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Salmonella Biofilm on Food Contact Surfaces and the Efficacy of Chemical Disinfectants: A Systematic Review

Xue Wei Tee and Noor Azira Abdul-Mutalib

Pertanika Journal of Science & Technology, Volume 31, Issue 5, August 2023

DOI: https://doi.org/10.47836/pjst.31.5.04

Keywords: Biofilm, disinfectant, efficacy, food contact surface, Salmonella

Published on: 31 July 2023

Foodborne illness has always been a major public health concern, usually caused by cross-contamination during food preparation. Salmonella is one of the most reported pathogens, which can attach to and survive on food contact surfaces by forming a biofilm. Biofilm formation enhances the persistence of food pathogens and protects them from external threats, and increases their resistance to chemical disinfectants. This systematic review aims to obtain an overview of the Salmonella biofilm formation on food contact surfaces and the efficacy of chemical disinfectants based on the latest scientific data. Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) guidelines were used to carry out the study. From the review, plastic (91%), stainless steel (64%), and sodium hypochlorite (86%) were most commonly tested. Most chemical disinfectants used in the reported studies were sodium hypochlorite (NaOCl, 100–500 mg/L), hydrogen peroxide (H2O2, 0.56%), and benzalkonium chloride (BAC, 100–400 µg/ml). The result showed that Salmonella contamination was more common on hydrophobic food contact surfaces like wood and concrete than on hydrophilic surfaces like glass. In addition, the previous studies also revealed that biofilm formation on stainless steel, plastic, and silicone rubber surfaces was not significantly different. Plus, most chemical disinfectants showed inefficacy in eliminating Salmonella biofilm at regular concentrations (<0.05%). It shows that frequent cleaning is important to avoid biofilm formation and ensure the maximum efficacy of the sanitisers.

  • Abeysundara, P. D. A., Dhowlaghar, N., Nannapaneni, R., Schilling, M. W., Mahmoud, B., Sharma, C. S., & Ma, D. P. (2018). Salmonella enterica growth and biofilm formation in flesh and peel cantaloupe extracts on four food-contact surfaces. International Journal of Food Microbiology, 280, 17-26. https://doi.org/10.1016/j.ijfoodmicro.2018.04.042

  • Akinola, A. A., Tshimpamba, M. E., Mwanza, M., & Ateba, A. N. (2020). Biofilm production potential of Salmonella serovars isolated from chickens in North West Province, South Africa. Polish Journal of Microbiology, 69(4), 427-439. https://doi.org/10.33073/pjm-2020-046

  • Anderson, M., Jaykus, L. A., Beaulieu, S., & Dennis, S. (2011). Pathogen-produce pair attribution risk ranking tool to prioritize fresh produce commodity and pathogen combinations for further evaluation (P3ARRT). Food Control, 22(12), 1865-1872. https://doi.org/10.1016/j.foodcont.2011.04.028

  • Ashrafudoulla, M., Na, K. W., Byun, K. H., Kim, D. H., Yoon, J. W., Mizan, M. F. R., Kang, I., & Ha, S. D. (2021). Isolation and characterization of Salmonella spp. from food and food contact surfaces in a chicken processing factory. Poultry Science, 100(8), Article 101234. https://doi.org/10.1016/j.psj.2021.101234

  • Bayoumi, M. A., Kamal, R. M., El Aal, S. F. A., & Awad, E. I. (2012). Assessment of a regulatory sanitization process in Egyptian dairy plants in regard to the adherence of some food-borne pathogens and their biofilms. International Journal of Food Microbiology, 158(3), 225-231. https://doi.org/10.1016/j.ijfoodmicro.2012.07.021

  • Byun, K. H., Han, S. H., Yoon, J., Park, S. H., & Ha, S. D. (2021). Efficacy of chlorine-based disinfectants (sodium hypochlorite and chlorine dioxide) on Salmonella Enteritidis planktonic cells, biofilms on food contact surfaces and chicken skin. Food Control, 123, Article 107838. https://doi.org/10.1016/j.foodcont.2020.107838

  • Cerca, N., Pier, G. B., Vilanova, M., Oliveira, R., & Azeredo, J. (2005). Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Research in Microbiology, 156(4), 506-514. https://doi.org/10.1016/j.resmic.2005.01.007

