Nonculturable response of animal enteropathogens in the agricultural environment and implications for food safety

Journal of Food Protection

Volumn 72, Issue 6, 2009, Pages 1342-1354

  Dinu, Laura Dorina ^a,b   Delaquis, Pascal ^a   Bach, Susan ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b UNIVERSITY OF AGRONOMIC SCIENCES AND VETERINARY MEDICINE OF BUCHAREST   (Romania)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LISTERIA MONOCYTOGENES; SALMONELLA; SHIGELLA;

EID: 67650084824     PISSN: 0362028X     EISSN: None     Source Type: Journal    
DOI: 10.4315/0362-028X-72.6.1342     Document Type: Review

References (118)

1. Aertsen, A., and C. W. Michiels. 2004. Stress and how bacteria cope with death and survival. Crit. Rev. Microbiol. 30:263-273.
2. Arana, I., M. Orruno, D. Perez-Pascual, C. Seco, A. Muela, and I. Barcina. 2007. Inability of Escherichia coli to resuscitate from the viable but nonculturable state. FEMS Microbiol. Ecol. 62:1-11.
3. Arana, I., M. Orruno, C. Seco, A. Muela, and I. Barcina. 2008. Is Urografin density gradient centrifugation suitable to separate nonculturable cells from Escherichia coli populations? Antonie Leeuwenhoek 93:249-257.
4. Arana, I., C. Seco, K. Epelde, A. Muela, A. Fernandez-Astorga, and I. Barcina. 2004. Relationships between Escherichia coli cells and the surrounding medium during survival processes. Antonie Leeuwenhoek 86:189-199.
5. Artz, R. R. E., L. M. Avery, D. L. Jones, and K. Killham. 2006. Potential pitfalls in the quantitative molecular detection of Escherichia coli O157:H7 in environmental matrices. Can. J. Microbiol. 52:482-488.
6. Asakura, H., S. Igimi, K. Kawamoto, S. Yamamoto, and S. Makino. 2005. Role of in vivo passage on the environmental adaptation of enterohemorrhagic Escherichia coli O157:H7: cross-induction of the viable but nonculturable state by osmotic and oxidative stresses. FEMS Microbiol. Lett. 253:243-249.
7. Asakura, H., S. Makino, T. Takagi, A. Kuri, T. Kurazono, M. Watarai, and T. Shirahata. 2002. Passage in mice causes a change in the ability of Salmonella enterica serovar Oranienburg to survive NaCl osmotic stress: resuscitation from the viable but non-culturable state. FEMS Microbiol. Lett. 212:87-93.
8. Asakura, H., N. Panutdaporn, K. Kawamoto, S. Igimi, S. Yamamoto, and S. Makino. 2007. Proteomic characterization of enterohemorrhagic Escherichia coli O157:H7 in the oxidation-induced viable but non-culturable state. Microbiol. Immunol. 51:875-881.
9. Awais, R., H. Fukudomi, K. Miyanaga, H. Unno, and Y. Tanji. 2006. A recombinant bacteriophage-based assay for the discriminative detection of culturable and viable but nonculturable Escherichia coli O157:H7. Biotechnol. Prog. 22:853-859.
10. Barer, M. R., R. J. Smith, R. P. Cooney, and P. T. Kimmitt. 2000. Relationships between culturability, activity and virulence in pathogenic bacteria. J. Infect. Chemother. 6:108-111.
11. Beattie, G. A., and S. E. Lindow. 1995. The secret life of foliar bacterial pathogens on leaves. Annu. Rev. Phytopathol. 33:145-172.
12. Besnard, V., M. Federighi, and J. M. Cappelier. 2000. Development of a direct viable count procedure for the investigation of VBNC state in Listeria monocytogenes. Lett. Appl. Microbiol. 31:77-81.
13. Besnard, V., M. Federighi, and J. M. Cappelier. 2000. Evidence of viable but nonculturable state in Listeria monocytogenes by direct viable count and CTC-DAPI double staining. Food Microbiol. 17: 697-704.
