Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Significance of Viable but Nonculturable Escherichia coli: Induction, Detection, and Control

  • Ding, Tian (Department of Food Science and Nutrition, Zhejiang Key Laboratory for Agro-Food Processing, Zhejiang University) ;
  • Suo, Yuanjie (Department of Food Science and Nutrition, Zhejiang Key Laboratory for Agro-Food Processing, Zhejiang University) ;
  • Xiang, Qisen (College of Food and Biological Engineering, Zhengzhou University of Light Industry) ;
  • Zhao, Xihong (Key Laboratory for Green Chemical Process of Ministry of Education, School of Chemical Engineering and Pharmacy, Wuhan Institute of Technology) ;
  • Chen, Shiguo (Department of Food Science and Nutrition, Zhejiang Key Laboratory for Agro-Food Processing, Zhejiang University) ;
  • Ye, Xingqian (Department of Food Science and Nutrition, Zhejiang Key Laboratory for Agro-Food Processing, Zhejiang University) ;
  • Liu, Donghong (Department of Food Science and Nutrition, Zhejiang Key Laboratory for Agro-Food Processing, Zhejiang University)
  • Received : 2016.10.04
  • Accepted : 2016.11.24
  • Published : 2017.03.28
Download PDF
⟨ Previous Next ⟩

Abstract

Diseases caused by foodborne or waterborne pathogens are emerging. Many pathogens can enter into the viable but nonculturable (VBNC) state, which is a survival strategy when exposed to harsh environmental stresses. Pathogens in the VBNC state have the ability to evade conventional microbiological detection methods, posing a significant and potential health risk. Therefore, controlling VBNC bacteria in food processing and the environment is of great importance. As the typical one of the gram-negatives, Escherichia coli (E. coli) is a widespread foodborne and waterborne pathogenic bacterium and is able to enter into a VBNC state in extreme conditions (similar to the other gram-negative bacteria), including inducing factors and resuscitation stimulus. VBNC E. coli has the ability to recover both culturability and pathogenicity, which may bring potential health risk. This review describes the concrete factors (nonthermal treatment, chemical agents, and environmental factors) that induce E. coli into the VBNC state, the condition or stimulus required for resuscitation of VBNC E. coli, and the methods for detecting VBNC E. coli. Furthermore, the mechanism of genes and proteins involved in the VBNC E. coli is also discussed in this review.

Keywords

References

  1. Burgess CM, Gianotti A, Gruzdev N, Holah J, Knochel S, Lehner A, et al. 2016. The response of foodborne pathogens to osmotic and desiccation stresses in the food chain. Int. J. Food Microbiol. 221: 37-53. https://doi.org/10.1016/j.ijfoodmicro.2015.12.014
  2. Scallan E, Griffin PM, Angulo FJ, Tauxe RV, Hoekstra RM. 2011. Foodborne illness acquired in the United States-unspecified agents. Emerg. Infect. Dis. 17: 16-22. https://doi.org/10.3201/eid1701.P21101
  3. Mead PS, Slutsker L, Dietz V, McCaig LF, Bresee JS, Shapiro C, et al. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5: 607-625. https://doi.org/10.3201/eid0505.990502
  4. Zhao C, Ge B, De Villena J, Sudler R, Yeh E, Zhao S, et al. 2001. Prevalence of Campylobacter spp., Escherichia coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the greater Washington, D. C., Area. Appl. Environ. Microbiol. 67: 5431-5436. https://doi.org/10.1128/AEM.67.12.5431-5436.2001
  5. Heiman KE, Mody RK, Johnson SD, Griffin PM, Gould LH. 2015. Escherichia coli O157 outbreaks in the United States, 2003-2012. Emerg. Infect. Dis. 21: 1293.
  6. Chekabab SM, Paquin-Veillette J, Dozois CM, Harel J. 2013. The ecological habitat and transmission of Escherichia coli O157:H7. FEMS Microbiol. Lett. 341: 1-12. https://doi.org/10.1111/1574-6968.12078
  7. Alvarez-Ordonez A, Broussolle V, Colin P, Nguyen-The C, Prieto M. 2015. The adaptive response of bacterial foodborne pathogens in the environment, host and food: implications for food safety. Int. J. Food Microbiol. 213: 99-109. https://doi.org/10.1016/j.ijfoodmicro.2015.06.004
  8. Oliver JD. 2005. The viable but nonculturable state in bacteria. J. Microbiol. 43: 93-100.
  9. Fakruddin M, Mannan KSB, Andrews S. 2013. Viable but nonculturable bacteria: food safety and public health perspective. ISRN Microbiol. 2013: 1-6.
