Control of Listeria monocytogenes contamination in an Iberian pork processing plant and selection of benzalkonium chloride-resistant strains

Food Microbiology

Volumn 39, Issue , 2014, Pages 81-88

  Ortiz, Sagrario ^a   López, Victoria ^b   Martínez Suárez, Joaquín V ^a  

^a INIA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Disinfectant resistance; Iberian pork; Listeria monocytogenes; Low virulence; Prolonged survival; Pulsed field gel electrophoresis types

Indexed keywords

BAC; BENZALKONIUM; BENZALKONIUM CHLORIDE; DISINFECTANT AGENT; ETHIDIUM BROMIDE; QUATERNARY AMMONIUM DERIVATIVE;

ANIMAL; ANTIBIOTIC RESISTANCE; ARTICLE; CLASSIFICATION; DISINFECTANT RESISTANCE; DRUG EFFECT; EQUIPMENT; ETBR; FOOD CONTAMINATION; FOOD HANDLING; GENETICS; IBERIAN PORK; ISOLATION AND PURIFICATION; LISTERIA MONOCYTOGENES; LOW VIRULENCE; MEAT; MICROBIOLOGY; MINIMUM INHIBITORY CONCENTRATION; PFGE; PMSC; PREMATURE STOP CODON; PROLONGED SURVIVAL; PULSED-FIELD GEL ELECTROPHORESIS; PULSED-FIELD GEL ELECTROPHORESIS TYPES; QAC; SLAUGHTERHOUSE; SPAIN; SWINE;

BAC; BENZALKONIUM CHLORIDE; DISINFECTANT RESISTANCE; ETBR; ETHIDIUM BROMIDE; IBERIAN PORK; LISTERIA MONOCYTOGENES; LOW VIRULENCE; MIC; MINIMAL INHIBITORY CONCENTRATION; PFGE; PMSC; PREMATURE STOP CODON; PROLONGED SURVIVAL; PULSED-FIELD GEL ELECTROPHORESIS; PULSED-FIELD GEL ELECTROPHORESIS TYPES; QAC; QUATERNARY AMMONIUM COMPOUND;

ABATTOIRS; ANIMALS; BENZALKONIUM COMPOUNDS; DISINFECTANTS; DRUG RESISTANCE, BACTERIAL; FOOD CONTAMINATION; FOOD HANDLING; LISTERIA MONOCYTOGENES; MEAT; SPAIN; SWINE;

EID: 84896948648     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2013.11.007     Document Type: Article

References (53)

