Skip to main content

Advertisement

SpringerLink
Log in

Biofilm formation by Listeria monocytogenes from the meat processing industry environment and the use of different combinations of detergents, sanitizers, and UV-A radiation to control this microorganism in planktonic and sessile forms

  • Food Microbiology - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

This study aimed to evaluate the ability of biofilm formation by L. monocytogenes from the meat processing industry environment, as well as the use of different combinations of detergents, sanitizers, and UV-A radiation in the control of this microorganism in the planktonic and sessile forms. Four L. monocytogenes isolates were evaluated and showed moderate ability to form biofilm, as well as carried genes related to biofilm production (agrB, agrD, prfA, actA, cheA, cheY, flaA, sigB), and genes related to tolerance to sanitizers (lde and qacH). The biofilm-forming isolates of L. monocytogenes were susceptible to quaternary ammonium compound (QAC) and peracetic acid (PA) in planktonic form, with minimum inhibitory concentrations of 125 and 75 ppm, respectively, for contact times of 10 and 5 min. These concentrations are lower than those recommended by the manufacturers, which are at least 200 and 300 ppm for QAC and PA, respectively. Biofilms of L. monocytogenes formed from a pool of isolates on stainless steel and polyurethane coupons were subjected to 14 treatments involving acid and enzymatic detergents, QAC and PA sanitizers, and UV-A radiation at varying concentrations and contact times. All treatments reduced L. monocytogenes counts in the biofilm, indicating that the tested detergents, sanitizers, and UV-A radiation exhibited antimicrobial activity against biofilms on both surface types. Notably, the biofilm formed on polyurethane showed greater tolerance to the evaluated compounds than the biofilm on stainless steel, likely due to the material’s surface facilitating faster microbial colonization and the development of a more complex structure, as observed by scanning electron microscopy. Listeria monocytogenes isolates from the meat processing industry carry genes associated with biofilm production and can form biofilms on both stainless steel and polyurethane surfaces, which may contribute to their persistence within meat processing lines. Despite carrying sanitizer tolerance genes, QAC and PA effectively controlled these microorganisms in their planktonic form. However, combinations of detergent (AC and ENZ) with sanitizers (QAC and PA) at minimum concentrations of 125 ppm and 300 ppm, respectively, were the most effective.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

All data generated or analyzed during this study are included in this article.

Code availability

Not applicable.

References

  1. EFSA ECDC (2019) The European Union One Health 2018 Zoonoses Report. EFSA J 276

  2. Zhang X, Wang S, Chen X, Qu C (2021) Review controlling Listeria monocytogenes in ready-to-eat meat and poultry products: an overview of outbreaks, current legislations, challenges, and future prospects. Trends Food Sci Technol 116:24–35

    Article  CAS  Google Scholar 

  3. Bergis H, Bonanno L, Asséré A (2018) EURL Lm Guidance Document to evaluate the competence of laboratories implementing challenge tests and durability studies related to Listeria monocytogenes in ready-to-eat foods Version 2. EURL Lm-ANSES 94701

  4. Britton BC, Cook KT, Wu ST, Burnett J, Wallar RC, den Bakker HC, Oliver HF (2022) Sanitation and customer service strategies implemented during COVID-19 correlated with lower Listeria monocytogenes prevalence in retail delicatessens. Food Control 134:108701

    Article  CAS  Google Scholar 

  5. Cavalcanti AAC, Limeira CH, de Siqueira IN, de Lima AC, de Medeiros FJP, de Souza JG, Medeiros NG, de Oliveira Filho A, de Melo AA (2022) The prevalence of Listeria monocytogenes in meat products in Brazil: a systematic literature review and meta-analysis. Res Vet Sci 145:169–176

    Article  CAS  PubMed  Google Scholar 

  6. Bolocan AS, Nicolau AI, Alvarez-Ordóñez A, Borda D, Oniciuc EA, Stessl B, Gurgu L, Wagner M, Jordan K (2016) Dynamics of Listeria monocytogenes colonisation in a newly-opened meat processing facility. Meat Sci 113:26–34

    Article  PubMed  Google Scholar 

  7. Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard JC, Naïtali M, Briandet R (2015) Biofilm-associated persistence of food-borne pathogens. Food Microbiol 45:167–178