  10. Xu H, Roberts N, Singleton FL, Attwell RW, Grimes DJ, Colwell RR. 1982. Survival and viability of nonculturable Escherichia coli and Vibrio cholerae in the estuarine and marine environment. Microb. Ecol. 8: 313-323. https://doi.org/10.1007/BF02010671
  11. Oliver JD. 2010. Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol. Rev. 34: 415-425. https://doi.org/10.1111/j.1574-6976.2009.00200.x
  12. Pinto D, Santos MA, Chambel L. 2013. Thirty years of viable but nonculturable state research: unsolved molecular mechanisms. Crit. Rev. Microbiol. 41: 61-76.
  13. Masmoudi S, Denis M, 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. https://doi.org/10.1016/j.marpolbul.2010.08.017
  14. 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. Antonie Van Leeuwenhoek 103: 979-988. https://doi.org/10.1007/s10482-013-9877-5
  15. Chaiyanan S, Chaiyanan S, Grim C, Maugel T, Huq A, Colwell RR. 2007. Ultrastructure of coccoid viable but nonculturable Vibrio cholerae. Environ. Microbiol. 9: 393-402. https://doi.org/10.1111/j.1462-2920.2006.01150.x
  16. Zhang S, Ye C, Lin H, Lv L, Yu X. 2015. UV disinfection induces a VBNC state in Escherichia coli and Pseudomonas aeruginosa. Environ. Sci. Technol. 49: 1721-1728. https://doi.org/10.1021/es505211e
  17. Lothigius A, Sjoling A, Svennerholm AM, Bolin 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. https://doi.org/10.1111/j.1365-2672.2009.04548.x
  18. Rao NV, Shashidhar R, Bandekar JR. 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. https://doi.org/10.1007/s11274-014-1640-1
  19. Amel BKN, Amine B, Amina B. 2008. Survival of Vibrio fluvialis in seawater under starvation conditions. Microbiol. Res. 163: 323-328. https://doi.org/10.1016/j.micres.2006.06.006
  20. Lleo MM, Bonato B, Tafi MC, Signoretto C, Boaretti M, Canepari P. 2001. Resuscitation rate in different enterococcal species in the viable but non-culturable state. J. Appl. Microbiol. 91: 1095-1102. https://doi.org/10.1046/j.1365-2672.2001.01476.x
  21. Li L, Mendis N, Trigui H, Oliver JD, Faucher SP. 2015. The importance of the viable but non-culturable state in human bacterial pathogens. Front. Microbiol. 5: 258.
  22. Hung WC, Jane WN, Wong HC. 2013. Association of a DAlanyl-D-Alanine carboxypeptidase gene with the formation of aberrantly shaped cells during the induction of viable but nonculturable Vibrio parahaemolyticus. Appl. Environ. Microb. 79: 7305-7312. https://doi.org/10.1128/AEM.01723-13
  23. Li H, Xu Z, Zhao F, Wang Y, Liao X. 2016. Synergetic effects of high-pressure carbon dioxide and nisin on the inactivation of Escherichia coli and Staphylococcus aureus. Innov. Food. Sci. Emerg. 33: 180-186. https://doi.org/10.1016/j.ifset.2015.11.013
  24. Du M, Chen J, Zhang X, Li A, Li Y, Wang Y. 2007. Retention of virulence in a viable but nonculturable Edwardsiella tarda isolate. Appl. Environ. Microbiol. 73: 1349-1354. https://doi.org/10.1128/AEM.02243-06
  25. Rahman I, Shahamat M, Kirchman PA, Russek-Cohen E, Colwell RR. 1994. Methionine uptake and cytopathogenicity of viable but nonculturable Shigella dysenteriae type 1. Appl. Environ. Microbiol. 60: 3573-3578.
