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Resistance of Bacteria to Biocides

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  • Author: Jean-Yves Maillard1
  • Editors: Frank Møller Aarestrup2, Stefan Schwarz3, Jianzhong Shen4, Lina Cavaco5
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Cardiff School of Pharmacy and Pharmaceutical Sciences, Cardiff University, Cardiff CF10 3NB United Kingdom; 2: Technical University of Denmark, Lyngby, Denmark; 3: Freie Universität Berlin, Berlin, Germany; 4: China Agricultural University, Beijing, China; 5: Statens Serum Institute, Copenhagen, Denmark
  • Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.ARBA-0006-2017
  • Received 20 January 2018 Accepted 17 February 2018 Published 19 April 2018
  • Jean-Yves Maillard, [email protected]
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  • Abstract:

    Biocides and formulated biocides are used worldwide for an increasing number of applications despite tightening regulations in Europe and in the United States. One concern is that such intense usage of biocides could lead to increased bacterial resistance to a product and cross-resistance to unrelated antimicrobials including chemotherapeutic antibiotics. Evidence to justify such a concern comes mostly from the use of health care-relevant bacterial isolates, although the number of studies of the resistance characteristics of veterinary isolates to biocides have increased the past few years. One problem remains the definition of “resistance” and how to measure resistance to a biocide. This has yet to be addressed globally, although the measurement of resistance is becoming more pressing, with regulators both in Europe and in the United States demanding that manufacturers provide evidence that their biocidal products will not impact on bacterial resistance. Alongside evidence of potential antimicrobial cross-resistance following biocide exposure, our understanding of the mechanisms of bacterial resistance and, more recently, our understanding of the effect of biocides to induce a mechanism(s) of resistance in bacteria has improved. This article aims to provide an understanding of the development of antimicrobial resistance in bacteria following a biocide exposure. The sections provide evidence of the occurrence of bacterial resistance and its mechanisms of action and debate how to measure bacterial resistance to biocides. Examples pertinent to the veterinary field are used where appropriate.

  • Citation: Maillard J. 2018. Resistance of Bacteria to Biocides. Microbiol Spectrum 6(2):ARBA-0006-2017. doi:10.1128/microbiolspec.ARBA-0006-2017.

References

1. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR). 2009. The antibiotic resistance effect of biocides. http://ec.europa.eu/health/ph_risk/committees/04_scenihr/docs/scenihr_o_021.pdf. Accessed January 2017.
2. Maillard J-Y. 2005. Usage of antimicrobial biocides and products in the healthcare environment: efficacy, policies, management and perceived problems. Ther Clin Risk Manag 1:340–370.
3. Maillard J-Y, Denyer SP. 2009. Emerging bacterial resistance following biocide exposure: should we be concerned? Chim Oggi 27:26–28.
4. O’Neill J. 2016. Tackling Drug-Resistant Infections Globally: Final Report and Recommendations. The Review on Antimicrobial Resistance. HM Government, London, United Kingdom.
5. Otter JA, Yezli S, French GL. 2011. The role played by contaminated surfaces in the transmission of nosocomial pathogens. Infect Control Hosp Epidemiol 32:687–699 http://dx.doi.org/10.1086/660363. [PubMed]
6. Lawley TD, Clare S, Deakin LJ, Goulding D, Yen JL, Raisen C, Brandt C, Lovell J, Cooke F, Clark TG, Dougan G. 2010. Use of purified Clostridium difficile spores to facilitate evaluation of health care disinfection regimens. Appl Environ Microbiol 76:6895–6900 http://dx.doi.org/10.1128/AEM.00718-10. [PubMed]
7. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L, Baric RS, Le Pendu J, Calderon RL. 2008. Norwalk virus: how infectious is it? J Med Virol 80:1468–1476 http://dx.doi.org/10.1002/jmv.21237. [PubMed]
8. Boyce JM, Potter-Bynoe G, Chenevert C, King T. 1997. Environmental contamination due to methicillin-resistant Staphylococcus aureus: possible infection control implications. Infect Control Hosp Epidemiol 18:622–627 http://dx.doi.org/10.1086/502213.
