Abstract
Biofilm formation (BF) and production in the food processing industry (FPI) is a continual threat to food safety and quality. Various bacterial pathogens possess the ability to adhere and produce biofilms on stainless steel (SS) in the FPI due to flagella, curli, pili, fimbrial adhesins, extra polymeric substances, and surface proteins. The facilitating environmental conditions (temperature, pressure, variations in climatic conditions), SS properties (surface energy, hydrophobicity, surface roughness, topography), type of raw food materials, pre-processing, and processing conditions play a significant role in the enhancement of bacterial adhesion and favorable condition for BF. Furthermore, biofilm formers can tolerate different sanitizers and cleaning agents due to the constituents, concentration, contact time, bacterial cluster distribution, and composition of bacteria within the biofilm. Also, bacterial biofilms’ ability to produce various endotoxins and exotoxins when consumed cause food infections and intoxications with serious health implications. It is thus crucial to understand BF’s repercussions and develop effective interventions against these phenomena that make persistent pathogens difficult to remove in the food processing environment.
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References
Aijuka M, Buys EM (2019) Persistence of foodborne diarrheagenic Escherichia coli in the agricultural and food production environment: implications for food safety and public health. Food Microbiol 82:363–370. https://doi.org/10.1016/j.fm.2019.03.018
Bezek K, Nipič D, Torkar K, Oder M, Dražić G, Abram A, Žibert J, Raspor P, Bohinc K (2019) Biofouling of stainless steel surfaces by four common pathogens: the effects of glucose concentration, temperature and surface roughness. Biofouling 35:273–283. https://doi.org/10.1080/08927014.2019.1575959
Armbruster CR, Parsek MR (2018) New insight into the early stages of biofilm formation. Proc Natl Acad Sci 115:4317–4319. https://doi.org/10.1073/pnas.1804084115
Aryal M, Muriana PM (2019) Efficacy of commercial sanitizers used in food processing facilities for inactivation of Listeria monocytogenes, E. coli O157: H7, and Salmonella Biofilms. Foods 8:639. https://doi.org/10.3390/foods812639
Behnke S, Parker AE, Woodall D, Camper AK (2011) Comparing the chlorine disinfection of detached biofilm clusters with those of sessile biofilms and planktonic cells in single- and dual-species cultures. Appl Environ Microbiol 77:7176–7184. https://doi.org/10.1128/AEM.05514-11
Bohinc K, Dražić G, Abram A, Jevšnik M, Jeršek B, Nipič D, Kurinčič M, Raspor P (2016) Metal surface characteristics dictate bacterial adhesion capacity. Int J Adhes Adhes 68:39–46. https://doi.org/10.1016/j.ijadhadh.2016.01.008
Boulange-Petermann L, Baroux B, Bellon-Fontaine M (1993) The influence of metallic surface wettability on bacterial adhesion. J Adhes Sci Technol 7:221–230. https://doi.org/10.1163/156856193X00673
Carballo J, Araújo A (2012) Evaluation of the efficacy of commercial sanitizers against adhered and planktonic cells of Listeria monocytogenes and Salmonella spp. Food Sci Technol 32:606–612. https://doi.org/10.1590/S0101-20612012005000084
Chmielewski R. Frank J. (2003) Biofilm formation and control in food processing facilities. Compr Rev Food Sci Food Saf 2:22–32. https://doi.org/10.1111/j.1541-4337.2003.tb00012.x
Colagiorgi A, Bruini I, Di Ciccio PA, Zanardi E, Ghidini S, Ianieri A (2017) Listeria monocytogenes biofilms in the wonderland of food industry. Pathogens 6:41. https://doi.org/10.3390/pathogens6030041
