Potential impact of the resistance to quaternary ammonium disinfectants on the persistence of Listeria monocytogenes in food processing environments

Frontiers in Microbiology

Volumn 7, Issue MAY, 2016, Pages

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

^a INIA   (Spain)

^b Unidad Funcional de Investigación en Enfermedades Crónicas   (Spain)

Author keywords

Bacterial persistence; Food processing; Listeria monocytogenes; Quaternary ammonium disinfectants; Resistance

Indexed keywords

QUATERNARY AMMONIUM DERIVATIVE;

ANTIMICROBIAL ACTIVITY; BACTERIAL GENE; BIOFILM; CELL SURVIVAL; DISINFECTION SYSTEM; ENVIRONMENTAL FACTOR; FOOD PROCESSING; GENE MUTATION; LISTERIA MONOCYTOGENES; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; QACH GENE; SHORT SURVEY;

EID: 84973473528     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00638     Document Type: Short Survey

References (73)

1. Aarestrup, F. M., Knöchel, S., and Hasman, H. (2007). Antimicrobial susceptibility of Listeria monocytogenes from food products. Foodborne Pathog. Dis. 4, 216-221. doi: 10.1089/fpd.2006.0078
2. Aase, B., Sundheim, G., Langsrud, S., and Rørvik, L. M. (2000). Occurrence of and a possible mechanism for resistance to a quaternary ammonium compound in Listeria monocytogenes. Int. J. Food Microbiol. 62, 57-63. doi: 10.1016/S0168-1605(00)00357-3
3. Berzinš, A., Hellström, S., Silinš, I., and Korkeala, H. (2010). Contamination patterns of Listeria monocytogenes in cold-smoked pork processing. J. Food Prot. 73, 2103-2109.
4. Blair, J. M., Webber, M. A., Baylay, A. J., Ogbolu, D. O., and Piddock, L. J. (2015). Molecular mechanisms of antibiotic resistance. Nat. Rev. Microbiol. 13, 42-51. doi: 10.1038/nrmicro3380
5. Bridier, A., Briandet, R., Thomas, V., and Dubois-Brissonnet, F. (2011). Resistance of bacterial biofilms to disinfectants: a review. Biofouling 27, 1017-1032. doi: 10.1080/08927014.2011.626899
6. Buffet-Bataillon, S., Tattevin, P., Bonnaure-Mallet, M., and Jolivet-Gougeon, A. (2012). Emergence of resistance to antibacterial agents: the role of quaternary ammonium compounds-a critical review. Int. J. Antimicrob. Agents 39, 381-389. doi: 10.1016/j.ijantimicag.2012.01.011
7. Carpentier, B., and Cerf, O. (2011). Review-persistence of Listeria monocytogenes in food industry equipment and premises. Int. J. Food Microbiol. 145, 1-8. doi: 10.1016/j.ijfoodmicro.2011.01.005
8. CDC (2014). Incidence and trends of infection with pathogens transmitted commonly through food-foodborne diseases active surveillance network, 10 U.S. sites, 2006-2013. Morb. Mortal. Wkly. Rep. 63, 328-332.
9. CLSI (2009). Clinical Laboratory Standards Institute. Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria that Grow Aerobically. Approved Standard, 8th ed. M7-A8. Wayne, PA: CLSI.
10. Cramer, M. M. (2006). Food Plant Sanitation. Design, Maintenance, and Good Manufacturing Practices. Boca Raton, FL: CRC Press.
11. de Noordhout, C. M., Devleesschauwer, B., Angulo, F. J., Verbeke, G., Haagsma, J., Kirk, M., et al. (2014). The global burden of listeriosis: a systematic review and meta-analysis. Lancet Infect. Dis. 14, 1073-1082. doi: 10.1016/S1473-3099(14)70870-9
12. Dutta, V., Elhanafi, D., and Kathariou, S. (2013). Conservation and distribution of the benzalkonium chloride resistance cassette bcrABC in Listeria monocytogenes. Appl. Environ. Microbiol. 79, 6067-6074. doi: 10.1128/AEM.01751-13
13. Ebner, R., Stephan, R., Althaus, D., Brisse, S., Maury, M., and Tasara, T. (2015). Phenotypic and genotypic characteristics of Listeria monocytogenes strains isolated during 2011-2014 from different food matrices in Switzerland. Food Control 57, 321-326. doi: 10.1016/j.foodcont.2015.04.030