14. Besnard, V., M. Federighi, E. Declerq, F. Jugiau, and J. M. Cappelier. 2002. Environmental and physico-chemical factors induce VBNC state in Listeria monocytogenes. Vet. Res. 33:359-370.
15. Beuchat, L. R. 2002. Ecological factors influencing survival and growth of human pathogens on raw fruits and vegetables. Microbes Infect. 4:413-423.
16. Bloomfield, S. F., G. S. A. B. Stewart, C. E. R. Dodd, I. R. Booth, and E. G. M. Power. 1998. The viable but non-culturable phenomenon explained? Microbiology 144:1-2.
17. Bogosian, G., and E. V. Bourneuf. 2001. A matter of bacterial life and death. EMBO Rep. 2:770-774.
18. Bogosian. G., P. J. Morris, and J. P. O'Neil. 1998. A mixed culture recovery method indicates that enteric bacteria do not enter the viable but nonculturable state. Appl. Environ. Microbiol. 64:1736-1742.
19. Brandl, M. T. 2006. Fitness of human enteric pathogens on plants and implication for foods safety. Annu. Rev. Phytopathol. 44:367-392.
20. Brandl, M. T., A. F. Haxo, A. H. Bates, and R. E. Mandrell. 2004. Comparison of survival of Campylobacter jejuni in the phyllosphere with that in the rhizosphere of spinach and radish plants. Appl. Environ. Microbiol. 70:1182-1189.
21. Brandl, M. T., and R. E. Mandrell. 2002. Fitness of Salmonella enterica serovar Thompson in the cilantro phyllosphere. Appl. Environ. Microbiol. 68:3614-3621.
22. Brandl, M. T., W. G. Miller, A. H. Bates, and R. E. Mandrell. 2005. Production of autoinducer 2 in Salmonella enterica serovar Thompson contributes to its fitness in chickens but not on cilantro leaf surfaces. Appl. Environ. Microbiol. 71:2653-2662.
23. Byrd, J. J., J. G. Leahy, and R. R. Colwell. 1992. Determination of plasmid DNA concentration maintained by nonculturable Escherichia coli in marine microcosms. Appl. Environ. Microbiol. 58: 2266-2270.
24. Cappelier, J. M., V. Besnard, S. Roche, N. Garrec, E. Zundel, P. Velge, and M. Federighi. 2005. Avirulence of viable but nonculturable Listeria monocytogenes cells demonstrated by in vitro and in vivo models. Vet. Res. 36:589-599.
25. Cappelier, J. M., V. Besnard, S. M. Roche, P. Velge, and M. Federighi. 2007. Avirulent viable but non culturable cells of Listeria monocytogenes need the presence of an embryo to be recovered in egg yolk and regain virulence after recovery. Vet. Res. 38: 573-583.
26. Caro, A., P. Got, J. Lesne, S. Binard, and B. Baleux. 1999. Viability and virulence of experimentally stressed nonculturable Salmonella typhimurium. Appl. Environ. Microbiol. 65:3229-3232.
27. Chmielewski, R. A., and J. F. Frank. 1995. Formation of viable but nonculturable Salmonella during starvation in chemically defined solutions. Lett. Appl. Microbiol. 20:380-384.
28. Cho, J. C., and S. J. Kim. 1999. Green fluorescent protein-based direct viable count to verify a viable but non-culturable state of Salmonella typhi in environmental samples. J. Microbiol. Methods 36:227-235.
29. Cho, J. C., and S. J. Kim. 1999. Viable, but non-culturable, state of a green fluorescence protein-tagged environmental isolate of Salmonella typhi in groundwater and pond water. FEMS Microbiol. Lett. 170:257-264.
30. Colwell, R. R. 2000. Viable but nonculturable bacteria: a survival strategy. J. Infect. Chemother. 6:121-125
31. Colwell, R. R., P. R. Brayton, D. J. Grimes, D. B. Roszak, S. A. Huq, and L. M. Palmer. 1985. Viable but non-culturable Vibrio and related pathogens in environment: implications for the release of genetically engineered microorganisms. Biotechnology 3:817-820.
