Effects of abiotic and biotic stresses on the internalization and dissemination of human norovirus surrogates in growing romaine lettuce

Applied and Environmental Microbiology

Volumn 81, Issue 14, 2015, Pages 4791-4800

  DiCaprio, Erin ^a   Purgianto, Anastasia ^b,c   Li, Jianrong ^a  

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

^b OHIO STATE UNIVERSITY   (United States)

^c H J Heinz Company   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLECTOR EFFICIENCY; DROUGHT; FLOODS; PLANTS (BOTANY); SOILS;

ABIOTIC STRESS; BIOTIC STRESS; CAUSATIVE AGENTS; DROUGHT STRESS; EFFECTIVE MEASURES; EXTREME WEATHER EVENTS; FRESH PRODUCE; PLAQUE ASSAY;

VIRUSES;

DROUGHT STRESS; FLOOD; GASTROENTERITIS; GROWTH RATE; LEAFY VEGETABLE; SURROGATE METHOD; VIRUS;

LACTUCA; LETTUCE MOSAIC VIRUS; MURINE NOROVIRUS 1; NOROVIRUS;

ANIMAL; CALICIVIRIDAE; CALICIVIRUS INFECTION; DROUGHT; FOOD CONTAMINATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; LETTUCE; NOROVIRUS; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PLANT LEAF; PLANT VIRUS; VIROLOGY; VIRUS ENTRY;

ANIMALS; CALICIVIRIDAE; CALICIVIRIDAE INFECTIONS; DROUGHTS; FOOD CONTAMINATION; HUMANS; LETTUCE; MOSAIC VIRUSES; NOROVIRUS; PLANT LEAVES; STRESS, PHYSIOLOGICAL; VIRUS INTERNALIZATION;

EID: 84931456613     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00650-15     Document Type: Article

References (72)

