Current perspectives on viable but non-culturable state in foodborne pathogens

Frontiers in Microbiology

Volumn 8, Issue APR, 2017, Pages

  Zhao, Xihong ^a   Zhong, Junliang ^a   Wei, Caijiao ^a   Lin, Chii Wann ^b   Ding, Tian ^c  

^a WUHAN INSTITUTE OF TECHNOLOGY   (China)

^b NATIONAL TAIWAN UNIVERSITY   (Taiwan)

^c ZHEJIANG UNIVERSITY   (China)

Author keywords

Detection method; Foodborne pathogens; Induction; Resuscitation; VBNC

Indexed keywords

DALFOPRISTIN PLUS QUINUPRISTIN; SORBATE POTASSIUM; VANCOMYCIN;

BACILLUS CEREUS; BIOLOGICAL ACTIVITY; CELL STRUCTURE; ENVIRONMENTAL STRESS; ESCHERICHIA COLI; FOOD POISONING; FOOD SAFETY; GENE EXPRESSION; GRAPEFRUIT JUICE; HUMAN; IRRADIATION; LAMP SYSTEM; METABOLIC ACTIVITY ASSAY; MICROBIOLOGY; MILK; NONHUMAN; POLYMERASE CHAIN REACTION; QUORUM SENSING; RESEARCH; RESUSCITATION; REVIEW; STAPHYLOCOCCUS AUREUS; STATIC ELECTRICITY; TEMPERATURE; VIBRIO ALGINOLYTICUS; VIBRIO PARAHAEMOLYTICUS;

EID: 85018348138     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2017.00580     Document Type: Review

References (136)

1. Abe, A., Ohashi, E., Ren, H., Hayashi, T., and Endo, H. (2006). Isolation of a viable but non-culturable suppression mutant of Vibrio vulnificus: role of antioxidant enzymes in surviving stationary phase and low temperatures. Fish. Sci. 72, 656-664. doi: 10.1111/j.1444-2906.2006.01196.x
2. Adams, B. L., Bates, T. C., and Oliver, J. D. (2003). Survival of Helicobacter pylori in a natural freshwater environment. Appl. Environ. Microbiol. 69, 7462-7466. doi: 10.1128/AEM.69.12.7462-7466.2003
3. Al-Bana, B. H., Haddad, M. T., and Garduño, R. A. (2014). Stationary phase and mature infectious forms of Legionella pneumophila produce distinct viable but non-culturable cells. Environ. Microbiol. 16, 382-395. doi: 10.1111/1462-2920.12219
4. Albertini, M. C., Accorsi, A., Teodori, L., Pierfelici, L., Uguccioni, F., Rocchi, M. B., et al. (2006). Use of multiparameter analysis for Vibrio alginolyticus viable but nonculturable state determination. Cytom. Part A 69, 260-265. doi: 10.1002/cyto.a.20263
5. Al-Qadiri, H. M., Lu, X., Al-Alami, N. I., and Rasco, B. A. (2011). Survival of Escherichia coli O157: H7 and Campylobacter jejuni in bottled purified drinking water under different storage conditions. J. Food. Protect. 74, 254-260. doi: 10.4315/0362-028X.JFP-10-368
6. Amel, B. K.-N., Amine, B., and Amina, B. (2008). Survival of Vibrio fluvialis in seawater under starvation conditions. Microbiol. Res. 163, 323-328. doi: 10.1016/j.micres.2006.06.006
7. Amel, D., and Amina, B. (2008). Resuscitation of seventeen-year stressed Salmonella typhimurium. Oceanol. Hydrobiol. Stud. 37, 69-82. doi: 10.2478/v10009-007-0038-x
8. Anderson, M., Bollinger, D., Hagler, A., Hartwell, H., Rivers, B., Ward, K., et al. (2004). Viable but nonculturable bacteria are present in mouse and human urine specimens. J. Clin. Microbiol. 42, 753-758. doi: 10.1128/JCM.42.2.753-758.2004
9. Anvarian, A. H., Smith, M. P., and Overton, T. W. (2016). The effects of orange juice clarification on the physiology of Escherichia coli; growth-based and flow cytometric analysis. Int. J. Food. Microbiol. 219, 38-43. doi: 10.1016/j.ijfoodmicro.2015.11.016
10. Asakura, H., Makino, S.-I., Takagi, T., Kuri, A., Kurazono, T., Watarai, M., et al. (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. doi: 10.1111/j.1574-6968.2002.tb11249.x
11. Aurass, P., Prager, R., and Flieger, A. (2011). EHEC/EAEC O104: H4 strain linked with the 2011 German outbreak of haemolytic uremic syndrome enters into the viable but non-culturable state in response to various stresses and resuscitates upon stress relief. Environ. Microbiol. 13, 3139-3148. doi: 10.1111/j.1462-2920.2011.02604.x
12. Aydin, I., Dimitropoulos, A., Chen, S. H., Thomas, C., and Roujeinikova, A. (2011). Purification, crystallization and preliminary X-ray crystallographic analysis of the putative resuscitation-promoting factor YeaZ. Acta. Crystallogr. F 67, 604-607. doi: 10.1107/S1744309111010219