  26. Lindback T, Rottenberg ME, Roche SM, Rorvik LM. 2010. The ability to enter into an avirulent viable but non-culturable (VBNC) form is widespread among Listeria monocytogenes isolates from salmon, patients and environment. Vet. Res. 41: 1-10. https://doi.org/10.1051/vetres/2009049
  27. Boaretti M, Del Mar Lleo M, Bonato B, Signoretto C, Canepari P. 2003. Involvement of rpoS in the survival of Escherichia coli in the viable but non-culturable state. Environ. Microbiol. 5: 986-996. https://doi.org/10.1046/j.1462-2920.2003.00497.x
  28. Kong IS, Bates TC, Hulsmann A, Hassan H, Smith BE, Olive JD. 2004. Role of catalase and oxyR in the viable but nonculturable state of Vibrio vulnificus. FEMS Microbiol. Ecol. 50: 133-142. https://doi.org/10.1016/j.femsec.2004.06.004
  29. Wang H, Chung CH, Ma TY, Wong HC. 2013. Roles of alkyl hydroperoxide reductase subunit C (AhpC) in viable but nonculturable Vibrio parahaemolyticus. Appl. Environ. Microbiol. 79: 3734-3743. https://doi.org/10.1128/AEM.00560-13
  30. Darcan C, Ozkanca R, IdIl O, Flint KP. 2009. Viable but non-culturable state (VBNC) of Escherichia coli related to EnvZ under the effect of pH, starvation and osmotic stress in sea water. J. Microbiol. 58: 307-317.
  31. Wu V. 2008. A review of microbial injury and recovery methods in food. Food Microbiol. 25: 735-744. https://doi.org/10.1016/j.fm.2008.04.011
  32. Liu Y, Wang C, Fung C, Li X. 2010. Quantification of viable but nonculturable Escherichia coli O157:H7 by targeting the rpoS mRNA. Anal. Chem. 82: 2612-2615. https://doi.org/10.1021/ac1003272
  33. Pienaar JA, Singh A, Barnard TG. 2016. The viable but nonculturable state in pathogenic Escherichia coli: a general review. Afr. J. Lab. Med. 5: 9.
  34. Kaper JB, Nataro JP, Mobley HLT. 2004. Pathogenic Escherichia coli. Nat. Rev. Microbiol. 2: 123-140. https://doi.org/10.1038/nrmicro818
  35. Phillips CA. 1999. The epidemiology, detection and control of Escherichia coli O157. J. Sci. Food Agric. 79: 1367-1381. https://doi.org/10.1002/(SICI)1097-0010(199908)79:11<1367::AID-JSFA374>3.0.CO;2-S
  36. Askar M, Faber M, Frank C, Bernard H, Gilsdorf A, Fruth A, et al. 2011. Update on the ongoing outbreak of haemolytic uraemic syndrome due to Shiga toxin-producing Escherichia coli (STEC) serotype O104, Germany, May 2011. Euro. Surveill. 16: 19883.
  37. Chapman PA, Siddons CA, Wright DJ, Norman P, Fox J, Crick E. 1993. Cattle as a possible source of verocytotoxinproducing Escherichia coli O157 infections in man. Epidemiol. Infect. 111: 439-447. https://doi.org/10.1017/S0950268800057162
  38. Cui Y, Qin J, Zhao X, Rohde H, Liang T, Wolters M, et al. 2011. Identification of the hybrid strain responsible for Germany food-poisoning outbreak by polymerase chain reaction. J. Clin. Microbiol. 49: 3439-3440. https://doi.org/10.1128/JCM.01312-11
  39. Frank C, Werber D, Cramer JP, Askar M, Faber M, Heiden M, et al. 2011. Epidemic profile of Shiga-toxin-producing Escherichia coli O104:H4 outbreak in Germany. N. Engl. J. Med. 365: 1771-1780. https://doi.org/10.1056/NEJMoa1106483
  40. Scheutz F, Nielsen EM, 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.
  41. Gault G, Weill F, Mariani-Kurkdjian P, Jourdan-da SN, King L, Aldabe B, et al. 2011. Outbreak of haemolytic uraemic syndrome and bloody diarrhoea due to Escherichia coli O104:H4, south-west France, June 2011. Euro Surveill. 16: 19905.