  • Chen, J., & Wang, Y. (2020). Genetic determinants of Salmonella enterica critical for attachment and biofilm formation. International Journal of Food Microbiology, 320, Article 108524. https://doi.org/10.1016/j.ijfoodmicro.2020.108524

  • Chia, G. S. Z., Green, A., Fong, Y. T., Lee, H. Y., & Ho, S. F. (2016). Rare case of type I hypersensitivity reaction to sodium hypochlorite solution in a healthcare setting. BMJ, 2016, 1-4. https://doi.org/10.1136/bcr-2016-217228

  • Chieng, B. W., Ibrahim, N. A., Daud, N. A., & Talib, Z. A. (2019). Functionalization of graphene oxide via gamma-ray irradiation for hydrophobic materials. In S. A. Rashid, R. N. I. R. Othman & M. Z. Hussein (Eds.), Synthesis, Technology and Applications of Carbon Nanomaterials (pp. 177-203). Elsevier. https://doi.org/10.1016/b978-0-12-815757-2.00008-5

  • Corcoran, M., Morris, D., de Lappe, N., O’Connor, J., Lalor, P., Dockery, P., & Cormican, M. (2013a). Commonly used disinfectants fail to eradicate Salmonella enterica biofilms from food contact surface materials. Applied and Environmental Microbiology, 80(4), 1507-1514. https://doi.org/10.1128/aem.03109-13

  • Corcoran, M., Morris, D., de Lappe, N., O’Connor, J., Lalor, P., Dockery, P., & Cormican, M. (2013b). Salmonella enterica biofilm formation and density in the centers for disease control and prevention’s biofilm reactor model is related to serovar and substratum. Journal of Food Protection, 76(4), 662-667. https://doi.org/10.4315/0362-028X.JFP-12-303

  • Dantas, S. T. A., Rossi, B. F., Bonsaglia, E. C. R., Castilho, I. G., Hernandes, R. T., Fernandes, A., & Rall, V. L. M. (2018). Cross-contamination and biofilm formation by Salmonella enterica serovar Enteritidis on various cutting boards. Foodborne Pathogens and Disease, 15(2), 81-85. https://doi.org/10.1089/fpd.2017.2341 44

  • Delaviz, Y., Santerre, J., & Cvitkovitch, D. (2015). Infection resistant biomaterials. In L. Barnes & I. R. Cooper (Eds.), Biomaterials and Medical Device - Associated Infections (pp. 223-254). Elsevier. https://doi.org/10.1533/9780857097224.2.223

  • De-la-Pinta, I., Cobos, M., Ibarretxe, J. Montoya, E., Eraso, E., Guraya, T., & Quindós, G. (2019). Effect of biomaterials hydrophobicity and roughness on biofilm development. Journal of Materials Science: Materials in Medicine, 30, Article 77. https://doi.org/10.1007/s10856-019-6281-3

  • Di Ciccio, P., Vergara, A., Festino, A., Paludi, D., Zanardi, E., Ghidini, S., & Ianieri, A. (2015). Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control, 50, 930-936. https://doi.org/10.1016/j.foodcont.2014.10.048

  • Djebbi-Simmons, D., Xu, W., Janes, M., & King, J. (2019). Survival and inactivation of Salmonella enterica serovar Typhimurium on food contact surfaces during log, stationary and long-term stationary phases. Food Microbiology, 84, Article 103272. https://doi.org/10.1016/j.fm.2019.103272

  • Fàbrega, A., & Vila, J. (2013). Salmonella enterica serovar Typhimurium skills to succeed in the host: Virulence and regulation. Clinical Microbiology Reviews, 26(2), 308-341. https://doi.org/10.1128/CMR.00066-12

  • Fraser, A. M., Anderson, J., Goncalves, J., Black, E., Starobin, A., Buckley, D., Grinstead, D., Manuel, C., & Hollingsworth, J. (2021). Sanitizers and disinfectants: A retail food and foodservice perspective. Food Protection Trends, 41(3), 358-367.