    Article  CAS  PubMed  Google Scholar 

  8. Kilic T, Bali EB (2023) Biofilm control strategies in the light of biofilm-forming microorganisms. World J Microbiol Biotechnol 39:131

    Article  CAS  PubMed  Google Scholar 

  9. Wang Y, Sun L, Hu L, Wang Z, Wang X, Dong Q (2022) Adhesion and kinetics of biofilm formation and related gene expression of Listeria monocytogenes in response to nutritional stress. Food Res Int 156:111143

    Article  CAS  PubMed  Google Scholar 

  10. Fagerlund A, Heir E, Møretrø T, Langsrud S (2020) Listeria monocytogenes biofilm removal using different commercial cleaning agents. Molecules 25:792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Somrani M, Debbabi H, Palop A (2022) Antibacterial and antibiofilm activity of essential oil of clove against Listeria monocytogenes and Salmonella Enteritidis. Food Sci Technol Int 28:331–339

    Article  CAS  PubMed  Google Scholar 

  12. Cherifi T, Jacques M, Quessy S, Fravalo P (2017) Impact of nutrient restriction on the structure of Listeria monocytogenes Biofilm grown in a Microfluidic System. Front Microbiol 8:1–13

    Article  Google Scholar 

  13. Crivello G, Fracchia L, Ciardelli G, Boffito M, Mattu C (2023) In Vitro models of bacterial biofilms: innovative tools to improve understanding and treatment of infections. Nanomaterials 13:904

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Koreňová J, Oravcová K, Véghová A, Karpíšková R, Kuchta T (2016) Biofilm formation in various conditions is not a key factor of persistence potential of Listeria monocytogenes in food-processing environment. J Food Nutr Res 55:189–193

    Google Scholar 

  15. Wang G, Qian W, Zhang X, Wang H, Ye K, Bai Y, Zhou G (2015) Prevalence, genetic diversity and antimicrobial resistance of Listeria monocytogenes isolated from ready-to-eat meat products in Nanjing, China. Food Control 50:202–208

    Article  CAS  Google Scholar 

  16. Ramires T, Kleinubing NR, Iglesias MA, Vitola HRS, Núncio ASP, Kroning IS, Moreira GMSG, Fiorentini ÂM, da Silva WP (2021) Genetic diversity, biofilm and virulence characteristics of Listeria monocytogenes in salmon sushi. Food Res Int 140:109871

    Article  CAS  PubMed  Google Scholar 

  17. Zetzmann M, Bucur FI, Crauwels P, Borda D, Nicolau AI, Grigore-Gurgu L, Seibold GM, Riedel CU (2019) Characterization of the biofilm phenotype of a Listeria monocytogenes mutant deficient in agr peptide sensing. Microbiologyopen 8:1–9

    Article  Google Scholar 

  18. Huang Y, Morvay AA, Shi X, Suo Y, Shi C, Knøchel S (2018) Comparison of oxidative stress response and biofilm formation of Listeria monocytogenes serotypes 4b and 1/2a. Food Control 85:416–422

    Article  CAS  Google Scholar 

  19. Zhang R, Wang Z, Tian Y, Yin Q, Cheng X, Lian M, Zhou B, Zhang X, Yang L (2019) Efficacy of antimicrobial peptide DP7, designed by machine-learning method, against methicillin-resistant staphylococcus aureus. Front Microbiol 10:1–13

    Google Scholar 

  20. Akrami-Mohajeri F, Derakhshan Z, Ferrante M, Hamidiyan N, Soleymani M, Conti GO, Tafti RD (2018) The prevalence and antimicrobial resistance of Listeria spp in raw milk and traditional dairy products delivered in Yazd, central Iran (2016). Food Chem Toxicol 114:141–144

  21. Rieu A, Weidmann S, Garmyn D, Piveteau P, Guzzo J (2007) Agr system of Listeria monocytogenes EGD-e: role in adherence and differential expression pattern. Appl Environ Microbiol 73:6125–6133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Guo W, Shan K, Xu B, Li J (2015) Determining the resistance of carbapenemresistant Klebsiella pneumoniae to common disinfectants and elucidating the underlying resistance mechanisms. Pathog Glob Health 109:184–192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Meier AB, Guldimann C, Markkula A, Pöntinen A, Korkeala H, Tasara T (2017) Comparative phenotypic and genotypic analysis of Swiss and Finnish Listeria monocytogenes isolates with respect to benzalkonium chloride resistance. Front Microbiol 8:1–9

