Tolerance to quaternary ammonium compound disinfectants may enhance growth of Listeria monocytogenes in the food industry

International Journal of Food Microbiology

Volumn 241, Issue , 2017, Pages 215-224

  Møretrø, Trond ^a   Schirmer, Bjørn C T ^a,b   Heir, Even ^a   Fagerlund, Annette ^a   Hjemli, Pernille ^a   Langsrud, Solveig ^a  

^a NOFIMA   (Norway)

^b NORWEGIAN VETERINARY INSTITUTE   (Norway)

Author keywords

Benzalkonium chloride; Listeria monocytogenes; Quaternary ammonium compound; Tolerance

Indexed keywords

BENZALKONIUM CHLORIDE; DISINFECTANT AGENT; QUATERNARY AMMONIUM DERIVATIVE;

ALLELE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL SURVIVAL; BACTERICIDAL ACTIVITY; BACTERIUM ISOLATE; BCRABC GENE; BIOFILM; CONTROLLED STUDY; DISINFECTION; FOOD CONTROL; FOOD INDUSTRY; FOOD PROCESSING; GENE LOCUS; GENE SEQUENCE; GENETIC RESISTANCE; LISTERIA MONOCYTOGENES; MEAT INDUSTRY; MICROBIAL DIVERSITY; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PREVALENCE; QACH GENE; SALMONINE; TANDEM REPEAT; ANALYSIS; ANIMAL; ANTIBIOTIC RESISTANCE; BOVINE; DRUG EFFECTS; FOOD CONTAMINATION; FOOD HANDLING; GROWTH, DEVELOPMENT AND AGING; MEAT; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; PREVENTION AND CONTROL;

ANIMALS; BIOFILMS; CATTLE; DISINFECTANTS; DRUG RESISTANCE, BACTERIAL; FOOD CONTAMINATION; FOOD HANDLING; FOOD-PROCESSING INDUSTRY; LISTERIA MONOCYTOGENES; MEAT; MICROBIAL SENSITIVITY TESTS; QUATERNARY AMMONIUM COMPOUNDS;

EID: 84992727840     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2016.10.025     Document Type: Article

References (58)