13. Ayrapetyan, M., and Oliver, J. D. (2016). The viable but non-culturable state and its relevance in food safety. Curr. Opin. Food Sci. 8, 127-133. doi: 10.1016/j.cofs.2016.04.010
14. Ayrapetyan, M., Williams, T. C., and Oliver, J. D. (2014). Interspecific quorum sensing mediates the resuscitation of viable but nonculturable vibrios. Appl. Environ. Microbiol. 80, 2478-2483. doi: 10.1128/AEM.00080-14
15. Ayrapetyan, M., Williams, T. C., and Oliver, J. D. (2015). Bridging the gap between viable but non-culturable and antibiotic persistent bacteria. Trends Microbiol. 23, 7-13. doi: 10.1016/j.tim.2014.09.004
16. Bari, S. M., Roky, M. K., Mohiuddin, M., Kamruzzaman, M., Mekalanos, J. J., and Faruque, S. M. (2013). Quorum-sensing autoinducers resuscitate dormant Vibrio cholerae in environmental water samples. Proc. Natl. Acad. Sci. U.S.A. 110, 9926-9931. doi: 10.1073/pnas.1307697110
17. Barron, J. C., and Forsythe, S. J. (2007). Dry stress and survival time of Enterobacter sakazakii and other Enterobacteriaceae in dehydrated powdered infant formula. J. Food Prot. 70, 2111-2117. doi: 10.4315/0362-028X-70.9.2111
18. Bates, T. C., and Oliver, J. D. (2004). The viable but nonculturable state of Kanagawa positive and negative strains of Vibrio parahaemolyticus. J. Microbiol. 42, 74-79
19. Bhagwat, A. A., Tan, J., Sharma, M., Kothary, M., Low, S., Tall, B. D., et al. (2006). Functional heterogeneity of RpoS in stress tolerance of enterohemorrhagic Escherichia coli strains. Appl. Environ. Microbiol. 72, 4978-4986. doi: 10.1128/AEM.02842-05
20. Bigger, J. (1944). Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244, 497-500. doi: 10.1016/S0140-6736(00)74210-3
21. Boaretti, M., Del Mar Lleò, M., Bonato, B., Signoretto, C., and Canepari, P. (2003). Involvement of rpoS in the survival of Escherichia coli in the viable but non-culturable state. Environ. Microbiol. 5, 986-996. doi: 10.1046/j.1462-2920.2003.00497.x
22. Bogosian, G., Morris, P. J., and O'Neil, J. P. (1998). A mixed culture recovery method indicates that enteric bacteria do not enter the viable but nonculturable state. Appl. Environ. Microbiol. 64, 1736-1742
23. Borkow, G. (2014). Use of Biocidal Surfaces for Reduction of Healthcare Acquired Infections. Heidelberg: Springer Press. doi: 10.1007/978-3-319-08057-4
24. Braden, C. R. (2006). Salmonella enterica serotype enteritidis and eggs: a national epidemic in the United States. Clin. Infect. Dis. 43, 512-517. doi: 10.1086/505973
25. Bridier, A., Hammes, F., Canette, A., Bouchez, T., and Briandet, R. (2015). Fluorescence-based tools for single-cell approaches in food microbiology. Int. J. Food Microbiol. 213, 2-16. doi: 10.1016/j.ijfoodmicro.2015.07.003
26. Capozzi, V., Di Toro, M. R., Grieco, F., Michelotti, V., Salma, M., Lamontanara, A., et al. (2016). Viable But Not Culturable (VBNC) state of Brettanomyces bruxellensis in wine: new insights on molecular basis of VBNC behaviour using a transcriptomic approach. Food Microbiol. 59, 196-204. doi: 10.1016/j.fm.2016.06.007
27. Cappelier, J. M., Besnard, V., Roche, S. M., Velge, P., and Federighi, M. (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. doi: 10.1051/vetres:2007017
28. Chaisowwong, W., Kusumoto, A., Hashimoto, M., Harada, T., Maklon, K., and Kawamoto, K. (2012). Physiological characterization of Campylobacter jejuni under cold stresses conditions: its potential for public threat. J. Vet. Med. Sci. 74, 43-50. doi: 10.1292/jvms.11-0305
29. Chaveerach, P., Ter Huurne, A., Lipman, L., and Van Knapen, F. (2003). Survival and resuscitation of ten strains of Campylobacter jejuni and Campylobacter coli under acid conditions. Appl. Environ. Microbiol. 69, 711-714. doi: 10.1128/AEM.69.1.711-714.2003
30. Clements, M. O., and Foster, S. J. (1998). Starvation recovery of Staphylococcus aureus 8325-4. Microbiology 144, 1755-1763. doi: 10.1099/00221287-144-7-1755
31. Costa, K., Bacher, G., Allmaier, G., Dominguez-Bello, M. G., Engstrand, L., Falk, P., et al. (1999). The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. J. Bacteriol. 181, 3710-3715