1. Hoffmann S, Batz MB, Morris JG, Jr. 2012. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J Food Prot 75:1292-1302. http://dx.doi.org/10.4315/0362-028X.JFP-11-417.
2. Hall AJ, Eisenbart VG, Etingue AL, Gould LH, Lopman BA, Parashar UD. 2012. Epidemiology of foodborne norovirus outbreaks, United States, 2001-2008. Emerg Infect Dis 18:1566-1573. http://dx.doi.org/10.3201/eid1810.120833.
3. Hall AJ, Lopman BA, Payne DC, Patel MM, Gastanaduy PA, Vinje J, Parashar UD. 2013. Norovirus disease in the United States. Emerg Infect Dis 19:1198-1205. http://dx.doi.org/10.3201/eid1908.130465.
4. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17:7-15. http://dx.doi.org/10.3201/eid1701.P11101.
5. US Centers for Disease Control and Prevention. 26 July 2013, posting date. Norovirus: facts for food handlers. Centers for Disease Control and Prevention, Atlanta, GA. http://www.cdc.gov/norovirus/downloads/foodhandlers.pdf.
6. 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. http://dx.doi.org/10.1017/S0950268808001969.
7. Doyle MP, Erickson MC. 2008. Summer meeting 2007-the problems with fresh produce: an overview. J Appl Microbiol 105:317-330. http://dx.doi.org/10.1111/j.1365-2672.2008.03746.x.
8. Jaykus LA, Escudero-Abarca B. 2010. Human pathogenic viruses in food, p 218-232. In Juneja VK, Sofos JN (ed), Pathogens and toxins in foods: challenges and interventions. ASM Press, Washington, DC.
9. 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. http://dx.doi.org/10.1146/annurev-food-022811-101234.
10. Herwaldt BL, Lew JF, Moe CL, Lewis DC, Humphrey CD, Monroe SS, Pon EW, Glass RI. 1994. Characterization of a variant strain of Norwalk virus from a food-borne outbreak of gastroenteritis on a cruise ship in Hawaii. J Clin Microbiol 32:861-866.
11. Falkenhorst G, Krusell L, Lisby M, Madsen SB, Bottiger B, Molbak K. 2005. Imported frozen raspberries cause a series of norovirus outbreaks in Denmark, 2005. Euro Surveill 10(38):pii=2795. http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=2795.
12. Le Guyader FS, Mittelholzer C, Haugarreau L, Hedlund KO, Alsterlund R, Pommepuy M, Svensson L. 2004. Detection of noroviruses in raspberries associated with a gastroenteritis outbreak. Int J Food Microbiol 97:179-186. http://dx.doi.org/10.1016/j.ijfoodmicro.2004.04.018.
13. Pönkä A, Maunula L, von Bonsdorff CH, Lyytikainen O. 1999. An outbreak of calicivirus associated with consumption of frozen raspberries. Epidemiol Infect 123:469-474. http://dx.doi.org/10.1017/S0950268899003064.
14. Sarvikivi E, Roivainen M, Maunula L, Niskanen T, Korhonen T, Lappalainen M, Kuusi M. 2012. Multiple norovirus outbreaks linked to imported frozen raspberries. Epidemiol Infect 140:260-267. http://dx.doi.org/10.1017/S0950268811000379.
15. Heaton JC, Jones K. 2008. Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. J Appl Microbiol 104:613-626. http://dx.doi.org/10.1111/j.1365-2672.2007.03587.x.
16. Barclay L, Park GW, Vega E, Hall A, Parashar U, Vinje J, Lopman B. 2014. Infection control for norovirus. Clin Microbiol Infect 20:731-740. http://dx.doi.org/10.1111/1469-0691.12674.
17. DiCaprio E, Ma Y, Hughes J, Li J. 2013. Epidemiology, prevention, and control of the number one foodborne illness: human norovirus. Infect Dis Clin North Am 27:651-674. http://dx.doi.org/10.1016/j.idc.2013.05.009.
18. Keswick BH, Satterwhite TK, Johnson PC, DuPont HL, Secor SL, Bitsura JA, Gary GW, Hoff JC. 1985. Inactivation of Norwalk virus in drinking water by chlorine. Appl Environ Microbiol 50:261-264.
19. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, Le Pendu J, Calderon RL. 2008. Norwalk virus: how infectious is it?. J Med Virol 80:1468-1476. http://dx.doi.org/10.1002/jmv.21237.
