Journal of Food Processing and Preservation

Volume 41, Issue 1 e12758

Original Article

Approaches to Removal and Killing of Salmonella Spp. Biofilms

Barbara Speranza,

Barbara Speranza

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Search for more papers by this author

Noemi Monacis,

Noemi Monacis

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Search for more papers by this author

Milena Sinigaglia,

Milena Sinigaglia

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Search for more papers by this author

Maria Rosaria Corbo,

Corresponding Author

Maria Rosaria Corbo

[email protected]

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Corresponding author. TEL: +39 0881 589232; EMAIL: [email protected]Search for more papers by this author

Barbara Speranza,

Barbara Speranza

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Search for more papers by this author

Noemi Monacis,

Noemi Monacis

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Search for more papers by this author

Milena Sinigaglia,

Milena Sinigaglia

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Search for more papers by this author

Maria Rosaria Corbo,

Corresponding Author

Maria Rosaria Corbo

[email protected]

Department of the Science of Agriculture, Food and Environment (SAFE), University of Foggia, Foggia, Italy

Corresponding author. TEL: +39 0881 589232; EMAIL: [email protected]Search for more papers by this author

First published: 15 April 2016

https://doi.org/10.1111/jfpp.12758

Citations: 9

Share a link

Email
Wechat
Bluesky

Abstract

This study aims to assess the effectiveness of three sanitizers (an alkaline solution, an acid solution and a quaternary ammonium salt) to remove biofilm formed by Salmonella spp. on stainless steel surfaces. To evaluate the individual or combined effects of sanitizer concentration, time (5.0–25 min) and temperature (25–65C) on survival of Salmonella spp. biofilms three different Central Composite Designs (CCD) were developed. Results highlighted that treatments containing NaOH were able to eliminate more than 82–83% of sessile population, whereas the total removal of biofilm was obtained using a solution at least 800 ppm for 15 min at 45C. Peracetic acid seemed to be more effective than NaOH assuring the total removal of biofilm at low temperature. Even the quaternary ammonium salt was able to remove completely Salmonella spp. biofilms at 60C using a solution at 12 ppm, or at higher temperature (65C), using a less concentrated solution (6 ppm).

Practical Applications

Due to the wide range of contributing factors (surface type, availability of nutrients and oxygen, microbial species, etc.) biofilms are quite diverse; in essence it can be said that each biofilm is different. Even if numerous attempts have been made to find standardized systems to prevent, remove and kill biofilm cells, until now there is no unique system that is able to remove all biofilms. Thus, a study on the factors affecting the resistance of Salmonella spp. biofilms against sanitizers may be useful into the development of new sanitation strategies in food industries.