1. Aase B., Sundheim G., Langsrud S., Rørvik L.M. Occurrence of and a possible mechanism for resistance to a quaternary ammonium compound in Listeria monocytogenes. Int. J. Food Microbiol. 2000, 62:57-63.
2. Briers Y., Klumpp J., Schuppler M., Loessner M.J. Genome sequence of Listeria monocytogenes Scott A, a clinical isolate from a food-borne listeriosis outbreak. J.Bacteriol. 2011, 193:4284-4285.
3. Carpentier B., Cerf O. Review. Persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 2011, 145:1-8.
4. Chen Y., Zhang W., Knabel S.J. Multi-virulence-locus sequence typing clarifies epidemiology of recent listeriosis outbreaks in the United States. J.Clin. Microbiol. 2005, 43:5291-5294.
5. CLSI Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. Clinical and Laboratory Standards Institute, Approved Standard 2008, CLSI, Wayne, PA, CLSI document M31-A3. third ed.
6. Di Bonaventura G., Piccolomini R., Paludi D., D'Orio V., Vergara A., Conter M., Ianieri A. Influence of temperature on biofilm formation by Listeria monocytogenes on various food-contact surfaces: relationship with motility and cell surface hydrophobicity. J.Appl. Microbiol. 2008, 104:1552-1561.
7. Doumith M., Buchrieser C., Glaser P., Jacquet C., Martin P. Differentiation of the major Listeria monocytogenes serovars by multiplex PCR. J.Clin. Microbiol. 2004, 42:3819-3822.
8. Earnshaw A.M., Lawrence L.M. Sensitivity to commercial disinfectants, and the occurrence of plasmids within various Listeria monocytogenes genotypes isolated from poultry products and the poultry processing environment. J.Appl. Microbiol. 1998, 84:642-648.
9. Elhanafi D., Dutta V., Kathariou S. Genetic characterization of plasmid-associated benzalkonium chloride resistance determinants in a Listeria monocytogenes strain from the 1998-1999 outbreak. Appl. Environ. Microbiol. 2010, 76:8231-8238.
10. Ferreira V., Barbosa J., Stasiewicz M., Vongkamjan K., Moreno Switt A., Hogg T., Gibbs P., Teixeira P., Wiedmann M. Diverse geno- and phenotypes of persistent Listeria monocytogenes isolates from fermented meat sausage production facilities in Portugal. Appl. Environ. Microbiol. 2011, 77:2701-2715.
11. Fox E.M., Leonard N., Jordan K. Physiological and transcriptional characterization of persistent and nonpersistent Listeria monocytogenes isolates. Appl. Environ. Microbiol. 2011, 77:6559-6569.
12. Gilbert P., McBain A.J. Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin. Microbiol. Rev. 2003, 16:189-208.
13. Halpin J.L., Garrett N.M., Ribot E.M., Graves L.M., Cooper K.L. Re-evaluation, optimization, and multilaboratory validation of the PulseNet-standardized pulsed-field gel electrophoresis protocol for Listeria monocytogenes. Foodborne Pathog. Dis. 2010, 7:293-298.
14. Harvey J., Gilmour A. Characterization of recurrent and sporadic Listeria monocytogenes isolates from raw milk and nondairy foods by pulsed-field gel electrophoresis, monocin typing, plasmid profiling, and cadmium and antibiotic resistance determination. Appl. Environ. Microbiol. 2001, 67:840-847.
15. Hegstad K., Langsrud S., Lunestad B.T., Scheie A.A., Sunde M., Yazdankhah S.P. Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health?. Microb. Drug Resist. 2010, 16:91-104.
16. Heir E., Lindstedt B.A., Røtterud O.J., Vardund T., Kapperud G., Nesbakken T. Molecular epidemiology and disinfectant susceptibility of Listeria monocytogenes from meat processing plants and human infections. Int. J. Food Microbiol. 2004, 96:85-96.
17. Holah J.T., Taylor J.H., Dawson D.J., Hall K.E. Biocide use in the food industry and the disinfectant resistance of persistent strains of Listeria monocytogenes and Escherichia coli. J.Appl. Microbiol. 2002, 92(Suppl.):111S-120S.
18. Holch A., Webb K., Lukjancenko O., Ussery D., Rosenthal B.M., Gram L. Genome sequencing identifies two nearly unchanged strains of persistent Listeria monocytogenes isolated at two different fish processing plants sampled 6 years apart. Appl. Environ. Microbiol. 2013, 79:2944-2951.
