Effect of acid tolerance response (ATR) on attachment of Listeria monocytogenes Scott A to stainless steel under extended exposure to acid or/and salt stress and resistance of sessile cells to subsequent strong acid challenge

International Journal of Food Microbiology

Volumn 145, Issue 2-3, 2011, Pages 400-406

  Chorianopoulos, Nikos ^a   Giaouris, Efstathios ^a   Grigoraki, Ioanna ^a   Skandamis, Panagiotis ^a   Nychas, George John ^a  

^a AGRICULTURAL UNIVERSITY OF ATHENS   (Greece)

Author keywords

Acid tolerance response; Acidity; Attachment; Conductance; Listeria monocytogenes; Salinity; Stainless steel

Indexed keywords

HYDROCHLORIC ACID; LACTIC ACID; SODIUM CHLORIDE; STAINLESS STEEL;

ACID TOLERANCE; ACID TOLERANCE RESPONSE; ACIDITY; ARTICLE; BACTERIAL CELL; BACTERIAL COUNT; BACTERIUM CONTAMINATION; COLONY FORMING UNIT; CONTROLLED STUDY; FOOD PROCESSING; LISTERIA MONOCYTOGENES; NONHUMAN; PH; PH MEASUREMENT; PLANKTON; SALINITY; SALT STRESS; SESSILE SPECIES; WASTE MANAGEMENT;

ACIDS; ADAPTATION, PHYSIOLOGICAL; BACTERIAL ADHESION; COLONY COUNT, MICROBIAL; HYDROGEN-ION CONCENTRATION; LISTERIA MONOCYTOGENES; SODIUM CHLORIDE; STAINLESS STEEL;

BACTERIA (MICROORGANISMS); LISTERIA MONOCYTOGENES;

EID: 79952192729     PISSN: 01681605     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2011.01.001     Document Type: Article

References (57)

