Ability of salmonella spp. to produce biofilm is dependent on temperature and surface material

Foodborne Pathogens and Disease

Volumn 11, Issue 6, 2014, Pages 478-483

  De Oliveira, Débora Cristina Vidal ^a   Fernandes Júnior, Ary ^a   Kaneno, Ramon ^a   Silva, Márcia Guimarães ^a   Araújo Júnior, João Pessoa ^a   Silva, Nathalia Cristina Cirone ^a   Rall, Vera Lúcia Mores ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

GLASS; POLYVINYLCHLORIDE; STAINLESS STEEL; BACTERIAL PROTEIN; FIMBRIA PROTEIN;

ADRA GENE; AGFD GENE; ARTICLE; BACTERIAL STRAIN; BACTERIUM ISOLATION; BIOFILM; BRAZIL; CONTROLLED STUDY; GENE; GENE EXPRESSION; MORPHOTYPE; NONHUMAN; POULTRY; PRIORITY JOURNAL; SALMONELLA; SURFACE PROPERTY; TEMPERATURE; ANIMAL; CHEMISTRY; CLASSIFICATION; COMPARATIVE STUDY; DEVICES; ECONOMICS; FOOD CONTAMINATION; FOOD HANDLING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; MATERIALS TESTING; MEAT; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PREVENTION AND CONTROL; SPECIES DIFFERENCE;

ANIMALS; BACTERIAL PROTEINS; BIOFILMS; BRAZIL; FIMBRIAE PROTEINS; FOOD CONTAMINATION; FOOD HANDLING; GENE EXPRESSION REGULATION, BACTERIAL; GLASS; MATERIALS TESTING; MEAT; POLYMERASE CHAIN REACTION; POLYVINYL CHLORIDE; POULTRY; SALMONELLA; SPECIES SPECIFICITY; STAINLESS STEEL; SURFACE PROPERTIES; TEMPERATURE;

EID: 84902013269     PISSN: 15353141     EISSN: 15567125     Source Type: Journal    
DOI: 10.1089/fpd.2013.1710     Document Type: Article

References (41)