32. Cooley, M. B., W. G. Miller, and R. E. Mandrell. 2003. Colonization of Arabidopsis thaliana with Salmonella enterica and enterohemorrhagic Escherichia coli O157:H7 and competition by Enterobacter asburiae. Appl. Environ. Microbiol. 69:4915-4926.
33. Davies, C. M., S. C. Apte, and S. M. Peterson. 1995. Beta-D-galactosidase activity, of viable non-culturable coliform bacteria in marine waters. Lett. Appl. Microbiol. 21:99-102.
34. Davies, C. M., and L. M. Evison. 1991. Sunlight and survival of enteric bacteria in natural waters. J. Appl. Bacteriol. 70:265-274.
35. Delaquis, P., S. Bach, and L.-D. Dinu. 2007. Behavior of Escherichia coli O157:H7 in leafy vegetables. J. Food Prot. 70:1966-1974.
36. Desmonts, C., J. Minet, R. Colwell, and M. Cormier. 1990. Fluorescent-antibody method useful for detecting viable but nonculturable Salmonella spp. in chlorinated wastewater. Appl. Environ. Microbiol. 56:1448-1452.
37. Dong, Y., A. L. Iniguez, B. M. Ahmer, and E. W. Triplett. 2003. Kinetics and strain specificity of rhizosphere and endophytic colonization by enteric bacteria on seedlings of Medicago sativa and Medicago truncatula. Appl Environ. Microbiol. 69:1783-1790.
38. Doyle, M. P., and M. Erickson. 2008. Summer meeting 2007-the problem with fresh produce: an overview. J. Appl. Microbiol. 105: 317-330.
39. Dreux, N., C. Albagnac, F. Carlin, C. E. Morris, and C. Nguyen-The. 2007. Fate of Listeria spp. on parsley leaves grown in laboratory and field cultures. J. Appl. Microbiol. 103:1821-1827.
40. Dreux, N., C. Albagnac, M. Federighi, F. Carlin, C. E. Morris, and C. Nguyen-The. 2007. Viable but non-culturable Listeria monocytogenes on parsley leaves and absence of recovery to a culturable state. J. Appl. Microbiol. 103:1272-1281.
41. Dreux, N., C. Albagnac, R. D. Sleator, C. Hill, F. Carlin, C. E. Morris, and C. Nguyen-The. 2008. Glycine betaine improves Listeria monocytogenes tolerance to desiccation on parsley leaves independent of the osmolyte transporters BetL, Gbu and OpuC. J. Appl. Microbiol. 104:1221-1227.
42. Edwards, C. 2000. Problems posed by natural environments for monitoring microorganisms. Mol. Biotechnol. 15:211-223.
43. Foong, S. C., and J. S. Dickson. 2004. Survival and recovery of viable but nonculturable Listeria monocytogenes cells in a nutritionally depleted medium. J. Food Prot. 67:1641-1645.
44. Gagliardi, J. V., and J. S. Karns. 2002. Persistence of Escherichia coli O157:H7 in soil and on plant roots. Environ. Microbiol. 4:89-96.
45. Gauthier, M. J. 2000. Environmental parameters associated with the viable but nonculturable state, p. 87-112. In R. R. Colwell and D. J. Grimes (ed.), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
46. Ghezzi, J. I., and T. R. Steck. 1999. Induction of the viable but non-culturable condition in Xanthomonas campestris pv. campestris in liquid microcosms and sterile soil. FEMS Microbiol. Ecol. 30: 203-208.
47. Grey, B., and T. R. Steck. 2001. Concentrations of copper thought to be toxic to Escherichia coli can induce the viable but nonculturable condition. Appl. Environ. Microbiol. 67:5325-5327.
48. Grey, B. E., and T. R. Steck. 2001. The viable but nonculturable state of Ralstonia solanacearum may be involved in long-term survival and plant infection. Appl. Environ. Microbiol. 67:3866-3872.
49. Gupte, A. R., C. L. De Rezende, and S. W. Joseph. 2003. Induction and resuscitation of viable but nonculturable Salmonella enterica serovar typhimurium DT104. Appl. Environ. Microbiol. 69:6669-6675.