32. Cunningham, E., O'Byrne, C., and Oliver, J. D. (2009). Effect of weak acids on Listeria monocytogenes survival: evidence for a viable but nonculturable state in response to low pH. Food Control 20, 1141-1144. doi: 10.1016/j.foodcont.2009.03.005
33. Ding, T., Suo, Y., Xiang, Q., Zhao, X., Chen, S., Ye, X., et al. (2016). Significance of viable but nonculturable Escherichia coli: induction, detection, and control. J. Microbiol. Biotechnol. doi: 10.4014/jmb.1609.09063 [Epub ahead of print]
34. Dinu, L. D., and Bach, S. (2011). Induction of viable but nonculturable Escherichia coli O157: H7 in the phyllosphere of lettuce: a food safety risk factor. Appl. Environ. Microbiol. 77, 8295-8302. doi: 10.1128/AEM.05020-11
35. Dinu, L.-D., and Bach, S. (2013). Detection of viable but non-culturable Escherichia coli O157: H7 from vegetable samples using quantitative PCR with propidium monoazide and immunological assays. Food Control 31, 268-273. doi: 10.1016/j.foodcont.2012.10.020
36. Du, M., Chen, J., Zhang, X., Li, A., and Li, Y. (2007). Characterization and resuscitation of viable but nonculturable Vibrio alginolyticus VIB283. Arch. Microbiol. 188, 283-288. doi: 10.1007/s00203-007-0246-5
37. Du, M., Chen, J., Zhang, X., Li, A., Li, Y., and Wang, Y. (2007). Retention of virulence in a viable but nonculturable Edwardsiella tarda isolate. Appl. Environ. Microbiol. 73, 1349-1354. doi: 10.1128/AEM.02243-06
38. Fakruddin, M., Mannan, K. S., and Andrews, S. (2013). Viable but nonculturable bacteria: food safety and public health perspective. ISRN Microbiol. 2013:703813. doi: 10.1155/2013/703813
39. Feng, Z., Wang, Y., An, H., Hao, Y., Hu, X., and Liao, X. (2016). New insights into the formation of viable but nonculturable Escherichia coli O157:H7 induced by high-pressure CO2. Mbio 7, e00961-16. doi: 10.1128/mBio.00961-16
40. Fernández-Delgado, M., García-Amado, M. A., Contreras, M., Incani, R. N., Chirinos, H., Rojas, H., et al. (2015). Survival, induction and resuscitation of Vibrio cholerae from the viable but non-culturable state in the Southern Caribbean Sea. Rev. Inst. Med. Trop. Sao Paulo 57, 21-26. doi: 10.1590/S0036-46652015000100003
41. Ganesan, B., Stuart, M. R., and Weimer, B. C. (2007). Carbohydrate starvation causes a metabolically active but nonculturable state in Lactococcus lactis. Appl. Environ. Microbiol. 73, 2498-2512. doi: 10.1128/AEM.01832-06
42. Gião, M. S., and Keevil, C. W. (2014). "Listeria monocytogenes" can form biofilms in tap water and enter into the viable but non-cultivable state. Microbiol. Ecol. 67, 603-611. doi: 10.1007/s00248-013-0364-3
43. Gunasekera, T. S., Sørensen, A., Attfield, P. V., Sørensen, S. J., and Veal, D. A. (2002). Inducible gene expression by nonculturable bacteria in milk after pasteurization. Appl. Environ. Microbiol. 68, 1988-1993. doi: 10.1128/AEM.68.4.1988-1993.2002
44. Gupte, A., De Rezende, C., and Joseph, S. (2003). Induction and resuscitation of viable but nonculturable Salmonella enterica serovar Typhimurium DT104. Appl. Environ. Microbiol. 69, 6669-6675. doi: 10.1128/AEM.69.11.6669-6675.2003
45. Habimana, O., Nesse, L., Møretrø, T., Berg, K., Heir, E., Vestby, L., et al. (2014). The persistence of Salmonella following desiccation under feed processing environmental conditions: a subject of relevance. Lett. Appl. Microbiol. 59, 464-470. doi: 10.1111/lam.12308
46. Hsueh, P. R., Teng, L. J., Tseng, S. P., Chang, C. F., Wan, J. H., Yan, J. J., et al. (2004). Ciprofloxacin-resistant Salmonella enterica Typhimurium and Choleraesuis from pigs to humans. Taiwan. Emerg. Infect. Dis. 10, 60-68. doi: 10.3201/eid1001.030171
47. Hu, Y., and Coates, A. (2012). "Nonmultiplying bacteria are profoundly tolerant to antibiotics," in Antibiotic Resistance, eds R. M. Anthony and A. Coates (Berlin: Springer Press), 99-119. doi: 10.1007/978-3-642-28951-4_7
48. Hung, W.-C., Jane, W.-N., and Wong, H.-C. (2013). Association of a d-alanyl-d-alanine carboxypeptidase gene with the formation of aberrantly shaped cells during the induction of viable but nonculturable Vibrio parahaemolyticus. Appl. Environ. Microbiol. 79, 7305-7312. doi: 10.1128/AEM.01723-13