Craveiro S, Alves-Barroco C, Barreto-Crespo MT, Salvador-Barreto A, Semedo-Lemsaddek T (2015) Aeromonas biofilm on stainless steel: efficiency of commonly used disinfectants. Int J Food Sci Technol 50:851–856. https://doi.org/10.1111/ijfs.12731
Decléty P (2003) Metals used in the food industry. Ency Food Sci Nutr. pp 3869–3876
Ebrahiminezhad A, Manafi Z, Berenjian A, Kianpour S, Ghasemi Y (2017) Iron-reducing bacteria and iron nanostructures. JAMSAT 3:9–16. https://doi.org/10.18869/nrip.jamsat
Fukuzaki S, Urano H, Yamada S (2007) Effect of pH on the efficacy of sodium hypochlorite solution as cleaning and bactericidal agents. J Surf Finish Soc Japan 58:465–465. https://doi.org/10.4139/sfj.58.465
Gahan, CGM, Hill C. (2005) Gastrointestinal phase of Listeria monocytogenes infection. J Appl Microbiol 98:1345–1353. https://doi.org/10.1111/j.1365-2672.2005.02559.x
Galié S, García-Gutiérrez C, Miguélez EM, Villar CJ, Lombó F (2018) Biofilms in the food industry: health aspects and control methods. Front Microbiol 9:898–898. https://doi.org/10.3389/fmicb.2018.00898
Garrett TR, Bhakoo M, Zhang Z (2008) Bacterial adhesion and biofilms on surfaces. Prog Nat Sci 18:1049–1056. https://doi.org/10.1016/j.pnsc.2008.04.001
Goller C, Romeo T (2008) Environmental influences on biofilm development. Bact Biofilms 322:37–66. https://doi.org/10.1007/978-3-540-75418-3_3
Grigore-Gurgu L, Bucur FI, Borda D, Alexa E, Neagu C, Nicolau AI (2019) Biofilms formed by pathogens in food and food processing environments. Bact Biofilms IntechOpen. https://doi.org/10.5772/intechopen.90176
Ibars JR, Moreno DA, Ranninger C (1992) Microbial corrosion of stainless steels Microbiologia-Madrid 8:63–63
Jamal M, Ahmad W, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, Ali M, Rafiq M, Kamil MA (2018) Bacterial biofilm and associated infections. J Chinese Med Assoc 81:7–11. https://doi.org/10.1016/j.jcma.2017.07.012
Jeyachandran Y, Venkatachalam S, Karunagaran B, Narayandass SK, Mangalaraj D, Bao C, Zhang C (2007) Bacterial adhesion studies on titanium, titanium nitride and modified hydroxyapatite thin films. Mater Sci Eng, C 27:35–41. https://doi.org/10.1016/j.msec.2006.01.004
Jindal S, Anand S, Huang K, Goddard J, Metzger L, Amamcharla J (2016) Evaluation of modified stainless steel surfaces targeted to reduce biofilm formation by common milk sporeformers. J Dairy Sci 99:9502–9513. https://doi.org/10.3168/jds.2016-11395
Jones EM, Cochrane CA, Percival SL (2015) The effect of ph on the extracellular matrix and biofilms. Adv Wound Care 4:431–439. https://doi.org/10.1089/wound.2014.0538
Jubelin G, Vianney A, Beloin C, Ghigo J, Lazzaroni J, Lejeune P, Dorel C (2005) CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187:2038–2049. https://doi.org/10.1128/JB.187.6.2038-2049.2005
Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347. https://doi.org/10.1128/MMBR.00041-08
Kathiresan S, Mohan B (2017) In-vitro bacterial adhesion study on stainless steel 316L subjected to magneto rheological abrasive flow finishing. Biomed Res 28:3169–3175
Katsikogianni M, Missirlis Y (2004) Bacterial adhesion and proliferation on biomaterials. Techniques to evaluate the adhesion process. The influence of surface chemistry/topography. Euro Cells Mater 7:38
Kavamura VN, de Melo IS (2014) Effects of different osmolarities on bacterial biofilm formation. Braz J Microbiol 45:627–631
Kawakami H, Kittaka K, Sato Y, Kikuchi Y (2010) Bacterial attachment and initiation of biofilms on the surface of copper containing stainless steel. ISIJ Int 50:133–138. https://doi.org/10.2355/isijinternational.50.133
Kiani-Khouzani M, Bahrami A, Hosseini-Abari A, Khandouzi M, Taheri P (2019) Microbiologically influenced corrosion of a pipeline in a petrochemical plant. Metals 9:459. https://doi.org/10.3390/met9040459
