Internalization and dissemination of human norovirus and animal caliciviruses in hydroponically grown romaine lettuce

Applied and Environmental Microbiology

Volumn 78, Issue 17, 2012, Pages 6143-6152

  DiCaprio, Erin ^a   Ma, Yuanmei ^a   Purgianto, Anastasia ^a   Hughes, John ^b   Li, Jianrong ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FEED WATER; FRESH PRODUCE; INFECTIOUS VIRUS; LOW LEVEL; PLAQUE ASSAY; POSTHARVEST; REVERSE TRANSCRIPTION;

ANIMALS; RNA; VEHICLE TRANSMISSIONS; VIRUSES;

POLYMERASE CHAIN REACTION;

VIRUS RNA;

DISEASE TRANSMISSION; GENOME; HARVESTING; HYDROPONICS; INOCULATION; LEAFY VEGETABLE; POLYMERASE CHAIN REACTION; REAL TIME; SHOOT; VIRUS;

ANIMAL; ARTICLE; CALICIVIRUS; DNA SEQUENCE; GENETICS; HUMAN; ISOLATION AND PURIFICATION; LETTUCE; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PLANT; PLANT LEAF; PLANT ROOT; VIROLOGY; VIRUS ENTRY; VIRUS LOAD;

ANIMALS; CALICIVIRIDAE; HUMANS; LETTUCE; MOLECULAR SEQUENCE DATA; PLANT LEAVES; PLANT ROOTS; PLANT SHOOTS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRAL LOAD; VIRUS INTERNALIZATION;

ANIMALIA; LACTUCA; MURINE NOROVIRUS; NOROVIRUS;

EID: 84866165056     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01081-12     Document Type: Article

References (57)