    Article  Google Scholar 

  24. Minarovičová J, Véghová A, Mikulášová M, Chovanová R, Šoltýs K, Drahovská H, Kaclíková E (2018) Benzalkonium chloride tolerance of Listeria monocytogenes strains isolated from a meat processing facility is related to presence of plasmid-borne bcrABC cassette. Antonie Van Leeuwenhoek Int J Gen Mol Microbiol 111:1913–1923

    Article  Google Scholar 

  25. Mullapudi S, Siletzky RM, Kathariou S (2008) Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of Turkey-processing plants. Appl Environ Microbiol 74:1464–1468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Müller A, Rychli K, Muhterem-Uyar M, Zaiser A, Stessl B, Guinane CM, Cotter PD, Wagner M, Schmitz-Esser S (2013) Tn6188 - A Novel Transposon in Listeria monocytogenes responsible for tolerance to Benzalkonium Chloride. PLoS ONE 8:1–11

    Article  Google Scholar 

  27. Noguchi N, Nakaminami H, Nishijima S, Kurokawa I, So H, Sasatsu M (2006) Antimicrobial agent of susceptibilities and antiseptic resistance gene distribution among methicillin-resistant Staphylococcus aureus isolates from patients with impetigo and staphylococcal scalded skin syndrome. J Clin Microbiol 44:2119–2125

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Boucher C, Waite-Cusic J, Stone D, Kovacevic J (2021) Relative performance of commercial citric acid and quaternary ammonium sanitizers against Listeria monocytogenes under conditions relevant to food industry. Food Microbiol 97:103752

    Article  CAS  PubMed  Google Scholar 

  29. Klopper KB, Bester E, Wolfaardt GM (2023) Listeria monocytogenes Biofilms are planktonic cell factories despite Peracetic Acid exposure under continuous Flow conditions. Antibiotics 12:209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Stoller A, Stevens MJA, Stephan R, Guldimann C (2019) Characteristics of listeria monocytogenes strains persisting in a meat processing facility over a 4-year period. Pathogens 8:32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Moreno-Andrés J, Tierno-Galán M, Romero-Martínez L, Acevedo-Merino A, Nebot E (2023) Inactivation of the waterborne marine pathogen Vibrio alginolyticus by photo-chemical processes driven by UV-A, UV-B, or UV-C LED combined with H2O2 or HSO5–. Water Res 232:119686

    Article  PubMed  Google Scholar 

  32. Liu D, Lawrence ML, Austin FW, Ainsworth AJ (2007) A multiplex PCR for species- and virulence-specific determination of Listeria monocytogenes. J Microbiol Methods 71:133–140

    Article  CAS  PubMed  Google Scholar 

  33. Millezi FM, Pereira MO, Batista NN, Camargos N, Auad I, Cardoso MDG, Piccoli RH (2012) Susceptibility of monospecies and dual-species biofilms of staphylococcus aureus and escherichia coli to essential oils. J Food Saf 32:351–359

    Article  CAS  Google Scholar 

  34. Divyashree S, Anjali PG, Somashekaraiah R, Sreenivasa MY (2021) Probiotic properties of Lactobacillus casei– MYSRD 108 and Lactobacillus plantarum-MYSRD 71 with potential antimicrobial activity against Salmonella paratyphi. Biotechnol Rep 32:e00672

    Article  CAS  Google Scholar 

  35. Beltrame CA, Kubiak GB, Lerin LA, Rottava I, Mossi AJ, de Oliveira D, Cansian RL, Treichel H, Toniazzo G (2012) Influence of different sanitizers on food contaminant bacteria: effect of exposure temperature, contact time, and product concentration. Food Sci Technol 32:228–232

    Article  Google Scholar 

  36. Kusumaningrum H, Riboldi G, Hazeleger W, Beumer R (2003) Survival of foodborne pathogens on stainless steel surfaces and cross-contamination to foods. Int J Food Microbiol 85:227–236

    Article  CAS  PubMed  Google Scholar 

  37. Rossoni EM, Gaylarde C (2000) Comparison of sodium hypochlorite and peracetic acid as sanitising agents for stainless steel food processing surfaces using epifluorescence microscopy. Int J Food Microbiol 61:81–85