20. Brassard J, Gagne MJ, Genereux M, Cote C. 2012. Detection of human food-borne and zoonotic viruses on irrigated, field-grown strawberries. Appl Environ Microbiol 78:3763-3766. http://dx.doi.org/10.1128/AEM.00251-12.
21. Verhaelen K, Bouwknegt M, Rutjes SA, de Roda Husman AM. 2013. Persistence of human norovirus in reconstituted pesticides-pesticide application as a possible source of viruses in fresh produce chains. Int J Food Microbiol 160:323-328. http://dx.doi.org/10.1016/j.ijfoodmicro.2012.11.007.
22. Stine SW, Song I, Choi CY, Gerba CP. 2011. Application of pesticide sprays to fresh produce: a risk assessment for hepatitis A and Salmonella. Food Environ Virol 3:86-91. http://dx.doi.org/10.1007/s12560-011-9061-x.
23. Borchardt MA, Bertz PD, Spencer SK, Battigelli DA. 2003. Incidence of enteric viruses in groundwater from household wells in Wisconsin. Appl Environ Microbiol 69:1172-1180. http://dx.doi.org/10.1128/AEM.69.2.1172-1180.2003.
24. Borchardt MA, Bradbury KR, Gotkowitz MB, Cherry JA, Parker BL. 2007. Human enteric viruses in groundwater from a confined bedrock aquifer. Environ Sci Technol 41:6606-6612. http://dx.doi.org/10.1021/es071110+.
25. Fout GS, Martinson BC, Moyer MW, Dahling DR. 2003. A multiplex reverse transcription-PCR method for detection of human enteric viruses in groundwater. Appl Environ Microbiol 69:3158-3164. http://dx.doi.org/10.1128/AEM.69.6.3158-3164.2003.
26. Gabrieli R, Maccari F, Ruta A, Pana A, Divizia M. 2009. Norovirus detection in groundwater. Food Environ Virol 1:92-96. http://dx.doi.org/10.1007/s12560-009-9014-9.
27. Haramoto E, Yamada K, Nishida K. 2011. Prevalence of protozoa, vi-ruses, coliphages and indicator bacteria in groundwater and river water in the Kathmandu Valley, Nepal. Trans R Soc Trop Med Hyg 105:711-716. http://dx.doi.org/10.1016/j.trstmh.2011.08.004.
28. Hörman A, Rimhanen-Finne R, Maunula L, von Bonsdorff CH, Torvela N, Heikinheimo A, Hanninen ML. 2004. Campylobacter spp., Giardia spp., Cryptosporidium spp., noroviruses, and indicator organisms in surface water in southwestern Finland, 2000-2001. Appl Environ Microbiol 70:87-95. http://dx.doi.org/10.1128/AEM.70.1.87-95.2004.
29. Koh SJ, Cho HG, Kim BH, Choi BY. 2011. An outbreak of gastroenteritis caused by norovirus-contaminated groundwater at a waterpark in Korea. J Korean Med Sci 26:28-32. http://dx.doi.org/10.3346/jkms.2011.26.1.28.
30. Lodder WJ, de Roda Husman AM. 2005. Presence of noroviruses and other enteric viruses in sewage and surface waters in The Netherlands. Appl Environ Microbiol 71:1453-1461. http://dx.doi.org/10.1128/AEM.71.3.1453-1461.2005.
31. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE, Neill FH, Graham DY. 2008. Norwalk virus shedding after experimental human infection. Emerg Infect Dis 14:1553-1557. http://dx.doi.org/10.3201/eid1410.080117.
32. Rodríguez-Lázaro D, Cook N, Ruggeri FM, Sellwood J, Nasser A, Nascimento MS, D'Agostino M, Santos R, Saiz JC, Rzezutka A, Bosch A, Girones R, Carducci A, Muscillo M, Kovac K, Diez-Valcarce M, Vantarakis A, von Bonsdorff CH, de Roda Husman AM, Hernandez M, van der Poel WH. 2012. Virus hazards from food, water and other contaminated environments. FEMS Microbiol Rev 36:786-814. http://dx.doi.org/10.1111/j.1574-6976.2011.00306.x.
33. Maunula L, Kaupke A, Vasickova P, Soderberg K, Kozyra I, Lazic S, van der Poel WH, Bouwknegt M, Rutjes S, Willems KA, Moloney R, D'Agostino M, de Roda Husman AM, von Bonsdorff CH, Rzezutka A, Pavlik I, Petrovic T, Cook N. 2013. Tracing enteric viruses in the European berry fruit supply chain. Int J Food Microbiol 167:177-185. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.09.003.