  • Giaouris, E., Chorianopoulos, N., Skandamis, P., & Nychas, G. J. (2012). Attachment and biofilm formation by Salmonella in food processing environments. In B. S. M. Mahmoud (Ed.), Salmonella - A Dangerous Foodborne Pathogen (pp. 157-180). Intech Open. https://doi.org/10.5772/1308

  • Graziani, C., Losasso, C., Luzzi, I., Ricci, A., Scavia, G., & Pasquali, P. (2017). Salmonella. In C. E. R. Dodd, T. Aldsworth, R. A. Stein, D. O. Cliver & H. P. Riemann (Eds.), Foodborne Diseases (3rd ed., pp. 133-169). Academic Press. https://doi.org/10.1016/b978-0-12-385007-2.00005-x

  • Jay, L. S., Davos, D., Frankish, E., & Lightfoot, D. (2003). Salmonella. In A. D. Hocking (Ed.), Foodborne Microorganisms of Public Health Significance (6th ed., pp. 207-266). Australian Institute of Food Science and Technology (NSW Branch), Food Microbiology Group.

  • Lee, K. H., Lee, J. Y., Roy, P. K., Mizan, M. F. R., Hossain, M. I., Park, S. H., & Ha, S. D. (2020). Viability of Salmonella Typhimurium biofilms on major food-contact surfaces and eggshell treated during 35 days with and without water storage at room temperature. Poultry Science, 99(9), 4558-4565. https://doi.org/10.1016/j.psj.2020.05.055

  • Møretrø, T., Vestby, L., Nesse, L., Storheim, S., Kotlarz, K., & Langsrud, S. (2009). Evaluation of efficacy of disinfectants against Salmonella from the feed industry. Journal of Applied Microbiology, 106(3), 1005-1012. https://doi.org/10.1111/j.1365-2672.2008.04067.x

  • Painter, J. A., Hoekstra, R. M., Ayers, T., Tauxe, R. V., Braden, C. R., Angulo, F. J., & Griffin, P. M. (2013). Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998-2008. Emerging Infectious Diseases, 19(3), 407-415. https://doi.org/10.3201/eid1903.111866

  • Rodrigues, D., Cerca, N., Teixeira, P., Oliveira, R., Ceri, H., & Azeredo, J. (2011). Listeria monocytogenes and Salmonella enterica enteritidis biofilms susceptibility to different disinfectants and stress-response and virulence gene expression of surviving cells. Microbial Drug Resistance, 17(2), 181-189. https://doi.org/10.1089/mdr.2010.0183

  • Rodríguez-Melcón, C., Riesco-Peláez, F., Carballo, J., García-Fernández, C., Capita, R., & Alonso-Calleja, C. (2018). Structure and viability of 24- and 72-h-old biofilms formed by four pathogenic bacteria on polystyrene and glass contact surfaces. Food Microbiology, 76, 513-517. https://doi.org/10.1016/j.fm.2018.06.016

  • Shao, L., Dong, Y., Chen, X., Xu, X., & Wang, H. (2020). Modeling the elimination of mature biofilms formed by Staphylococcus aureus and Salmonella spp. using combined ultrasound and disinfectants. Ultrasonics Sonochemistry, 69, Article 105269. https://doi.org/10.1016/j.ultsonch.2020.105269

  • Silva, I. D., Careli, R. T., Lima, J. C., & Andrade, N. J. (2010). Effectiveness of cleaning and sanitizing procedures in controlling the adherence of Pseudomonas fluorescens, Salmonella Enteritidis, and Staphylococcus aureus to domestic kitchen surfaces. Food Science and Technology, 30(1), 231-236. https://doi.org/10.1590/s0101-20612010005000015

  • Singla, R., Goel, H., & Ganguli, A. (2014). Novel synergistic approach to exploit the bactericidal efficacy of commercial disinfectants on the biofilms of Salmonella enterica serovar Typhimurium. Journal of Bioscience and Bioengineering, 118(1), 34-40. https://doi.org/10.1016/j.jbiosc.2013.12.025

  • WHO. (2020, April 30). Food safety. World Health Organization. https://www.who.int/news-room/fact-sheets/detail/food-safety#:%7E:text=An%20estimated%20600%20million%20%E2%80%93%20almost,healthy%20life%20years%20(DALYs).&text=Children%20under%205%20years%20of,125%20000%20deaths%20every%20year

  • Zhang, J., Wang, J., Zhao, D., & Hao, J. (2021). Efficacy of the two-step disinfection with slightly acidic electrolyzed water for reduction of Listeria monocytogenes contamination on food raw materials. LWT - Food Science and Technology, 140, Article 110699, https://doi.org/10.1016/j.lwt.2020.110699

ISSN 0128-7680

e-ISSN 2231-8526

Article ID

JST-3660-2022

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