Stability of and attachment to lettuce by a culturable porcine sapovirus surrogate for human caliciviruses

Applied and Environmental Microbiology

Volumn 78, Issue 11, 2012, Pages 3932-3940

  Wang, Qiuhong ^a   Zhang, Zhenwen ^a   Saif, Linda J ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALICIVIRUS; CULTURABLE; ETHANOL TREATMENT; FELINE CALICIVIRUS; FOOD-BORNE ILLNESS; HEAT INACTIVATION; INFECTIVITY ASSAY; ISO-ELECTRIC POINTS; LOW CONCENTRATIONS; NOROVIRUSES; PHYSICO-CHEMICAL TREATMENT; TRANSMISSION ROUTE; VIRAL PARTICLES; VIRAL RNA;

ETHANOL; POLYMERASE CHAIN REACTION; RNA; TISSUE CULTURE; VIRUSES;

CHLORINE;

ALCOHOL; CHLORINE; DISINFECTANT AGENT;

CHLORINE; CONCENTRATION (COMPOSITION); DISINFECTION; ETHANOL; LEAFY VEGETABLE; PH; PHYSICOCHEMICAL PROPERTY; STABILIZATION; VIRUS;

ANIMAL; ARTICLE; CELL LINE; DISINFECTION; DRUG EFFECT; FOOD CONTAMINATION; GENETICS; HEAT; HUMAN; LETTUCE; NOROVIRUS; PATHOGENICITY; PH; PHYSIOLOGY; SAPOVIRUS; SWINE; VIROLOGY; VIRUS INACTIVATION;

ANIMALS; CELL LINE; CHLORINE; DISINFECTANTS; DISINFECTION; ETHANOL; FOOD CONTAMINATION; HOT TEMPERATURE; HUMANS; HYDROGEN-ION CONCENTRATION; LETTUCE; NOROVIRUS; SAPOVIRUS; SWINE; VIRUS INACTIVATION;

CALICIVIRIDAE; FELINE CALICIVIRUS; LACTUCA; MIRIDAE; MURINAE; SAPOVIRUS; SUS;

EID: 84864082076     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.06600-11     Document Type: Article

References (55)