    Article  CAS  PubMed  Google Scholar 

  38. Scherba G, Weigel RM, O’Brien WD (1991) Quantitative assessment of the germicidal efficacy of ultrasonic energy. Appl Environ Microbiol 57:2079–2084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Webber B, Canova R, Esper LM, Perdoncini G, Pinheiro Do Nascimento V, Pilotto F, Ruschel L, Santos D, Rodrigues LB (2015) The Use of Vortex and Ultrasound techniques for the in vitro removal of Salmonella spp. Biofilms Acta Sci Vet 43:1332

    Google Scholar 

  40. Ning Y, Yan A, Yang K, Wang Z, Li X, Jia Y (2017) Antibacterial activity of phenyllactic acid against Listeria monocytogenes and Escherichia coli by dual mechanisms. Food Chem 228:533–540

    Article  CAS  PubMed  Google Scholar 

  41. Stepanović S, Vuković D, Hola V, Di Bonaventura G, Djukić S, Ćirković I, Ruzicka F (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Apmis 115:891–899

    Article  PubMed  Google Scholar 

  42. Duze ST, Marimani M, Patel M (2021) Tolerance of Listeria monocytogenes to biocides used in food processing environments. Food Microbiol 97:103758

    Article  CAS  PubMed  Google Scholar 

  43. Ricci A, Allende A, Bolton D et al (2018) Listeria monocytogenes contamination of ready-to-eat foods and the risk for human health in the EU. EFSA J 16:5134

    Google Scholar 

  44. D’Arrigo M, Mateo-Vivaracho L, Guillamón E, Fernández-León MF, Bravo D, Peirotén Á, Medina M, García-Lafuente A (2020) Characterization of persistent Listeria monocytogenes strains from ten dry-cured ham processing facilities. Food Microbiol 92:103581 Contents

  45. Mpundu P, Muma JB, Mukumbuta N, Mukubesa AN, Muleya W, Kapila P, Hang’ombe BM, Munyeme M (2022) Isolation, discrimination, and molecular detection of Listeria species from slaughtered cattle in Namwala District, Zambia. BMC Microbiol 22:1–12

    Article  Google Scholar 

  46. Ferreira V, Wiedmann M, Teixeira P, Stasiewicz MJ (2014) Listeria monocytogenes persistence in food-associated environments: Epidemiology, strain characteristics, and implications for public health. J Food Prot 77:150–170

    Article  CAS  PubMed  Google Scholar 

  47. Figueroa-López AM, Maldonado-Mendoza IE, López-Cervantes J, Verdugo-Fuentes AA, Ruiz-Vega DA, Cantú-Soto EU (2019) Prevalence and characterization of Listeria monocytogenes isolated from pork meat and on inert surfaces. Brazilian J Microbiol 50:817–824

    Article  Google Scholar 

  48. Chasseignaux E, Toquin MT, Ragimbeau C, Salvat G, Colin P, Ermel G (2001) Molecular epidemiology of Listeria monocytogenes isolates collected from the environment, raw meat and raw products in two poultry- and pork-processing plants. J Appl Microbiol 91:888–899

    Article  CAS  PubMed  Google Scholar 

  49. Thévenot D, Delignette-Muller ML, Christieans S, Vernozy-Rozand C (2005) Prevalence of Listeria monocytogenes in 13 dried sausage processing plants and their products. Int J Food Microbiol 102:85–94

    Article  PubMed  Google Scholar 

  50. Mazaheri T, Ripolles-Avila C, Hascoët AS, Rodríguez-Jerez JJ (2020) Effect of an enzymatic treatment on the removal of mature Listeria monocytogenes biofilms: a quantitative and qualitative study. Food Control 114:107266

    Article  CAS  Google Scholar 

  51. Lianou A, Nychas GJE, Koutsoumanis KP (2020) Strain variability in biofilm formation: a food safety and quality perspective. Food Res Int 137:109424

    Article  CAS  PubMed  Google Scholar 

  52. Banerji R, Karkee A, Kanojiya P, Patil A, Saroj SD (2022) Bacterial communication in the regulation of stress response in Listeria monocytogenes. Lwt 154:112703