34. Blatchley ER, III, Gong WL, Alleman JE, Rose JB, Huffman DE, Otaki M, Lisle JT. 2007. Effects of wastewater disinfection on waterborne bacteria and viruses. Water Environ Res 79:81-92. http://dx.doi.org/10.2175/106143006X102024.
35. Block JC. 1983. Viruses in environmental waters, p 117-145. In Berg G (ed), Viral pollution of the environment. CRC Press Inc, Boca Raton, FL.
36. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. 2008. Norovirus pathogenesis: mechanisms of persistence and immune evasion in human populations. Immunol Rev 225:190-211. http://dx.doi.org/10.1111/j.1600-065X.2008.00680.x.
37. Donaldson EF, Lindesmith LC, Lobue AD, Baric RS. 2010. Viral shapeshifting: norovirus evasion of the human immune system. Nat Rev Microbiol 8:231-241. http://dx.doi.org/10.1038/nrmicro2296.
38. Hardy ME. 2005. Norovirus protein structure and function. FEMS Microbiol Lett 253:1-8. http://dx.doi.org/10.1016/j.femsle.2005.08.031.
39. Bozkurt H, D'Souza DH, Davidson PM. 2013. Determination of the thermal inactivation kinetics of the human norovirus surrogates, murine norovirus and feline calicivirus. J Food Prot 76:79-84. http://dx.doi.org/10.4315/0362-028X.JFP-12-327.
40. 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.
41. Cromeans T, Park GW, Costantini V, Lee D, Wang Q, Farkas T, Lee A, Vinje J. 2014. Comprehensive comparison of cultivable norovirus surrogates in response to different inactivation and disinfection treatments. Appl Environ Microbiol 80:5743-5751. http://dx.doi.org/10.1128/AEM.01532-14.
42. Hirneisen KA, Kniel KE. 2013. Comparing human norovirus surrogates: murine norovirus and Tulane virus. J Food Prot 76:139-143. http://dx.doi.org/10.4315/0362-028X.JFP-12-216.
43. Kniel KE. 2014. The makings of a good human norovirus surrogate. Curr Opin Virol 4:85-90. http://dx.doi.org/10.1016/j.coviro.2014.01.002.
44. Wobus CE, Thackray LB, Virgin HW, IV. 2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol 80: 5104-5112. http://dx.doi.org/10.1128/JVI.02346-05.
45. 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. http://dx.doi.org/10.1128/JVI.00070-08.
46. Farkas T, Cross RW, Hargitt E, III, Lerche NW, Morrow AL, Sestak K. 2010. Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. J Virol 84:8617-8625. http://dx.doi.org/10.1128/JVI.00630-10.
47. DiCaprio E, Ma Y, Purgianto A, Hughes J, Li J. 2012. Internalization and dissemination of human norovirus and animal caliciviruses in hydroponically grown romaine lettuce. Appl Environ Microbiol 78:6143-6152. http://dx.doi.org/10.1128/AEM.01081-12.
48. Esseili MA, Wang Q, Zhang Z, Saif LJ. 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. http://dx.doi.org/10.1128/AEM.01295-12.
49. Ward RL, Mahler RJ. 1982. Uptake of bacteriophage f2 through plant roots. Appl Environ Microbiol 43:1098-1103.
50. Hirneisen KA, Kniel KE. 2013. Comparative uptake of enteric viruses into spinach and green onions. Food Environ Virol 5:24-34. http://dx.doi.org/10.1007/s12560-012-9093-x.
51. Erickson MC. 2012. Internalization of fresh produce by foodborne pathogens. Annu Rev Food Sci Technol 3:283-310. http://dx.doi.org/10.1146/annurev-food-022811-101211.
52. Chancellor DD, Tyagi S, Bazaco MC, Bacvinskas S, Chancellor MB, Dato VM, de Miguel F. 2006. Green onions: potential mechanism for hepatitis A contamination. J Food Prot 69:1468-1472.
53. Urbanucci A, Myrmel M, Berg I, von Bonsdorff CH, Maunula L. 2009. Potential internalisation of caliciviruses in lettuce. Int J Food Microbiol 135:175-178. http://dx.doi.org/10.1016/j.ijfoodmicro.2009.07.036.