50. Guy, R. A., A. Kapoor, J. Holicka, D. Shepherd, and P. A. Horgen. 2006. A rapid molecular-based assay for direct quantification of viable bacteria in slaughterhouses. J. Food Prot. 69:1265-1272.
51. Heaton, J. C., and K. Jones. 2007. Microbial contamination of fruit and vegetables and the behaviour of enteropathogens in the phyllosphere: a review. J. Appl. Microbiol. 104:613-626.
52. Hirano, S. S., and C. D. Upper. 2000. Bacteria in the leaf ecosystem with emphasis on Pseudomonas syringae-a pathogen, ice nucleus, and epiphyte. Microb. Mol. Biol. Rev. 64:624-653.
53. Huq, A., I. N. G. Rivera, and R. R. Colwell. 2000. Epidemiological significance of viable but nonculturable microorganisms, p. 301-323. In R. R. Colwell and D. J. Grimes (ed.), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
54. Ibekwe, A. M., C. M. Grieve, and C. H. Yang. 2007. Survival of Escherichia coli O157:H7 in soil and on lettuce after soil fumigation. Can. J. Microbiol. 53:623-635.
55. Ibekwe, A. M., P. J. Shouse, and C. M. Grieve. 2006. Quantification of survival of Escherichia coli O157:H7 on plants affected by contaminated irrigation water. Eng. Life Sci. 6:566-572.
56. Ibekwe, A. M., P. M. Watt, P. J. Shouse, and C. M. Grieve. 2004. Fate of Escherichia coli O157:H7 in irrigation water on soils and plants as validated by culture method and real-time PCR. Can. J. Microbiol. 50:1007-1014.
57. Islam, M., M. P. Doyle. S. C. Phatak, P. Millner, and X. Jiang. 2004. Persistence of enterohemorrhagic Escherichia coli O157:H7 in soil and on leaf lettuce and parsley grown in fields treated with contaminated manure composts or irrigation water. J. Food Prot. 67:1365-1370.
58. Islam, M., J. Morgan, M. P. Doyle, S. C. Phatak, P. Millner, and X. Jiang. 2004. Persistence of Salmonella enterica serovar typhimurium on lettuce and parsley and in soils on which they were grown in fields treated with contaminated manure composts and irrigation water. Foodborne Pathog. Dis. 91:27-35.
59. Islam, M. S., M. K. Hasan, M. A. Miah, G. C. Sur, A. Felsenstein, M. Venkatesan, R. B. Sack, and M. J. Albert. 1993. Use of polymerase chain reaction and fluorescent-antibody methods for detecting viable but nonculturable Shigella dysenteriae type 1 in laboratory microcosms. Appl. Environ. Microbiol. 59:536-540.
60. Jablasone, J., K. Warriner, and M. Griffiths. 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.
61. Jiang, X., J. Morgan, and M. P. Doyle. 2002. Fate of Escherichia coli O157:H7 in manure-amended soil. Appl. Environ. Microbiol. 68:2605-2609.
62. Jolivet-Gougeon, A., F. Sauvager, M. Bonnaure-Mallet, R. R. Colwell, and M. Cormier. 2006. Virulence of viable but nonculturable S. Typhimurium LT2 after peracetic acid treatment. Int. J. Food Microbiol. 112:147-152.
63. Keep, N. H., J. M. Ward, G. Robertson, M. Cohen-Gonsaud, and B. Henderson. 2006. Bacterial resuscitation factors: revival of viable but non-culturable bacteria. Cell. Mol. Life Sci. 63:2555-2559.
64. Kell, D. B., A. S. Kaprelyants, D. H. Weichart, C. R. Harwood, and M. R. Barer. 1998. Viability and activity in readily culturable bacteria: a review and discussion of the practical issues. Antonie Leeuwenhoek 73:169-187.
65. Kell, D. B., and M. Young. 2000. Bacterial dormancy and culturability: the role of autocrine growth factors. Curr. Opin. Microbiol. 3:238-243.
