Cleaning and disinfection of biofilms composed of Listeria monocytogenes and background microbiota from meat processing surfaces

Applied and Environmental Microbiology

Volumn 83, Issue 17, 2017, Pages

  Fagerlund, Annette ^a   Møretrø, Trond ^a   Heir, Even ^a   Briandet, Romain ^b   Langsruda, Solveig ^a  

^a NOFIMA   (Norway)

^b UNIVERSITÉ PARIS SACLAY   (France)

Author keywords

Biofilm; Cleaning; Conveyor belt; Disinfection; Listeria monocytogenes

Indexed keywords

EID: 85027445371     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01046-17     Document Type: Article

References (66)

1. Maillard JY. 2002. Bacterial target sites for biocide action. J Appl Microbiol 92(Suppl):1-21.
2. Coughlan LM, Cotter PD, Hill C, Alvarez-Ordóñez A. 2016. New weapons to fight old enemies: novel strategies for the (bio)control of bacterial biofilms in the food industry. Front Microbiol 7:1641. https://doi.org/10.3389/fmicb.2016.01641.
3. El-Azizi M, Farag N, Khardori N. 2016. Efficacy of selected biocides in the decontamination of common nosocomial bacterial pathogens in biofilm and planktonic forms. Comp Immunol Microbiol Infect Dis 47:60-71. https://doi.org/10.1016/j.cimid.2016.06.002.
4. Bridier A, Briandet R, Thomas V, Dubois-Brissonnet F. 2011. Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27:1017-1032. https://doi.org/10.1080/08927014.2011.626899.
5. Brightwell G, Boerema J, Mills J, Mowat E, Pulford D. 2006. Identifying the bacterial community on the surface of Intralox belting in a meat boning room by culture-dependent and culture-independent 16S rDNA sequence analysis. Int J Food Microbiol 109:47-53. https://doi.org/10.1016/j.ijfoodmicro.2006.01.008.
6. Møretrø T, Langsrud S, Heir E. 2013. Bacteria on meat abattoir meat production process surfaces after sanitation: characterisation of survival properties of Listeria monocytogenes and the commensal bacterial flora. Adv Microbiol 3:255-264. https://doi.org/10.4236/aim.2013.33037.
7. Mettler E, Carpentier B. 1998. Variations over time of microbial load and physicochemical properties of floor materials after cleaning in food industry premises. J Food Prot 61:57-65. https://doi.org/10.4315/0362-028X-61.1.57.
8. Stephan R, Althaus D, Kiefer S, Lehner A, Hatz C, Schmutz C, Jost M, Gerber N, Baumgartner A, Hächler H, Mäusezahl-Feuz M. 2015. Foodborne transmission of Listeria monocytogenes via ready-to-eat salad: a nationwide outbreak in Switzerland, 2013-2014. Food Control 57:14-17. https://doi.org/10.1016/j.foodcont.2015.03.034.
9. Miettinen MK, Björkroth KJ, Korkeala HJ. 1999. Characterization of Listeria monocytogenes from an ice cream plant by serotyping and pulsed-field gel electrophoresis. Int J Food Microbiol 46:187-192. https://doi.org/10.1016/S0168-1605(98)00185-8.
10. 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. https://doi.org/10.4315/0362-028X.JFP-13-150.
11. Larsen MH, Dalmasso M, Ingmer H, Langsrud S, Malakauskas M, Mader A, Møretrø T, Mozina SS, Rychli K, Wagner M, Wallace RJ, Zentek J, Jordan K. 2014. Persistence of foodborne pathogens and their control in primary and secondary food production chains. Food Control 44:92-109. https://doi.org/10.1016/j.foodcont.2014.03.039.
12. Morganti M, Scaltriti E, Cozzolino P, Bolzoni L, Casadei G, Pierantoni M, Foni E, Pongolini S. 2015. Processing-dependent and clonal contamination patterns of Listeria monocytogenes in the cured ham food chain revealed by genetic analysis. Appl Environ Microbiol 82:822-831. https://doi.org/10.1128/AEM.03103-15.
13. Stasiewicz MJ, Oliver HF, Wiedmann M, den Bakker HC. 2015. Wholegenome sequencing allows for improved identification of persistent Listeria monocytogenes in food-associated environments. Appl Environ Microbiol 81:6024-6037. https://doi.org/10.1128/AEM.01049-15.
14. Carpentier B, Cerf O. 2011. Review-persistence of Listeria monocytogenes in food industry equipment and premises. Int J Food Microbiol 145:1-8. https://doi.org/10.1016/j.ijfoodmicro.2011.01.005.