54. Wei J, Jin Y, Sims T, Kniel KE. 2011. Internalization of murine norovirus 1 by Lactuca sativa during irrigation. Appl Environ Microbiol 77:2508-2512. http://dx.doi.org/10.1128/AEM.02701-10.
55. 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. http://dx.doi.org/10.1128/AEM.01918-10.
56. Wang J, Provin T, Zhang H. 15 January 2015, posting date. Measurement of soil salinity and sodicity. http://www.academia.edu/7745212/Measurement_of_Soil_Salinity_and_Sodicity.
57. Ge C, Lee C, Nangle E, Li J, Gardner D, Kleinhenz M, Lee J. 2014. Impact of phytopathogen infection and extreme weather stress on internalization of Salmonella Typhimurium in lettuce. Int J Food Microbiol 168-169:24-31. http://dx.doi.org/10.1016/j.ijfoodmicro.2013.10.010.
58. Wong K, Mukherjee B, Kahler AM, Zepp R, Molina M. 2012. Influence of inorganic ions on aggregation and adsorption behaviors of human adenovirus. Environ Sci Technol 46:11145-11153. http://dx.doi.org/10.1021/es3028764.
59. Attinti R, Wei J, Kniel K, Sims JT, Jin Y. 2010. Virus' (MS2, ϕX174, and Aichi) attachment on sand measured by atomic force microscopy and their transport through sand columns. Environ Sci Technol 44:2426-2432. http://dx.doi.org/10.1021/es903221p.
60. Ge CT, Lee C, Lee J. 2012. The impact of extreme weather events on Salmonella internalization in lettuce and green onion. Food Res Int 45: 1118-1122. http://dx.doi.org/10.1016/j.foodres.2011.06.054.
61. Santamaría J, Toranzos GA. 2003. Enteric pathogens and soil: a short review. Int Microbiol 6:5-9. http://dx.doi.org/10.1007/s10123-003-0096-1.
62. Herbold-Paschke K, Straub U, Hahn T, Teutsch G, Botzenhart K. 1991. Behaviour of pathogenic bacteria, phages and viruses in ground water during transport and adsorption. Water Sci Technol 24:301-304.
63. Yates MV, Gerba CP. 1985. Factors controlling the survival of viruses in groundwater. Water Sci Technol 17:681-687.
64. Keswick BH, Gerba CP. 1980. Viruses in groundwater. Environ Sci Technol 14:1290-1297. http://dx.doi.org/10.1021/es60171a602.
65. Sobsey MD, Dean CH, Knuckles ME, Wagner RA. 1980. Interactions and survival of enteric viruses in soil materials. Appl Environ Microbiol 40:92-101.
66. Sobsey MD, Hickey AR. 1985. Effects of humic and fulvic acids on poliovirus concentration from water by microporous filtration. Appl Environ Microbiol 49:259-264.
67. Tanner W, Beevers H. 2001. Transpiration, a prerequisite for longdistance transport of minerals in plants?. Proc Natl Acad Sci USA 98: 9443-9447. http://dx.doi.org/10.1073/pnas.161279898.
68. Farooq M, Hussain M, Wahid A, Siddique KHM. 2012. Drought stress in plants: an overview, p 1-33. In Aroca R (ed), Plant responses to drought stress. Springer-Verlag, Berlin, Germany.
69. Melotto M, Underwood W, Koczan J, Nomura K, He SY. 2006. Plant stomata function in innate immunity against bacterial invasion. Cell 126: 969-980. http://dx.doi.org/10.1016/j.cell.2006.06.054.
70. Pink DAC, Kostova D, Walkey DGA. 1992. Differentiation of pathotypes of lettuce mosaic virus. Plant Pathol 41:5-12. http://dx.doi.org/10.1111/j.1365-3059.1992.tb02308.x.
71. Prevost B, Lucas FS, Goncalves A, Richard F, Moulin L, Wurtzer S. 2015. Large scale survey of enteric viruses in river and waste water underlines the health status of the local population. Environ Int 79:42-50. http://dx.doi.org/10.1016/j.envint.2015.03.004.
72. Grondahl-Rosado RC, Yarovitsyna E, Trettenes E, Myrmel M, Robertson LJ. 2014. A one year study on the concentrations of norovirus and enteric adenoviruses in wastewater and a surface drinking water source in Norway. Food Environ Virol 6:232-245. http://dx.doi.org/10.1007/s12560-014-9161-5.