  42. Aurass P, Prager R, 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. https://doi.org/10.1111/j.1462-2920.2011.02604.x
  43. Liu Y, Wang C, Tyrrell G, Li X. 2010. Production of Shigalike toxins in viable but nonculturable Escherichia coli O157:H7. Water Res. 44: 711-718. https://doi.org/10.1016/j.watres.2009.10.005
  44. Barcina I, Lebaron P, Vives-Rego J. 1997. Survival of allochthonous bacteria in aquatic systems: a biological approach. FEMS Microbiol. Ecol. 23: 1-9. https://doi.org/10.1111/j.1574-6941.1997.tb00385.x
  45. Muela A, Seco C, Camafeita E, Arana I, Orruno M, Lopez JA, et al. 2008. Changes in Escherichia coli outer membrane subproteome under environmental conditions inducing the viable but nonculturable state. FEMS Microbiol. Ecol. 64: 28-36. https://doi.org/10.1111/j.1574-6941.2008.00453.x
  46. Cook KL, Bolster CH. 2007. Survival of Campylobacter jejuni and Escherichia coli in groundwater during prolonged starvation at low temperatures. J. Appl. Microbiol. 103: 573-583. https://doi.org/10.1111/j.1365-2672.2006.03285.x
  47. March SB, Ratnam S. 1986. Sorbitol-MacConkey medium for detection of Escherichia coli 0157:H7 associated with hemorrhagic colitis. J. Clin. Microbiol. 23: 869-872.
  48. Dolezalova E, Lukes P. 2015. Membrane damage and active but nonculturable state in liquid cultures of Escherichia coli treated with an atmospheric pressure plasma jet. Bioelectrochemistry 103: 7-14. https://doi.org/10.1016/j.bioelechem.2014.08.018
  49. Dolezalova E, Prukner V, Lukes P, Simek M. 2016. Stress response of Escherichia coli induced by surface streamer discharge in humid air. J. Phys. D Appl. Phys. 49: 075401. https://doi.org/10.1088/0022-3727/49/7/075401
  50. Kacem M, Bru-Adan V, Goetz V, Steyer JP, Plantard G, Sacco D, et al. 2016. Inactivation of Escherichia coli by $TiO_2$-mediated photocatalysis evaluated by a culture method and viability-qPCR. J. Photochem. Photobiol. A 317: 81-87. https://doi.org/10.1016/j.jphotochem.2015.11.020
  51. Said MB, Masahiro O, Hassen A. 2010. Detection of viable but non cultivable Escherichia coli after UV irradiation using a lytic Q${\beta}$ phage. Ann. Microbiol. 60: 121-127. https://doi.org/10.1007/s13213-010-0017-4
  52. Zhao F, Bi F, Hao Y, Liao X. 2013. Induction of viable but nonculturable Escherichia coli O157:H7 by high pressure$CO_2$ and its characteristics. PLoS One 8: e62388. https://doi.org/10.1371/journal.pone.0062388
  53. Wingender J, Flemming H. 2011. Biofilms in drinking water and their role as reservoir for pathogens. Int. J. Hyg. Environ. Health 214: 417-423. https://doi.org/10.1016/j.ijheh.2011.05.009
  54. Grey B, Steck TR. 2001. Concentrations of copper thought to be toxic to Escherichia coli can induce the viable but nonculturable condition. Appl. Environ. Microbiol. 67: 5325-5327. https://doi.org/10.1128/AEM.67.11.5325-5327.2001
  55. Santo CE, Taudte N, Nies DH, Grass G. 2008. Contribution of copper ion resistance to survival of Escherichia coli on metallic copper surfaces. Appl. Environ. Microbiol. 74: 977-986. https://doi.org/10.1128/AEM.01938-07
  56. Munna MS, Nur I, Rahman T, Noor R. 2013. Influence of exogenous oxidative stress on Escherichia coli cell growth, viability and morphology. Am. J. BioSci. 1: 59-62. https://doi.org/10.11648/j.ajbio.20130104.12
  57. Chen H, Shen J, Pan G, Liu J, Li J, Hu Z. 2015. Correlations between cyanobacterial density and bacterial transformation to the viable but nonculturable (VBNC) state in four freshwater water bodies. Ecotoxicology 24: 1459-1466. https://doi.org/10.1007/s10646-015-1476-y
  58. Dinu LD, 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. https://doi.org/10.1128/AEM.05020-11
  59. Asakura H, Kawamoto K, Haishima Y, Igimi S, Yamamoto S, Makino S. 2008. Differential expression of the outer membrane protein W (OmpW) stress response in enterohemorrhagic Escherichia coli O157:H7 corresponds to the viable but nonculturable state. Res. Microbiol. 159: 709-717. https://doi.org/10.1016/j.resmic.2008.08.005
  60. Juhna T, Birzniece D, Rubulis J. 2007. Effect of phosphorus on survival of Escherichia coli in drinking water biofilms. Appl. Environ. Microbiol. 73: 3755-3758. https://doi.org/10.1128/AEM.00313-07