15. Lundén JM, Miettinen MK, Autio TJ, Korkeala HJ. 2000. Persistent Listeria monocytogenes strains show enhanced adherence to food contact surface after short contact times. J Food Prot 63:1204-1207. https://doi.org/10.4315/0362-028X-63.9.1204.
16. 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. https://doi.org/10.3389/fmicb.2016.00638.
17. Bridier A, Sanchez-Vizuete P, Guilbaud M, Piard JC, Naitali M, Briandet R. 2015 Biofilm-associated persistence of food-borne pathogens. Food Microbiol 45:167-178. https://doi.org/10.1016/j.fm.2014.04.015.
18. Ortiz S, López-Alonso V, Rodríguez P, Martínez-Suárez JV. 2015. The connection between persistent, disinfectant-resistant Listeria monocytogenes strains from two geographically separate Iberian pork processing plants: evidence from comparative genome analysis. Appl Environ Microbiol 82:308-317. https://doi.org/10.1128/AEM.02824-15.
19. Borucki MK, Peppin JD, White D, Loge F, Call DR. 2003. Variation in biofilm formation among strains of Listeria monocytogenes. Appl Environ Microbiol 69:7336-7342. https://doi.org/10.1128/AEM.69.12.7336-7342.2003.
20. Kadam SR, den Besten HM, van der Veen S, Zwietering MH, Moezelaar R, Abee T. 2013. Diversity assessment of Listeria monocytogenes biofilm formation: impact of growth condition, serotype and strain origin. Int J Food Microbiol 165:259-264. https://doi.org/10.1016/j.ijfoodmicro.2013.05.025.
21. Poimenidou SV, Chrysadakou M, Tzakoniati A, Bikouli VC, Nychas GJ, Skandamis PN. 2016. Variability of Listeria monocytogenes strains in biofilm formation on stainless steel and polystyrene materials and resistance to peracetic acid and quaternary ammonium compounds. Int J Food Microbiol 237:164-171. https://doi.org/10.1016/j.ijfoodmicro.2016.08.029.
22. 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. https://doi.org/10.1016/j.ijfoodmicro.2016.10.025.
23. Sanchez-Vizuete P, Orgaz B, Aymerich S, Le Coq D, Briandet R. 2015. Pathogens protection against the action of disinfectants in multispecies biofilms. Front Microbiol 6:705. https://doi.org/10.3389/fmicb.2015.00705.
24. Giaouris E, Heir E, Hébraud M, Chorianopoulos N, Langsrud S, Møretrø T, Habimana O, Desvaux M, Renier S, Nychas GJ. 2014. Attachment and biofilm formation by foodborne bacteria in meat processing environments: causes, implications, role of bacterial interactions and control by alternative novel methods. Meat Sci 97:298-309. https://doi.org/10.1016/j.meatsci.2013.05.023.
25. Røder HL, Raghupathi PK, Herschend J, Brejnrod A, Knøchel S, Sørensen SJ, Burmølle M. 2015. Interspecies interactions result in enhanced biofilm formation by co-cultures of bacteria isolated from a food processing environment. Food Microbiol 51:18-24. https://doi.org/10.1016/j.fm.2015.04.008.
26. Burmølle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S. 2006. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol 72:3916-3923. https://doi.org/10.1128/AEM.03022-05.
27. Gilbert P, Maira-Litran T, McBain AJ, Rickard AH, Whyte FW. 2002. The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol 46:202-256.
28. van der Veen S, Abee T. 2011. Mixed species biofilms of Listeria monocytogenes and Lactobacillus plantarum show enhanced resistance to benzalkonium chloride and peracetic acid. Int J Food Microbiol 144: 421-431. https://doi.org/10.1016/j.ijfoodmicro.2010.10.029.
29. Carpentier B, Chassaing D. 2004. Interactions in biofilms between Listeria monocytogenes and resident microorganisms from food industry premises. Int J Food Microbiol 97:111-122. https://doi.org/10.1016/j.ijfoodmicro.2004.03.031.
30. Møretrø T, Sonerud T, Mangelrød E, Langsrud S. 2006. Evaluation of the antimicrobial effect of a triclosan-containing industrial floor used in the food industry. J Food Prot 69:627-633. https://doi.org/10.4315/0362-028X-69.3.627.
31. Hood S, Zottola E. 1997. Isolation and identification of adherent gramnegative microorganisms from four meat-processing facilities. J Food Prot 60:1135-1138. https://doi.org/10.4315/0362-028X-60.9.1135.