14. EFSA (2008). Scientific opinion of the panel on biological hazards on a request from the European Food Safety Authority on foodborne antimicrobial resistance as a biological hazard. EFSA J. 765, 1-87.
15. EFSA and ECDC (2014). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2012. EFSA J. 12, 3547.
16. Elhanafi, D., Dutta, V., and Kathariou, S. (2010). Genetic characterisation of plasmid associated benzalkonium chloride resistance determinants in a strain of Listeria monocytogenes from the 1998-1999 outbreak. Appl. Environ. Microbiol. 76, 8231-8238. doi: 10.1128/AEM.02056-10
17. EUCAST (2000). European committee on antimicrobial susceptibility testing. Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by agar dilution. Definitive document E.DEF 3.1. Clin. Microbiol. Infect. 6, 509-515.
18. European Committee for Standardisation (2010). European Standard EN 1276:2009/AC:2010. Chemical Disinfectants and Antiseptics-Quantitative Suspension Test for the Evaluation of Bactericidal Activity of Chemical Disinfectants and Antiseptics used in Food, Industrial, Domestic and Institutional Areas-Test Method and Requirements (phase 2, step 1). Brussels: European Committee for Standardisation.
19. Fatemi, P., and Frank, J. F. (1999). Inactivation of Listeria monocytogenes/Pseudomonas biofilms by peracid sanitizers. J. Food Prot. 62, 761-765.
20. Ferreira, V., Barbosa, J., Stasiewicz, M., Vongkamjan, K., Moreno Switt, A., Hogg, T., et al. (2011). Diverse geno-and phenotypes of persistent Listeria monocytogenes isolates from fermented meat sausage production facilities in Portugal. Appl. Environ. Microbiol. 77, 2701-2715. doi: 10.1128/AEM.02553-10
21. Ferreira, V., Wiedmann, M., Teixeira, P., and Stasiewicz, M. J. (2014). Listeria monocytogenes persistence in food-associated environments: epidemiology, strain characteristics, and implications for public health. J. Food Prot. 77, 150-170. doi: 10.4315/0362-028X.JFP-13-150
22. Fox, E. M., Leonard, N., and Jordan, K. (2011). Physiological and transcriptional characterization of persistent and nonpersistent Listeria monocytogenes isolates. Appl. Environ. Microbiol. 77, 6559-6569. doi: 10.1128/AEM.05529-11
23. Gandhi, M., and Chikindas, M. L. (2007). Listeria: a foodborne pathogen that knows how to survive. Int. J. Food Microbiol. 113, 1-15. doi: 10.1016/j.ijfoodmicro.2006.07.008
24. Garner, D., and Kathariou, S. (2016). Fresh produce-associated listeriosis outbreaks, sources of concern, teachable moments, and insights. J. Food Prot. 79, 337-344. doi: 10.4315/0362-028X.JFP-15-387
25. Gerba, C. P. (2015). Quaternary ammonium biocides: efficacy in application. Appl. Environ. Microbiol. 81, 464-469. doi: 10.1128/AEM.02633-2614
26. Hegstad, K., Langsrud, S., Lunestad, B. T., Scheie, A. A., Sunde, M., and Yazdankhah, S. P. (2010). Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb. Drug Resist. 16, 91-104. doi: 10.1089/mdr.2009.0120
27. Heir, E., Lindstedt, B. A., Røtterud, O. J., Vardund, T., Kapperud, G., and Nesbakken, T. (2004). Molecular epidemiology and disinfectant susceptibility of Listeria monocytogenes from meat processing plants and human infections. Int. J. Food Microbiol. 96, 85-96. doi: 10.1016/j.ijfoodmicro.2004.03.014
28. Jiang, X., Yu, T., Liang, Y., Ji, S., Guo, X., Ma, J., et al. (2015). Efflux pump-mediated benzalkonium chloride resistance in Listeria monocytogenes isolated from retail food. Int. J. Food Microbiol. 217, 141-145. doi: 10.1016/j.ijfoodmicro.2015.10.022
