naraghi-Arani P, Charkowski AO. 2005. Salmonella enterica virulence genes are required for bacterial attachment to plant tissue. Appl. Environ. Microbiol. 71:5685-5691.
11. Wu FM, Beuchat LR, Wells JG, Slutsker L, Doyle MP, Swaminathan B. 2001. Factors influencing the detection and enumeration of Escherichia coli O157: H7 on alfalfa seeds. Int. J. Food Microbiol. 71:93-99.
12. Fu TJ, Reineke KF, Chirtel S, Vanpelt OM. 2008. Factors influencing the growth of Salmonella during sprouting of naturally contaminated alfalfa seeds. J. Food Prot. 71:888-896.
13. Charkowski AO, Sarreal CZ, Mandrell RE. 2001. Wrinkled alfalfa seeds harbor more aerobic bacteria and are more difficult to sanitize than smooth seeds. J. Food Prot. 64:1292-1298.
14. Hall AJ, Eisenbart VG, Etingüe AL, Gould LH, Lopman BA, Parashar UD. 2012. Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008. Emerg. Infect. Dis. 18:1566-1573.
15. DeWaal CS, Bhuiya F. 2007. Outbreaks by the numbers: fruits and vegetables 1990-2005. Poster presentation P3-03. 94th Annual Meeting of the International Association for Food Protection, Lake Buena Vista, FL, 8 to 11 July 2007.
16. Wei J, Kniel KE. 2010. Pre-harvest viral contamination of crops originating from fecal matter. Food Environ. Virol. 2:195-206.
17. National Advisory Committee on Microbiological Criteria for Foods. 1999. Microbiological safety evaluations and recommendations on sprouted seeds. Int. J. Food Microbiol. 52:123-153.
18. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson M-A, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
19. Koopmans M, Duizer E. 2004. Foodborne viruses: an emerging problem. Int. J. Food Microbiol. 90:23-41.
20. Patel MM, Hall AJ, Vinjé J, Parashar UD. 2009. Noroviruses: a comprehensive review. J. Clin. Virol. 44:1-8.
21. Teunis PFM, Moe CL, Liu P, Miller ES, Lindesmith L, Baric RS, Le Pendu J, Calderon RL. 2008. Norwalk virus: how infectious is it? J. Med. Virol. 80:1468-1476.
22. Sair AI, D'Souza DH, Jaykus LA. 2002. Human enteric viruses as causes of foodborne disease. Compr. Rev. Food Sci. Food Saf. 1:73-89.
23. 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. 2:2076-2084. doi:10.1371/journal.pbio.0020432.
24. Farkas T, Sestak K, Wei C, Jiang X. 2008. Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. J. Virol. 82:5408-5416.
25. Hirneisen KA, Kniel KE. 2013. Comparing human norovirus surrogates: murine norovirus and tulane virus. J. Food Prot. 76:139-143.
26. Farkas T, Cross RW, Hargitt E, Lerche NW, Morrow AL, Sestak K. 2010. Genetic diversity and histo-bood group antigen interactions of rhesus enteric caliciviruses. J. Virol. 84:8617-8625.
27. Reed LJ, Muench H. 1938. A simple method of estimating fifty percent endpoints. Am. J. Hyg. (Lond.) 27:493-497.
28. Schwab KJ, De Leon R, Baric RS, Sobsey MD. 1991. Detection of rotaviruses, enteroviruses, and hepatitis A virus by reverse transcriptasepolymerase chain reaction, p 475-491. In Advances in water analysis and treatment. Proceedings of theAWWAWater Quality Technology Conference, Orlando, FL, 10 to 14 November 1991. American Water Works Association, Denver, CO.
29. Hsu CC, Wobus CE, Steffen EK, Riley LK, Livingston RS. 2005. Development of a microsphere-based serologic multiplexed fluorescent immunoassay and a reverse transcriptase PCR assay to detect murine norovirus 1 infection in mice. Clin. Diagn. Lab. Immun. 12:1145-1151.
30. Erdozain MS, Allen KJ, Morley KA, Powell DA. 2013. Failures in sprouts-related risk communication. Food Control 30:649-656.
31. Howard MB, Hutcheson SW. 2003. Growth dynamics of Salmonella enterica strains on alfalfa sprouts and in waste seed irrigation water. Appl. Environ. Microbiol. 69:548-553.
32. Greig JD, Todd ECD, Bartleson CA, Michaels BS. 2007. Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 1. Description of the problem, methods, and agents involved. J. Food Prot. 70:1752-1761.
33. Chung H, Sobsey MD. 1993. Comparative survival of indicator viruses and enteric viruses in seawater and sediment. Water Sci. Technol. 27:425- 428.
34. Seitz SR, Leon JS, Schwab KJ, Lyon GM, Dowd M, McDaniels M, Abdulhafid G, Fernandez ML, Lindesmith LC, Baric RS, Moe CL. 2011. Norovirus infectivity in humans and persistence in water. Appl. Environ. Microbiol. 77:6884-6888.
35. Mbithi JN, Springthorpe VS, Sattar SA. 1991. Effect of relative humidity and air temperature on survival of hepatitis A virus on environmental surfaces. Appl. Environ. Microbiol. 57:1394-1399.
36. Terpstra FG, van den Blink AE, Bos LM, Boots AGC, Brinkhuis FHM, Gijsen E, van Remmerden Y, Schuitemaker H, van't Wout AB. 2007. Resistance of surface-dried virus to common disinfection procedures. J. Hosp. Infect. 66:332-338.