49. Imamura, D., Mizuno, T., Miyoshi, S. I, and Shinoda, S. (2015). Stepwise changes in viable but nonculturable Vibrio cholerae cells. Microbiol. Immunol. 59, 305-310. doi: 10.1111/1348-0421.12246
50. Inglis, T. J., and Sagripanti, J.-L. (2006). Environmental factors that affect the survival and persistence of Burkholderia pseudomallei. Appl. Environ. Microbiol. 72, 6865-6875. doi: 10.1128/AEM.01036-06
51. Jeffreys, A. G., Hak, K. M., Steffan, R. J., Foster, J. W., and Bej, A. K. (1998). Growth, survival and characterization of cspA in Salmonella enteritidis following cold shock. Curr. Microbiol. 36, 29-35. doi: 10.1007/s002849900275
52. Jiang, Y., Yan, P., and Liang, J. (2014). Biological changes of Enterococcus faecalis in the viable but nonculturable state. Genet. Mol. Res. 14, 14790-14801. doi: 10.4238/2015.November.18.44
53. Keep, N. H., Ward, J. M., Cohen-Gonsaud, M., and Henderson, B. (2006). Wake up! Peptidoglycan lysis and bacterial non-growth states. Trends Microbiol. 14, 271-276. doi: 10.1016/j.tim.2006.04.003
54. Keep, N. H., Ward, J. M., Robertson, G., Cohen-Gonsaud, M., and Henderson, B. (2006). Bacterial resuscitation factors: revival of viable but non-culturable bacteria. Cell. Mol. Life Sci. 63, 2555-2559. doi: 10.1007/s00018-006-6188-2
55. Kell, D. B., Kaprelyants, A. S., Weichart, D. H., Harwood, C. R., and Barer, M. R. (1998). Viability and activity in reality culturable bacteria: a review and discussion of the practical issues. Antonie. Van Leeuwenhoek 73, 169-187. doi: 10.1023/A:1000664013047
56. Kogure, K., Simidu, U., and Taga, N. (1979). A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25, 415-420. doi: 10.1139/m79-063
57. Kramer, B., and Muranyi, P. (2014). Effect of pulsed light on structural and physiological properties of Listeria innocua and Escherichia coli. J. Appl. Microbiol. 116, 596-611. doi: 10.1111/jam.12394
58. Kusumoto, A., Asakura, H., and Kawamoto, K. (2012). General stress sigma factor RpoS influences time required to enter the viable but non-culturable state in Salmonella enterica. Microbiol. Immunol. 56, 228-237. doi: 10.1111/j.1348-0421.2012.00428.x
59. Lahtinen, S., Ahokoski, H., Reinikainen, J. P., Gueimonde, M., Nurmi, J., Ouwehand, A. C., et al. (2008). Degradation of 16S rRNA and attributes of viability of viable but nonculturable probiotic bacteria. Lett. Appl. Microbiol. 46, 693-698. doi: 10.1111/j.1472-765X.2008.02374.x
60. Lai, C. J., Chen, S. Y., Lin, I. H., Chang, C. H., and Wong, H. C. (2009). Change of protein profiles in the induction of the viable but nonculturable state of Vibrio parahaemolyticus. Int. J. Food Microbiol. 135, 118-124. doi: 10.1016/j.ijfoodmicro.2009.08.023
61. Lázaro, B., Cárcamo, J., Audícana, A., Perales, I., and Fernández-Astorga, A. (1999). Viability and DNA maintenance in nonculturable spiral Campylobacter jejuni cells after long-term exposure to low temperatures. Appl. Environ. Microbiol. 65, 4677-4681
62. Léonard, L., Bouarab Chibane, L., Ouled Bouhedda, B., Degraeve, P., and Oulahal, N. (2016). Recent advances on multi-parameter flow cytometry to characterize antimicrobial treatments. Front. Microbiol. 7:1225. doi: 10.3389/fmicb.2016.01225
63. Li, J., Ahn, J., Liu, D., Chen, S., Ye, X., and Ding, T. (2016). Evaluation of ultrasound-induced damage to Escherichia coli and Staphylococcus aureus by flow cytometry and transmission electron microscopy. Appl. Environ. Microbiol. 82, 1828-1837. doi: 10.1128/AEM.03080-15
64. Li, L., Mendis, N., Trigui, H., Oliver, J. D., and Faucher, S. P. (2014). The importance of the viable but non-culturable state in human bacterial pathogens. Front. Microbiol. 5:258. doi: 10.3389/fmicb.2014.00258
65. Lin, Y.-W., Li, D., Gu, A. Z., Zeng, S. Y., and He, M. (2016). Bacterial regrowth in water reclamation and distribution systems revealed by viable bacterial detection assays. Chemosphere 144, 2165-2174. doi: 10.1016/j.chemosphere.2015.10.071
66. Linder, K., and Oliver, J. D. (1989). Membrane fatty acid and virulence changes in the viable but nonculturable state of Vibrio vulnificus. Appl. Environ. Microbiol. 55, 2837-2842