1. Atmar RL. 2010. Noroviruses-state of the art. Food Environ. Virol. 2:117-126.
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. Belliot G, Lavaux A, Souihel D, Agnello D, Pothier P. 2008. Use of murine norovirus as a surrogate to evaluate resistance of human norovirus to disinfectants. Appl. Environ. Microbiol. 74:3315-3318.
4. 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.
5. CDC. 2011. Updated norovirus outbreak management and disease prevention guidelines. MMWR Recommend. Rep. 60:1-20.
6. Chan MC, et al. 2006. Fecal viral load and norovirus-associated gastroenteritis. Emerg. Infect. Dis. 12:1278 -1280.
7. Chang KO, et al. 2004. Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc. Natl. Acad. Sci. U. S. A. 101:8733- 8738.
8. Chiba S, Nakata S, Numata-Kinoshita K, Honma S. 2000. Sapporo virus: history and recent findings. J. Infect. Dis. 181(Suppl. 2):S303-S308.
9. da Silva AK, Kavanagh OV, Estes MK, Elimelech M. 2011. Adsorption and aggregation properties of norovirus GI and GII virus-like particles demonstrate differing responses to solution chemistry. Environ. Sci. Technol. 45:520 -526.
10. Dolin R, et al. 1972. Biological properties of Norwalk agent of acute infectious nonbacterial gastroenteritis. Proc. Soc. Exp. Biol. Med. 140: 578-583.
11. Duizer E, et al. 2004. Inactivation of caliciviruses. Appl. Environ. Microbiol. 70:4538-4543.
12. Esseili MA, Wang Q, Saif LJ. 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.
13. Flynn WT, Saif LJ. 1988. Serial propagation of porcine enteric caliciviruslike virus in primary porcine kidney cell cultures. J. Clin. Microbiol. 26: 206-212.
14. Flynn WT, Saif LJ, Moorhead PD. 1988. Pathogenesis of porcine enteric calicivirus-like virus in four-day-old gnotobiotic pigs. Am. J. Vet. Res. 49:819-825.
15. Glass RI, et al. 2000. The epidemiology of enteric caliciviruses from humans: a reassessment using new diagnostics. J. Infect. Dis. 181(Suppl. 2):S254 -S261.
16. Guo M, Qian Y, Chang KO, Saif LJ. 2001. Expression and self-assembly in baculovirus of porcine enteric calicivirus capsids into virus-like particles and their use in an enzyme-linked immunosorbent assay for antibody detection in swine. J. Clin. Microbiol. 39:1487-1493.
17. Herman KM, Ayers TL, Lynch M. 2008. Foodborne disease outbreaks associated with leafy greens, 1973-2006, p 27. Abstr. Int. Conf. Emerg. Infect. Dis., Atlanta, GA, 16 to 19 March 2008.
18. Johnston CP, et al. 2007. Outbreak management and implications of a nosocomial norovirus outbreak. Clin. Infect. Dis. 45:534 -540.
19. Kageyama T, et al. 2003. Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J. Clin. Microbiol. 41:1548 -1557.
20. Keswick BH, et al. 1985. Inactivation of Norwalk virus in drinking water by chlorine. Appl. Environ. Microbiol. 50:261-264.
21. Kitajima M, et al. 2010. Development and application of a broadly reactive real-time reverse transcription-PCR assay for detection of murine noroviruses. J. Virol. Methods 169:269 -273.
22. Koseki S, Isobe S, Itoh K. 2004. Efficacy of acidic electrolyzed water ice for pathogen control on lettuce. J. Food Prot. 67:2544 -2549.
23. Kurdziel AS, Wilkinson N, Langton S, Cook N. 2001. Survival of poliovirus on soft fruit and salad vegetables. J. Food Prot. 64:706 -709.
24. Lamhoujeb S, Fliss I, Ngazoa SE, Jean J. 2008. Evaluation of the persistence of infectious human noroviruses on food surfaces by using real-time nucleic acid sequence-based amplification. Appl. Environ. Microbiol. 74: 3349-3355.
25. Liu P, et al. 2009. Persistence of human noroviruses on food preparation surfaces and human hands. Food Environ. Virol. 1:141-147.
26. Liu P, et al. 2011. Comparison of the activity of alcohol-based handrubs against human noroviruses using the fingerpad method and quantitative real-time PCR. Food Environ. Virol. 3:35- 42.
27. Liu P, Yuen Y, Hsiao HM, Jaykus LA, Moe C. 2010. Effectiveness of liquid soap and hand sanitizer against Norwalk virus on contaminated hands. Appl. Environ. Microbiol. 76:394 -399.
28. 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.
29. Macinga DR, Sattar SA, Jaykus LA, Arbogast JW. 2008. Improved inactivation of nonenveloped enteric viruses and their surrogates by a novel alcohol-based hand sanitizer. Appl. Environ. Microbiol. 74:5047- 5052.
30. Malek M, et al. 2009. Outbreak of norovirus infection among river rafters associated with packaged delicatessen meat, Grand Canyon, 2005. Clin. Infect. Dis. 48:31-37.
31. Mattison K, et al. 2007. Survival of calicivirus in foods and on surfaces: experiments with feline calicivirus as a surrogate for norovirus. J. Food Prot. 70:500 -503.
32. Mead PS, et al. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607- 625.
33. Moe CL. 2009. Preventing norovirus transmission: how should we handle food handlers? Clin. Infect. Dis. 48:38-40.
34. Mullis L, Saif LJ, Zhang Y, Zhang X, Azevedo MS. 2012. Stability of bovine coronavirus on lettuce surfaces under household refrigeration conditions. Food Microbiol. 30:180 -186.
35. Mumphrey SM, et al. 2007. Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J. Virol. 81:3251-3263.
36. Nowak P, et al. 2011. Measurement of the virolysis of human GII.4 norovirus in response to disinfectants and sanitisers. J. Virol. Methods 174:7-11.
37. Nuanualsuwan S, Cliver DO. 2003. Capsid functions of inactivated human picornaviruses and feline calicivirus. Appl. Environ. Microbiol. 69: 350-357.
38. Nuanualsuwan S, Cliver DO. 2003. Infectivity of RNA from inactivated poliovirus. Appl. Environ. Microbiol. 69:1629 -1632.
39. Nuanualsuwan S, Cliver DO. 2002. Pretreatment to avoid positive RTPCR results with inactivated viruses. J. Virol. Methods 104:217-225.
40. Park GW, et al. 2010. Comparative efficacy of seven hand sanitizers against murine norovirus, feline calicivirus, and GII.4 norovirus. J. Food Prot. 73:2232-2238.
41. Park GW, Sobsey MD. 2011. Simultaneous comparison of murine norovirus, feline calicivirus, coliphage MS2, and GII.4 norovirus to evaluate the efficacy of sodium hypochlorite against human norovirus on a fecally soiled stainless steel surface. Foodborne Pathog. Dis. 8:1005-1010.
42. Parwani AV, Flynn WT, Gadfield KL, Saif LJ. 1991. Serial propagation of porcine enteric calicivirus in a continuous cell line. Effect of medium supplementation with intestinal contents or enzymes. Arch. Virol. 120: 115-122.
43. Pecson BM, Ackermann M, Kohn T. 2011. Framework for using quantitative PCR as a nonculture based method to estimate virus infectivity. Environ. Sci. Technol. 45:2257-2263.
44. Pecson BM, Martin LV, Kohn T. 2009. Quantitative PCR for determining the infectivity of bacteriophage MS2 upon inactivation by heat, UV-B radiation, and singlet oxygen: advantages and limitations of an enzymatic treatment to reduce false-positive results. Appl. Environ. Microbiol. 75: 5544-5554.
45. Radford AD, Coyne KP, Dawson S, Porter CJ, Gaskell RM. 2007. Feline calicivirus. Vet. Res. 38:319 -335.
46. Scallan E, et al. 2011. Foodborne illness acquired in the United States- major pathogens. Emerg. Infect. Dis. 17:7-15.
47. Shin GA, Sobsey MD. 2008. Inactivation of norovirus by chlorine disinfection of water. Water Res. 42:4562- 4568.
48. Takanashi S, et al. 2011. Characterization of emerging GII.g/GII.12 noroviruses from a gastroenteritis outbreak in the United States in 2010. J. Clin. Microbiol. 49:3234 -3244.
49. Tan M, Jiang X. 2010. Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog. 6:e1000983.
50. Teunis PF, et al. 2008. Norwalk virus: how infectious is it? J. Med. Virol. 80:1468 -1476.
51. Wang QH, Chang KO, Han MG, Sreevatsan S, Saif LJ. 2006. Development of a new microwell hybridization assay and an internal control RNA for the detection of porcine noroviruses and sapoviruses by reverse transcription-PCR. J. Virol. Methods 132:135-145.
52. Wang QH, et al. 2005. Porcine noroviruses related to human noroviruses. Emerg. Infect. Dis. 11:1874 -1881.
53. Wang QH, et al. 2005. Genetic diversity and recombination of porcine sapoviruses. J. Clin. Microbiol. 43:5963-5972.
54. Wobus CE, Thackray LB, Virgin HW IV. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80: 5104-5112.
55. Zheng DP, et al. 2006. Norovirus classification and proposed strain nomenclature. Virology 346:312-323.