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. 62 (2000), 57–63.
2. Anastassiades, M., Lehotay, S.J., Stajnbaher, D., Schenck, F.J., Fast and easy multiresidue method employing acetonitrile extraction/partitioning and “dispersive solid-phase extraction” for the determination of pesticide residues in produce. J. AOAC Int. 86 (2003), 412–431.
3. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Son, P., Prjibelski, A.D., Pyshkin, A.V., Sirotkin, A.V., Vyahhi, N., Tesler, G., Alekseyev, M.A., Pevzner, P.A., SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19 (2012), 455–477.
4. Bertuzzi, T., Pietri, A., Determination of benzalkonium homologues and didecyldimethylammonium in powdered and liquid milk for infants by hydrophilic interaction liquid chromatography-mass spectrometry. Food Anal. Methods 7 (2014), 1278–1284.
5. Borucki, M.K., Peppin, J.D., White, D., Loge, F., Call, D.R., Variation in biofilm formation among strains of Listeria monocytogenes. Appl. Environ. Microbiol. 69 (2003), 7336–7342.
6. Carpentier, B., Cerf, O., Review - persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 145 (2011), 1–8.
7. Chinard, F.P., Interactions of quaternary ammonium compounds and proteins - a simple method for the rapid estimation of urinary protein concentrations with alkyldimethylbenzylammonium compounds. J. Biol. Chem. 176 (1948), 1439–1447.
8. Costerton, J.W., Lewandowski, Z., Caldwell, D.E., Korber, D.R., Lappin-Scott, H.M., Microbial biofilms. Annu. Rev. Microbiol. 49 (1995), 711–742.
9. Djordjevic, D., Wiedmann, A., McLandsborough, L.A., Microtiter plate assay for assessment of Listeria monocytogenes biofilm formation. Appl. Environ. Microbiol. 68 (2002), 2950–2958.
10. Drevets, D.A., Bronze, M.S., Listeria monocytogenes: epidemiology, human disease, and mechanisms of brain invasion. FEMS Immunol. Med. Microbiol. 53 (2008), 151–165.
11. Dutta, V., Elhanafi, D., Kathariou, S., Conservation and distribution of the benzalkonium chloride resistance cassette bcrABC in Listeria monocytogenes. Appl. Environ. Microbiol. 79 (2013), 6067–6074.
12. Dutta, V., Elhanafi, D., Osborne, J., Martinez, M.R., Kathariou, S., Genetic characterization of plasmid-associated triphenylmethane reductase in Listeria monocytogenes. Appl. Environ. Microbiol. 80 (2014), 5379–5385.
13. 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. 76 (2010), 8231–8238.
14. European Commision, Regulation (EC) no 396/2005 of the European Parliament and of the Council of 23 February 2005 on maximum residue levels of pesticides in or on food and feed of plant and animal origin and amending council directive 91/414/EEC. L70, 2005, OJEU, 1–16.
15. European Commision, Commission Regulation (EU) No 1119/2014 of 16 October 2014 amending Annex III to Regulation (EC) No 396/2005 of the European Parliament and of the Council as Regards Maximum Residue Levels for Benzalkonium Chloride and Didecyldimethylammonium Chloride in or on Certain Products. L304, 2014, OJEU, 43–74.
16. European Food Safety Authority, Evaluation of monitoring data on residues of didecyldimethylammonium chloride (DDAC) and benzalkonium chloride (BAC). EFSA Supporting Publication 2013, 2013, 30 (EN-483).
17. European Food Safety Authority, The European Union summary report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks in 2014. EFSA J., 13, 2015, 3991.
18. European Reference Laboratories for Residues of Pesticides, Analysis of BACs and DDAC in Milk Using QuEChERS Method and LC-MS/MS. EURL SRM. Version 2. 2014 (05.05.2014).
19. Ferreira, V., Wiedmann, M., Teixeira, P., Stasiewicz, M.J., Listeria monocytogenes persistence in food-associated environments: Epidemiology, strain characteristics, and implications for public health. J. Food Prot. 77 (2014), 150–170.
20. Fox, E.M., Leonard, N., Jordan, K., Physiological and transcriptional characterization of persistent and nonpersistent Listeria monocytogenes isolates. Appl. Environ. Microbiol. 77 (2011), 6559–6569.
21. Fretz, R., Pichler, J., Sagel, U., Much, P., Ruppitsch, W., Pietzka, A.T., Stoeger, A., Huhulescu, S., Heuberger, S., Appl, G., Werber, D., Stark, K., Prager, R., Flieger, A., Karpiskova, R., Pfaff, G., Allerberger, F., Update: Multinational listeriosis outbreak due to ‘Quargel’, a sour milk curd cheese, caused by two different L. monocytogenes serotype 1/2a strains, 2009-2010. Eurosurveillance 15 (2010), 2–3.
22. Gardy, J., Loman, N.J., Rambaut, A., Real-time digital pathogen surveillance - the time is now. Genome Biol., 16, 2015.
23. Gaulin, C., Ramsay, D., Bekal, S., Widespread listeriosis outbreak attributable to pasteurized cheese, which led to extensive cross-contamination affecting cheese retailers, Quebec, Canada, 2008. J. Food Prot. 75 (2012), 71–78.
24. Gerba, C.P., Quaternary ammonium biocides: efficacy in application. Appl. Environ. Microbiol. 81 (2015), 464–469.
25. Gilbert, P., Moore, L.E., Cationic antiseptics: diversity of action under a common epithet. J. Appl. Microbiol. 99 (2005), 703–715.
26. Gottlieb, S.L., Newbern, E.C., Griffin, P.M., Graves, L.M., Hoekstra, R.M., Baker, N.L., Hunter, S.B., Holt, K.G., Ramsey, F., Head, M., Levine, P., Johnson, G., Schoonmaker-Bopp, D., Reddy, V., Kornstein, L., Gerwel, M., Nsubuga, J., Edwards, L., Stonecipher, S., Hurd, S., Austin, D., Jefferson, M.A., Young, S.D., Hise, K., Chernak, E.D., Sobel, J., Listeriosis Outbreak Working, G., Multistate outbreak of listeriosis linked to Turkey deli meat and subsequent changes in US regulatory policy. Clin. Infect. Dis. 42 (2006), 29–36.
27. Harvey, J., Keenan, K.P., Gilmour, A., Assessing biofilm formation by Listeria monocytogenes strains. Food Microbiol. 24 (2007), 380–392.
28. 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. 96 (2004), 85–96.
