Correlation between antibiotic and biocide resistance in mesophilic and psychrotrophic Pseudomonas spp. isolated from slaughterhouse surfaces throughout meat chain production

Food Microbiology

Volumn 51, Issue , 2015, Pages 33-44

  Lavilla Lerma, Leyre ^a   Benomar, Nabil ^a   Casado Muñoz, María del Carmen ^a   Gálvez, Antonio ^a   Abriouel, Hikmate ^a  

^a UNIVERSITY OF JAÉN   (Spain)

Author keywords

Antibiotics; Biocides; ECOFF; Lamb slaughterhouse; Pseudomonas sp.

Indexed keywords

CAPRA HIRCUS; PSEUDOMONAS; PSEUDOMONAS SP.;

ANTIINFECTIVE AGENT; DISINFECTANT AGENT; TOPICAL ANTIINFECTIVE AGENT; TRICLOSAN;

ANIMAL; ANTIBIOTIC RESISTANCE; CLASSIFICATION; DEVICES; DISINFECTION; DRUG EFFECTS; FOOD CONTROL; GOAT; ISOLATION AND PURIFICATION; MEAT; MICROBIAL SENSITIVITY TEST; PHYSIOLOGY; PSEUDOMONAS; SHEEP; SLAUGHTERHOUSE;

ABATTOIRS; ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFECTIVE AGENTS, LOCAL; DISINFECTANTS; DISINFECTION; DRUG RESISTANCE, BACTERIAL; FOOD MICROBIOLOGY; GOATS; MEAT; MICROBIAL SENSITIVITY TESTS; PSEUDOMONAS; SHEEP; TRICLOSAN;

EID: 84929376874     PISSN: 07400020     EISSN: 10959998     Source Type: Journal    
DOI: 10.1016/j.fm.2015.04.010     Document Type: Article

References (44)