1. Abbaszadegan M, LeChevallier M, Gerba CP. 2003. Occurrence of viruses in US groundwater. J. Am. Water Works Assoc. 95:107-120.
2. Bae J, Schwab KJ. 2008. Evaluation of murine norovirus, feline calicivirus, poliovirus, and MS2 as surrogates for human norovirus in a model of viral persistence in surface water and groundwater. Appl. Environ. Microbiol. 74:477-484.
3. Baert L, et al. 2011. Review: norovirus prevalence in Belgian, Canadian and French fresh produce: a threat to human health Int. J. Food Microbiol. 151:261-269.
4. Bernstein N, Sela S, Pinto R, Ioffe M. 2007. Evidence for internalization of Escherichia coli into the aerial parts of maize via the root system. J. Food Prot. 70:471-475.
5. Borchardt MA, Bertz PD, Spencer SK, Battiagelli DA. 2003. Incidence of enteric viruses in groundwater from household wells in Wisconsin. Appl. Environ. Microbiol. 69:1172-1180.
6. Bosch JC. 1983. Viruses in environmental waters, p 148-177. In Berg G (ed), Viral pollution of the environment. CRC Press, Inc., Boca Raton, FL.
7. Cannon JL, et al. 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.
8. Centers for Disease Control and Prevention. 2010. CDC reports 1 in 6 get sick from foodborne illnesses each year. CDC, Atlanta, GA. www.cdc.gov/media/pressrel/2010/r101215.html.
9. Chancellor DD, et al. 2006. Green onions: potential mechanism for hepatitis contamination. J. Food Prot. 69:1468-1472.
10. Choi C, Song I, Stine S, Pimentel J, Gerba CP. 2004. Role of irrigation and wastewater: comparison of subsurface irrigation and furrow irrigation. Water Sci. Technol. 50:61-68.
11. DeWaal CS, Bhuiya F. 2007. Outbreaks by the numbers: fruits and vegetables 1990-2005. Presented at the 2007 Annual Meeting of the International Association for Food Protection, Lake Buena Vista, Florida. http://www.cspinet.org/foodsafety/IAFPPoster.pdf.
12. de Wit PJ. 2007. How plants recognize pathogens and defend themselves. Cell. Mol. Life Sci. 64:2726-2732.
13. Doyle MP, Erickson MC. 2008. Summer meeting 2007-the problems with fresh produce: an overview. J. Appl. Microbiol. 105:317-330.
14. Duizer E, et al. 2004. Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 85:79-87.
15. Erickson MC, et al. 2010. Infrequent internalization of Escherichia coli O157:H7 into field-grown leafy greens. J. Food Prot. 73:500-506.
16. Esseili MA, Wang Q, Saif LJ. 2012. Human GII.4 norovirus-like particles (VLPs) bind to carbohydrates of Romaine lettuce leaf cell wall materials. Appl. Environ. Microbiol. 78:786-794.
17. Farkas T, et al. 2010. Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. J. Virol. 84:8617-8625.
18. 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.
19. 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. 77:3507-3517.
20. Gandhi KM, Mandrell RE, Tian P. 2010. Binding of Norwalk virus viral-like particles to veins of romaine lettuce. Appl. Environ. Microbiol. 76:7997-8003.
21. Heaton JC, Jones K. 2008. Microbial contamination of fruit and vegetables and the behavior of enteropathogens in the phyllosphere: a review. J. App. Microbiol. 104:613-626.
22. Hirneisen KA, Sharma M, Kniel KE. 2012. Human enteric pathogen internalization by root uptake into food crops. Foodborne Pathog. Dis. 9:396-405.
23. Huang P, et al. 2005. Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns. J. Virol. 79:6714-6722.
24. Hutson AM, Atmar RL, Graham DY, Estes MK. 2002. Norwalk virus infection and disease is associated with ABO histo-blood group type. J. Infect. Dis. 185:1335-1337.
25. Jablasone J, Warriner K, Griffiths M. 2005. Interactions of Escherichia coli O157:H7, Salmonella typhimurium and Listeria monocytogenes plants cultivated in a gnotobiotic system. Int. J. Food Microbiol. 99:7-18.
26. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW IV. 2003. STAT 1-dependent innate immunity to a Norwalk-like virus. Science 299:1575-1578.
27. Koopmans M, Duizer E. 2004. Foodborne viruses: an emerging problem. Int. J. Food Microbiol. 90:23-41.
28. Le Guyader FS, et al. 2006. Norwalk virus-specific binding to oyster digestive tissues. Emerg. Infect. Dis. 12:931-936.
29. Li J, Predmore A, Divers E, Lou F. 2012. New interventions against human norovirus: progress, opportunities, and challenges. Annu. Rev. Food Sci. Technol. 3:331-352.
30. Lou F, Neetoo H, Chen H, Li J. 2011. Inactivation of a human norovirus surrogate by high-pressure processing: effectiveness, mechanism, and potential application in the fresh produce industry. Appl. Environ. Microbiol. 77:1862-1871.
31. Lou F, Neetoo H, Li J, Chen H, Li J. 2011. 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. 77:8538-8547.
32. Lynch MF, Tauxe RV, Hedberg CW. 2009. The growing burden of foodborne outbreaks due to contaminated fresh produce: risks and opportunities. Epidemiol. Infect. 137:307-315.
33. Ma Y, Li J. 2011. Vesicular stomatitis virus as a vector to deliver human norovirus virus-like particles: a new vaccine candidate against an important non-cultivable virus. J. Virol. 85:2942-2952.
34. Maalouf H, et al. 2011. Strain-dependent norovirus bioaccumulation in oysters. Appl. Environ. Microbiol. 77:3189-3196.
35. Mead PS, et al. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
36. Moreno IM, Thompson JR, García-Arenal F. 2004. Analysis of the systemic colonization of cucumber plants by cucumber green mottle mosaic virus. J. Gen. Virol. 85:749-759.
37. Oron G, Goemans M, Manor Y, Feyen J. 1995. Poliovirus distribution in the soil-plant system under reuse of secondary wastewater. Water Res. 29:1069-1078.
38. Ponka A, Maunula L, Von Bonsdorff CH, Lyytikainen O. 1999. An outbreak of calicivirus associated with the consumption of frozen raspberries. Epidemiol. Infect. 123:469-474.
39. Postel S, Kemmerling B. 2009. Plant systems for recognition of pathogenassociated molecular patterns. Semin. Cell Dev. Biol. 20:1025-1031.
40. Predmore A, Li J. 2011. Enhanced removal of a human norovirus surrogate from fresh vegetables and fruits by a combination of surfactants and sanitizers. Appl. Environ. Microbiol. 77:4829-4838.
41. Rawsthorne H, Phister TG, Jaykus LA. 2009. Development of a fluorescent in situ method for visualization of enteric viruses. Appl. Environ. Microbiol. 75:7822-7827.
42. Richards GP. 2012. Critical review of norovirus surrogates in food safety research: rationale for considering volunteer studies. Food Environ. Virol. 4:6-13.
43. Scallan E, et al. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
44. Scipioni A, Mauroy A, Vinje J, Thiry E. 2008. Animal noroviruses. Vet. J. 178:32-45.
45. Seymour IJ, Appleton H. 2001. Foodborne viruses and fresh produce. J. Appl. Microbiol. 91:759-773.
46. Sharma M, et al. 2009. A novel approach to investigate the uptake and internalization of Escherichia coli O157:H7 in spinach cultivated in soil and hydroponic medium. J. Food Prot. 72:1513-1520.
47. Tan M, Jiang X. 2005. Norovirus and its histo-blood group antigen receptors: an answer to a historical puzzle. Trends Microbiol. 13:285-293.
48. Taube S, et al. 2009. Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J. Virol. 83:4092-4101.
49. Teunis PFM, et al. 2008. Norwalk virus: How infectious is it? J. Med. Virol. 80:1468-1476.
50. Tian P, Engelbrektson AL, Jiang X, Zhong W, Mandrell RE. 2007. Norovirus recognizes histo-blood group antigens on gastrointestinal cells of clams, mussels, and oysters: a possible mechanism of bioaccumulation. J. Food Prot. 70:2140-2147.
51. Tian P, Yang D, Mandrell R. 2011. Differences in the binding of human norovirus to and from romaine lettuce and raspberries by water and electrolyzed waters. J. Food Prot. 74:1364-1369.
52. Urbanucci A, Myrmel M, Berg I, von Bonsdorff CH, Maunula L. 2009. Potential internalization of caliciviruses in lettuce. Int. J. Food Microbiol. 135:175-178.
53. Ward RL, Mahler RJ. 1982. Uptake of bacteriophage f2 through plant roots. Appl. Environ. Microbiol. 43:1098-1103.
54. 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. 76:578-583.
55. Wei J, Jin Y, Sims T, Kniel KE. 2011. Murine norovirus-1 internalization into Lactuca sativa during irrigation. Appl. Environ. Microbiol. 77:2508-2512.
56. Wobus CE, Thackray LB, Virgin HW IV. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80:5104-5112.
57. Zheng DP, et al. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312-323.