9. Bhalla A, Pultz NJ, Gries DM, Ray AJ, Eckstein EC, Aron DC, Donskey CJ. 2004. Acquisition of nosocomial pathogens on hands after contact with environmental surfaces near hospitalized patients. Infect Control Hosp Epidemiol 25:164–167 http://dx.doi.org/10.1086/502369. [PubMed]
10. Vonberg RP, Kuijper EJ, Wilcox MH, Barbut F, Tüll P, Gastmeier P, van den Broek PJ, Colville A, Coignard B, Daha T, Debast S, Duerden BI, van den Hof S, van der Kooi T, Maarleveld HJ, Nagy E, Notermans DW, O’Driscoll J, Patel B, Stone S, Wiuff C, European C difficile-Infection Control Group, European Centre for Disease Prevention and Control (ECDC). 2008. Infection control measures to limit the spread of Clostridium difficile. Clin Microbiol Infect 14(Suppl 5) :2–20 http://dx.doi.org/10.1111/j.1469-0691.2008.01992.x. [PubMed]
11. Kramer A, Schwebke I, Kampf G. 2006. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect Dis 6:130–138 http://dx.doi.org/10.1186/1471-2334-6-130. [PubMed]
12. Fawley WN, Wilcox MH. 2001. Molecular epidemiology of endemic Clostridium difficile infection. Epidemiol Infect 126:343–350 http://dx.doi.org/10.1017/S095026880100557X. [PubMed]
13. Talon D. 1999. The role of the hospital environment in the epidemiology of multi-resistant bacteria. J Hosp Infect 43:13–17 http://dx.doi.org/10.1053/jhin.1999.0613. [PubMed]
14. Hota B. 2004. Contamination, disinfection, and cross-colonization: are hospital surfaces reservoirs for nosocomial infection? Clin Infect Dis 39:1182–1189 http://dx.doi.org/10.1086/424667. [PubMed]
15. Cheeseman KE, Denyer SP, Hosein IK, Williams GJ, Maillard J-Y. 2009. Evaluation of the bactericidal efficacy of three different alcohol hand rubs against 57 clinical isolates of S. aureus. J Hosp Infect 72:319–325 http://dx.doi.org/10.1016/j.jhin.2009.04.018. [PubMed]
16. Williams GJ, Denyer SP, Hosein IK, Hill DW, Maillard J-Y. 2009. Limitations of the efficacy of surface disinfection in the healthcare setting. Infect Control Hosp Epidemiol 30:570–573 http://dx.doi.org/10.1086/597382. [PubMed]
17. Siani H, Cooper C, Maillard J-Y. 2011. Efficacy of “sporicidal” wipes against Clostridium difficile. Am J Infect Control 39:212–218 http://dx.doi.org/10.1016/j.ajic.2011.01.006. [PubMed]
18. Maillard J-Y, Bloomfield S, Coelho JR, Collier P, Cookson B, Fanning S, Hill A, Hartemann P, McBain AJ, Oggioni M, Sattar S, Schweizer HP, Threlfall J. 2013. Does microbicide use in consumer products promote antimicrobial resistance? A critical review and recommendations for a cohesive approach to risk assessment. Microb Drug Resist 19:344–354 http://dx.doi.org/10.1089/mdr.2013.0039. [PubMed]
19. Department for Environment, Food & Rural Affairs. 2012. Controlling disease in farm animals. https://www.gov.uk/guidance/controlling-disease-in-farm-animals. Accessed January 2017.
20. Pedrouzo M, Borrull F, Marcé RM, Pocurull E. 2009. Ultra-high-performance liquid chromatography-tandem mass spectrometry for determining the presence of eleven personal care products in surface and wastewaters. J Chromatogr A 1216:6994–7000 http://dx.doi.org/10.1016/j.chroma.2009.08.039. [PubMed]
21. Kumar KS, Priya SM, Peck AM, Sajwan KS. 2010. Mass loadings of triclosan and triclocarbon from four wastewater treatment plants to three rivers and landfill in Savannah, Georgia, USA. Arch Environ Contam Toxicol 58:275–285 http://dx.doi.org/10.1007/s00244-009-9383-y.