1. Aiello A.E., Larson E. Antibacterial cleaning and hygiene products as an emerging risk factor for antibiotic resistance in the community. Lancet Infect. Dis. 2003, 3:501-506.
2. Bhargava H.N., Leonard P.A. Triclosan: applications and safety. Am. J. Infect. Control 1996, 24:209-218.
3. Brauodaki M., Hilton A.C. Mechanisms of resistance in Salmonella enterica adapted to erythromycin, benzalkonium chloride and triclosan. Int. J. Antimicrob. Agents 2005, 25:31-37.
4. Buffet-Bataillon S., Le Jeune A., Le Gall-David S., Bonnaure-Mallet M., Jolivet-Gougeon A. Molecular mechanisms of higher MICs of antibiotics and quaternary ammonium compounds for Escherichia coli isolated from bacteraemia. J.Antimicrob. Chemother. 2012, 67:2837-2842.
5. Chuanchuen R., Beinlich K., Hoang T.T., Becher A., Karkhoff-Schweizer R.R., Schweizer H.P. Crossresistance between triclosan and antibiotics in Pseudomonas aeruginosa is mediated by multidrug efflux pumps: exposure of a susceptible mutant strain to triclosan selects nfxB mutants overexpressing MexCD-OprJ. Antimicrob. Agents Chemother. 2001, 45:428-432.
6. Chuanchuen R., Karkhoff-Schweizer R.R., Schweizer H.P. High-level triclosan resistance in Pseudomonas aeruginosa is solely due to efflux. Am. J. Infect. Control 2003, 31:124-127.
7. Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing, 22nd Informational Supplement 2012, CLSI M100-S22, Clinical and Laboratory Standards Institute, Wayne, PA.
8. Dancey C., Reidy J. Statistics Without Maths for Psychology: Using SPSS for Windows 2004, Prentice Hall, London.
9. Davin-Regli A., Pagès J.M. Cross-resistance between biocides and antimicrobials: an emerging question. Rev. Sci. Tech. 2012, 31:89-104.
10. De Muynck W., De Belie N., Verstraete W. Antimicrobial mortar surfaces for the improvement of hygienic conditions. J.Appl. Microbiol. 2010, 108:62-72.
11. De Oliveira K.M.P., Pericles D.D.S., GRISOLIA A.B. Antimicrobial susceptibility profile of Pseudomonas spp. isolated from a swine slaughterhouse in Dourados, Mato Grosso do Sul State, Brazil. Rev. Argent. Microbiol. 2013, 45:57-60.
12. Du D., Venter H., Pos K.M., Luisi B.F. Microbial Efflux Pumps: Current Research Ch. 3 (Caister Academic, 2013) 2013.
13. Du D., Wang Z., James N.R., Voss J.E., Klimont E., Ohene-Agyei T., Venter H., Chiu W., Luisi B.F. Structure of the AcrAB-TolC multidrug efflux pump. Nature 2014, 509:512-515.
14. EUCAST (European Committee on Antimicrobial Susceptibility Testing) Breakpoint Tablesfor Interpretation of MICs and Zone Diameters. Version 5.0 2013, Eucast.
15. Fraud S., Campigotto A.J., Chen Z., Poole K. MexCD-OprJ multidrug efflux system of Pseudomonas aeruginosa: involvement in chlorhexidine resistance and induction by membrane-damaging agents dependent upon the AlgU stress response sigma factor. Antimicrob. Agents Chemother. 2008, 52:4478-4482.
16. Frimodt-Møller N., Kolmos H.J. Selektion og spredning af antibiotikaresistente bakterier. Ugeskr. Laeg. 2011, 173:2885-2888.
17. Jones R.D., Jampani H.B., Newman J.L., Lee A.S. Triclosan: a review of effectiveness and safety in health care settings. Am. J. Infect. Control 2000, 28:184-196.
18. Kahlmeter G., Brown D.F., Goldstein F.W., MacGowan A.P., Mouton J.W., et al. European harmonization of MIC breakpoints for antimicrobial susceptibility testing of bacteria. J.Antimicrob. Chemother. 2003, 52:145-148.
19. Lavilla Lerma L., Benomar N., Gálvez A., Abriouel H. Prevalence of bacteria resistant to antibiotics and/or biocides on meat processing plant surfaces throughout meat chain production. Int. J. Food Microbiol. 2013, 161:97-106.
20. Lavilla Lerma L., Benomar N., Casado Muñoz M.D., Gálvez A., Abriouel H. Antibiotic multi-resistance analysis of mesophilic and psychrotrophic Pseudomonas sp. isolated from goat and lamb slaughterhouse surfaces throughout meat chain production. Appl. Environ. Microbiol. 2014, 80:6792-6806.
21. Lavilla Lerma L., Benomar N., Knapp C.W., Correa Galeote D., Gálvez A., Abriouel H. Diversity, distribution and quantification of antibiotic resistance genes in goat and lamb slaughterhouse surfaces and meat products. PLoS ONE 2014, 9(12):e114252.
22. Levy S.B. Antibiotic and antiseptic resistance: impact on public health. Pediatr. Infect. Dis. J. 2000, 19:S120-S122.
23. Levy S.B. Antibacterial household products: cause for concern. Emerg. Infect. Dis. 2001, 7:512-515.
24. Livermore D.M. Multiple mechanisms of antimicrobial resistance in Pseudomonas aeruginosa: our worst nightmare?. Clin. Infect. Dis. 2002, 34:634-640.
25. McBain A.J., Rickard A.H., Gilbert P. Possible implications of biocide accumulation in the environment on the prevalence of bacterial antibiotic resistance. J.Ind. Microbiol. 2002, 29:326-330.
26. McMurry L.M., Oethinger M., Levy S.B. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol. Lett. 1998, 166:305-309.
27. Meyer B., Cookson B. Does microbial resistance or adaptation to biocides create a hazard in infection prevention and control?. J.Hosp. Infect. 2010, 76:200-205.
28. Mima T., Joshi S., Gomez-Escalada M., Schweizer H.P. Identification and characterization of TriABC-OpmH, a Triclosan efflux pump of Pseudomonas aeruginosa requiring two membrane fusion proteins. J.Bacteriol. 2007, 189:7600-7609.
29. Morrissey I., Maher K., Hawser S. Activity of iclaprim against clinical isolates of Streptococcus pyogenes and Streptococcus agalactiae. J.Antimicrob. Chemother. 2009, 63:413-414.
30. Morrissey I., Oggioni M.R., Knight D., Curiao T., Coque T., Kalkanci A., Martinez J.L. Evaluation of epidemiological cut-off values indicates that biocide resistant subpopulations are uncommon in natural isolates of clinically-relevant microorganisms. PLoS ONE 2014, 9(1):e86669. BIOHYPO Consortium.
31. Palleroni N.J. Pseudomonas. Topley and Wilson's microbiology and microbial infections 2010, John Wiley and Sons, Ltd.
32. Pfaller M.A., Andesb D., Diekemaa D.J., Espinel-Ingroffc A., Sheehand D. Wild-type MIC distributions, epidemiological cutoff values and species-specific clinical breakpoints for fluconazole and Candida: Time for harmonization of CLSI and EUCAST broth microdilution methods. Drug Resist. Updat. 2010, 13:180-195. The CLSI Subcommittee for Antifungal Susceptibility Testing.
33. Regulation (EU) no 528/2012 of the European Parliament and of the Council of 22 May 2012 Concerning the Making Available on the Market and Use of Biocidal Products, 2012.
34. Romanova N., Favrin S., Griffiths M.W. Sensitivity of Listeria monocytogenes to sanitizers used in the meat processing industry. Appl. Environ. Microbiol. 2002, 68:6405-6409.
35. Russell A.D. Mechanisms of bacterial insusceptibility to biocides. Am. J. Infect. Control 2001, 29:259-261.
36. Russell A.D. Similarities and differences in the responses of microorganisms to biocides. J.Antimicrob. Chemother. 2003, 52:750-763.
37. SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks) Effects of the Active Substances in Biocidal Products on Antibiotic Resistance 2008, 1-83. European Commission, Brussels, Belgium.
38. SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks) Assessment of the Antibiotic Resistance Effects of Biocides 2009, 1-87. European Commission, Brussels, Belgium.
39. SCENIHR (Scientific Committee on Emerging and Newly Identified Health Risks) Research Strategy to Address the Knowledge Gaps on the Antimicrobial Resistance Effects of Biocides 2010, 1-34. European Commission, Brussels, Belgium.
40. Schweizer H.P. Triclosan: a widely used biocide and its link to antibiotics. FEMS Microbiol. Lett. 2001, 202:1-7.
41. Summers A.O. Generally overlooked fundamentals of bacterial genetics and ecology. Clin. Infect. Dis. 2002, 34:S85-S92.
42. Turnidge J., Paterson D.L. Setting and revising antibacterial susceptibility breakpoints. Clin. Microbiol. Rev. 2007, 20:391-408.
43. Vaz-Moreira I., Nunes O.C., Manaia C.M. Diversity and antibiotic resistance in Pseudomonas spp. from drinking water. Sci. Total Environ. 2012, 426:366-374.
44. Yuk H.G., Marshall D.L. Effect of trisodium phosphate adaptation on changes in membrane lipid composition, verotoxin secretion, and acid resistance of Escherichia coli O157:H7 in simulated gastric fluid. Int. J. Food Microbiol. 2006, 106:39-44.