Postharvest survival of porcine sapovirus, a human norovirus surrogate, on phytopathogen-infected leafy greens

Journal of Food Protection

Volumn 78, Issue 8, 2015, Pages 1472-1480

  Esseili, Malak A ^a   Chin, Ashlina ^b   Saif, Linda ^a   Miller, Sally A ^b   Qu, Feng ^b   Lewis Ivey, Melanie L ^b,c   Wang, Qiuhong ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c LOUISIANA STATE UNIVERSITY AGRICULTURAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA (MICROORGANISMS); CUCUMBER MOSAIC VIRUS; LACTUCA; NOROVIRUS; SAPOVIRUS; SPINACIA OLERACEA; SUS; XANTHOMONAS CAMPESTRIS PV. VITIANS;

ANIMAL; CALICIVIRUS INFECTION; CUCUMOVIRUS; FOOD SAFETY; GASTROENTERITIS; GENETICS; HUMAN; LETTUCE; MICROBIOLOGY; NOROVIRUS; PHYSIOLOGY; PIG; PLANT DISEASE; PLANT LEAF; REAL TIME POLYMERASE CHAIN REACTION; SAPOVIRUS; SPINACH; VIROLOGY; XANTHOMONAS CAMPESTRIS;

ANIMALS; CALICIVIRIDAE INFECTIONS; CUCUMOVIRUS; FOOD SAFETY; GASTROENTERITIS; HUMANS; LETTUCE; NOROVIRUS; PLANT DISEASES; PLANT LEAVES; REAL-TIME POLYMERASE CHAIN REACTION; SAPOVIRUS; SPINACIA OLERACEA; SWINE; XANTHOMONAS CAMPESTRIS;

EID: 84938372424     PISSN: 0362028X     EISSN: 19449097     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-14-518     Document Type: Article

References (50)