1. Aarnisalo K., Salo S., Miettinen H., Suihko M.-L., Wirtanen G., Autio T., Lunden J., Korkeala H., Sjoberg A.-M. Bactericidal efficiencies of commercial disinfectants against Listeria monocytogenes on surfaces. Journal of Food Safety 2000, 20:237-250.
2. Abee T., Wouters J.A. Microbial stress response in minimal processing. International Journal of Food Microbiololgy 1999, 50:65-91.
3. Abram F., Starr E., Karatzas K.A.G., Matlawska-Wasowska K., Boyd A., Wiedmann M., Boor K.J., Connally D., O'Byrne C.P. Identification of components of the sigma B regulon in Listeria monocytogenes that contribute to acid and salt tolerance. Applied and Environmental Microbiology 2008, 74:6848-6858.
4. Adriao A., Vieira M., Fernandes I., Barbosa M., Sol M., Tenreiro R.P., Chambel L., et al. Marked intra-strain variation in response of Listeria monocytogenes dairy isolates to acid or salt stress and the effect of acid or salt adaptation on adherence to abiotic surfaces. International Journal of Food Microbiology 2008, 123:142-150.
5. Beresford M.R., Andrew P.W., Shama G. Listeria monocytogenes adheres to many materials found in food-processing environments. Journal of Applied Microbiology 2001, 90:1000-1005.
6. Briandet R., Leriche V., Carpentier B., Bellon-Fontaine M.-N. Effects of the growth procedure on the surface hydrophobicity of Listeria monocytogenes cells and their adhesion to stainless steel. Journal of Food Protection 1999, 62:994-998.
7. Buchanan R.L., Edelson S.G. Culturing enterohemorrhagic Escherichia coli in the presence and absence of glucose as a simple means of evaluating the acid tolerance of stationary-phase cells. Applied and Environmental Microbiology 1996, 62:4009-4013.
8. Chorianopoulos N.G., Giaouris E.D., Skandamis P.N., Haroutounian S.A., Nychas G.-J.E. Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage and pathogenic bacteria: bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers. Journal of Applied Microbiology 2008, 104:1586-1596.
9. Datta A.R., Benjamin M.M. Factors controlling acid tolerance of Listeria monocytogenes: effects of nisin and other ionophores. Applied and Environmental Microbiology 1997, 63:4123-4126.
10. Davis M.J., Coote P.J., O'Byrne C.P. Acid tolerance in Listeria monocytogenes: the adaptive acid tolerance response (ATR) and growth-phase-dependent acid resistance. Microbiology 1996, 142:2975-2982.
11. EFSA-ECDC The Community Summary Report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2006. The EFSA Journal 2007, 130:2-352.
12. Flint S.H., Brooks J.D., Bremer P.J. Use of the Malthus conductance growth analyser to determine numbers of thermophilic streptococci on stainless steel. Journal of Applied Microbiology 1997, 83:335-339.
13. Frank J.F., Koffi R.A. Surface-adherent growth of Listeria monocytogenes is associated with increased resistance to surfactant sanitizers and heat. Journal of Food Protection 1990, 53:550-554.
14. Gahan C.G.B., O'Driscoll B., Hill C. Acid adaptation of L. monocytogenes can enhance survival in acidic foods and during milk fermentation. Applied and Environmental Microbiology 1996, 62:3128-3132.
15. Gandhi M., Chikindas M.L. Listeria: a foodborne pathogen that knows how to survive. International Journal of Food Microbiology 2007, 113:1-15.
16. Giaouris E.D., Nychas G.-J.E. The adherence of Salmonella enteritidis PT4 to stainless steel: the importance of the air-liquid interface and nutrient availability. Food Microbiology 2006, 23:747-752.
17. Gordon Greer G., Dilts B.D. Lactic acid inhibition of the growth of spoilage bacteria and cold tolerant pathogens on pork. International Journal of Food Microbiology 1995, 25:141-151.
18. Gounadaki A.S., Skandamis P.N., Drosinos E.H., Nychas G.-J.E. Microbial ecology of food contact surfaces and products of small-scale facilities producing traditional sausages. Food Microbiology 2008, 25:313-323.
19. Hill C., Cotter P.D., Sleator R.D., Gahan C.G.M. Bacterial stress response in Listeria monocytogenes: jumping the hurdles imposed by minimal processing. International Dairy Journal 2002, 12:273-283.
20. Hill C., O'Driscoll B., Booth I. Acid adaptation and food poisoning microorganisms. International Journal of Food Microbiology 1995, 28:245-254.
21. Hood S.K., Zottola E.A. Growth media and surface conditioning influence the adherence of Pseudomonas fragi, Salmonella typhimurium, and Listeria monocytogenes cells to stainless steel. Journal of Food Protection 1997, 60:1034-1037.
22. Jensen A., Larsen M.H., Ingmer H., Vogel B.F., Gram L. Sodium chloride enhances adherence and aggregation and strain variation influences invasiveness of Listeria monocytogenes strains. Journal of Food Protection 2007, 70:592-599.
23. Kathariou S. Listeria monocytogenes virulence and pathogenicity, a food safety perspective. Journal of Food Protection 2002, 65:1811-1829.
24. Koutsoumanis K.P., Kendall P.A., Sofos J.N. Effect of food processing - related stresses on acid tolerance of Listeria monocytogenes. Applied and Environmental Microbiology 2003, 69:7514-7516.
25. Koutsoumanis K.P., Sofos J.N. Comparative acid stress of Listeria monocytogenes, Escherichia coli 0157:H7 and Salmonella Typhimurium after habituation at different pH conditions. Letters in Applied Microbiology 2004, 38:321-326.
26. Kroll R.G., Patchett R.A. Induced acid tolerance in Listeria monocytogenes. Letters in Applied Microbiology 1992, 14:224-227.
27. Lambert R.J., Stratford M. Weak-acid preservatives: modelling microbial inhibition and response. Journal of Applied Microbiology 1999, 86:157-164.
28. Leistner L. Basic aspects of food preservation by hurdle technology. International Journal of Food Microbiology 2000, 55:181-186.
29. Leyer G.J., Johnson E.A. Acid adaptation induces cross-protection against environmental stresses in Salmonella Typhimurium. Applied and Environmental Microbiology 1993, 59:1842-1847.