19. Jacquet C., Doumith M., Gordon J.I., Martin P.M., Cossart P., Lecuit M. Amolecular marker for evaluating the pathogenic potential of foodborne Listeria monocytogenes. J.Infect. Dis. 2004, 189:2094-2100.
20. Jensen A., Thomsen L.E., Jørgensen R.L., Larsen M.H., Roldgaard B.B., Christensen B.B., Vogel B.F., Gram L., Ingmer H. Processing plant persistent strains of Listeria monocytogenes appear to have a lower virulence potential than clinical strains in selected virulence models. Int. J. Food Microbiol. 2008, 123:254-261.
21. Kastbjerg V.G., Gram L. Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure. Int. J. Food Microbiol. 2012, 160:11-15.
22. Kastbjerg V., Gram L. Model systems allowing quantification of sensitivity to disinfectants and comparison of disinfectant susceptibility of persistent and presumed nonpersistent Listeria monocytogenes. J.Appl. Microbiol. 2009, 106:1667-1681.
23. Keto-Timonen R., Tolvanen R., Lundén J., Korkeala H. An 8-year surveillance of the diversity and persistence of Listeria monocytogenes in a chilled food processing plant analyzed by amplified fragment length polymorphism. J.Food Prot. 2007, 70:1866-1873.
24. Kornacki J.L., Gurtler J.B. Incidence and control of Listeria in food processing facilities. Listeria, Listeriosis and Food Safety 2007, 681-766. CRC Press, Boca Raton, FL. E.T. Ryser, E.H. Marth (Eds.).
25. Kovacevic J., Arguedas-Villa C., Wozniak A., Tasara T., Allen K.J. Examination of food chain-derived Listeria monocytogenes strains of different serotypes reveals considerable diversity in inlA genotypes, mutability, and adaptation to cold temperatures. Appl. Environ. Microbiol. 2013, 79:1915-1922.
26. Kümmerer K., Eitel A., Braun U., Hubner P., Daschner F., Mascart G., Milandri M., Reinthaler F., Verhoef J. Analysis of benzalkonium chloride in the effluent from European hospitals by solid-phase extraction and high-performance liquid chromatography with post-column ion-pairing and fluorescence detection. J.Chromatogr. A 1997, 774:281-286.
27. Leclercq A., Chenal-Francisque V., Dieye H., Cantinelli T., Drali R., Brisse S., Lecuit M. Characterization of the novel Listeria monocytogenes PCR serogrouping profile IVb-v1. Int. J. Food Microbiol. 2011, 147:74-77.
28. Lemon K.P., Freitag N.E., Kolter R. The virulence regulator PrfA promotes biofilm formation by Listeria monocytogenes. J.Bacteriol. 2010, 192:3969-3976.
29. Lindbäck T., Secic I., Rørvik L.M. Acontingency locus in prfA in a Listeria monocytogenes subgroup allows reactivation of the PrfA virulence regulator during infection in mice. Appl. Environ. Microbiol. 2011, 77:3478-3483.
30. López V., Navas J., Martínez-Suárez J.V. Low potential virulence associated with mutations in the inlA and prfA genes in Listeria monocytogenes isolated from raw retail poultry meat. J.Food Prot. 2013, 76:129-132.
31. López V., Ortiz S., Corujo A., López P., Poza D., Navas J., Moreno R., Martínez-Suárez J.V. Different contamination patterns of lineage I and II strains of Listeria monocytogenes in a Spanish broiler abattoir. Poult. Sci. 2008, 87:1874-1882.
32. Lundén J., Autio T., Markkula A., Hellström S., Korkeala H. Adaptive and cross-adaptive responses of persistent and non-persistent Listeria monocytogenes strains to disinfectants. Int. J. Food Microbiol. 2003, 82:265-272.
33. McDonnell G., Russell A.D. Antiseptics and disinfectants: activity, action, and resistance. Clin. Microbiol. Rev. 1999, 12:147-179.
34. Mereghetti L., Quentin R., Marquet-Van Der Mee N., Audurier A. Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl. Environ. Microbiol. 2000, 66:5083-5086.
35. Mertins S., Joseph B., Goetz M., Ecke R., Seidel G., Sprehe M., Hillen W., Goebel W., Müller-Altrock S. Interference of components of the phosphoenolpyruvate phosphotransferase system with the central virulence gene regulator PrfA of Listeria monocytogenes. J.Bacteriol. 2007, 189:473-490.