References

Akbas, M.Y. and Kokumer, T. 2015. The prevention and removal of biofilm formation of Staphylococcus aureus strains isolated from raw milk samples by citric acid treatments. Int. J. Food Sci. Technol. 50, 1666–1672.
10.1111/ijfs.12823
CAS Web of Science® Google Scholar
Akbas, M.Y. and Olmez, H. 2007. Inactivation of Escherichia coli and Listeria monocytogenes on iceberg lettuce by dip wash treatments with organic acids. Lett. Appl. Microbiol. 44, 619–624.
10.1111/j.1472-765X.2007.02127.x
CAS PubMed Web of Science® Google Scholar
Amaral, V.C.S., Machinski, M., Santos, P.R., Da Silva, A.F., Mikcha, J.M.G. and Santos, R.D. 2015. Effect of carvacrol and thymol on Salmonella spp. biofilms on polypropylene. Int. J. Food Sci. Technol. 50, 2509–2518.
10.1111/ijfs.12934
CAS Web of Science® Google Scholar
Ammor, S., Chevallier, I., Laguet, A., Labadie, J., Talon, R. and Dufour, E. 2004. Investigation of the selective bactericidal effect of several decontaminating solutions on bacterial biofilms including useful, spoilage and/or pathogenic bacteria. Food Microbiol. 21, 11–17.
10.1016/S0740-0020(03)00051-0
CAS Web of Science® Google Scholar
Anang, D.M., Rusul, G., Bakar, J. and Ling, F.H. 2007. Effects of lactic acid and lauricidin on the survival of Listeria monocytogenes, Salmonella enteritidis and Escherichia coli O157: H7 in chicken breast stored at 4C. Food Control 18, 961–969.
10.1016/j.foodcont.2006.05.015
CAS Web of Science® Google Scholar
Bevilacqua, A., Corbo, M.R. and Sinigaglia, M. 2010 . Design of experiments: A powerful tool in food microbiology. In Current Research, Technology and Educational Topic in Applied Microbiology and Microbial Biotecnology ( A. MendéZ-Vilas, ed.) pp. 1419–1429, Formatex Research Center, Badajoz.
Google Scholar
Chaitiemwong, N., Hazeleger, W.C. and Beumer, R.R. 2010. Survival of Listeria monocytogenes on a conveyor belt material with or without antimicrobial additives. Int. J. Food Microbiol. 142, 260–263.
10.1016/j.ijfoodmicro.2010.06.021
CAS PubMed Web of Science® Google Scholar
Chavant, P., Gaillard-Martinie, B. and Hebraud, M. 2004. Antimicrobial effects of sanitizers against planktonic and sessile Listeria monocytogenes cells according to the growth phase. FEMS Microbiol. Lett. 236, 241–248.
10.1111/j.1574-6968.2004.tb09653.x
PubMed Web of Science® Google Scholar
Chmielewsky, R.N. and Frank, J.F. 2003. Biofilm formation and control in food processing facilities. Compr. Rev. Food Sci Food Safety 2, 22–32.
10.1111/j.1541-4337.2003.tb00012.x
Google Scholar
Cloete, T.E. 2003. Resistance mechanisms of bacteria to antimicrobial compounds. Int. Biodeter. Biodegr. 51, 277–282.
10.1016/S0964-8305(03)00042-8
CAS Web of Science® Google Scholar
Corbo, M.R., Speranza, B. and Sinigaglia, M. 2009. Microbial biofilms in the food industry: Only negative implications? In Biofilms: Formation, Development and Properties, ( W.C. Bailey, ed.) pp. 585–594, Nova Science Publishers, Hauppauge.
Google Scholar
Craveiro, S., Alves-Barroco, C., Barreto Crespo, M.T., Barreto, A.S. and Semedo-Lemsaddek, T. 2015. Aeromonas biofilm on stainless steel: Efficiency of commonly used disinfectants. Int. J. Food Sci. Technol. 50, 851–856.
10.1111/ijfs.12731
CAS Web of Science® Google Scholar
Das, J.R., Bhakoo, M., Jones, M.V. and Gilbert, P. 1998. Changes in the biocide susceptibility of Staphylococcus epidermis and Escherichia coli cells associated with rapid attachment to plastic surfaces. J. Appl. Microbiol. 84, 852–858.
10.1046/j.1365-2672.1998.00422.x
CAS PubMed Web of Science® Google Scholar
Davies, D. 2003. Understanding biofilm resistance to antibacterial agents. Nat. Rev. Drug Discov. 2, 114–122.
10.1038/nrd1008
CAS PubMed Web of Science® Google Scholar
Eswaranandam, S., Hettiarachchy, N.S. and Johnson, M.G. 2004. Antimicrobial activity of citric, lactic, malic, or tartaric acids and nisin-incorporated soy protein film against Listeria monocytogenes, Escherichia coli O157:H7, and Salmonella Gaminara. J. Food Sci. 69, 79–84.
Web of Science® Google Scholar
Frank, J.F. 2000 . Control of biofilm in the food and beverage industry. In Industrial Biofouling ( J. Walker, S. Surman and J. Jass, eds.) pp. 205–224, John Wiley & Sons Ltd. Chichester.
Google Scholar
Jay, J.M., Loessner, M.J. and Golden, D.A. 2005. Modern Food Microbiology, Springer Science and Business Media Inc., New York, NY.
Google Scholar
Joseph, B., Otta, S.K. and Karunsagar, I. 2001. Biofilm formation by Salmonella spp. on food contact surfaces and their sensitivity to sanitizers. Int. J. Food Microbiol. 64, 367–372.
10.1016/S0168-1605(00)00466-9