22. Wilson B, Chen RF, Cantwell M, Gontz A, Zhu J, Olsen CR. 2009. The partitioning of triclosan between aqueous and particulate bound phases in the Hudson River Estuary. Mar Pollut Bull 59:207–212 http://dx.doi.org/10.1016/j.marpolbul.2009.03.026. [PubMed]
23. Scientific Committee on Consumer Safety. 2010. Opinion on triclosan antimicrobial resistance. http://ec.europa.eu/health//sites/health/files/scientific_committees/consumer_safety/docs/sccs_o_054.pdf. Accessed January 2017.
24. Knapp L, Rushton L, Stapleton H, Sass A, Stewart S, Amezquita A, McClure P, Mahenthiralingam E, Maillard J-Y. 2013. The effect of cationic microbicide exposure against Burkholderia cepacia complex (Bcc); the use of Burkholderia lata strain 383 as a model bacterium. J Appl Microbiol 115:1117–1126 http://dx.doi.org/10.1111/jam.12320. [PubMed]
25. Wesgate R, Grasha P, Maillard J-Y. 2016. Use of a predictive protocol to measure the antimicrobial resistance risks associated with biocidal product usage. Am J Infect Control 44:458–464 http://dx.doi.org/10.1016/j.ajic.2015.11.009. [PubMed]
26. Oggioni MR, Furi L, Coelho JR, Maillard JY, Martínez JL. 2013. Recent advances in the potential interconnection between antimicrobial resistance to biocides and antibiotics. Expert Rev Anti Infect Ther 11:363–366 http://dx.doi.org/10.1586/eri.13.16. [PubMed]
27. Cookson B. 2005. Clinical significance of emergence of bacterial antimicrobial resistance in the hospital environment. J Appl Microbiol 99:989–996 http://dx.doi.org/10.1111/j.1365-2672.2005.02693.x. [PubMed]
28. Maillard J-Y. 2007. Bacterial resistance to biocides in the healthcare environment: should it be of genuine concern? J Hosp Infect 65(Suppl 2) :60–72 http://dx.doi.org/10.1016/S0195-6701(07)60018-8.
29. Siani H, Maillard J-Y. 2015. Best practice in healthcare environment decontamination. Eur J Clin Microbiol Infect Dis 34:1–11 http://dx.doi.org/10.1007/s10096-014-2205-9. [PubMed]
30. Chapman JS. 1998. Characterizing bacterial resistance to preservatives and disinfectants. Int Biodeter Biodeg 41:241–245 http://dx.doi.org/10.1016/S0964-8305(98)00025-0.
31. Chapman JS, Diehl MA, Fearnside KB. 1998. Preservative tolerance and resistance. Int J Cosmet Sci 20:31–39 http://dx.doi.org/10.1046/j.1467-2494.1998.171733.x. [PubMed]
32. Hammond SA, Morgan JR, Russell AD. 1987. Comparative susceptibility of hospital isolates of Gram-negative bacteria to antiseptics and disinfectants. J Hosp Infect 9:255–264 http://dx.doi.org/10.1016/0195-6701(87)90122-8. [PubMed]
33. Russell AD. 2003. Biocide use and antibiotic resistance: the relevance of laboratory findings to clinical and environmental situations. Lancet Infect Dis 3:794–803 http://dx.doi.org/10.1016/S1473-3099(03)00833-8. [PubMed]
34. Cloete TE. 2003. Resistance mechanisms of bacteria to antimicrobial compounds. Int Biodeter Biodegrad 51:277–282 http://dx.doi.org/10.1016/S0964-8305(03)00042-8.
35. Dettenkofer M, Wenzler S, Amthor S, Antes G, Motschall E, Daschner FD. 2004. Does disinfection of environmental surfaces influence nosocomial infection rates? A systematic review. Am J Infect Control 32:84–89 http://dx.doi.org/10.1016/j.ajic.2003.07.006. [PubMed]
36. Poole K. 2002. Mechanisms of bacterial biocide and antibiotic resistance. J Appl Microbiol 92(Suppl) :55S–64S http://dx.doi.org/10.1046/j.1365-2672.92.5s1.8.x. [PubMed]
37. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR). 2010. Research strategy to address the knowledge gaps on the antimicrobial resistance effects of biocides. http://ec.europa.eu/health/scientific_committees/emerging/docs/scenihr_o_028.pdf. Accessed January 2017.