Kielemoes J, Bultinck I, Storms H, Boon N, Verstraete W (2002) Occurrence of manganese-oxidizing microorganisms and manganese deposition during biofilm formation on stainless steel in a brackish surface water. FEMS Microbiol 39:41–55. https://doi.org/10.1111/j.1574-6941.2002.tb00905.x
Kip N, van-Veen JA, (2015) The dual role of microbes in corrosion. The ISME J 9:542–551. https://doi.org/10.1038/ismej.2014.169
Li B, Logan BE (2004) Bacterial adhesion to glass and metal-oxide surfaces. Colloids Surf, B 36:81–90. https://doi.org/10.1016/j.colsurfb.2004.05.006
Liu H, Sharma M, Wang J, Cheng Y, Liu H (2018) Microbiologically influenced corrosion of 316L stainless steel in the presence of Chlorella vulgaris. Int Biodeterior Biodegradation 129:209–216. https://doi.org/10.1016/j.ibiod.2018.03.001
Luef B, Fakra SC, Csencsits R, Wrighton KC, Williams KH, Wilkins M, Downing KH, Long P, Comolli LR, Banfield JF (2013) Iron-reducing bacteria accumulate ferric oxyhydroxide nanoparticle aggregates that may support planktonic growth. The ISME J 7:338–350. https://doi.org/10.1038/ismej.2012.103
Ma Z, Bumunang E, Stanford K, Bie X, Niu Y, McAllister T (2019) Biofilm formation by Shiga toxin-producing Escherichia coli on stainless steel coupons as affected by temperature and incubation time. Microorganisms 7:95. https://doi.org/10.3390/microorganisms7040095
Machado I, Silva LR, Giaouris ED, Melo LF, Simões M (2020) Quorum sensing in food spoilage and natural-based strategies for its inhibition. Food Res Int 127:108754. https://doi.org/10.1016/j.foodres.2019.108754
Malhotra R, Dhawan B, Garg B, Shankar V, Nag TC (2019) A comparison of bacterial adhesion and biofilm formation on commonly used orthopaedic metal implant materials: an in-vitro study. Indian J Orthop 53:148–153. https://doi.org/10.4103/ortho.IJOrtho_66_18
McClements DJ, Xiao H (2017) Is nano safe in foods? Establishing the factors impacting the gastrointestinal fate and toxicity of organic and inorganic food-grade nanoparticles. NPJ Sci Food 1:6. https://doi.org/10.1038/s41538-017-0005-1
Mediaswanti K (2016) Influence of physicochemical aspects of substratum nanosurface on bacterial attachment for bone implant applications. J Nanotechnol. https://doi.org/10.1155/2016/5026184
Meesilp N, Mesil N (2019) Effect of microbial sanitizers for reducing biofilm formation of Staphylococcus aureus and Pseudomonas aeruginosa on stainless steel by cultivation with UHT milk. Food Sci Biotechnol 28:289–296. https://doi.org/10.1007/s10068-018-0448-4
Meliani A, Bensoltane A (2015) Review of Pseudomonas attachment and biofilm formation in food industry. Poult Fish Wildl Sci 3:2–7. https://doi.org/10.4172/2375-446X.1000126
Nan L, Yang K, Ren G (2015) Anti-biofilm formation of a novel stainless steel against Staphylococcus aureus. Mater Sci Eng: C 51:356–361. https://doi.org/10.1016/j.msec.2015.03.012
Perrin C, Briandet R, Jubelin G, Lejeune P, Mandrand-Berthelot MA, Rodrigue A, Dorel C (2009) Nickel promotes biofilm formation by Escherichia coli K-12 strains that produce curli. Appl Environ Microbiol 75:1723–1733. https://doi.org/10.1128/AEM.02171-08
Persat A, Nadell CD, Kim MK, Ingremeau F, Siryaporn A, Drescher K, Wingreen NS, Bassler BL, Gitai Z, Stone HA (2015) The mechanical world of bacteria. Cell 161:988–997. https://doi.org/10.1016/j.cell.2015.05.005
Reffuveille F, Josse J, Vallé Q, Gangloff C Gangloff SC (2017) Staphylococcus aureus biofilms and their impact on the medical field. In: Enany S, Alexander LC (eds) The rise of virulence and antibiotic resistance in Staphylococcus aureus. IntechOpen, London, United Kingdom pp 187–193. https://doi.org/10.5772/66380