    Article  CAS  Google Scholar 

  53. Lee YJ, Wang C (2020) Links between S-adenosylmethionine and agr-based quorum sensing for biofilm development in Listeria monocytogenes EGD-e. Microbiologyopen 9:1–12

    Article  Google Scholar 

  54. Pinheiro J, Lisboa J, Pombinho R et al (2018) MouR controls the expression of the Listeria monocytogenes agr system and mediates virulence. Nucleic Acids Res 46:9338–9352

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Gandra TKV, Volcan D, Kroning IS, Marini N, de Oliveira AC, Bastos CP, da Silva WP (2019) Expression levels of the agr locus and prfA gene during biofilm formation by Listeria monocytogenes on stainless steel and polystyrene during 8 to 48 h of incubation 10 to 37°C. Int J Food Microbiol 300:1–7

    Article  CAS  PubMed  Google Scholar 

  56. Xayarath B, Alonzo F, Freitag NE (2015) Identification of a peptide-pheromone that enhances Listeria monocytogenes escape from Host Cell Vacuoles. PLoS Pathog 11:1–35

    Article  Google Scholar 

  57. Reniere ML, Whiteley AT, Hamilton KL, John SM, Lauer P, Brennan RG, Portnoy DA (2015) Glutathione activates virulence gene expression of an intracellular pathogen. Nature 517:170–173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Scortti M, Monzó HJ, Lacharme-Lora L, Lewis DA, Vázquez-Boland JA (2007) The PrfA virulence regulon. Microbes Infect 9:1196–1207

    Article  CAS  PubMed  Google Scholar 

  59. Matereke LT, Okoh AI (2020) Listeria monocytogenes virulence, antimicrobial resistance and environmental persistence: a review. Pathogens 9:1–12

    Article  Google Scholar 

  60. Travier L, Lecuit M (2014) Listeria monocytogenes ActA: a new function for a classic virulence factor. Curr Opin Microbiol 17:53–60

    Article  CAS  PubMed  Google Scholar 

  61. Sibanda T, Buys EM (2022) Listeria monocytogenes Pathogenesis: the role of stress adaptation. Microorganisms 10:1522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Van Der Veen S, Abee T (2010) Importance of SigB for listeria monocytogenes static and continuous-flow biofilm formation and disinfectant resistance. Appl Environ Microbiol 76:7854–7860

    Article  PubMed  PubMed Central  Google Scholar 

  63. Todhanakasem T, Young GM (2008) Loss of flagellum-based motility by Listeria monocytogenes results in formation of hyperbiofilms. J Bacteriol 190:6030–6034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Williams T, Joseph B, Beier D, Goebel W, Kuhn M (2005) Response regulator DegU of Listeria monocytogenes regulates the expression of flagella-specific genes. FEMS Microbiol Lett 252:287–298

    Article  CAS  PubMed  Google Scholar 

  65. Colin R, Ni B, Laganenka L, Sourjik V (2021) Multiple functions of flagellar motility and chemotaxis in bacterial physiology. FEMS Microbiol Rev 45:1–19

    Article  Google Scholar 

  66. Lemon KP, Higgins DE, Kolter R (2007) Flagellar motility is critical for Listeria monocytogenes biofilm formation. J Bacteriol 189:4418–4424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Zhang H, Hu Y, Zhou C et al (2018) Stress resistance, motility and biofilm formation mediated by a 25 kb plasmid pLMSZ08 in Listeria monocytogenes. Food Control 94:345–352

    Article  CAS  Google Scholar 

  68. Choi NY, Kim BR, Bae YM, Lee SY (2013) Biofilm formation, attachment, and cell hydrophobicity of foodborne pathogens under varied environmental conditions. J Korean Soc Appl Biol Chem 56:207–220

    Article  CAS  Google Scholar 

  69. Fan Y, Qiao J, Lu Z, Fen Z, Tao Y, Lv F, Zhao H, Zhang C, Bie X (2020) Influence of different factors on biofilm formation of Listeria monocytogenes and the regulation of cheY gene. Food Res Int 137:109405

    Article  CAS  PubMed  Google Scholar 

  70. Bonneville L, Maia V, Barroso I, Martínez-Suárez JV, Brito L (2021) Lactobacillus plantarum in dual-species Biofilms with Listeria monocytogenes enhanced the Anti-listeria activity of a commercial disinfectant based on Hydrogen Peroxide and Peracetic Acid. Front Microbiol 12:1–11