38. Scientific Committee on Consumer Safety (SCCS). 2010. Opinion on triclosan antimicrobial resistance. http://ec.europa.eu/health//sites/health/files/scientific_committees/consumer_safety/docs/sccs_o_054.pdf. Accessed January 2017.
39. U.S. Food and Drug Administration. 2016. Safety and effectiveness of consumer antiseptics; topical antimicrobial drug products for over-the-counter human use. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/ucm517478.htm. Accessed January 2017.
40. Lavilla Lerma L, Benomar N, Casado Muñoz MC, Gálvez A, Abriouel H. 2015. Correlation between antibiotic and biocide resistance in mesophilic and psychrotrophic Pseudomonas spp. isolated from slaughterhouse surfaces throughout meat chain production. Food Microbiol 51:33–44 http://dx.doi.org/10.1016/j.fm.2015.04.010. [PubMed]
41. Cowley NL, Forbes S, Amézquita A, McClure P, Humphreys GJ, McBain AJ. 2015. Effects of formulation on microbicide potency and mitigation of the development of bacterial insusceptibility. Appl Environ Microbiol 81:7330–7338 http://dx.doi.org/10.1128/AEM.01985-15. [PubMed]
42. Sasatsu M, Shimizu K, Noguchi N, Kono M. 1993. Triclosan-resistant Staphylococcus aureus. Lancet 341:756 http://dx.doi.org/10.1016/0140-6736(93)90526-M. [PubMed]
43. Heath RJ, Yu YT, Shapiro MA, Olson E, Rock CO. 1998. Broad spectrum antimicrobial biocides target the FabI component of fatty acid synthesis. J Biol Chem 273:30316–30320 http://dx.doi.org/10.1074/jbc.273.46.30316. [PubMed]
44. Bamber AI, Neal TJ. 1999. An assessment of triclosan susceptibility in methicillin-resistant and methicillin-sensitive Staphylococcus aureus. J Hosp Infect 41:107–109 http://dx.doi.org/10.1016/S0195-6701(99)90047-6.
45. Randall LP, Cooles SW, Piddock LJ, Woodward MJ. 2004. Effect of triclosan or a phenolic farm disinfectant on the selection of antibiotic-resistant Salmonella enterica. J Antimicrob Chemother 54:621–627 http://dx.doi.org/10.1093/jac/dkh376. [PubMed]
46. McMurry LM, Oethinger M, Levy SB. 1998. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol Lett 166:305–309 http://dx.doi.org/10.1111/j.1574-6968.1998.tb13905.x. [PubMed]
47. McMurry LM, McDermott PF, Levy SB. 1999. Genetic evidence that InhA of Mycobacterium smegmatis is a target for triclosan. Antimicrob Agents Chemother 43:711–713. [PubMed]
48. Cottell A, Denyer SP, Hanlon GW, Ochs D, Maillard JY. 2009. Triclosan-tolerant bacteria: changes in susceptibility to antibiotics. J Hosp Infect 72:71–76 http://dx.doi.org/10.1016/j.jhin.2009.01.014. [PubMed]
49. Curiao T, Marchi E, Viti C, Oggioni MR, Baquero F, Martinez JL, Coque TM. 2015. Polymorphic variation in susceptibility and metabolism of triclosan-resistant mutants of Escherichia coli and Klebsiella pneumoniae clinical strains obtained after exposure to biocides and antibiotics. Antimicrob Agents Chemother 59:3413–3423 http://dx.doi.org/10.1128/AAC.00187-15. [PubMed]
50. Adair FW, Geftic SG, Gelzer J. 1971. Resistance of Pseudomonas to quaternary ammonium compounds. II. Cross-resistance characteristics of a mutant of Pseudomonas aeruginosa. Appl Microbiol 21:1058–1063. [PubMed]
51. Russell AD. 2002. Introduction of biocides into clinical practice and the impact on antibiotic-resistant bacteria. J Appl Microbiol 92(Suppl) :121S–135S http://dx.doi.org/10.1046/j.1365-2672.92.5s1.12.x. [PubMed]
52. Chapman JS. 2003. Disinfectant resistance mechanisms, cross-resistance, and co-resistance. Int Biodeter Biodegrad 51:271–276 http://dx.doi.org/10.1016/S0964-8305(03)00044-1.