  61. Pinto D, Almeida V, Almeida SM, Chambel L. 2011. Resuscitation of Escherichia coli VBNC cells depends on a variety of environmental or chemical stimuli. J. Appl. Microbiol. 110: 1601-1611. https://doi.org/10.1111/j.1365-2672.2011.05016.x
  62. Waturangi DE, Amadeus S, Kelvianto YE. 2015. Survival of enteroaggregative Escherichia coli and Vibrio cholerae in frozen and chilled foods. J. Infect. Dev. Ctries. 9: 837-843. https://doi.org/10.3855/jidc.6626
  63. Reissbrodt R, Rienaecker I, Romanova JM, Freestone PPE, Haigh RD, Lyte M, et al. 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. https://doi.org/10.1128/AEM.68.10.4788-4794.2002
  64. Epstein SS. 2009. Microbial awakenings. Nature 457: 1083. https://doi.org/10.1038/4571083a
  65. Kolling GL, Matthews KL. 2001. Examination of recovery in vitro and in vivo of nonculturable Escherichia coli O157:H7. Appl. Environ. Microbiol. 67: 3928-3933. https://doi.org/10.1128/AEM.67.9.3928-3933.2001
  66. Trevors JT. 2011. Viable but non-culturable (VBNC) bacteria: gene expression in planktonic and biofilm cells. J. Microbiol. Methods 86: 266-273. https://doi.org/10.1016/j.mimet.2011.04.018
  67. Zhu W, Plikaytis BB, Shinnick TM. 2003. Resuscitation factors from mycobacteria: homologs of Micrococcus luteus proteins. Tuberculosis 83: 261-269. https://doi.org/10.1016/S1472-9792(03)00052-0
  68. Desnues B, Cuny C, Gregori G, Dukan S, Aguilaniu H, Nystrom T. 2003. Differential oxidative damage and expression of stress defence regulons in culturable and non-culturable Escherichia coli cells. EMBO Rep. 4: 400-404. https://doi.org/10.1038/sj.embor.embor799
  69. Charoenwong D, Andrews S, Mackey B. 2011. Role of rpoS in the development of cell envelope resilience and pressure resistance in stationary-phase Escherichia coli. Appl. Environ. Microbiol. 77: 5220-5229. https://doi.org/10.1128/AEM.00648-11
  70. Magnusson LU, Farewell A, Nystrom T. 2005. ppGpp: a global regulator in Escherichia coli. Trends Microbiol. 13: 236-242. https://doi.org/10.1016/j.tim.2005.03.008
  71. Kusumoto A, Asakura H, 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. https://doi.org/10.1111/j.1348-0421.2012.00428.x
  72. Boulos L, Prevost M, Barbeau, B, Coallier J, Desjardins R. 1999. LIVE/DEAD(R) $BacLight^{TM}$: application of a new rapid staining method for direct enumeration of viable and total bacteria in drinking water. J. Microbiol. Methods 37: 77-86. https://doi.org/10.1016/S0167-7012(99)00048-2
  73. Mizunoe Y, Wai SN, Takade A, Yoshida S. 1999. Restoration of culturability of starvation-stressed and low-temperaturestressed Escherichia coli O157 cells by using $H_2O_2$-degrading compounds. Arch. Microbiol. 172: 63-67. https://doi.org/10.1007/s002030050741
  74. Fischer D, Li Y, Ahlemeyer B, Krieglstein J, Kissel T. 2003. In vitro cytotoxicity testing of polycations: influence of polymer structure on cell viability and hemolysis. Biomaterials 24: 1121-1131. https://doi.org/10.1016/S0142-9612(02)00445-3
  75. Muller S, Nebe-von-Caron G. 2010. Functional single-cell analyses: flow cytometry and cell sorting of microbial populations and communities. FEMS Microbiol. Rev. 34: 554-587. https://doi.org/10.1111/j.1574-6976.2010.00214.x
  76. Anvarian AHP, Smith MP, Overton TW. 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. https://doi.org/10.1016/j.ijfoodmicro.2015.11.016
  77. Kogure K, Simidu U, Taga N. 1979. A tentative direct microscopic method for counting living marine bacteria. Can. J. Microbiol. 25: 415-420. https://doi.org/10.1139/m79-063
  78. Fischer-Le Saux M, Hervio-Heath D, Loaec S, Colwel RR, Pommepuy M. 2002. Detection of cytotoxin-hemolysin mRNA in nonculturable populations of environmental and clinical Vibrio vulnificus strains in artificial seawater. Appl. Environ. Microbiol. 68: 5641-5646. https://doi.org/10.1128/AEM.68.11.5641-5646.2002
  79. Jiang Q, Fu B, Chen Y, Wang Y, Liu H. 2013. Quantification of viable but nonculturable bacterial pathogens in anaerobic digested sludge. Appl. Microbiol. Biotechnol. 97: 6043-6050. https://doi.org/10.1007/s00253-012-4408-2
  80. Desmarchelier PM, Blige SS, Fegan N, Mills L, Vary Jr JC, Tarr PI. 1998. A PCR specific for Escherichia coli O157 based on the rfb locus encoding O157 lipopolysaccharide. J. Clin. Microbiol. 36: 1801-1804.