29. Kastbjerg, V. G., and Gram, L. (2009). Model systems allowing quantification of sensitivity to disinfectants and comparison of disinfectant susceptibility of persistent and presumed nonpersistent Listeria monocytogenes. J. Appl. Microbiol. 106, 1667-1681. doi: 10.1111/j.1365-2672.2008.04134.x
30. Kastbjerg, V. G., and Gram, L. (2012). Industrial disinfectants do not select for resistance in Listeria monocytogenes following long term exposure. Int. J. Food Microbiol. 160, 11-15. doi: 10.1016/j.ijfoodmicro.2012.09.009
31. Katharios-Lanwermeyer, S., Rakic-Martinez, M., Elhanafi, D., Ratani, S., Tiedje, J. M., and Kathariou, S. (2012). Coselection of cadmium and benzalkonium chloride resistance in conjugative transfers from nonpathogenic Listeria spp. to other Listeriae. Appl. Environ. Microbiol. 78, 7549-7556. doi: 10.1128/AEM.02245-2212
32. Kovacevic, J., Ziegler, J., Walecka-Zacharska, E., Reimer, A., Kitts, D. D., and Gilmour, M. W. (2015). Tolerance of Listeria monocytogenes to quaternary ammonium sanitizers is mediated by a novel efflux pump encoded by emrE. Appl. Environ. Microbiol. 82, 939-953. doi: 10.1128/AEM.03741-15
33. Lemaitre, J. P., Echchannaoui, H., Michaut, G., Divies, C., and Rousset, A. (1998). Plasmid-mediated resistance to antimicrobial agents among listeriae. J. Food Protect. 61, 1459-1464.
34. Lianou, A., and Sofos, J. N. (2007). A review of the incidence and transmission of Listeria monocytogenes in ready-to-eat products in retail and food service environments. J. Food Prot. 70, 2172-2198.
35. Liu, X., Marrakchi, M., Jahne, M., Rogers, S., and Andreescu, S. (2016). Real-time investigation of antibiotics-induced oxidative stress and superoxide release in bacteria using an electrochemical biosensor. Free Radic. Biol. Med. 91, 25-33. doi: 10.1016/j.freeradbiomed.2015.12.001
36. Lundén, J. M., Autio, T. J., Markkula, A., Hellström, S., and Korkeala, H. (2003a). Adaptive and cross-adaptive responses of persistent and nonpersistent Listeria monocytogenes strains to disinfectants. Int. J. Food Microbiol. 82, 265-272. doi: 10.1016/S0168-1605(02)00312-4
37. Lundén, J. M., Autio, T. J., Sjoberg, A. M., and Korkeala, H. J. (2003b). Persistent and nonpersistent Listeria monocytogenes contamination in meat and poultry processing plants. J. Food Prot. 66, 2062-2069.
38. Malley, T. J., Butts, J., and Wiedmann, M. (2015). Seek and destroy process: Listeria monocytogenes process controls in the ready-to-eat meat and poultry industry. J. Food Prot. 78, 436-445. doi: 10.4315/0362-028X.JFP-13-507
39. McLauchlin, J., Mitchell, R. T., Smerdon, W. J., and Jewell, K. (2004). Listeria monocytogenes and listeriosis: a review of hazard characterisation for use in microbiological risk assessment of foods. Int. J. Food Microbiol. 92, 15-33. doi: 10.1016/S0168-1605(03)00326-X
40. Mereghetti, L., Quentin, R., Mee, N., and Audurier, A. (2000). Low sensitivity of Listeria monocytogenes to quaternary ammonium compounds. Appl. Environ. Microbiol. 66, 5083-5086. doi: 10.1128/AEM.66.11.5083-5086.2000
41. Morganti, M., Scaltriti, E., Cozzolino, P., Bolzoni, L., Casadei, G., Pierantoni, M., et al. (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. doi: 10.1128/AEM.03103-15
42. Morrissey, I., Oggioni, M. R., Knight, D., Curiao, T., Coque, T., Kalkanci, A., et al. (2014). Evaluation of epidemiological cut-off values indicates that biocide resistant subpopulations are uncommon in natural isolates of clinically-relevant microorganisms. PLoS ONE 9:e86669. doi: 10.1371/journal.pone.0086669
43. Mullapudi, S., Siletzky, R. M., and 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. doi: 10.1128/AEM.02426-07