32. Stellato G, La Storia A, De Filippis F, Borriello G, Villani F, Ercolini D. 2016. Overlap of spoilage-associated microbiota between meat and the meat processing environment in small-scale and large-scale retail distribu-tions. Appl Environ Microbiol 82:4045-4054. https://doi.org/10.1128/AEM.00793-16.
33. Marouani-Gadri N, Augier G, Carpentier B. 2009. Characterization of bacterial strains isolated from a beef-processing plant following cleaning and disinfection-influence of isolated strains on biofilm formation by Sakai and EDL 933 E. coli O157:H7. Int J Food Microbiol 133:62-67. https://doi.org/10.1016/j.ijfoodmicro.2009.04.028.
34. Hultman J, Rahkila R, Ali J, Rousu J, Björkroth KJ. 2015. Meat processing plant microbiome and contamination patterns of cold-tolerant bacteria causing food safety and spoilage risks in the manufacture of vacuumpackaged cooked sausages. Appl Environ Microbiol 81:7088-7097. https://doi.org/10.1128/AEM.02228-15.
35. Bhargava N, Sharma P, Capalash N. 2014. Pyocyanin stimulates quorum sensing-mediated tolerance to oxidative stress and increases persister cell populations in Acinetobacter baumannii. Infect Immun 82: 3417-3425. https://doi.org/10.1128/IAI.01600-14.
36. Hansen SK, Haagensen JA, Gjermansen M, Jørgensen TM, Tolker-Nielsen T, Molin S. 2007. Characterization of a Pseudomonas putida rough variant evolved in a mixed-species biofilm with Acinetobacter sp. strain C6. J Bacteriol 189:4932-4943. https://doi.org/10.1128/JB.00041-07.
37. Langsrud S, Moen B, Møretrø T, Løype M, Heir E. 2016. Microbial dynamics in mixed culture biofilms of bacteria surviving sanitation of conveyor belts in salmon-processing plants. J Appl Microbiol 120:366-378. https://doi.org/10.1111/jam.13013.
38. Fagerlund A, Langsrud S, Schirmer BC, Møretrø T, Heir E. 2016. Genome analysis of Listeria monocytogenes sequence type 8 strains persisting in salmon and poultry processing environments and comparison with related strains. PLoS One 11:e0151117. https://doi.org/10.1371/journal.pone.0151117.
39. Elias S, Banin E. 2012. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36:990-1004. https://doi.org/10.1111/j.1574-6976.2012.00325.x.
40. Liu W, Røder HL, Madsen JS, Bjarnsholt T, Sørensen SJ, Burmølle M. 2016. Interspecific bacterial interactions are reflected in multispecies biofilm spatial organization. Front Microbiol 7:1366. https://doi.org/10.3389/fmicb.2016.01366.
41. Rodríguez-López P, Saá-Ibusquiza P, Mosquera-Fernández M, López-Cabo M. 2015. Listeria monocytogenes-carrying consortia in food industry. Composition, subtyping and numerical characterisation of monospecies biofilm dynamics on stainless steel. Int J Food Microbiol 206: 84-95. https://doi.org/10.1016/j.ijfoodmicro.2015.05.003.
42. Overney A, Jacques-André-Coquin J, Ng P, Carpentier B, Guillier L, Firmesse O. 2017. Impact of environmental factors on the culturability and viability of Listeria monocytogenes under conditions encountered in food processing plants. Int J Food Microbiol 244:74-81. https://doi.org/10.1016/j.ijfoodmicro.2016.12.012.
43. Pan Y, Breidt F, Jr, Kathariou S. 2006. Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl Environ Microbiol 72:7711-7717. https://doi.org/10.1128/AEM.01065-06.
44. Saá Ibusquiza P, Herrera JJ, Cabo ML. 2011. Resistance to benzalkonium chloride, peracetic acid and nisin during formation of mature biofilms by Listeria monocytogenes. Food Microbiol 28:418-425. https://doi.org/10.1016/j.fm.2010.09.014.
45. Müller A, Rychli K, Zaiser A, Wieser C, Wagner M, Schmitz-Esser S. 2014. The Listeria monocytogenes transposon Tn6188 provides increased tolerance to various quaternary ammonium compounds and ethidium bromide. FEMS Microbiol Lett 361:166-173. https://doi.org/10.1111/1574-6968.12626.
46. Tolvanén R, Lunden J, Korkeala H, Wirtanen G. 2007. Ultrasonic cleaning of conveyor belt materials using Listeria monocytogenes as a model organism. J Food Prot 70:758-761. https://doi.org/10.4315/0362-028X-70.3.758.
47. Doijad SP, Barbuddhe SB, Garg S, Poharkar KV, Kalorey DR, Kurkure NV, Rawool DB, Chakraborty T. 2015. Biofilm-forming abilities of Listeria monocytogenes serotypes isolated from different sources. PLoS One 10:e0137046. https://doi.org/10.1371/journal.pone.0137046.