37. Vega E, Smith J, Garland J, Matos A, Pillai SD. 2005. Variability of virus attachment patterns to butterhead lettuce. J. Food Prot. 68:2112-2117.
38. Vega E, Garland J, Pillai SD. 2008. Electrostatic forces control nonspecific virus attachment to lettuce. J. Food Prot. 71:522-529.
39. Kukavica-Ibrulj I, Darveau A, Jean J, Fliss I. 2004. Hepatitis A virus attachment to agri-food surfaces using immunological, virological and thermodynamic assays. J. Appl. Microbiol. 97:923-934.
40. Langlet J, Gaboriaud F, Gantzer C, Duval JFL. 2008. Impact of chemical and structural anisotropy on the electrophoretic mobility of spherical soft multilayer particles: the case of bacteriophage MS2. Biophys. J. 94:3293- 3312.
41. Le Guyader FS, Atmar RL. 2008. Binding and inactivation of viruses on and in food, with a focus on the role of the matrix, p 189-208. In Doyle MP, Koopmans MPG, Cliver DO, Bosch AB (ed), Foodborne viruses: progress and challenges. ASM Press, Washington, DC.
42. Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinje 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.
43. Davidson I, Nagar S, Haddas R, Ben-Shabat M, Golender N, Lapin E, Altory A, Simanov L, Ribshtein I, Panshin A, Perk S. 2010. Avian influenza virus H9N2 survival at different temperatures and pHs. Avian Dis. 54:725-728.
44. Weagant SD, Bound AJ. 2001. Evaluation of techniques for enrichment and isolation of Escherichia coli O157:H7 from artificially contaminated sprouts. Int. J. Food Microbiol. 71:87-92.
45. Feng YY, Ong SL, Hu JY, Tan XL, Ng WJ. 2003. Effects of pH and temperature on the survival of coliphages MS2 and Q beta. J. Ind. Microbiol. Biotechnol. 30:549-552.
46. Sinclair RG, Rose JB, Hashsham SA, Gerba CP, Haas CN. 2012. Criteria for selection of surrogates used to study the fate and control of pathogens in the environment. Appl. Environ. Microbiol. 78:1969-1977.
47. Mahon BE, Ponka A, Hall WN, Komatsu K, Dietrich SE, Siitonen A, Cage G, Hayes PS, Lambert-Fair MA, Bean NH, Griffin PM, Slutsker L. 1997. An international outbreak of Salmonella infections caused by alfalfa sprouts grown from contaminated seeds. J. Infect. Dis. 175:876-882.
48. Breuer T, Benkel DH, Shapiro RL, Hall WN, Winnett MM, Linn MJ, Neimann J, Barrett TJ, Dietrich S, Downes FP, Toney DM, Pearson JL, Rolka H, Slutsker L, Griffin PM, Investigation Team. 2001. A multistate outbreak of Escherichia coli O157:H7 infections linked to alfalfa sprouts grown from contaminated seeds. Emerg. Infect. Dis. 7:977-982.
49. Mohle-Boetani JC, Farrar JA, Werner SB, Minassian D, Bryant R, Abbott S, Slutsker L, Vugia DJ, Investigation Team. 2001. Escherichia coli O157 and Salmonella infections associated with sprouts in California, 1996-1998. Ann. Intern. Med. 135:239-247.
50. Croci L, De Medici D, Scalfaro C, Fiore A, Toti L. 2002. The survival of hepatitis A virus in fresh produce. Int. J. Food Microbiol. 73:29-34.
51. Baert L, Uyttendaele M, Vermeersch M, Van Coillie E, Debevere J. 2008. Survival and transfer of murine norovirus 1, a surrogate for human noroviruses, during the production process of deep-frozen onions and spinach. J. Food Prot. 71:1590-1597.
52. DiCaprio E, Ma YM, Purgianto A, Hughes J, Li JR. 2012. Internalization and dissemination of human norovirus and animal caliciviruses in hydroponically grown romaine lettuce. Appl. Environ. Microbiol. 78:6143- 6152.
53. Hamilton AJ, Stagnitti F, Xiong XZ, Kreidl SL, Benke KK, Maher P. 2007. Wastewater irrigation: the state of play. Vadose Zone J. 6:823-840.
54. Petterson SR, Ashbolt NJ. 2001. Viral risks associated with wastewater reuse: modeling virus persistence on wastewater irrigated salad crops. Water Sci. Technol. 43:23-26.
55. Fu T, Stewart D, Reineke K, Ulaszek J, Schlesser J, Tortorello M. 2001. Use of spent irrigation water for microbiological analysis of alfalfa sprouts. J. Food Prot. 64:802-806.
56. Neetoo H, Ye M, Chen HQ. 2008. Potential application of high hydrostatic pressure to eliminate Escherichia coli O157:H7 on alfalfa sprouted seeds. Int. J. Food Microbiol. 128:348-353.
57. Waje C, Kwon JH. 2007. Improving the food safety of seed sprouts through irradiation treatment. Food Sci. Biotechnol. 16:171-176.
58. Suslow TV, Wu JC, Fett WF, Harris LJ. 2002. Detection and elimination of Salmonella Mbandaka from naturally contaminated alfalfa seed by treatment with heat or calcium hypochlorite. J. Food Prot. 65:452-458.