66. Kolling, G. L., and K. R. Matthews. 2001. Examination of recovery in vitro and in vivo of nonculturable Escherichia coli O157:H7. Appl. Environ. Microbiol. 67:3928-3933.
67. Li, J., G. L. Kolling, K. R. Matthews, and M. L. Chikindas. 2003. Cold and carbon dioxide used as multi-hurdle preservation do not induce appearance of viable but non-culturable Listeria monocytogenes. J. Appl. Microbiol. 94:48-53.
68. Liu, Y., A. Gilchrist, J. Zhang, and X. F. Li. 2008. Detection of viable but non-culturable Escherichia coli O157:H7 in drinking water and river water. Appl. Environ. Microbiol. 74:1502-1507.
69. Makino, S. I., T. Kii, H. Asakura, T. Shirahata, T. Ikeda, K. Takeshi, and K. Itoh. 2000. Does enterohemorrhagic Escherichia coli enter the viable but nonculturable state in salted salmon roe? Appl. Environ. Microbiol. 66:5536-5539.
70. Marsh, P., Z. M. Nathan, and E. M. H. Wellington. 1998. Quantitative molecular detection of Salmonella typhimurium in soil and demonstration of persistence of an active but non-culturable population. FEMS Microb. Ecol. 27:351-363.
71. Maule, A. 2000. Survival of verocytotoxigenic Escherichia coli O157:H7 in soil, water and on surfaces. Symp. Ser. Soc. Appl. Microbiol. 29:71S-78S.
72. McDougald, D., S. A. Rice, D. Weichart, and S. Kjelleberg. 1998. Nonculturability: adaptation or debilitation? FEMS Microbiol. Ecol. 25:1-9.
73. Mizunoe, Y., S. N. Wai, A. Takade, and S. Yoshida. 1999. Restoration of culturability of starvation-stressed and low-temperaturestressed Escherichia coli O157 cells by using H2O2-degrading compounds. Arch. Microbiol. 172:63-67.
74. Muela, A., C. Seco, E. Camafeita, I. Arana, M. Orruno, J. A. Lopez, and I. Barcina. 2008. Changes in Escherichia coli outer membrane subproteome under environmental conditions inducing the viable but nonculturable state. FEMS Microbiol. Ecol. 64:28-36.
75. Munro, P. M., G. N. Flatau, R. L. Clement, and M. J. Gauthier. 1995. Influence of the RpoS (KatF) sigma factor on maintenance of viability and culturability of Escherichia coli and Salmonella typhimurium in sea water. Appl. Environ. Microbiol. 61:1853-1858.
76. Nystrom, T. 2003. Nonculturable bacteria: programmed survival forms or cells at death's door? Bioessays 25:204-211.
77. Oda, M., M. Morita, H. Unno, and Y. Tanji. 2004. Rapid detection of Escherichia coli O157:H7 by using green fluorescent proteinlabeled PP01 bacteriophage. Appl. Environ. Microbiol. 70:527-534.
78. Ohtomo, R., and M. Saito. 2001. Increase in the culturable cell number of Escherichia coli during recovery from saline stress: possible implication for resuscitation from the VBNC state. Microb. Ecol. 42:208-214.
79. Oliver, J. D. 2000. The public health significance of viable but nonculturable bacteria, p. 277-300. In R. R. Colwell and D. J. Grimes (ed.), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
80. Oliver, J. D. 2000. The viable but nonculturable state and cellular resuscitation, p. 723-730. In C. R. Bell, M. Brylinsky, and P. Johnson-Green (ed.), Microbial biosystems: new frontiers. Atlantic Canada Society for Microbial Ecology, Halifax, Canada.
81. Oliver, J. D. 2005. Viable but nonculturable bacteria in food environments, p. 99-112. In P. M. Fratamico, A. K. Bhunia, and J. L. Smith (ed.), Foodborne pathogens: microbiology and molecular biology. Horizon Scientific Press, Norfolk. UK.