67. Liu, J., Rong, Z., Lin, L., Peters, B. M., Bing, L., Lin, C. W., et al. (2016). Viable but non-culturable state and toxin gene expression of enterohemorrhagic Escherichia coli O157 under cryopreservation. Res. Microbiol. 168, 188-193. doi: 10.1016/j.resmic.2016.11.002
68. Lleo, M., Bonato, B., Tafi, M., Signoretto, C., Boaretti, M., and Canepari, P. (2001). Resuscitation rate in different enterococcal species in the viable but non-culturable state. J. Appl. Microbiol. 91, 1095-1102. doi: 10.1046/j.1365-2672.2001.01476.x
69. Lothigius, A., Sjoling, A., Svennerholm, A. M., and Bölin, I. (2010). Survival and gene expression of enterotoxigenic Escherichia coli during long-term incubation in sea water and freshwater. J. Appl. Microbiol. 108, 1441-1449. doi: 10.1111/j.1365-2672.2009.04548.x
70. Magajna, B. A., Schraft, H., and Schraft, H. (2015). Campylobacter jejuni biofilm cells become viable but non-culturable (VBNC) in low nutrient conditions at 4°C more quickly than their planktonic counterparts. Food Control 50, 45-50. doi: 10.1016/j.foodcont.2014.08.022
71. Magnusson, L. U., Farewell, A., and Nyström, T. (2005). ppGpp: a global regulator in Escherichia coli. Trends Microbiol. 13, 236-242. doi: 10.1016/j.tim.2005.03.008
72. Makino, S.-I., Kii, T., Asakura, H., Shirahata, T., Ikeda, T., Takeshi, K., et al. (2000). Does Enterohemorrhagic Escherichia coli O157: H7 enter the viable but nonculturable state in salted salmon roe? Appl. Environ. Microbiol. 66, 5536-5539. doi: 10.1128/AEM.66.12.5536-5539.2000
73. Masmoudi, S., Denis, M., and Maalej, S. (2010). Inactivation of the gene katA or sodA affects the transient entry into the viable but non-culturable response of Staphylococcus aureus in natural seawater at low temperature. Mar. Pollut. Bull. 60, 2209-2214. doi: 10.1016/j.marpolbul.2010.08.017
74. Mathur, H., Rea, M., Fallico, V., Cotter, P., Hill, C., and Ross, P. (2016). Flow cytometry as a tool to study the effects of bacteriocins on prokaryotic and eukaryotic cells. J. Mol. Biomark. Diagn. S8:013. doi: 10.4172/2155-9929.S8-013
75. Meyer, B. (2006). Does microbial resistance to biocides create a hazard to food hygiene? Int. J. Food. Microbiol. 112, 275-279. doi: 10.1016/j.ijfoodmicro.2006.04.012
76. Moorhead, S., and Griffiths, M. (2011). Expression and characterization of cell-signalling molecules in Campylobacter jejuni. J. Appl. Microbiol. 110, 786-800. doi: 10.1111/j.1365-2672.2010.04934.x
77. Morishige, Y., Fujimori, K., and Amano, F. (2013). Differential resuscitative effect of pyruvate and its analogues on VBNC (Viable But Non-Culturable) Salmonella. Microbes Environ. 28, 180-186. doi: 10.1264/jsme2.ME12174
78. Mukamolova, G. V., Kaprelyants, A. S., Kell, D. B., and Young, M. (2003). Adoption of the transiently non-culturable state-a bacterial survival strategy? Adv. Microb. Physiol. 47, 65-129. doi: 10.1016/S0065-2911(03)47002-1
79. Mukamolova, G. V., Kaprelyants, A. S., Young, D. I., Young, M., and Kell, D. B. (1998). A bacterial cytokine. Proc. Natl. Acad. Sci. U.S.A. 95, 8916-8921. doi: 10.1073/pnas.95.15.8916
80. Nicolò, M. S., Gioffrè, A., Carnazza, S., Platania, G., Silvestro, I. D., and Guglielmino, S. P. (2010). Viable but nonculturable state of foodborne pathogens in grapefruit juice: a study of laboratory. Foodborne Pathog. Dis. 8, 11-17. doi: 10.1089/fpd.2009.0491
81. Nicolò, M. S., and Guglielmino, S. P. P. (2012). "Viable but nonculturable bacteria in food," in Public Health-Methodology, Environmental and Systems Issues, ed. J. Maddock (Rjeka: InTech), 189-216. doi: 10.5772/38118
82. Nocker, A., and Camper, A. K. (2009). Novel approaches toward preferential detection of viable cells using nucleic acid amplification techniques. FEMS. Microbiol. Lett. 291, 137-142. doi: 10.1111/j.1574-6968.2008.01429.x
83. Nowakowska, J., and Oliver, J. D. (2013). Resistance to environmental stresses by Vibrio vulnificus in the viable but nonculturable state. FEMS. Microbiol. Ecol. 84, 213-222. doi: 10.1111/1574-6941.12052