48. Nadkarni MA, Martin FE, Jacques NA, Hunter N. 2002. Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148:257-266. https://doi.org/10.1099/00221287-148-1-257.
49. Malley TJ, Stasiewicz MJ, Gröhn YT, Roof S, Warchocki S, Nightingale K, Wiedmann M. 2013. Implementation of statistical tools to support identification and management of persistent Listeria monocytogenes contamination in smoked fish processing plants. J Food Prot 76:796-811. https://doi.org/10.4315/0362-028X.JFP-12-236.
50. Ragon M, Wirth T, Hollandt F, Lavenir R, Lecuit M, Le Monnier A, Brisse S. 2008. A new perspective on Listeria monocytogenes evolution. PLoS Pathog 4:e1000146. https://doi.org/10.1371/journal.ppat.1000146.
51. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455-477. https://doi.org/10.1089/cmb.2012.0021.
52. Mann EE, Wozniak DJ. 2012. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev 36:893-916. https://doi.org/10.1111/j.1574-6976.2011.00322.x.
53. Nilsson M, Chiang WC, Fazli M, Gjermansen M, Givskov M, Tolker-Nielsen T. 2011. Influence of putative exopolysaccharide genes on Pseudomonas putida KT2440 biofilm stability. Environ Microbiol 13:1357-1369. https://doi.org/10.1111/j.1462-2920.2011.02447.x.
54. Longo F, Vuotto C, Donelli G. 2014. Biofilm formation in Acinetobacter baumannii. New Microbiol 37:119-127.
55. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL. 2009. BLAST+: architecture and applications. BMC Bioinformatics 10:421. https://doi.org/10.1186/1471-2105-10-421.
56. Darling AC, Mau B, Blattner FR, Perna NT. 2004. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394-1403. https://doi.org/10.1101/gr.2289704.
57. Diancourt L, Passet V, Nemec A, Dijkshoorn L, Brisse S. 2010. The population structure of Acinetobacter baumannii: expanding multiresistant clones from an ancestral susceptible genetic pool. PLoS One 5:e10034. https://doi.org/10.1371/journal.pone.0010034.
58. Mulet M, Lalucat J, García-Valdés E. 2010. DNA sequence-based analysis of the Pseudomonas species. Environ Microbiol 12:1513-1530. https://doi.org/10.1111/j.1462-2920.2010.02181.x.
59. Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol Biol Evol 33: 1870-1874. https://doi.org/10.1093/molbev/msw054.
60. Fortineau N, Trieu-Cuot P, Gaillot O, Pellegrini E, Berche P, Gaillard JL. 2000 Optimization of green fluorescent protein expression vectors for in vitro and in vivo detection of Listeria monocytogenes. Res Microbiol 151:353-360. https://doi.org/10.1016/S0923-2508(00)00158-3.
61. Monk IR, Gahan CG, Hill C. 2008. Tools for functional postgenomic analysis of Listeria monocytogenes. Appl Environ Microbiol 74: 3921-3934. https://doi.org/10.1128/AEM.00314-08.
62. Illumina. 2013. 16S metagenomic sequencing library preparation guide. http://support.illumina.com/documents/documentation/chemistry _documentation/16s/16s-metagenomic-library-prep-guide-15044223-b.pdf.
63. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335-336. https://doi.org/10.1038/nmeth.f.303.
64. de Chaumont F, Dallongeville S, Chenouard N, Hervé N, Pop S, Provoost T, Meas-Yedid V, Pankajakshan P, Lecomte T, Le Montagner Y, Lagache T, Dufour A, Olivo-Marin JC. 2012. Icy: an open bioimage informatics platform for extended reproducible research. Nat Methods 9:690-696. https://doi.org/10.1038/nmeth.2075.
65. Sanchez-Vizuete P, Le Coq D, Bridier A, Herry JM, Aymerich S, Briandet R. 2015 Identification of ypqP as a new Bacillus subtilis biofilm determinant that mediates the protection of Staphylococcus aureus against antimicrobial agents in mixed-species communities. Appl Environ Microbiol 81:109-118. https://doi.org/10.1128/AEM.02473-14.
66. Lindstedt BA, Tham W, Danielsson-Tham ML, Vardund T, Helmersson S, Kapperud G. 2008. Multiple-locus variable-number tandem-repeats analysis of Listeria monocytogenes using multicolour capillary electrophoresis and comparison with pulsed-field gel electrophoresis typing. J Microbiol Methods 72:141-148. https://doi.org/10.1016/j.mimet.2007.11.012.