53. Stickler DJ. 1974. Chlorhexidine resistance in Proteus mirabilis. J Clin Pathol 27:284–287 http://dx.doi.org/10.1136/jcp.27.4.284. [PubMed]
54. Gillespie MT, May JW, Skurray RA. 1986. Plasmid-encoded resistance to acriflavine and quaternary ammonium compounds in methicillin-resistant Staphylococcus aureus. FEMS Microbiol Lett 34:47–51 http://dx.doi.org/10.1111/j.1574-6968.1986.tb01346.x.
55. Randall LP, Cooles SW, Sayers AR, Woodward MJ. 2001. Association between cyclohexane resistance in Salmonella of different serovars and increased resistance to multiple antibiotics, disinfectants and dyes. J Med Microbiol 50:919–924 http://dx.doi.org/10.1099/0022-1317-50-10-919.
56. Romão CMCPA, Faria YN, Pereira LR, Asensi MD. 2005. Susceptibility of clinical isolates of multiresistant Pseudomonas aeruginosa to a hospital disinfectant and molecular typing. Mem Inst Oswaldo Cruz 100:541–548 http://dx.doi.org/10.1590/S0074-02762005000500015. [PubMed]
57. Winder CL, Al-Adham IS, Abdel Malek SM, Buultjens TE, Horrocks AJ, Collier PJ. 2000. Outer membrane protein shifts in biocide-resistant Pseudomonas aeruginosa PAO1. J Appl Microbiol 89:289–295 http://dx.doi.org/10.1046/j.1365-2672.2000.01119.x. [PubMed]
58. O’Rourke E, Runyan D, O’Leary J, Stern J. 2003. Contaminated iodophor in the operating room. Am J Infect Control 31:255–256 http://dx.doi.org/10.1067/mic.2003.13. [PubMed]
59. Griffiths PA, Babb JR, Bradley CR, Fraise AP. 1997. Glutaraldehyde-resistant Mycobacterium chelonae from endoscope washer disinfectors. J Appl Microbiol 82:519–526 http://dx.doi.org/10.1046/j.1365-2672.1997.00171.x. [PubMed]
60. van Klingeren B, Pullen W. 1993. Glutaraldehyde resistant mycobacteria from endoscope washers. J Hosp Infect 25:147–149 http://dx.doi.org/10.1016/0195-6701(93)90107-B.