29. 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. 92 (2002), 111S–120S.
30. Ivanek, R., Grohn, Y.T., Wiedmann, M., The cost and benefit of Listeria monocytogenes food safety measures. Crit. Rev. Food Sci. Nutr. 44 (2004), 513–523.
31. Johnsen, B.O., Lingaas, E., Torfoss, D., Strom, E.H., Nordoy, I., A large outbreak of Listeria monocytogenes infection with short incubation period in a tertiary care hospital. J. Infect. 61 (2010), 465–470.
32. Kastbjerg, V.G., Gram, L., Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure. Int. J. Food Microbiol. 160 (2012), 11–15.
33. Kovacevic, J., Ziegler, J., Walecka-Zacharska, E., Reimer, A., Kitts, D.D., Gilmour, M.W., Tolerance of Listeria monocytogenes to quaternary ammonium sanitizers is mediated by a novel efflux pump encoded by emrE. Appl. Environ. Microbiol. 82 (2016), 939–953.
34. Kwong, J.C., Mercoulia, K., Tomita, T., Easton, M., Li, H.Y., Bulach, D.M., Stinear, T.P., Seemann, T., Howden, B.P., Prospective whole-genome sequencing enhances national surveillance of Listeria monocytogenes. J. Clin. Microbiol. 54 (2016), 333–342.
35. Lado, B.H., Yousef, A.E., Characteristics of Listeria monocytogenes important to food processes. Ryser, E.T., Marth, E.M., (eds.) Listeria, Listeriosis and Food Safety, 2007, CRC Press, 157–213.
36. Laksanalamai, P., Joseph, L.A., Silk, B.J., Burall, L.S., Tarr, C.L., Gerner-Smidt, P., Datta, A.R., Genomic characterization of Listeria monocytogenes strains Involved in a multistate listeriosis outbreak associated with cantaloupe in US. PLoS One, 7, 2012.
37. Lindstedt, B.A., Tham, W., Danielsson-Tham, M.L., Vardund, T., Helmersson, S., Kapperud, G., 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 (2008), 141–148.
38. Lunden, J.M., Miettinen, M.K., Autio, T.J., Korkeala, H.J., Persistent Listeria monocytogenes strains show enhanced adherence to food contact surface after short contact times. J. Food Prot. 63 (2000), 1204–1207.
39. Lunden, J.M., Autio, T.J., Sjöberg, A.-M., Korkeala, H.J., Persistent and nonpersistent Listeria monocytogenes contamination in meat and poultry processing plants. J. Food Prot. 66 (2003), 2062–2069.
40. Malley, T.J.V., Stasiewicz, M.J., Groehn, Y.T., Roof, S., Warchocki, S., Nightingale, K., Wiedmann, M., Implementation of statistical tools to support identification and management of persistent Listeria monocytogenes contamination in smoked fish processing plants. J. Food Prot. 76 (2013), 796–811.
41. Mereghetti, L., Quentin, R., Marquet-van der Mee, N., Audurier, A., Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl. Environ. Microbiol. 66 (2000), 5083–5086.
42. Møretrø, T., Langsrud, S., Listeria monocytogenes: biofilm formation and persistence in food processing environments. Biofilms 1 (2004), 107–121.
43. Müller, A., Rychli, K., Muhterem-Uyar, M., Zaiser, A., Stessl, B., Guinane, C.M., Cotter, P.D., Wagner, M., Schmitz-Esser, S., Tn6188 - a novel transposon in Listeria monocytogenes responsible for tolerance to benzalkonium chloride. PLoS One, 8, 2013.
44. Müller, A., Rychli, K., Zaiser, A., Wieser, C., Wagner, M., Schmitz-Esser, S., The Listeria monocytogenes transposon Tn6188 provides increased tolerance to various quaternary ammonium compounds and ethidium bromide. FEMS Microbiol. Lett. 361 (2014), 166–173.
45. NMKL No 136, Listeria monocytogenes. Detection in foods and feeding stuffs and enumeration in foods. 4th ed., 2007, Nordic Committee on Food Analysis, Norway.
46. Norwood, D.E., Gilmour, A., Adherence of Listeria monocytogenes strains to stainless steel coupons. J. Appl. Microbiol. 86 (1999), 576–582.
47. Nyarko, E.B., Donnelly, C.W., Listeria monocytogenes: strain heterogeneity, methods, and challenges of subtyping. J. Food Sci. 80 (2015), M2868–M2878.
48. Ortiz, S., Lopez, V., Martinez-Suarez, J.V., Control of Listeria monocytogenes contamination in an Iberian pork processing plant and selection of benzalkonium chloride-resistant strains. Food Microbiol. 39 (2014), 81–88.
49. Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Le Monnier, A., Brisse, S., A new perspective on Listeria monocytogenes evolution. PLoS Pathog., 4, 2008, e1000146.
50. Romanova, N.A., Wolffs, P.F.G., Brovko, L.Y., Griffiths, M.W., Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl. Environ. Microbiol. 72 (2006), 3498–3503.
51. Romanova, N.A., Gawande, P.V., Brovko, L.Y., Griffiths, M.W., Rapid methods to assess sanitizing efficacy of benzalkonium chloride to Listeria monocytogenes biofilms. J. Microbiol. Methods 71 (2007), 231–237.
52. Swaminathan, B., Gerner-Smidt, P., The epidemiology of human listeriosis. Microbes Infect. 9 (2007), 1236–1243.
53. Tezel, U., Pavlostathis, S.G., Quaternary ammonium disinfectants: microbial adaptation, degradation and ecology. Curr. Opin. Biotechnol. 33 (2015), 296–304.
54. Tham, W., Ericsson, H., Loncarevic, S., Unnerstad, H., Danielsson-Tham, M.L., Lessons from an outbreak of listeriosis related to vacuum-packed gravad and cold-smoked fish. Int. J. Food Microbiol. 62 (2000), 173–175.
55. To, M.S., Favrin, S., Romanova, N., Griffiths, M.W., Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl. Environ. Microbiol. 68 (2002), 5258–5264.
56. Van Acker, H., Van Dijck, P., Coenye, T., Molecular mechanisms of antimicrobial tolerance and resistance in bacterial and fungal biofilms. Trends Microbiol. 22 (2014), 326–333.
57. Warriner, K., Namvar, A., What is the hysteria with Listeria?. Trends Food Sci. Technol. 20 (2009), 245–254.
58. Wesley, I.V., Harmon, K.M., Dickson, J.S., Schwartz, A.R., Application of a multiplex polymerase chain reaction assay for the simultaneous confirmation of Listeria monocytogenes and other Listeria species in turkey sample surveillance. J. Food Prot. 65 (2002), 780–785.