84. Nyström, T. (2003). Nonculturable bacteria: programmed survival forms or cells at death's door? Bioessays. 25, 204-211. doi: 10.1002/bies.10233
85. Oh, E., McMullen, L., and Jeon, B. (2015). Impact of oxidative stress defense on bacterial survival and morphological change in Campylobacter jejuni under aerobic conditions. Front. Microbiol 6:295. doi: 10.3389/fmicb.2015.00295
86. Oliver, J. D. (2005). The viable but nonculturable state in bacteria. J. Microbiol. 43, 93-100
87. Oliver, J. D. (2010). Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS. Microbiol. Rev. 34, 415-425. doi: 10.1111/j.1574-6976.2009.00200.x
88. Oliver, J. D., and Bockian, R. (1995). In vivo resuscitation, and virulence towards mice, of viable but nonculturable cells of Vibrio vulnificus. Appl. Environ. Microbiol. 61, 2620-2623. doi: 10.3109/02713680903477824
89. Orman, M. A., and Brynildsen, M. P. (2013). Establishment of a method to rapidly assay bacterial persister metabolism. Antimicrob. Agents Chemother. 57, 4398-4409. doi: 10.1128/AAC.00372-13
90. Paniel, N., Baudart, J., Hayat, A., and Barthelmebs, L. (2013). Aptasensor and genosensor methods for detection of microbes in real world samples. Methods 64, 229-240. doi: 10.1016/j.ymeth.2013.07.001
91. Panutdaporn, N., Kawamoto, K., Asakura, H., and Makino, S. I. (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. doi: 10.1016/j.ijfoodmicro.2005.06.022
92. Pasquaroli, S., Citterio, B., Cesare, A. D., Amiri, M., Manti, A., Vuotto, C., et al. (2014). Role of daptomycin in the induction and persistence of the viable but non-culturable state of Staphylococcus aureus biofilms. Pathogens 3, 759-768. doi: 10.3390/pathogens3030759
93. Pasquaroli, S., Zandri, G., Vignaroli, C., Vuotto, C., Donelli, G., and Biavasco, F. (2013). Antibiotic pressure can induce the viable but non-culturable state in Staphylococcus aureus growing in biofilms. J. Antimicrob. Chemother. 68, 1812-1817. doi: 10.1093/jac/dkt086
94. Patrone, V., Campana, R., Vallorani, L., Dominici, S., Federici, S., Casadei, L., et al. (2013). CadF expression in Campylobacter jejuni strains incubated under low-temperature water microcosm conditions which induce the viable but non-culturable (VBNC) state. Antoni. Van Leeuwenhoek 103, 979-988. doi: 10.1007/s10482-013-9877-5
95. Pawlowski, D. R., Metzger, D. J., Raslawsky, A., Howlett, A., Siebert, G., Karalus, R. J., et al. (2011). Entry of Yersinia pestis into the viable but nonculturable state in a low-temperature tap water microcosm. PLoS ONE 6:e17585. doi: 10.1371/journal.pone.0017585
96. Peneau, S., Chassaing, D., and Carpentier, B. (2007). First evidence of division and accumulation of viable but nonculturable Pseudomonas fluorescens cells on surfaces subjected to conditions encountered at meat processing premises. Appl. Environ. Microbiol. 73, 2839-2846. doi: 10.1128/AEM.02267-06
97. Pianetti, A., Battistelli, M., Barbieri, F., Bruscolini, F., Falcieri, E., Manti, A., et al. (2012). Changes in adhesion ability of Aeromonas hydrophila during long exposure to salt stress conditions. J. Appl. Microbiol. 113, 974-982. doi: 10.1111/j.1365-2672.2012.05399.x
98. Pinto, D., Almeida, V., Almeida Santos, M., and Chambel, L. (2011). Resuscitation of Escherichia coli VBNC cells depends on a variety of environmental or chemical stimuli. J. Appl. Microbiol. 110, 1601-1611. doi: 10.1111/j.1365-2672.2011.05016.x
99. Pinto, D., Santos, M. A., and Chambel, L. (2015). Thirty years of viable but nonculturable state research: unsolved molecular mechanisms. Crit. Rev. Microbiol. 41, 61-76. doi: 10.3109/1040841X.2013.794127
100. Pinto, D., Sãojosé, C., Santos, M. A., and Chambel, L. (2013). Characterization of two resuscitation promoting factors of Listeria monocytogenes. Microbiology 159, 1390-1401. doi: 10.1099/mic.0.067850-0
101. Pommepuy, M., Butin, M., Derrien, A., Gourmelon, M., Colwell, R., and Cormier, M. (1996). Retention of enteropathogenicity by viable but nonculturable Escherichia coli exposed to seawater and sunlight. Appl. Environ. Microbiol. 62, 4621-4626