    Article  Google Scholar 

  71. Guérin A, Bridier A, Le Grandois P et al (2021) Exposure to quaternary ammonium compounds selects resistance to ciprofloxacin in listeria monocytogenes. Pathogens 10:1–11

    Article  Google Scholar 

  72. Gerba CP (2015) Quaternary ammonium biocides: efficacy in application. Appl Environ Microbiol 81:464–469

    Article  PubMed  PubMed Central  Google Scholar 

  73. Bolten S, Harrand AS, Skeens J, Wiedmann M (2022) Nonsynonymous mutations in fepR are Associated with Adaptation of Listeria monocytogenes and other Listeria spp. to low concentrations of Benzalkonium Chloride but do not increase survival of L. monocytogenes and other Listeria spp. after exposure to Benz. Appl Environ Microbiol. https://doi.org/10.1128/aem.00486-22

    Article  PubMed  PubMed Central  Google Scholar 

  74. Belessi CEA, Gounadaki AS, Psomas AN, Skandamis PN (2011) Efficiency of different sanitation methods on Listeria monocytogenes biofilms formed under various environmental conditions. Int J Food Microbiol 145:S46–S52

    Article  PubMed  Google Scholar 

  75. Rokhina EV, Makarova K, Golovina EA, Van As H, Virkutyte J (2010) Free radical reaction pathway, thermochemistry of peracetic acid homolysis, and its application for phenol degradation: spectroscopic study and quantum chemistry calculations. Environ Sci Technol 44:6815–6821

    Article  CAS  PubMed  Google Scholar 

  76. Skowron K, Hulisz K, Gryń G, Olszewska H, Wiktorczyk N, Paluszak Z (2018) Comparison of selected disinfectants efficiency against Listeria monocytogenes biofilm formed on various surfaces. Int Microbiol 21:23–33

    Article  CAS  PubMed  Google Scholar 

  77. Gombas D, Luo Y, Brennan J et al (2017) Guidelines to validate control of cross-contamination during washing of fresh-cut leafy vegetables. J Food Prot 80:312–330

    Article  CAS  PubMed  Google Scholar 

  78. Barroso I, Maia V, Cabrita P, Martínez-Suárez JV, Brito L (2019) The benzalkonium chloride resistant or sensitive phenotype of Listeria monocytogenes planktonic cells did not dictate the susceptibility of its biofilm counterparts. Food Res Int 123:373–382

    Article  CAS  PubMed  Google Scholar 

  79. Noll M, Trunzer K, Vondran A, Vincze S, Dieckmann R, Al Dahouk S, Gold C (2020) Benzalkonium chloride induces a VBNC state in Listeria monocytogenes. Microorganisms 8:4–6

    Article  Google Scholar 

  80. Haubert L, Zehetmeyr, Maiara Lindemann Silva WP (2019) da Resistance to benzalkonium chloride and cadmium chloride in Listeria monocytogenes isolates from food and food-processing environments in southern Brazil. Can. J. Microbiol. 65

  81. Martínez-Suárez JV, Ortiz S, López-Alonso V (2016) Potential impact of the resistance to quaternary ammonium disinfectants on the persistence of Listeria monocytogenes in food processing environments. Front Microbiol 7:638

    Article  PubMed  PubMed Central  Google Scholar 

  82. Bland R, Brown SRB, Waite-Cusic J, Kovacevic J (2022) Probing antimicrobial resistance and sanitizer tolerance themes and their implications for the food industry through the Listeria monocytogenes lens. Compr Rev Food Sci Food Saf 21:1777–1802

    Article  PubMed  Google Scholar 

  83. Chen G, Lin M, Chen Y, Xu W, Zhang H (2021) Induction of a viable but nonculturable state, thermal and sanitizer tolerance, and gene expression correlation with desiccation-adapted biofilm and planktonic salmonella in powdered infant formula. J Food Prot 84:1194–1201

    Article  CAS  PubMed  Google Scholar 

  84. Midelet G, Carpentier B (2002) Transfer of microorganisms, including Listeria monocytogenes, from various materials to beef. Appl Environ Microbiol 68:4015–4024