Renner LD, Weibel DB (2011) Physicochemical regulation of biofilm formation. MRS Bull 36:347–355. https://doi.org/10.1557/mrs.2011.65
Rhee JY, Jung DS, Peck KR (2016) Clinical and therapeutic implications of Aeromonas bacteremia: 14 Years Nation-Wide Experiences in Korea. Infect Chemother 48:274–284. https://doi.org/10.3947/ic.2016.48.4.274
Schlisselberg DB, Yaron S (2013) The effects of stainless steel finish on Salmonella typhimurium attachment, biofilm formation and sensitivity to chlorine. Food Microbiol 35:65–72. https://doi.org/10.1016/j.fm.2013.02.005
Schütz MK, Schlegel ML, Libert M, Bildstein O (2015) Impact of iron-reducing bacteria on the corrosion rate of carbon steel under simulated geological disposal conditions. Environ Sci Technol 49:7483–7490. https://doi.org/10.1021/acs.est.5b00693
Shi X, Zhu X (2009) Biofilm formation and food safety in food industries. Trends Food Sci Technol 20:407–413. https://doi.org/10.1016/j.tifs.2009.01.054
Tasneem U, Yasin N, Nisa I (2018) Biofilm producing bacteria: a serious threat to public health in developing countries. J Food Sci Nutr. 2018; 1(2):25–31. https://doi.org/10.35841/food-science
Teughels W, Van Assche N, Sliepen I, Quirynen M (2006) Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 17:68–81. https://doi.org/10.1111/j.1600-0501.2006.01353.x
Valencia-Cantero E, Peña-Cabriales JJ (2014) Effects of iron-reducing bacteria on carbon steel corrosion induced by thermophilic sulfate-reducing consortia. J Microbiol Biotechnol 24:280–286. https://doi.org/10.4014/jmb.1310.10002
Wang R, Schmidt JW, Harhay DM, Bosilevac JM, King DA, Arthur TM (2017) Biofilm formation, antimicrobial resistance, and sanitizer tolerance of Salmonella enterica strains isolated from beef trim. Foodborne Pathog Dis 14:687–695. https://doi.org/10.1089/fpd.2017.2319
Xu C, Zhang Y, Cheng G, Zhu W (2006) Corrosion and electrochemical behavior of 316L stainless steel in sulfate-reducing and iron-oxidizing bacteria solutions1 1supported by the National Natural Science Foundation of China (No.20576108). Chin J Chem Eng 14:829–834. https://doi.org/10.1016/S1004-9541(07)60021-4
Zhang YH, Xu CM, Cheng GX, Zhu WS (2007) Pitting initiation of 316L stainless steel in the media of sulfate-reducing and iron-oxidizing bacteria. Inorg Mater 43:614–621. https://doi.org/10.1134/S0020168507060118
Zameer F, Rukmangada M, Chauhan JB, Khanum SA, Kumar P, Devi AT, Nagendra PM, Dhananjaya B (2016) Evaluation of adhesive and anti-adhesive properties of Pseudomonas aeruginosa biofilms and their inhibition by herbal plants. Iran J Microbiol 8:108. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4906717/
Acknowledgements
The authors are grateful to students and staff in the Food and Enzyme Laboratories, Department of Biotechnology and Food Technology, Durban University of Technology for their support.
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This work is based on the research supported in part by the National Research Foundation, South Africa, for the grant, Unique Grant no. 118910.
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SD, TAA, and OAI made significant contributions to the idea of this review and wrote the manuscript. All authors read and approved the final manuscript to ensure accuracy and proper report of the work.
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Dula, S., Ajayeoba, T.A. & Ijabadeniyi, O.A. Bacterial biofilm formation on stainless steel in the food processing environment and its health implications. Folia Microbiol 66, 293–302 (2021). https://doi.org/10.1007/s12223-021-00864-2
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DOI: https://doi.org/10.1007/s12223-021-00864-2