102. Radomski, N., Moilleron, R., Lucas, F. S., and Falkinham, I. I. I. J. (2010). "Challenges in environmental monitoring of pathogens: case study in Mycobacterium avium," in Current Research, Technology and Education Topics in Applied Microbiology and Microbial Biotechnology, ed. A. Méndez-Vilas (Extremadura: Formatex Research Center), 1551-1561
103. Rahman, F., and Noor, R. (2012). Prevalence of pathogenic bacteria in common salad vegetables. Bangl. J. Bot. 41, 159-162
104. Rahman, I., Shahamat, M., Chowdhury, M., and Colwell, R. (1996). Potential virulence of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 62, 115-120
105. Rahman, I., Shahamat, M., Kirchman, P., Russek-Cohen, E., and Colwell, R. (1994). Methionine uptake and cytopathogenicity of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 60, 3573-3578
106. Ramamurthy, T., Ghosh, A., Pazhani, G. P., and Shinoda, S. (2014). Current Perspectives on Viable but Non-Culturable (VBNC) Pathogenic Bacteria. Front. Public Health 2:103. doi: 10.3389/fpubh.2014.00103
107. Rao, N. V., Shashidhar, R., and Bandekar, J. R. (2014). Induction, resuscitation and quantitative real-time polymerase chain reaction analyses of viable but nonculturable Vibrio vulnificus in artificial sea water. World J. Microbiol. Biotechnol. 30, 2205-2212. doi: 10.1007/s11274-014-1640-1
108. Ravel, J., Knight, I. T., Monahan, C. E., Hill, R. T., and Colwell, R. R. (1995). Temperature-induced recovery of Vibrio cholerae from the viable but nonculturable state: growth or resuscitation? Microbiology 141, 377-383. doi: 10.1099/13500872-141-2-377
109. Roszak, D., Grimes, D., and Colwell, R. (1984). Viable but nonrecoverable stage of Salmonella enteritidis in aquatic systems. Can. J. Microbiol. 30, 334-338. doi: 10.1139/m84-049
110. Rowan, N. J. (2004). Viable but non-culturable forms of food and waterborne bacteria: quo vadis? Trends Food Sci. Technol. 15, 462-467. doi: 10.1016/j.tifs.2004.02.009
111. Rowan, N. J., Valdramidis, V. P., and Gomez-Lopez, V. M. (2015). A review of quantitative methods to describe efficacy of pulsed light generated inactivation data that embraces the occurrence of viable but non culturable state microorganisms. Trends Food Sci. Technol. 44, 79-92. doi: 10.1016/j.tifs.2015.03.006
112. Sachidanandham, R., and Gin, K. (2009). A dormancy state in nonspore-forming bacteria. Appl. Microbiol. Biotechnol. 81, 927-941. doi: 10.1007/s00253-008-1712-y
113. Scheutz, F., Nielsen, E. M., Frimodt-Moller, J., Boisen, N., Morabito, S., Tozzoli, R., et al. (2011). Characteristics of the enteroaggregative Shiga toxin/verotoxin-producing Escherichia coli O104: H4 strain causing the outbreak of haemolytic uraemic syndrome in Germany, May to June 2011. Euro Surveill. 16, 19889
114. Senoh, M., Ghosh-Banerjee, J., Ramamurthy, T., Hamabata, T., Kurakawa, T., Takeda, M., et al. (2010). Conversion of viable but nonculturable Vibrio cholerae to the culturable state by co-culture with eukaryotic cells. Microbiol. Immunol. 54, 502-507. doi: 10.1111/j.1348-0421.2010.00245.x
115. Sheridan, G. E. C., Masters, C. I., Shallcross, J. A., and Mackey, B. M. (1998). Detection of mRNA by reverse transcription-PCR as an indicator of viability in Escherichia coli cells. Appl. Environ. Microbiol. 64, 1313-1318
116. Signoretto, C., del Mar Lleo, M., and Canepari, P. (2002). Modification of the peptidoglycan of Escherichia coli in the viable but nonculturable state. Curr. Microbiol. 44, 125-131. doi: 10.1007/s00284-001-0062-0
117. Signoretto, C., Lleò, M. M., Tafi, M. C., and Canepari, P. (2000). Cell wall chemical composition of Enterococcus faecalis in the viable but nonculturable state. Appl. Environ. Microbiol. 66, 1953-1959. doi: 10.1128/AEM.66.5.1953-1959.2000
118. Smith, B., and Oliver, J. D. (2006). In situ and in vitro gene expression by Vibrio vulnificus during entry into, persistence within, and resuscitation from the viable but nonculturable state. Appl. Environ. Microbiol. 72, 1445-1451. doi: 10.1128/AEM.72.2.1445-1451.2006