82. Oliver, J. D. 2005. The viable but non-culturable state in bacteria. J. Microbiol. 43:93-100.
83. Oliver, J. D.. M. Dagher, and K. Linden. 2005. Induction of Escherichia coli and Salmonella typhimurium into the viable but nonculturable state following chlorination of wastewater. J. Water Health 3:249-257.
84. Palmer, L. M., A. M. Baya, D. J. Grimes, and R. R. Colwell. 1984. Molecular genetic and phenotypic alteration of Escherichia coli in natural water microcosms containing toxic chemicals. FEMS Microbiol. Lett. 21:169-173.
85. Panutdaporn, N., K. Kawamoto, H. Asakura, and S. I. Makino. 2006. Resuscitation of the viable but non-culturable state of Salmonella enterica serovar Oranienburg by recombinant resuscitation-promoting factor derived from Salmonella Typhimurium strain LT2. Int. J. Food Microbiol. 106:241-247.
86. Pedersen, J. C., and T. D. Leser. 1992. Survival of Enterobacter cloacae on leaves and in soil detected by immunofluorescence microscopy in comparison with selective plating. Microb. Releases 1: 95-102.
87. Porter, J., C. Edwards, and R. W. Pickup. 1995. Rapid assessment of physiological status in Escherichia coli using fluorescent probes. J. Appl. Bacteriol. 79:399-408.
88. Rahman, I., M. Shahamat, M. A. Chowdhury, and R. R. Colwell. 1996. Potential virulence of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 62:115-120.
89. Rahman, I., M. Shahamat, P. A. Kirchman, E. Russek-Cohen, and R. R. Colwell. 1994. Methionine uptake and cytopathogenicity of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 60:3573-3578.
90. Reissbrodt, R., I, Rienaecker, J. M. Romanova, P. P. Freestone, R. D. Haigh, M. Lyte, H. Tschape, and P. H. Williams. 2002. Resuscitation of Salmonella enterica serovar typhimurium and enterohemorrhagic Escherichia coli from the viable but nonculturable state by heat-stable enterobacterial autoinducer. Appl. Environ. Microbiol. 68:4788-4794.
91. Rigsbee, W., L. M. Simpson, and J. D. Oliver. 1997. Detection of the viable but nonculturable state in Escherichia coli O157:H7. J. Food Saf. 16:255-262.
92. Roszak, D. B., and R. R. Colwell. 1987. Metabolic activity of bacterial cells enumerated by direct viable count. Appl. Environ. Microbiol. 53:2889-2893.
93. Roszak, D. B., D. J. Grimes, and R. R. Colwell. 1984. Viable but nonrecoverable stage of Salmonella enteritidis in aquatic systems. Can. J. Microbiol. 30:334-338.
94. Rowan, N. J. 2004. Viable but non-culturable forms of food and waterborne bacteria: quo vadis? Trends Food Sci. Technol. 15:462-467.
95. Rudi, K., K. Naterstad, S. M. Dromtorp, and H. Holo. 2005. Detection of viable and dead Listeria monocytogenes on gouda-like cheeses by real-time PCR. Lett. Appl. Microbiol. 40:301-306.
96. Signoretto, C., M. M. Lleo, and P. Capepari. 2002. Modification of the peptidoglycan of Escherichia coli in the viable but nonculturable state. Curr. Microbiol. 44:125-131.
97. Smith, J. J., J. P. Howington, and G. A. McFeters. 1994. Survival, physiological response and recovery of enteric bacteria exposed to a polar marine environment. Appl. Environ. Microbiol. 60:2977-2984.
98. Smith, R. J., S. C. Kehoe, K. G. McGuigan, and M. R. Barer. 2000. Effects of simulated solar disinfection of water on infectivity of Salmonella typhimurium. Lett. Appl. Microbiol. 31:284-288.
99. Smith, R. J., A. T. Newton. C. R. Harwood, and M. R. Barer. 2002. Active but nonculturable cells of Salmonella enterica serovar Typhimurium do not infect or colonize mice. Microbiology 148:2717-2726.