36. Møretrø T., Langsrud S. Listeria monocytogenes: biofilm formation and persistence in food-processing environments. Biofilms 2004, 1:107-121.
37. Mullapudi S., Siletzky R.M., Kathariou S. Heavy-metal and benzalkonium chloride resistance of Listeria monocytogenes isolates from the environment of turkey-processing plants. Appl. Environ. Microbiol. 2008, 74:1464-1468.
38. Nilsson R.E., Ross T., Bowman J.P. Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. Int. J. Food Microbiol. 2011, 150:14-24.
39. Orgaz B., Puga C.H., Martínez-Suárez J.V., SanJose C. Biofilm recovery from chitosan action: a possible clue to understand Listeria monocytogenes persistence in food plants. Food Control 2013, 32:484-489.
40. Orsi R.H., den Bakker H.C., Wiedmann M. Listeria monocytogenes lineages: genomics, evolution, ecology, and phenotypic characteristics. Int. J. Med. Microbiol. 2011, 301:79-96.
41. Ortiz S., López V., Villatoro D., López P., Dávila J.C., Martínez-Suárez J.V. A3-year surveillance of the genetic diversity and persistence of Listeria monocytogenes in an Iberian pig slaughterhouse and processing plant. Foodborne Pathog. Dis. 2010, 7:1177-1184.
42. Pan Y., Breidt F., Gorski L. Synergistic effects of sodium chloride, glucose, and temperature on biofilm formation by Listeria monocytogenes serotype 1/2a and 4b strains. Appl. Environ. Microbiol. 2010, 76:1433-1441.
43. Ragon M., Wirth T., Hollandt F., Lavenir R., Lecuit M., Le Monnier A., Brisse S. Anew perspective on Listeria monocytogenes evolution. PLOS Pathog. 2008, 4:e1000146.
44. Rakic-Martinez M., Drevets D.A., Dutta V., Katic V., Kathariou S. Listeria monocytogenes strains selected on ciprofloxacin or the disinfectant benzalkonium chloride exhibit reduced susceptibility to ciprofloxacin, gentamicin, benzalkonium chloride, and other toxic compounds. Appl. Environ. Microbiol. 2011, 77:8714-8721.
45. Renier S., Hébraud M., Desvaux M. Molecular biology of surface colonization by Listeria monocytogenes: an additional facet of an opportunistic Gram-positive foodborne pathogen. Environ. Microbiol. 2011, 13:835-850.
46. Roche S.M., Grépinet O., Kerouanton A., Ragon M., Leclercq A., Témoin S., Schaeffer B., Skorski G., Mereghetti L., Le Monnier A., Velge P. Polyphasic characterization and genetic relatedness of low-virulence and virulent Listeria monocytogenes isolates. BMC Microbiol. 2012, 12:304.
47. Romanova N.A., Wolffs P.F., Brovko L.Y., Griffiths M.W. Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl. Environ. Microbiol. 2006, 72:3498-3503.
48. Sidhu M.S., Sørum H., Holck A. Resistance to quaternary ammonium compounds in food-related bacteria. Microb. Drug Resist. 2002, 8:393-399.
49. Soumet C., Ragimbeau C., Maris P. Screening of benzalkonium chloride resistance in Listeria monocytogenes strains isolated during cold smoked fish production. Lett. Appl. Microbiol. 2005, 41:291-296.
50. Thévenot D., Dernburg A., Vernozy-Rozand C. An updated review of Listeria monocytogenes in the pork meat industry and its products. J.Appl. Microbiol. 2006, 101:7-17.
51. van Stelten A., Simpson J.M., Ward T.J., Nightingale K.K. Revelation by single nucleotide polymorphism genotyping that mutations leading to a premature stop codon in inlA are common among Listeria monocytogenes isolates from ready-to-eat foods but not human listeriosis cases. Appl. Environ. Microbiol. 2010, 76:2783-2790.
52. Verghese B., Lok M., Wen J., Alessandria V., Chen Y., Kathariou S., Knabel S. comK prophage junction fragments as markers for Listeria monocytogenes genotypes unique to individual meat and poultry processing plants and a model for rapid niche-specific adaptation, biofilm formation, and persistence. Appl. Environ. Microbiol. 2011, 77:3279-3292.
53. Wulff G., Gram L., Ahrens P., Vogel B.F. One group of genetically similar Listeria monocytogenes strains frequently dominates and persists in several fish slaughter- and smokehouses. Appl. Environ. Microbiol. 2006, 72:4313-4322.