Influence of serotype on the growth kinetics and the ability to form biofilms of Salmonella isolates from poultry

Food Microbiology

Volumn 31, Issue 2, 2012, Pages 173-180

  Díez García, Miryam ^a   Capita, Rosa ^a   Alonso Calleja, Carlos ^a  

^a UNIVERSITY OF LEÓN   (Spain)

Author keywords

Biofilms; Growth kinetics; Poultry; Salmonella serotypes

Indexed keywords

ANIMAL; ANIMAL SALMONELLOSIS; ARTICLE; BIOFILM; BIRD DISEASE; CHICKEN; CLASSIFICATION; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; KINETICS; MICROBIOLOGY; PHYSIOLOGY; POULTRY; SALMONELLA; SEROTYPING;

ANIMALS; BIOFILMS; CHICKENS; KINETICS; POULTRY; POULTRY DISEASES; SALMONELLA; SALMONELLA INFECTIONS, ANIMAL; SEROTYPING;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERITIDIS; SALMONELLA PARATYPHI; SALMONELLA POONA; SALMONELLA TYPHI;

EID: 84861005660     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2012.03.012     Document Type: Article

References (38)

1. Bridier A., Dubois-Brissonnet F., Boubetra A., Thomas V., Briandet R. The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. Journal of Microbiological Methods 2010, 82:64-70.
2. Buncič S., Avery S.M., Rocourt J., Dimitrijevic M. Can food-related environmental factors induce different behaviour in two key serovars, 4b and 1/2a, of Listeria monocytogenes?. International Journal of Food Microbiology 2001, 65:201-212.
3. Capita, R., Alonso-Calleja, C., Antibiotic-resistant bacteria: a challenge for the food industry. Critical Reviews in Food Science and Nutrition, doi:10.1080/10408398.2010.519837.
4. Capita R., Alonso-Calleja C., García-Fernández M.C., Moreno B. Influence of strain and trisodium phosphate concentration on growth parameters of Listeria monocytogenes in vitro. Letters in Applied Microbiology 2001, 32:428-432.
5. Capita R., Alonso-Calleja C., Prieto M. Prevalence of Salmonella enterica serovars and genovars from chicken carcasses from slaughterhouses in Spain. Journal of Applied Microbiology 2007, 103:1366-1375.
6. CDC (Centers for Disease and Control Prevention) CDC Estimates of Food-borne Illness in the United States 2011, Available at:, (Date last accessed 03.12.11.). http://www.cdc.gov/foodborneburden/2011-foodborne-estimates.html.
7. Dalgaard P., Ross T., Kamperman L., Neumeyer K., McMeekin T.A. Estimation of bacterial growth rates from turbidimetric and viable count data. International Journal of Food Microbiology 1994, 23:391-404.
8. Del Río E., González de Caso B., Prieto M., Alonso-Calleja C., Capita R. Effect of poultry decontaminants concentration on growth kinetics for pathogenic and spoilage bacteria. Food Microbiology 2008, 25:888-894.
9. Dunsmore D.G., Bates P.J. Attachment of bacteria to glass surfaces immersed in milk. Australian Journal of Dairy Technology 1982, 37:35-36.
10. EFSA The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2009. EFSA Journal 2011, 9(3):2090-2477. Available at:, (Date last accessed 03.12.11.). http://www.efsa.europa.eu/en/efsajournal/doc/2090.pdf.
11. European Commission The Rapid Alert System for Food and Feed (RASFF) 2010, Annual Report 2009, EU Directorate General for Health and Consumers, Luxemburg, Available at:, (Date last accessed 03.12.11.). http://ec.europa.eu/food/food/rapidalert/report2009_en.pdf.
12. Garthright W.E. Refinements in the prediction of microbial growth curves. Food Microbiology 1991, 8:239-248.
13. Girard M.P., Steele D., Chaignat C.-L., Kieny M.P. A review of vaccine research and development: human enteric infections. Vaccine 2006, 24:2732-2750.
14. Hood S.K., Zottola E.A. Adherence to stainless steel by foodborne microorganisms during growth in model food systems. International Journal of Food Microbiology 1997, 37:145-153.
15. Ibuchi R., Hara-Kudo Y., Hasegawa A., Kumagai S. Survival of Salmonella on a polypropylene surface under dry conditions in relation to biofilm-formation capability. Journal of Food Protection 2010, 73(8):1506-1510.
16. Jain S., Chen J. Attachment and biofilm formation by various serotypes of Salmonella as influenced by cellulose production and thin aggregative fimbriae biosynthesis. Journal of Food Protection 2007, 70(11):2473-2479.
17. Juneja V.K., Marks H.M., Huang L. Growth and heat resistance kinetic variation among various isolates of Salmonella and its application to risk assessment. Risk Analysis 2003, 23:199-213.
18. Kim S.H., Wei Ch.-I. Biofilm formation by multidrug-resistant Salmonella enterica serotype Typhimurium phage type DT104 and other pathogens. Journal of Food Protection 2007, 70(1):22-29.