  81. Fields PI, Blom K, Hughes HJ, Helsel LO, Feng P, Swaminathan B. 1997. Molecular characterization of the gene encoding H antigen in Escherichia coli and development of a PCR-restriction fragment length polymorphism test for identification of E. coli O157:H7 and O157:NM. J. Clin. Microbiol. 35: 1066-1070.
  82. Gannon VPJ, King RK, Kim JY, Thomas EJG. 1992. Rapid and sensitive method for detection of Shiga-like toxin-producing Escherichia coli in ground beef using the polymerase chain reaction. Appl. Environ. Microbiol. 58: 3809-3815.
  83. Schmidt H, Plaschke B, Franke S, Russmann H, Schwarzkopf A, Heesemann J, et al. 1994. Differentiation in virulence patterns of Escherichia coli possessing eae genes. Med. Microbiol. Immunol. 183: 23-31.
  84. Yaron S, Matthews KR. 2002. A reverse transcriptasepolymerase chain reaction assay for detection of viable Escherichia coli O157:H7: investigation of specific target genes. J. Appl. Microbiol. 92: 633-640. https://doi.org/10.1046/j.1365-2672.2002.01563.x
  85. Nogva H K, D romtorp S M, N issen H, R udi K. 2 003. Ethidium monoazide for DNA-based differentiation of viable and dead bacteria by 5’-nuclease PCR. Biotechniques 34: 804-813.
  86. Truchado P, Gil MI, Kostic T, Allende A. 2016. Optimization and validation of a PMA qPCR method for Escherichia coli quantification in primary production. Food Control 62: 150-156. https://doi.org/10.1016/j.foodcont.2015.10.014
  87. Liu Y, Gilchrist A, Zhang J, Li XF. 2008. Detection of viable but nonculturable Escherichia coli O157:H7 bacteria in drinking water and river water. Appl. Environ. Microbiol. 74: 1502-1507. https://doi.org/10.1128/AEM.02125-07
  88. Oliver JD, Dagher M, Linden K. 2005. Induction of Escherichia coli and Salmonella typhimurium into the viable but nonculturable state following chlorination of wastewater. J. Water Health 3: 249-257. https://doi.org/10.2166/wh.2005.040
  89. Nishida T, Orikasa Y, Ito Y, Yu R, Yamada A, Watanabe K, et al. 2006. Escherichia coli engineered to produce eicosapentaenoic acid becomes resistant against oxidative damages. FEBS Lett. 580: 2731-2735. https://doi.org/10.1016/j.febslet.2006.04.032