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Heydorn A, Nielsen AT, Hentzer M, Sternberg C, Givskov M, Ersboll BK, Molin S (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146:2395–2407

    Article  CAS  PubMed  Google Scholar 

  86. Carrascosa C, Raheem D, Ramos F, Saraiva A, Raposo A (2021) Microbial biofilms in the food industry—a comprehensive review. Int J Environ Res Public Health 18:1–31

    Article  Google Scholar 

  87. Xavier JB, Picioreanu C, Abdul Rani S, van Loosdrecht MCM, Stewart PS (2005) Biofilm-control strategies based on enzymic disruption of the extracellular polymeric substance matrix - A modelling study. Microbiology 151:3817–3832

    Article  CAS  PubMed  Google Scholar 

  88. Ibusquiza PS, Herrera JJR, Cabo ML (2011) Resistance to benzalkonium chloride, peracetic acid and nisin during formation of mature biofilms by Listeria monocytogenes. Food Microbiol 28:418–425

    Article  CAS  Google Scholar 

  89. Van Acker H, Van Dijck P, Coenye T (2014) Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol 22:326–333

    Article  PubMed  Google Scholar 

  90. Paspaliari DK, Mollerup MS, Kallipolitis BH, Ingmer H, Larsen MH (2014) Chitinase expression in Listeria monocytogenes is positively regulated by the agr system. PLoS ONE 9:1–8

    Article  Google Scholar 

  91. Møretrø T, Schirmer BCT, Heir E, Fagerlund A, Hjemli P, Langsrud S (2017) Tolerance to quaternary ammonium compound disinfectants may enhance growth of Listeria monocytogenes in the food industry. Int J Food Microbiol 241:215–224

    Article  PubMed  Google Scholar 

  92. Ortiz S, López V, Martínez-Suárez JV (2014) The influence of subminimal inhibitory concentrations of benzalkonium chloride on biofilm formation by listeria monocytogenes. Int J Food Microbiol 189:106–112

    Article  CAS  PubMed  Google Scholar 

  93. Rossi F, Rizzotti L, Felis GE, Torriani S (2014) Horizontal gene transfer among microorganisms in food: current knowledge and future perspectives. Food Microbiol 42:232–243

    Article  CAS  PubMed  Google Scholar 

  94. Jakubovics NS, Shields RC, Rajarajan N, Burgess JG (2013) Life after death: the critical role of extracellular DNA in microbial biofilms. Lett Appl Microbiol 57:467–475

    Article  CAS  PubMed  Google Scholar 

  95. Bintsis T, Litopoulou-Tzanetaki E, Robinson RK (2000) Existing and potential applications of ultraviolet light in the food industry - A critical review. J Sci Food Agric 80:637–645

    Article  CAS  PubMed  Google Scholar 

  96. Harada AMM, Nascimento MS (2021) Efficacy of dry sanitizing methods on Listeria monocytogenes biofilms. Food Control 124:107897

    Article  CAS  Google Scholar 

  97. Kim Dkyun, Kang DH (2020) Effect of surface characteristics on the bactericidal efficacy of UVC LEDs. Food Control 108:106869

    Article  CAS  Google Scholar 

  98. Montgomery NL, Banerjee P (2015) Inactivation of Escherichia coli O157:H7 and Listeria monocytogenes in biofilms by pulsed ultraviolet light. BMC Res Notes 8:1–12

    Article  CAS  Google Scholar 

  99. Rutala WA, Gergen MF, Weber DJ (2008) Impact of an oil-based lubricant on the effectiveness of the sterilization processes. Infect Control Hosp Epidemiol 29:69–72

    Article  PubMed  Google Scholar 

  100. Pilchová T, Hernould M, Prévost H, Demnerová K, Pazlarová J, Tresse O (2014) Influence of food processing environments on structure initiation of static biofilm of listeria monocytogenes. Food Control 35:366–372

    Article  Google Scholar 

  101. Adetunji VO, Kehinde AO, Bolatito OK, Chen J (2014) Biofilm formation by Mycobacterium bovis: influence of surface kind and temperatures of sanitizer treatments on biofilm control. Biomed Res Int 2014:7