119. Su, C. P., Jane, W. N., and Wong, H. C. (2013). Changes of ultrastructure and stress tolerance of Vibrio parahaemolyticus upon entering viable but nonculturable state. Int. J. Food. Microbiol. 160, 360-366. doi: 10.1016/j.ijfoodmicro.2012.11.012
120. Trevors, J., Elsas, J., and Bej, A. (2012). The molecularly crowded cytoplasm of bacterial cells: dividing cells contrasted with viable but non-culturable (VBNC) bacterial cells. Curr. Issues Mol. Biol. 15, 1-6
121. Trevors, J. T. (2011). Viable but non-culturable (VBNC) bacteria: gene expression in planktonic and biofilm cells. J. Microbiol. Methods 86, 266. doi: 10.1016/j.mimet.2011.04.018
122. Trinh, N. T. T., Dumas, E., Thanh, M. L., Degraeve, P., Amara, C. B., Gharsallaoui, A., et al. (2015). Effect of a Vietnamese Cinnamomum cassia essential oil and its major component trans-cinnamaldehyde on the cell viability, membrane integrity, membrane fluidity, and proton motive force of Listeria innocua. Can. J. Microbiol. 61, 263-271. doi: 10.1139/cjm-2014-0481
123. Trudeau, K., Vu, K. D., Shareck, F., and Lacroix, M. (2012). Capillary electrophoresis separation of protein composition of γ-irradiated food pathogens Listeria monocytogenes and Staphylococcus aureus. PLoS ONE 7:e32488. doi: 10.1371/journal.pone.0032488
124. Whitesides, M. D., and Oliver, J. D. (1997). Resuscitation of Vibrio vulnificus from the viable but nonculturable state. Appl. Environ. Microbiol. 63, 1002-1005
125. Wong, H. C., and Wang, P. (2004). Induction of viable but nonculturable state in Vibrio parahaemolyticus and its susceptibility to environmental stresses. J. Appl. Microbiol. 96, 359-366. doi: 10.1046/j.1365-2672.2004.02166.x
126. Xu, H. S., Roberts, N., Singleton, F. L., Attwell, R. W., Grimes, D. J., and Colwell, R. R. (1982). Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8, 313-323. doi: 10.1007/BF02010671
127. Xuan, X. T., Ding, T., Li, J., Ahn, J. H., Zhao, Y., Chen, S. G., et al. (2017). Estimation of growth parameters of Listeria monocytogenes after sublethal heat and slightly acidic electrolyzed water (SAEW) treatment. Food Control 71, 17-25. doi: 10.1016/j.foodcont.2016.06.018
128. Yaron, S., and Matthews, K. (2002). A reverse transcriptase-polymerase chain reaction assay for detection of viable Escherichia coli O157: H7: investigation of specific target genes. J. Appl. Microbiol. 92, 633-640. doi: 10.1046/j.1365-2672.2002.01563.x
129. Zeng, B., Zhao, G., Cao, X., Yang, Z., Wang, C., and Hou, L. (2012). Formation and resuscitation of viable but nonculturable Salmonella typhi. BioMed. Res. Int. 2013:907170. doi: 10.1155/2013/907170
130. Zhang, S., Ye, C., Lin, H., Lv, L., and Yu, X. (2015). UV disinfection induces a VBNC state in Escherichia coli and Pseudomonas aeruginosa. Environ. Sci. Technol. 49, 1721-1728. doi: 10.1021/es505211e
131. Zhao, F., Bi, X., Hao, Y., and Liao, X. (2013). Induction of viable but nonculturable Escherichia coli O157: H7 by high pressure CO2 and its characteristics. PLoS ONE 8:e62388. doi: 10.1371/journal.pone.0062388
132. Zhao, X., Lin, C. W., Wang, J., and Oh, D. H. (2014). Advances in rapid detection methods for foodborne pathogens. J. Microbiol. Biotechnol. 24, 297-312. doi: 10.4014/jmb.1310.10013
133. Zhao, X., Wang, J., Forghani, F., Park, J. H., Park, M. S., Seo, K. H., et al. (2013). Rapid detection of viable Escherichia coli O157 by coupling propidium monoazide with loop-mediated isothermal amplification. J. Microbiol. Biotechnol. 23, 1708-1716. doi: 10.4014/jmb.1306.06003
134. Zhao, X., Wei, C., Zhong, J., and Jin, S. (2016). Research advance in rapid detection of foodborne Staphylococcus aureus. Biotechnol. Biotechnol. Equip. 30, 1-7. doi: 10.1080/13102818.2016.1209433
135. Zhong, Q., Tian, J., Wang, B., and Wang, L. (2016). PMA based real-time fluorescent LAMP for detection of Vibrio parahaemolyticus in viable but nonculturable state. Food Control 63, 230-238. doi: 10.1016/j.foodcont.2015.11.043
136. Ziprin, R. L., Droleskey, R. E., Hume, M. E., and Harvey, R. B. (2003). Failure of viable nonculturable Campylobacter jejuni to colonize the cecum of newly hatched leghorn chicks. Avian. Dis. 47, 753-758. doi: 10.1637/7015