1. Aruscavage, D., S. A. Miller, M. L. Ivey, K. Lee, and J. T. LeJeune. 2008. Survival and dissemination of Escherichia coli O157:H7 on physically and biologically damaged lettuce plants. J. Food Prot. 71: 2384-2388.
2. Aruscavage, D., P. L. Phelan, K. Lee, and J. T. LeJeune. 2010. Impact of changes in sugar exudate created by biological damage to tomato plants on the persistence of Escherichia coli O157:H7. Food Microbiol. Saf. 75:187-192.
3. Barak, J. D., and A. S. Liang. 2008. Role of soil, crop debris, and a plant pathogen in Salmonella enterica contamination of tomato plants. PLoS One 3:e1657.
4. Bebber, D. P., T. Holmes, D. Smith, and S. J. Gurr. 2014. Economic and physical determinants of the global distributions of crop pests and pathogens. New Phytol. 202:901-910.
5. Berger, C. N., D. J. Brown, R. K. Shaw, F. Minuzzi, B. Feys, and G. Frankel. 2011. Salmonella enterica strains belonging to O serogroup 1,3,19 induce chlorosis and wilting of Arabidopsis thaliana leaves. Environ Microbiol. 13:1299-1308.
6. Beuchat, L. R., and J. H. Ryu. 1997. Produce handling and processing practices. Emerg. Infect. Dis. 3:459-465.
7. Bidawid, S., J. M. Farber, and S. A. Sattar. 2001. Survival of hepatitis A virus on modified atmosphere-packaged (MAP) lettuce. Food Microbiol. 18:95-102.
8. Blancard, D., H. Lot, and B. Maisonneuve. 2006. A color atlas of diseases of lettuce and related salad crops: observation, biology and control. Academic Press, Burlington, MA.
9. Brandl, M. T. 2008. Plant lesions promote the rapid multiplication of Escherichia coli O157:H7 on postharvest lettuce. Appl. Environ. Microbiol. 74:5285-5289.
10. Centers for Disease Control and Prevention. 2011. Estimates of foodborne illness in the United States. Available at: http://www.cdc. gov/foodborneburden/. Accessed 8 January 2014.
11. Croci, L., D. De Medici, C. Scalfaro, A. Fiore, and L. Toti. 2002. The survival of hepatitis A virus in fresh produce. Int. J. Food Microbiol. 73:29-34.
12. Ding, S. W., B. J. Anderson, H. R. Haase, and R. H. Symons. 1994. New overlapping gene encoded by the cucumber mosaic virus genome. Virology 198:593-601.
13. Dingman, D. W. 2000. Growth of Escherichia coli O157:H7 in bruised apple (Malus domestica) tissue as influenced by cultivar, date of harvest, and source. Appl. Environ. Microbiol. 66:1077-1083.
14. Esseili, M. A., Q. Wang, and L. J. Saif. 2012. Binding of human GII.4 norovirus virus-like particles to carbohydrates of romaine lettuce leaf cell wall materials. Appl. Environ. Microbiol. 78:786-794.
15. Esseili, M. A., Q. Wang, Z. Zhang, and L. J. Saif. 2012. Internalization of sapovirus, a surrogate for norovirus, in romaine lettuce and the effect of lettuce latex on virus infectivity. Appl. Environ. Microbiol. 78:6271-6279.
16. Flood, J. 2010. The importance of plant health to food security. Food Secur. 2:215-231.
17. Frampton, R. A., A. R. Pitman, and P. C. Fineran. 2012. Advances in bacteriophage-mediated control of plant pathogens. Int. J. Microbiol. 2012:326452.
18. Gandhi, K. M., R. E. Mandrell, and P. Tian. 2010. Binding of viruslike particles of Norwalk virus to romaine lettuce veins. Appl. Environ. Microbiol. 76:7997-8003.
19. Ge, C., C. Lee, E. Nangle, J. Li, D. Gardner, M. Kleinhenz, and J. Lee. 2014. Impact of phytopathogen infection and extreme weather stress on internalization of Salmonella Typhimurium in lettuce. Int. J. Food Microbiol. 168-169:24-31.
20. Glass, R. I., U. D. Parashar, and M. K. Estes. 2009. Norovirus gastroenteritis. N. Engl. J. Med. 361:1776-1785.
21. Hall, A. J., M. E. Wikswo, K. Pringle, L. H. Gould, U. D. Parashar, and Division of Viral Diseases, National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention. 2014. Vital signs: foodborne norovirus outbreaks-United States, 2009-2012. Morb. Mortal. Wkly. Rep. 63:491-495.
22. Herman, M. A. B., S. Restrepo, and C. D. Smart. 2007. Defense gene expression patterns of three SAR-induced tomato cultivars in the field. Physiol. Mol. Plant Pathol. 71:192-200.
23. Hora, R., K. Warriner, B. J. Shelp, and M. W. Griffiths. 2005. Internalization of Escherichia coli O157:H7 following biological and mechanical disruption of growing spinach plants. J. Food Prot. 68: 2506-2509.
24. Hull, R. 2014. Plant virology, 5th ed. Elsevier Academic Press, Amsterdam.
25. Iniguez, A. L., Y. Dong, H. D. Carter, B. M. Ahmer, J. M. Stone, and E. W. Triplett. 2005. Regulation of enteric endophytic bacterial colonization by plant defenses. Mol. Plant Microbe Interact. 18:169-178.
26. Janisiewicz, W. J., W. S. Conway, M. W. Brown, G. M. Sapers, P. Fratamico, and R. L. Buchanan. 1999. Fate of Escherichia coli O157:H7 on fresh-cut apple tissue and its potential for transmission by fruit flies. Appl. Environ. Microbiol. 65:1-5.