19. Lestari S.I., Han F., Wang F., Ge B. Prevalence and antimicrobial resistance of Salmonella serovars in conventional and organic chickens from Louisiana retail stores. Journal of Food Protection 2009, 72:1165-1172.
20. Lianou A., Koutsoumanis K.P. Effect of the growth environment on the strain variability of Salmonella enterica kinetic behavior. Food Microbiology 2011, 28:828-837.
21. Marin C., Hernandez A., Lainez M. Biofilm development capacity of Salmonella strains isolated in poultry risk factors and their resistance against disinfectants. Poultry Science 2009, 88:424-431.
22. Martínez E.V., Varela M.C., Cevallos C., Hernández-Pezzi G., Torres A., Ordóñez P. Brotes de enfermedades transmitidas por alimentos. España, 2004-2007 (excluye brotes hídricos). Boletín Epidemiológico Semanal 2008, 16:241-252. Available at:, (Date last accessed 03.12.11.). http://www.marm.es/es/ganaderia/temas/sanidad-animal-e-higiene-ganadera/brotes_enfermadades_tcm7-6000.pdf.
23. Oliveira K., Oliveira T., Teixeira P., Azeredo J., Henriques M., Oliveira R. Comparison of the adhesion ability of different Salmonella Enteritidis serotypes to materials used in kitchens. Journal of Food Protection 2006, 69:2352-2356.
24. Oscar T.P. Variation of lag time and specific growth rate among 11 strains of Salmonella inoculated onto sterile ground chicken breast burgers and incubated at 25 °C. Journal of Food Safety 2000, 20:225-236.
25. Patel J., Sharma M. Differences in attachment of Salmonella enterica serovars to cabbage and lettuce leaves. International Journal of Food Microbiology 2010, 139:41-47.
26. Peeters E., Nelis H.J., Coenye T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. Journal of Microbiological Methods 2008, 72:157-165.
27. Pui C.F., Wong W.C., Chai L.C., Lee H.Y., Tang J.Y.H., Noorlis A., Farinazleen M.G., Cheah Y.K., Son R. Biofilm formation by Salmonella Typhi and Salmonella Typhimurium on plastic cutting board and its transfer to dragon fruit. International Food Research Journal 2011, 18:31-38.
28. Ramesh N., Joseph S.W., Carr L.E., Douglass L.W., Wheaton F.W. Evaluation of chemical disinfectants for the elimination of Salmonella biofilms form poultry transport containers. Poultry Science 2002, 81:904-910.
29. Rattanasomboon N., Bellara S.R., Harding C.L., Fryer P.J., Thomas C.R., Al-Rubeai M., McFarlane C.M. Growth nd enumeration of the meat spoilage bacterium Brochothrix thermosphacta. International Journal of Food Microbiology 1999, 51:145-158.
30. Rodrigues D., Teixeira P., Oliveira R., Azeredo J. Salmonella enterica Enteritidis biofilm formation and viability on regular and triclosan-impregnated bench cover materials. Journal of Food Protection 2011, 74:32-37.
31. Sánchez M.X., Fluckey W.M., Brashears M.M., McKee S.R. Microbial profile and antibiotic susceptibility of Campylobacter spp. and Salmonella spp. in broilers processed in air-chilled and immersion-chilled environments. Journal of Food Protection 2002, 65:948-956.
32. Shi X., Zhu X. Biofilm formation and food safety in food industries. Trends in Food Science and Technology 2009, 20:407-413.
33. Steenackers H., Hermans K., Vanderleyden J., De Keersmaecker S.C.J. Salmonella biofilms: an overview on occurrence, structure, regulation and eradication. Food Research International 2011, 45:502-531.
34. Stepanović S., ćirković I., Mijać V., Švabić-Vlahović M. Influence of the incubation temperature, atmosphere and dynamic conditions on biofilm formation by Salmonella spp. Food Microbiology 2003, 20:339-343.
35. Stepanović S., ćirković I., Ranin L., Švabić-Vlahović M. Biofilm formation by Salmonella spp. and Listeria monocytogenes on plastic surface. Letters in Applied Microbiology 2004, 38:428-432.
36. Tondo E.C., Machado T.R.M., Malheiros P.da S., Padrão D.K., Carvalho A.L.de, Brandelli A. Adhesion and biociddes inactivation of Salmonella on stainless steel and polyethylene. Brazilian Journal of Microbiology 2010, 41:1027-1037.
37. Velasco L., Sobrino L., García M., Soler P., Martinez E. Infecciones por Salmonella Typhi y Salmonella Paratyphi en España. Sistema de Información Microbiológica. Años 1998-2008. Boletín Epidemiológico Semanal 2009, 17:205-216. Available at:, (Date last accessed 03.12.11.). http://revistas.isciii.es/bes/index.php/bes/article/view/121/120.
38. Vestby L.K., Møretrø T., Langsrud S., Heir E., Nesse L. Biofilm forming abilities of Salmonella are correlated with persistence in fish meal- and feed factories. BMC Veterinary Research 2009, 5:20-25.