30. Lianou A., Stopforth J.D., Yoon Y., Wiedmann M., Sofos J.N. Growth and stress resistance variation in culture broth among Listeria monocytogenes strains of various serotypes and origins. Journal of Food Protection 2006, 69:2640-2647.
31. Lin J., Smith M.P., Chapin K.C., Baik H.S., Bennett G.N., Foster J.W. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Applied and Environmental Microbiology 1996, 62:3094-3100.
32. Lou Y., Yousef A.E. Resistance of Listeria monocytogenes to heat after adaptation to environmental stresses. Journal of Food Protection 1996, 59:465-471.
33. Lou Y., Yousef A.E. Adaptation to sublethal environmental stresses protects Listeria monocytogenes against lethal preservation factors. Applied and Environmental Microbiology 1997, 63:1252-1255.
34. Lundén J.M., Miettinen M.K., Autio T.J., Korkeala H.J. Persistent Listeria monocytogenes strains show enhanced adherence to food contact surface after short contact times. Journal of Food Protection 2000, 63:1204-1207.
35. Mead P.S., Slutsker L., Dietz V., McCaig L.F., Breese J.S., Shapiro C., Griffin P.M., Tauxe R.V. Food-related illness and death in the United States. Emerging Infectious Diseases 1999, 5:607-625.
36. Møretrø T., Langsrud S. Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms 2004, 1:107-121.
37. O'Driscoll B., Gahan C.G.M., Hill C. Adaptive acid tolerance response in Listeria monocytogenes: isolation of an acid-tolerant mutant which demonstrates increased virulence. Applied and Environmental Microbiology 1996, 62:1693-1698.
38. O'Driscoll B., Gahan C.G.M., Hill C. Two-dimensional polyacrylamide gel electrophoresis analysis of the acid tolerance response in Listeria monocytogenes LO28. Applied and Environmental Microbiology 1997, 63:2679-2685.
39. Phan-Thanh L., Montagne A. Physiological and biochemical aspects of the acid survival of Listeria monocytogenes. The Journal of General and Applied Microbiology 1998, 44:183-191.
40. Phan-Thanh L., Mahouin F. A proteomic approach to study the acid response in Listeria monocytogenes. Electrophoresis 1999, 20:2214-2224.
41. Poimenidou S., Belessi C.A., Giaouris E.D., Gounadaki A.S., Nychas G.-J.E., Skandamis P.N. Listeria monocytogenes attachment to and detachment from stainless steel surfaces in a simulated dairy processing environment. Applied and Environmental Microbiology 2009, 75:7182-7188.
42. Rodriguez A., McLandsborough L.A. Evaluation of the transfer of Listeria monocytogenes from stainless steel and high-density polyethylene to bologna and American cheese. Journal of Food Protection 2007, 70:600-606.
43. Ryan S., Hill C., Gahan C.G.M. Acid stress responses in Listeria monocytogenes. Advances in Applied Microbiology 2008, 65:67-91.
44. Rychlik I., Barrow P.A. Salmonella stress management and its relevance to behaviour during intestinal colonization and infection. FEMS Microbiology Reviews 2005, 29:1021-1040.
45. Samelis J., Ikeda J.S., Sofos J.N. Evaluation of the pH-dependent, stationary-phase acid tolerance in Listeria monocytogenes and Salmonella Typhimurium DT104 induced by culturing in media with 1% glucose: a comparative study with Escherichia coli 0157:H7. Journal of Applied Microbiology 2003, 95:563-575.
46. Shabala L., Lee S.H., Cannesson P., Ross T. Acid and NaCl limits to growth of Listeria monocytogenes and influence of sequence of inimical acid and NaCl levels on inactivation kinetics. Journal of Food Protection 2008, 71:1169-1177.
47. Silley P., Forsythe S. Impedance microbiology - a rapid change for microbiologists. The Journal of Applied Bacteriology 1996, 80:233-243.
48. Silva S., Teixeira P., Oliveira R., Azeredo J. Adhesion to and viability of Listeria monocytogenes on food contact surfaces. Journal of Food Protection 2008, 71:1379-1385.
49. Skandamis P.N., Yoon Y., Stopforth J.D., Kendall P.A., Sofos J.N. Heat and acid tolerance of Listeria monocytogenes after exposure to single and multiple sublethal stresses. Food Microbiology 2008, 25:294-303.
50. Skandamis P.N., Stopforth J.D., Yoon Y., Kendall P.A., Sofos J.N. Heat and acid tolerance responses of Listeria monocytogenes as affected by sequential exposure to hurdles during growth. Journal of Food Protection 2009, 72:1412-1418.
51. Smoot L.M., Pierson M.D. Effect of environmental stress on the ability of Listeria monocytogenes ScottA to attach to food contact surfaces. Journal of Food Protection 1998, 61:1293-1298.
52. Stopforth J.D., Samelis J., Sofos J.N., Kendall P.A., Smith G.C. Biofilm formation by acid-adapted and nonadapted Listeria monocytogenes in fresh beef decontamination washings and its subsequent inactivation with sanitizers. Journal of Food Protection 2002, 65:1717-1727.
53. Tiganitas A., Zeaki N., Gounadaki A.S., Drosinos E.H., Skandamis P.N. Study of the effect of lethal and sublethal pH and aw stresses on the inactivation or growth of Listeria monocytogenes and Salmonella Typhimurium. International Journal of Food Microbiology 2009, 134:104-112.
54. Tompkin R.B. Control of Listeria monocytogenes in the food-processing environment. Journal of Food Protection 2002, 65:709-725.
55. Tresse O., Lebret V., Benezech T., Faille C. Comparative evaluation of adhesion, surface properties, and surface protein composition of Listeria monocytogenes strains after cultivation at constant pH of 5 and 7. Journal of Applied Microbiology 2006, 101:53-62.
56. Wiedmann M., Arvik T.J., Hurley R.J., Boor K.J. General stress transcription factor σB and its role in acid tolerance and virulence of Listeria monocytogenes. Journal of Bacteriology 1998, 180:3650-3656.
57. Wilks S.A., Michels H.T., Keevil C.W. Survival of Listeria monocytogenes ScottA on metal surfaces: implications for cross-contamination. International Journal of Food Microbiology 2006, 111:93-98.