    Article  Google Scholar 

  102. Bonsaglia ECR, Silva NCC, Fernades Júnior A, Araújo Júnior JP, Tsunemi MH, Rall VLM (2014) Production of biofilm by Listeria monocytogenes in different materials and temperatures. Food Control 35:386–391

    Article  CAS  Google Scholar 

  103. Bos R, Van Der Mei HC, Gold J, Busscher HJ (2000) Retention of bacteria on a substratum surface with micro-patterned hydrophobicity. FEMS Microbiol Lett 189:311–315

    Article  CAS  PubMed  Google Scholar 

  104. Smoot LM, Pierson MD (1998) Influence of environmental stress on the kinetics and strength of attachment of Listeria monocytogenes Scott A to Buna-N rubber and stainless steel. J Food Prot 61:1286–1292

    Article  CAS  PubMed  Google Scholar 

  105. Hua Z, Korany AM, El-Shinawy SH, Zhu MJ (2019) Comparative evaluation of different sanitizers against Listeria monocytogenes Biofilms on Major Food-Contact surfaces. Front Microbiol 10:1–8

    Article  Google Scholar 

  106. Chakraborty T, Leimeister-Wachter M, Domann E, Hartl M, Goebel W, Nichterlein T, Notermans S (1992) Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174:568–574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Lomonaco S, Patti R, Knabel SJ, Civera T (2012) Detection of virulence-associated genes and epidemic clone markers in Listeria monocytogenes isolates from PDO Gorgonzola cheese. Int J Food Microbiol 160:76–79

    Article  CAS  PubMed  Google Scholar 

  108. Elhanafi D, Utta V, Kathariou S (2010) Genetic characterization of plasmid-associated benzalkonium chloride resistance determinants in a listeria monocytogenes train from the 1998–1999 outbreak. Appl Environ Microbiol 76:8231–8238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors are thankful for the Multi-User Facility infrastructure of Santa Catarina State University’s Technological Sciences Center.

Funding

This study was supported by the Fundação de Amparo a Pesquisa e Inovação do Estado de Santa Catarina (FAPESC, Brazil − 2023TR564). Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq – process 312715/2023-4) and Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul (FAPERGS – grant 21/2551-0002247-7).

Author information

Authors and Affiliations

  1. Departamento de Engenharia de Alimentos e Engenharia Química, Universidade do Estado de Santa Catarina, Pinhalzinho, SC, 89870-000, Brazil

    Larissa Siqueira Lima, Taís Nunzio Müller, Rafaela Ansiliero, Marcia Bär Schuster & Liziane Schittler Moroni

  2. Centro Multiusuário, Centro de Ciências Tecnológicas, Universidade do Estado de Santa Catarina, Joinville, SC, 89219-710, Brazil

    Bruna Louise Silva

  3. Departamento de Ciência e Tecnologia Agroindustrial, Faculdade de Agronomia, Universidade Federal de Pelotas, Capão do Leão, RS, 96001-970, Brazil

    Itiane Barcellos Jaskulski & Wladimir Padilha da Silva

  4. Centro de Desenvolvimento Tecnológico, Departamento de Biotecnologia, Universidade Federal de Pelotas, Pelotas, RS, 960110-610, Brazil

    Itiane Barcellos Jaskulski & Wladimir Padilha da Silva

Authors
  1. Larissa Siqueira Lima
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Taís Nunzio Müller
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rafaela Ansiliero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Marcia Bär Schuster
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bruna Louise Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Itiane Barcellos Jaskulski
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Wladimir Padilha da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Liziane Schittler Moroni
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to the conception and design of the study. LSM, TNM, IBJ and RA performed the experiments and statistical analysis of the data; MBS and BLS contributed to the development of microscopic analyzes and interpretation of results; LSM and WPS guidance and study planning, manuscript writing. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Liziane Schittler Moroni.

Ethics declarations

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declared no competing interests.

Additional information

Editorial Responsibility: Beatriz Ernestina Cabilio Guth.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lima, L.S., Müller, T.N., Ansiliero, R. et al. Biofilm formation by Listeria monocytogenes from the meat processing industry environment and the use of different combinations of detergents, sanitizers, and UV-A radiation to control this microorganism in planktonic and sessile forms. Braz J Microbiol (2024). https://doi.org/10.1007/s42770-024-01361-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s42770-024-01361-7

Keywords

Search

Navigation