44. Müller, A., Rychli, K., Muhterem-Uyar, M., Zaiser, A., Stessl, B., Guinane, C. M., et al. (2013). Tn6188-a novel transposon in Listeria monocytogenes responsible for tolerance to benzalkonium chloride. PLoS ONE 8:e76835. doi: 10.1371/journal.pone.0076835
45. Nakamura, H., Takakura, K., Sone, Y., Itano, Y., and Nishikawa, Y. (2013). Biofilm formation and resistance to benzalkonium chloride in Listeria monocytogenes isolated from a fish processing plant. J. Food Prot. 76, 1179-1186. doi: 10.4315/0362-028X.JFP-12-225
46. Nakari, U. M., Rantala, L., Pihlajasaari, A., Toikkanen, S., Johansson, T., Hellsten, C., et al. (2014). Investigation of increased listeriosis revealed two fishery production plants with persistent Listeria contamination in Finland in 2010. Epidemiol. Infect. 142, 2261-2269. doi: 10.1017/S095026881300349X
47. Norwood, D., and Gilmour, A. (2000). The growth and resistance to sodium hypochlorite of Listeria monocytogenes in a steady-state multispecies biofilm. J. Appl. Microbiol. 88, 512-520. doi: 10.1046/j.1365-2672.2000.00990.x
48. Orsi, R. H., Borowsky, M. L., Lauer, P., Young, S. K., Nusbaum, C., Galagan, J. E., et al. (2008). Short-term genome evolution of Listeria monocytogenes in a non-controlled environment. BMC Genomics 9:539. doi: 10.1186/1471-2164-9-539
49. Ortiz, S. (2015). Diversidad Genética y Persistencia Ambiental de Listeria monocytogenes En Dos Plantas de Procesado de Carne de Cerdo Ibérico: Influencia de la Resistencia a Desinfectantes de Amonio Cuaternario. Ph.D. thesis, Universidad Complutense de Madrid, Madrid.
50. Ortiz, S., López, V., and Martínez-Suárez, J. V. (2014a). Control of Listeria monocytogenes contamination in an Iberian pork processing plant and selection of benzalkonium chloride-resistant strains. Food Microbiol. 39, 81-88. doi: 10.1016/j.fm.2013.11.007
51. Ortiz, S., López, V., and Martínez-Suárez, J. V. (2014b). The influence of subminimal inhibitory concentrations of benzalkonium chloride on biofilm formation by Listeria monocytogenes. Int. J. Food Microbiol. 189, 106-112. doi: 10.1016/j.ijfoodmicro.2014.08.007
52. Ortiz, S., López, V., Villatoro, D., López, P., Dávila, J. C., and Martínez-Suárez, J. V. (2010). A 3-year surveillance of the genetic diversity and persistence of Listeria monocytogenes in an Iberian pig slaughterhouse and processing plant. Foodborne Pathog. Dis. 7, 1177-1184. doi: 10.1089/fpd.2010.0535
53. Ortiz, S., López-Alonso, V., Rodríguez, P., and Martínez-Suárez, J. V. (2016). 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. doi: 10.1128/AEM.02824-15
54. Pan, Y., Breidt, F. Jr., and Kathariou, S. (2006). Resistance of Listeria monocytogenes biofilms to sanitizing agents in a simulated food processing environment. Appl. Environ. Microbiol. 72, 7711-7717. doi: 10.1128/AEM.01065-06
55. Piddock, L. J. (2006). Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin. Microbiol. Rev. 19, 382-402. doi: 10.1128/CMR.19.2.382-402.2006
56. Rakic-Martinez, M., Drevets, D. A., Dutta, V., Katic, V., and Kathariou, S. (2011). 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. 77, 8714-8721. doi: 10.1128/AEM.05941-11
57. Ratani, S. S., Siletzky, R. M., Dutta, V., Yildirim, S., Osborne, J. A., Lin, W., et al. (2012). Heavy metal and disinfectant resistance of Listeria monocytogenes from foods and food processing plants. Appl. Environ. Microbiol. 78, 6938-6945. doi: 10.1128/AEM.01553-12