1. th ed. Downes FP, Ito K (eds.). Washington, DC: APHA, 2001, pp. 357-380.
2. Anriany YA, Weiner RM, Johnson JA, Rezende CE, Joseph SW. Salmonella enterica serovar Typhimurium DT104 displays a rugose phenotype. Appl Environ Microbiol 2001;67: 4048-4056.
3. Arnold JW, Yates IE. Interventions for control of Salmonella: Clearance of microbial growth from rubber picker fingers. Poult Sci 2009;88:1292-1298.
4. Arnold T, Scholz HC, Marg H, Rosler U, Hensel A. Impact of invA-PCR and culture detection methods on occurrence and survival of Salmonella in the flesh, internal organs and lym-phoid tissues of experimentally infected pigs. J Vet Med Ser B 2004;51:459-463.
5. Austin JW, Bergeron G. Development of bacterial biofilms in dairy processing lines. J Dairy Res 1995;62:509-519.
6. Boulanger-Peterson L. Process of bioadhesion on stainless steel surfaces and cleanability: A review with special reference to the food industry. Biofouling 1996;10:275-300.
7. Collinson SK, Clouthier SC, Doran JL, Banser PA, Kay WW. Salmonella Enteritidis agfBAC operon encoding thin, aggregative fimbriae. J Bacteriol 1996;178:662-667.
8. Davies RH, Wales AD. Investigations into Salmonella contamination in poultry feedmills in the United Kingdom. J Appl Microbiol 2010;109:1430-1440.
9. Gerstel U, Römling U. Oxygen tension and nutrient starvation are major signals that regulate agfD promoter activity and expression of the multicellular morphotype in Salmonella typhimurium. Environ Microbiol 2001;3:638-648.
10. Gerstel U, Römling U. The csgD promoter, a control unit for biofilm formation in Salmonella Typhimurium. Res Micro-biol 2003;154:659-667.
11. Grantcharova N, Peters V, Monteiro C, Zakikhany K, Römling U. Bistable expression of CsgD in biofilm development of Salmonella enterica Serovar Typhimurium. J Bacteriol 2010; 192:456-466.
12. Hasegawa A, Hara-Kudo Y, Kumagai S. Survival of Salmonella strains differing in their biofilm-formation capability upon exposure to hydrochloric and acetic acid and to high salt. J Vet Med Sci 2011;73:1163-1168.
13. Hurrell E, Kucerova E, Loughlin M, Caubilla-Barron J, Forsythe SJ. Biofilm formation on enteral feeding tubes by-Cronobacter sakazakii, Salmonella serovars and other En-terobacteriaceae. Int J Food Microbiol 2009;136:227-231.
14. Joseph B, Otta SK, Karunasagar I, Karunasagar I. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int J Food Microbiol 2001;64: 367-372.
15. Kim S, Wei C. Molecular characterization of biofilm formation and attachment of Salmonella enteric serovar Typhimurium DT104 on food contact surfaces. J Food Protect 2009;72: 1841-1847.
16. Lapidot A, Römling U, Yaron S. Biofilm formation and the survival of Salmonella Typhimurium on parsley. Int J Food Microbiol 2006;109:229-233.
17. Latasa C, Roux A, Toledo-Arana A, Ghigo JM, Gamazo C, Penadés JR, Lasa I. BapA, a large secreted protein required for biofilm formation and host colonization of Salmonella enterica serovar Enteritidis. Mol Microbiol 2005;58:1322-1339.
18. Lu Y, Dong H, Chen S, Chen Y, Peng D, Liu X. Characterization of biofilm formation by Salmonella enterica Serovar Pullorum strains. Afr J Microbiol Res 2011;5:2428-2437.
19. Malcova M, Hradecka H, Karpiskova R, Rychlik I. Biofilm formation in field strains of Salmonella enterica serovar Typhimurium: Identification of a new colony morphology type and the role of SGI1 in biofilm formation. Vet Microbiol 2008;129:360-366.
20. [MAPA] Ministerio da Agricultura, Pecuaria e Abastecimento. Anexo I: Regulamento Tecnico da Inspeção Tecnologica e Higienico-Sanitaria de Carne de Aves. Portaria N° 210, 1998.
21. Moretro T, Vestby LK, Nesse LL, Hannevik S, Kotlarz K, Lansrud S. Evaluation of efficiency of disinfectants against Salmonella from the feed industry. J Appl Microbiol 2009; 106:1005-1012.
22. Mulcahy H, Charron-Mazenod L, Lewenza S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudo-monas aeruginosa biofilms. PLoS Pathog 2008; 5:e1000213.
23. Oliveira K, Oliveira T, Teixeira P, Azeredo J, Oliveira R. Adhesion of Salmonella Enteritidis to stainless steel surfaces. Braz J Microbiol 2007;38:318-323.
24. Patel MK, Chen S, Pringle J, Russo E, Vinaras J, Weiss J, Anderson S, Sunenshine R, Komatsu K, Schumacher M, Flood D, Theobald L, Bopp C, Wannemuehler K, White P, Angulo FJ, Behravesh CB. A prolonged outbreak of Salmonella Montevideo infections associated with multiple locations of a restaurant chain in Phoenix, Arizona, 2008. J Food Protect 2010;73:1858-1863.
25. Prouty AM, Gunn JS. Comparative analysis of Salmonella enterica serovar Typhimurium biofilm formation in gallstones and on glass. Infect Immun 2003;70:2640-2649.
26. Romling U, Sierralta WD, Eriksson K, Normark S. Multicellular and aggregative behaviour of Salmonella typhimurium strains is controlled by mutations in the agfD promoter. Mol Microbiol 1998;28:249-264.
27. Romling U, Rohde M, Olsen A, Normark S, Reinkoster J. AgfD, the checkpoint of multicellular and aggregative behavior in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol 2000;36:10-23.
28. Romling U. Molecular biology of cellulose production in bacteria. Res Microbiol 2002;153:205-212.
29. Romling U, Bokranz W, Rabsch W, Zogaj X, Nimtz M, Tschape H. Occurrence and regulation of the multicellular morphotype in Salmonella serovars important in human disease. Inter J Med Microbiol 2003;293:273-285.
30. Scher K, Romling U, Yaron S. Effect of heat, acidification, and chlorination on Salmonella enterica serovar Typhimurium cells in a biofilm formed at the air-liquid interface. Appl Environ Microbiol 2005;71:1163-1168.
31. Simões M, Simões LC, Cleto S, Pereira MO, Vieira MJ. The effects of a biocide and a surfactant on the detachment of Pseudomonas fluorescens from glass surfaces. Int J Food Microbiol 2008;121:335-341.
32. Sinde E, Carballo J. Attachment of Salmonella spp. and Listeria monocytogenes to stainless steel, rubber, and poly-tetrafluoroethylene: The influence of free energy and the effect of commercial sanitizers. Food Microbiol 2000;17: 439-447.
33. Solano C, Garcia B, Valle J, Berasain C, Ghigo JM, Gamazo C, Lasa I. Genetic analysis of Salmonella enteritidis biofilm formation: Critical role of cellulose. Mol Microbiol 2002; 43:793-808.
34. Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods 2000; 40:175-179.
35. Stepanovic S, Cirkovic I, Mijac M, Svabic-Vlahovic M. Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiol 2003;20:339-343.
36. Stepanovic S, Cirkovic I, Ranin L, Svabic-Vlahovic M. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Lett Appl Microbiol 2004;38;428-432.
37. Trachoo N, Frank JF, Stern NJ. Survival of Campylobacter jejuni in biofilms isolated from chicken houses. J Food Protect 2002;65:1110-1116.
38. Vestby LK, Moretro T, Langsrud S, Heir E, Nesse LL. Biofilm forming abilities of Salmonella are correlated with persistence in fish meal-and feed factories. BMC Vet Res 2009;5:20.
39. White AP, Gibson DL, Kim W, Kay WW, Surette MG. Thin aggregative fimbriae and cellulose enhance long-term survival and persistence of Salmonella. J Bacteriol 2006;188: 3219-3227.
40. Xu H, Lee HY, Ahn J. Growth and virulence properties of biofilm-forming Salmonella enterica serovar Typhimurium under different acidic conditions. Appl Environ Microbiol 2010;76:7910-7917.
41. Zakikhany K, Harrington CR, Nimtz M, Hinton JC, Römling U. Unphosphorylated csgD controls biofilm formation in Salmonella enterica serovar Typhimurium. Mol Microbiol 2010; 77:771-786.