CAS PubMed Web of Science® Google Scholar
Leriche, V., Briandet, R. and Carpentier, B. 2003. Ecology of mixed biofilms subjected daily to a chlorinated alkaline solution: Spatial distribution of bacterial species suggests a protective effect of one species to another. Environ. Microbiol. 5, 64–71.
10.1046/j.1462-2920.2003.00394.x
CAS PubMed Web of Science® Google Scholar
Martin-Espada, M.C., Dors, A., Bartolome', M.C., Pereira, M. and Sanchez-Fortun, S. 2014. Peracetic acid disinfectant efficacy against Pseudomonas aeruginosa biofilms on polystyrene surfaces and comparison between methods to measure it. LWT - Food Sci. Technol. 56, 58–61.
Web of Science® Google Scholar
Meyer, B. 2003. Approaches to prevention, removal and killing of biofilms. Int. Biodeter. Biodegr. 5, 249–253.
Google Scholar
Moretro, T., Vestby, L., Nesse, L., Storheim, S., Kotlarz, K. and Langsrud, S. 2009. Evaluation of efficacy of disinfectants against Salmonella from the feed industry. J. Appl. Microbiol. 106, 1005–1012.
10.1111/j.1365-2672.2008.04067.x
CAS PubMed Web of Science® Google Scholar
Nguyen, H.D.N. and Yuk, H.G. 2013. Changes in resistance of Salmonella Typhimurium biofilms formed under various conditions to industrial sanitizers. Food Control 29, 236–240.
10.1016/j.foodcont.2012.06.006
CAS Web of Science® Google Scholar
Pan, Y., Breidt, F.J. and Kathariou, S. 2006. Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl. Environ. Microbiol. 72, 7711–7717.
10.1128/AEM.01065-06
CAS PubMed Web of Science® Google Scholar
Peng, J., Tsai, W. and Chou, C. 2002. Inactivation and removal of Bacillus cereus by sanitizer and detergent. Int. J. Food Microbiol. 77, 11–18.
10.1016/S0168-1605(02)00060-0
CAS PubMed Web of Science® Google Scholar
Ramesh, N., Joseph, S., Carr, L., Douglas, L. and Wheaton, F. 2002. Evaluation of chemical disinfectants for the elimination of Salmonella biofilms from poultry transport containers. Poultry Sci. 81, 904–910.
10.1093/ps/81.6.904
CAS PubMed Web of Science® Google Scholar
Scannell, A.G.M., Hill, C., Buckley, D.J. and Arendt, E.K. 1997. Determination of the influence of organic acids and nisin on shelf life and microbiological safety aspects on fresh pork sausage. J. Appl. Microbiol. 83, 407–412.
10.1046/j.1365-2672.1997.00248.x
CAS PubMed Web of Science® Google Scholar
Shi, X. and Zhu, X. 2009. Biofilm formation and food safety in food industries. Trends Food Sci. Tech. 20, 407–413.
10.1016/j.tifs.2009.01.054
CAS Web of Science® Google Scholar
Simoes, M., Simoes, L.C. and Vieira, M.J. 2010. A review of current and emergent biofilm control strategies. LWT -Food Sci. Technol. 43, 573–583.
10.1016/j.lwt.2009.12.008
CAS Web of Science® Google Scholar
Somers, E. and Wong, A. 2004. Efficacy of two cleaning and sanitizing combinations on Listeria monocytogenes biofilms formed at low temperature on a variety of materials in the presence of ready-to-eat meat residue. J. Food Protect. 67, 2218–2229.
10.4315/0362-028X-67.10.2218
PubMed Web of Science® Google Scholar
Souza, E.L., Meira, Q.G.S., Barbosa, I.M., Athayde, A.J.A.A., Conceicao, M.L. and Siquieira Junior, J.P. 2014. Biofilm formation by Staphylococcus aureus from food contact surfaces in a meat-based broth and sensitivity to sanitizers. Braz. J. Microbiol. 45, 67–75.
10.1590/S1517-83822014000100010
PubMed Web of Science® Google Scholar
Speranza, B., Corbo, M.R. and Sinigaglia, M. 2011. Effects of nutritional and environmental conditions on Salmonella sp. biofilm formation. J. Food Sci. 76, 12–16.
10.1111/j.1750-3841.2010.01936.x
CAS PubMed Web of Science® Google Scholar
Vasseur, C., Rigaud, N., Hebraud, M. and Labadie, J. 2001. Combined effect of NaCl, NaOH and biocides (monolaurin or lauric acid) on inactivation of Listeria monocytogenes and Pseudomonas spp. J. Food Protect. 64, 1442–1445.
10.4315/0362-028X-64.9.1442
CAS PubMed Web of Science® Google Scholar
Verran, J., Boyd, R.D., Hall, K. and West, R.H. 2001. Microbiological and chemical analyses of stainless steel and ceramics subjected to repeated soiling and cleaning treatments. J. Food Protect. 64, 1377–1387.
10.4315/0362-028X-64.9.1377
CAS PubMed Web of Science® Google Scholar

Citing Literature

All articles

Approaches to Removal and Killing of Salmonella Spp. Biofilms

Abstract

Practical Applications

References

Citing Literature

References

Information

About Wiley Online Library

Help & Support

Opportunities

Connect with Wiley

Approaches to Removal and Killing of Salmonella Spp. Biofilms

Abstract

Practical Applications

References

Citing Literature

References

Related

Information