  90. Dinu L, 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. https://doi.org/10.1016/j.foodcont.2012.10.020
  91. Ohtomo R, Saito M. 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.
  92. Servais P, Prats J, Passerat J, Garcia-Armisen T. 2009. Abundance of culturable versus viable Escherichia coli in freshwater. Can. J. Microbiol. 55: 905-909. https://doi.org/10.1139/W09-043
  93. Marouani-Gadri N, Firmesse O, Chassaing D, Sandris-Nielsen D, Arneborg N, Carpentier B. 2010. Potential of Escherichia coli O157:H7 to persist and form viable but nonculturable cells on a food-contact surface subjected to cycles of soiling and chemical treatment. Int. J. Food Microbiol. 144: 96-103. https://doi.org/10.1016/j.ijfoodmicro.2010.09.002

Cited by

  1. Transcriptional reprogramming in cellular quiescence vol.14, pp.7, 2017, https://doi.org/10.1080/15476286.2017.1327510
  2. Current Perspectives on Viable but Non-culturable State in Foodborne Pathogens vol.8, pp.None, 2017, https://doi.org/10.3389/fmicb.2017.00580
  3. Simple and Precise Counting of Viable Bacteria by Resazurin-Amplified Picoarray Detection vol.90, pp.15, 2017, https://doi.org/10.1021/acs.analchem.8b02096
  4. Study the Features of 57 Confirmed CRISPR Loci in 38 Strains of Staphylococcus aureus vol.9, pp.None, 2017, https://doi.org/10.3389/fmicb.2018.01591
  5. Survey of verotoxin-producing Escherichia coli and faecal coliforms in beef carcasses destined for export at slaughterhouses in Brazil vol.38, pp.1, 2017, https://doi.org/10.1590/1678-457x.37816
  6. Indoor air purification by dielectric barrier discharge combined with ionic wind: physical and microbiological investigations vol.51, pp.16, 2018, https://doi.org/10.1088/1361-6463/aab48b
  7. Comparison of conventional plating, PMA-qPCR, and flow cytometry for the determination of viable enterotoxigenic Escherichia coli along a gastrointestinal in vitro model vol.102, pp.22, 2017, https://doi.org/10.1007/s00253-018-9380-z
  8. The Association of Cell Division Regulated by DicC With the Formation of Viable but Non-culturable Escherichia coli O157:H7 vol.10, pp.None, 2017, https://doi.org/10.3389/fmicb.2019.02850
  9. Metagenomic Profiling of Microbial Pathogens in the Little Bighorn River, Montana vol.16, pp.7, 2017, https://doi.org/10.3390/ijerph16071097
  10. EmPis-1L, an Effective Antimicrobial Peptide Against the Antibiotic-Resistant VBNC State Cells of Pathogenic Bacteria vol.11, pp.2, 2017, https://doi.org/10.1007/s12602-018-9446-3
  11. Induction, detection, formation, and resuscitation of viable but non‐culturable state microorganisms vol.19, pp.1, 2017, https://doi.org/10.1111/1541-4337.12513
  12. Evaluation by Flow Cytometry of Escherichia coli Viability in Lettuce after Disinfection vol.9, pp.1, 2020, https://doi.org/10.3390/antibiotics9010014
  13. Investigation into the Physiological State of Heat Stressed Escherichia coli Used in the Evaluation Testing of an Intrinsic Fluorescence-Based RMM. vol.25, pp.2, 2017, https://doi.org/10.4265/bio.25.91
  14. The fate of cold‐stressed or TETRACYCLINE‐RESISTANTVibrio spp. in precooked shrimp during frozen storage vol.40, pp.4, 2017, https://doi.org/10.1111/jfs.12798
  15. Viable but non culturable state and expression of pathogenic genes of ESCHERICHIA COLI O157 : H7 in salted silver carp vol.40, pp.5, 2017, https://doi.org/10.1111/jfs.12843
  16. Effects of quorum sensing on the biofilm formation and viable but non-culturable state vol.137, pp.None, 2017, https://doi.org/10.1016/j.foodres.2020.109742
  17. Endophytic Fungi: From Symbiosis to Secondary Metabolite Communications or Vice Versa? vol.12, pp.None, 2017, https://doi.org/10.3389/fpls.2021.791033
  18. How to Evaluate Non-Growing Cells-Current Strategies for Determining Antimicrobial Resistance of VBNC Bacteria vol.10, pp.2, 2017, https://doi.org/10.3390/antibiotics10020115
  19. Development of a New Predictive index (Bathing Water Quality Index, BWQI) Based on Escherichia coli Physiological States for Bathing Waters Monitoring vol.9, pp.2, 2021, https://doi.org/10.3390/jmse9020120
  20. The diagnostic tools for viable but nonculturable pathogens in the food industry: Current status and future prospects vol.20, pp.2, 2021, https://doi.org/10.1111/1541-4337.12695
  21. Survival of escherichia coli in Water Microcosm Study and Rethinking its Use as Indicator vol.90, pp.2, 2017, https://doi.org/10.1134/s0026261721020107