27. Janisiewicz, W. J., W. S. Conway, and B. Leverentz. 1999. Biological control of postharvest decays of apple can prevent growth of Escherichia coli O157:H7 in apple wounds. J. Food Prot. 62: 1372-5.
28. Koo, H. L., N. Ajami, R. L. Atmar, and H. L. DuPo. 2010. Noroviruses: the principal cause of foodborne disease worldwide. Discov. Med. 10:61-70.
29. Kunkel, B. N., and D. M. Brooks. 2002. Cross talk between signaling pathways in pathogen defense. Curr. Opin. Plant Biol. 5:325-331.
30. Loebenstein, G. 2009. Local lesions and induced resistance. Adv. Virus Res. 75:73-117.
31. Mochizuki, T., and S. T. Ohki. 2012. Cucumber mosaic virus: viral genes as virulence determinants. Mol. Plant Pathol. 13:217-225.
32. Mukherjee, A., D. Speh, A. T. Jones, K. M. Buesing, and F. Diez-Gonzalez. 2006. Longitudinal microbiological survey of fresh produce grown by farmers in the upper midwest. J. Food Prot. 69: 1928-1936.
33. Nakamura, K., Y. Saga, M. Iwai, M. Obara, E. Horimoto, S. Hasegawa, T. Kurata, H. Okumura, M. Nagoshi, and T. Takizawa. 2010. Frequent detection of noroviruses and sapoviruses in swine and high genetic diversity of porcine sapovirus in Japan during fiscal year 2008. J. Clin. Microbiol. 48:1215-1222.
34. Palukaitis, P., M. J. Roossinck, R. G. Dietzgen, and R. I. Francki. 1992. Cucumber mosaic virus. Adv. Virus Res. 41:281-348.
35. Pang, X. L., B. E. Lee, G. J. Tyrrell, and J. K. Preiksaitis. 2009. Epidemiology and genotype analysis of sapovirus associated with gastroenteritis outbreaks in Alberta, Canada: 2004-2007. J. Infect. Dis. 199:547-551.
36. Reinders, R. D., S. Biesterveld, and P. G. Bijker. 2001. Survival of Escherichia coli O157:H7 ATCC 43895 in a model apple juice medium with different concentrations of proline and caffeic acid. Appl. Environ. Microbiol. 67:2863-2866.
37. Sahin, F., P. A. Abbasi, M. L. L. Ivey, J. Zhang, and S. A. Miller. 2003. Diversity among strains of Xanthomonas campestris pv. vitians from lettuce. Phytopathology 93:64-70.
38. Sahin, F., and S. A. Miller. 1997. Identification of the bacterial leaf spot pathogen of lettuce, Xanthomonas campestris pv. vitians, in Ohio, and assessment of cultivar resistance and seed treatment. Plant Dis. 81:1443-1446.
39. Scallan, E., R. M. Hoekstra, F. J. Angulo, R. V. Tauxe, M. A. Widdowson, S. L. Roy, J. L. Jones, and P. M. Griffin. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
40. Schikora, A., I. Virlogeux-Payant, E. Bueso, A. V. Garcia, T. Nilau, A. Charrier, S. Pelletier, P. Menanteau, M. Baccarini, P. Velge, and H. Hirt. 2011. Conservation of Salmonella infection mechanisms in plants and animals. PLoS One 6:e24112.
41. Seo, S., and K. R. Matthews. 2012. Influence of the plant defense response to Escherichia coli O157:H7 cell surface structures on survival of that enteric pathogen on plant surfaces. Appl. Environ. Microbiol. 78:5882-5889.
42. Shirron, N., and S. Yaron. 2011. Active suppression of early immune response in tobacco by the human pathogen Salmonella Typhimurium. PLoS One 6:e18855.
43. Smith-Becker, J., N. T. Keen, and J. O. Becker. 2003. Acibenzolar-Smethyl induces resistance to Colletotrichum lagenarium and cucumber mosaic virus in cantaloupe. Crop Prot. 22:769-774.
44. Takeuchi, K., C. M. Matute, A. N. Hassan, and J. F. Frank. 2000. Comparison of the attachment of Escherichia coli O157:H7, Listeria monocytogenes, Salmonella typhimurium, and Pseudomonas fluorescens to lettuce leaves. J. Food Prot. 63:1433-1437.
45. Teunis, P. F., C. L. Moe, P. Liu, S. E. Miller, L. Lindesmith, R. S. Baric, J. Le Pendu, and R. L. Calderon. 2008. Norwalk virus: how infectious is it? J Med Virol. 80:1468-1476.
46. Tukey, J. H. B., and J. V. Morgan. 1963. Injury to foliage and its effect upon tbe leaching of nutrients from above-ground plant parts. Physiol. Plant. 16:557-564.
47. Wang, Q., Z. Zhang, and L. J. Saif. 2012. Stability of and attachment to lettuce by a culturable porcine sapovirus surrogate for human caliciviruses. Appl. Environ. Microbiol. 78:3932-3940.
48. Wang, Q. H., V. Costantini, and L. J. Saif. 2007. Porcine enteric caliciviruses: genetic and antigenic relatedness to human caliciviruses, diagnosis and epidemiology. Vaccine 25:5453-5466.
49. Wells, J. M., and J. E. Butterfield. 1997. Salmonella contamination associated with bacterial soft rot of fresh fruits and vegetables in the marketplace. Plant Dis. 81:867-872.
50. Yigit, F. 2011. Acibenzolar-S-methyl induces lettuce resistance against Xanthomonas campestris pv. vitians. Afr. J. Biotechnol. 10: 9606-9612.