58. Renier, S., Hébraud, M., and Desvaux, M. (2011). Molecular biology of surface colonization by Listeria monocytogenes: an additional facet of an opportunistic Gram-positive foodborne pathogen. Environ. Microbiol. 13, 835-850. doi: 10.1111/j.1462-2920.2010.02378.x
59. Romanova, N., Favrin, S., and Griffiths, M. W. (2002). Sensitivity of Listeria monocytogenes to sanitizers used in the meat processing industry. Appl. Environ. Microbiol. 68, 6405-6409. doi: 10.1128/AEM.68.12.6405-6409.2002
60. Romanova, N. A., Wolffs, P. F., Brovko, L. Y., and Griffiths, M. W. (2006). Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl. Environ. Microbiol. 72, 3498-3503. doi: 10.1128/AEM.72.5.3498-3503.2006
61. SCENIHR (2009). Scientific Committee on Emerging and Newly Identified Health Risks. Assessment of the Antibiotic Resistance Effects of Biocides. Brussels: European Commission. Health & Consumer Protection DG.
62. Schmitz-Esser, S., Müller, A., Stessl, B., and Wagner, M. (2015). Genomes of sequence type 121 Listeria monocytogenes strains harbor highly conserved plasmids and prophages. Front. Microbiol. 6:380. doi: 10.3389/fmicb.2015.00380
63. Shapiro, R. S. (2015). Antimicrobial-induced DNA damage and genomic instability in microbial pathogens. PLoS Pathog. 11:e1004678. doi: 10.1371/journal.ppat.1004678
64. Silk, B. J., Date, K. A., Jackson, K. A., Pouillot, R., Holt, K. G., Graves, L. M., et al. (2012). Invasive listeriosis in the foodborne diseases active surveillance network (FoodNet), 2004-2009: further targeted prevention needed for higher-risk groups. Clin. Infect. Dis. 54(Suppl. 5), S396-S404. doi: 10.1093/cid/cis268
65. Soumet, C., Ragimbeau, C., and Maris, P. (2005). Screening of benzalkonium chloride resistance in Listeria monocytogenes strains isolated during cold smoked fish production. Lett. Appl. Microbiol. 41, 291-296. doi: 10.1111/j.1472-765X.2005.01763.x
66. Stopforth, J. D., Samelis, J., Sofos, J. N., Kendall, P. A., and Smith, G. C. (2002). Biofilm formation by acid-adapted and nonadapted Listeria monocytogenes in fresh beef decontamination washings and its subsequent inactivation with sanitizers. J. Food Prot. 65, 1717-1727.
67. Tezel, U., and Pavlostathis, S. G. (2015). Quaternary ammonium disinfectants: microbial adaptation, degradation and ecology. Curr. Opin. Biotechnol. 33, 296-304. doi: 10.1016/j.copbio.2015.03.018
68. Thévenot, D., Dernburg, A., and Vernozy-Rozand, C. (2006). An updated review of Listeria monocytogenes in the pork meat industry and its products. J. Appl. Microbiol. 101, 7-17. doi: 10.1111/j.1365-2672.2006.02962.x
69. To, M. S., Favrin, S., Romanova, N., and Griffiths, M. W. (2002). Postadaptational resistance to benzalkonium chloride and subsequent physicochemical modifications of Listeria monocytogenes. Appl. Environ. Microbiol. 68, 5258-5264. doi: 10.1128/AEM.68.11.5258-5264.2002
70. Tompkin, R. B. (2002). Control of Listeria monocytogenes in the food-processing environment. J. Food Prot. 65, 709-725.
71. van der Veen, S., and Abee, T. (2010). Importance of SigB for Listeria monocytogenes static and continuous-flow biofilm formation and disinfectant resistance. Appl. Environ. Microbiol. 76, 7854-7860. doi: 10.1128/AEM.01519-10
72. Xu, D., Li, Y., Zahid, M. S., Yamasaki, S., Shi, L., Li, J. R., et al. (2014). Benzalkonium chloride and heavy-metal tolerance in Listeria monocytogenes from retail foods. Int. J. Food Microbiol. 190, 24-30. doi: 10.1016/j.ijfoodmicro.2014.08.017
73. Zhang, H., Zhou, Y., Bao, H., Zhang, L., Wang, R., and Zhou, X. (2015). Plasmid-borne cadmium resistant determinants are associated with the susceptibility of Listeria monocytogenes to bacteriophage. Microbiol. Res. 172, 1-6. doi: 10.1016/j.micres.2015.01.008