100. Solomon, E. B., H. J. Pang, and K. R. Matthews. 2003. Persistence of Escherichia coli O157:H7 on lettuce plants following spray irrigation with contaminated water. J. Food Prot. 66:2198-2202.
101. Steele, M.. and J. Odumeru. 2004. Irrigation water as source of foodborne pathogens on fruit and vegetables. J. Food Prot. 67: 2839-2849.
102. Sylvester, D. M., R. Taylor, and T. R. LaHann. 2001. Viable but nonculturable bacteria: a public health threat? Infect. Dis. Rev. 3: 70-82.
103. Tang, X., Y. Xiao, and J. M. Zhou. 2006. Regulation of the type III secretion system in phytopathogenic bacteria. Mol. Plant-Microbe Interact. 19:1159-1166.
104. Toth, I. K., L. Pritchard, and P. R. J. Birch. 2006. Comparative genomics reveals what makes an enterobacterial plant pathogen. Annu. Rev. Phytopathol. 44:305-336.
105. Turpin, P. E., K. A. Maycroft, C. L. Rowlands, and E. M. Wellington. 1993. Viable but non-culturable salmonellas in soil. J. Appl. Bacteriol. 74:421-427.
106. Van Elsas, J. D., P. Kastelein, P. M. de Vries, and L. S. van Overbeek. 2001. Effects of ecological factors on the survival and physiology of Ralstonia solanacearum bv. 2 in irrigation water. Can. J. Microbiol. 47:842-854.
107. Wachtel, M. R., and A. O. Charkowski. 2002. Cross-contamination of lettuce with Escherichia coli O157:H7. J. Food Prot. 65:465-470.
108. Wachtel, M. R., J. L. McEvoy, Y. Luo, A. M. Williams-Campbell, and M. B. Solomon. 2003. Cross-contamination of lettuce (Lactuca sativa L.) with Escherichia coli O157:H7 via contaminated ground beef. J. Food Prot. 66:1176-1183.
109. Wang, G., and M. P. Doyle. 1998. Survival of enterohemorrhagic Escherichia coli O157:H7 in water. J. Food Prot. 61:662-667.
110. Wang, G., T. Zhao, and M. P. Doyle. 1996. Fate of enterohemorrhagic Escherichia coli O157:H7 in bovine feces. Appl. Environ. Microbiol. 62:2567-2570.
111. Wery, N., A. M. Pourcher, V. Stan, J. P. Delgenes, F. Picard-Bonnaud, and J. J. Godon. 2006. Survival of Listeria monocytogenes and Enterococcus faecium in sludge evaluated by real-time PCR and culture methods. Lett. Appl. Microbiol. 43:131-136.
112. Wilson, M., and S. E. Lindow. 1992. Relationship of total viable and culturable cells in epiphytic populations of Pseudomonas syringae. Appl. Environ. Microbiol. 58:3908-3913.
113. Wilson, M., and S. E. Lindow. 2000. Viable but nonculturable cells in plant-associated bacterial populations, p. 229-241. In R. R. Colwell and D. J. Grimes (ed.), Nonculturable microorganisms in the environment. ASM Press, Washington, DC.
114. Winfield, M. D., and E. A. Groisman. 2003. Role of nonhost environments in the lifestyles of Salmonella and Escherichia coli. Appl. Environ. Microbiol. 69:3687-3694.
115. Xu, H.-S., N. Roberts, F. L. Singleton, R. W. Attwell, D. J. Grimes, and R. R. Colwell. 1982. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8:313-323.
116. Yamamoto, H. 2000. Viable but nonculturable state as a general phenomenon of non-spore-forming bacteria, and its modeling. J. Infect. Chemother. 6:112-114.
117. Yaron, S., and K. R. Matthews. 2002. A reverse-transcriptase-polymerase reaction assay for detection of viable Escherichia coli O157:H7: investigation of specific target genes. J. Appl. Microbiol. 92:633-640.
118. Zhao, L., and K. R. Matthews. 2000. Influence of starvation, temperature, and pH on culturability of enterohemorrhagic Escherichia coli O157:H7. J. Food Saf. 20:193-208.