61. Manzoor SE, Lambert PA, Griffiths PA, Gill MJ, Fraise AP. 1999. Reduced glutaraldehyde susceptibility in Mycobacterium chelonae associated with altered cell wall polysaccharides. J Antimicrob Chemother 43:759–765 http://dx.doi.org/10.1093/jac/43.6.759. [PubMed]
62. Fraud S, Maillard J-Y, Russell AD. 2001. Comparison of the mycobactericidal activity of ortho- phthalaldehyde, glutaraldehyde and other dialdehydes by a quantitative suspension test. J Hosp Infect 48:214–221 http://dx.doi.org/10.1053/jhin.2001.1009. [PubMed]
63. Walsh SE, Maillard J-Y, Russell AD, Hann AC. 2001. Possible mechanisms for the relative efficacies of ortho-phthalaldehyde and glutaraldehyde against glutaraldehyde-resistant Mycobacterium chelonae. J Appl Microbiol 91:80–92 http://dx.doi.org/10.1046/j.1365-2672.2001.01341.x. [PubMed]
64. Nomura K, Ogawa M, Miyamoto H, Muratani T, Taniguchi H. 2004. Antibiotic susceptibility of glutaraldehyde-tolerant Mycobacterium chelonae from bronchoscope washing machines. Am J Infect Control 32:185–188 http://dx.doi.org/10.1016/j.ajic.2003.07.007. [PubMed]
65. Martin DJH, Denyer SP, McDonnell G, Maillard J-Y. 2008. Resistance and cross-resistance to oxidising agents of bacterial isolates from endoscope washer disinfectors. J Hosp Infect 69:377–383 http://dx.doi.org/10.1016/j.jhin.2008.04.010. [PubMed]
66. Greenberg JT, Demple B. 1989. A global response induced in Escherichia coli by redox-cycling agents overlaps with that induced by peroxide stress. J Bacteriol 171:3933–3939 http://dx.doi.org/10.1128/jb.171.7.3933-3939.1989. [PubMed]
67. Greenberg JT, Monach P, Chou JH, Josephy PD, Demple B. 1990. Positive control of a global antioxidant defense regulon activated by superoxide-generating agents in Escherichia coli. Proc Natl Acad Sci USA 87:6181–6185 http://dx.doi.org/10.1073/pnas.87.16.6181. [PubMed]
68. Dukan S, Touati D. 1996. Hypochlorous acid stress in Escherichia coli: resistance, DNA damage, and comparison with hydrogen peroxide stress. J Bacteriol 178:6145–6150 http://dx.doi.org/10.1128/jb.178.21.6145-6150.1996. [PubMed]
69. Walsh SE, Maillard J-Y, Russell AD, Catrenich CE, Charbonneau DL, Bartolo RG. 2003. Development of bacterial resistance to several biocides and effects on antibiotic susceptibility. J Hosp Infect 55:98–107 http://dx.doi.org/10.1016/S0195-6701(03)00240-8. [PubMed]
70. Tattawasart U, Maillard J-Y, Furr JR, Russell AD. 1999. Development of resistance to chlorhexidine diacetate and cetylpyridinium chloride in Pseudomonas stutzeri and changes in antibiotic susceptibility. J Hosp Infect 42:219–229 http://dx.doi.org/10.1053/jhin.1999.0591. [PubMed]
71. Thomas L, Maillard J-Y, Lambert RJW, Russell AD. 2000. Development of resistance to chlorhexidine diacetate in Pseudomonas aeruginosa and the effect of a “residual” concentration. J Hosp Infect 46:297–303 http://dx.doi.org/10.1053/jhin.2000.0851. [PubMed]
72. Thomas L, Russell AD, Maillard J-Y. 2005. Antimicrobial activity of chlorhexidine diacetate and benzalkonium chloride against Pseudomonas aeruginosa and its response to biocide residues. J Appl Microbiol 98:533–543 http://dx.doi.org/10.1111/j.1365-2672.2004.02402.x. [PubMed]
73. Molina-González D, Alonso-Calleja C, Alonso-Hernando A, Capita R. 2014. Effect of sub-lethal concentrations of biocides on the susceptibility to antibiotics of multi-drug resistant Salmonella enterica strains. Food Control 40:329–334 http://dx.doi.org/10.1016/j.foodcont.2013.11.046.
74. Duarte RS, Lourenço MCS, Fonseca LS, Leão SC, Amorim EL, Rocha IL, Coelho FS, Viana-Niero C, Gomes KM, da Silva MG, Lorena NS, Pitombo MB, Ferreira RM, Garcia MH, de Oliveira GP, Lupi O, Vilaça BR, Serradas LR, Chebabo A, Marques EA, Teixeira LM, Dalcolmo M, Senna SG, Sampaio JL. 2009. Epidemic of postsurgical infections caused by Mycobacterium massiliense. J Clin Microbiol 47:2149–2155 http://dx.doi.org/10.1128/JCM.00027-09. [PubMed]
75. Wisplinghoff H, Schmitt R, Wöhrmann A, Stefanik D, Seifert H. 2007. Resistance to disinfectants in epidemiologically defined clinical isolates of Acinetobacter baumannii. J Hosp Infect 66:174–181 http://dx.doi.org/10.1016/j.jhin.2007.02.016. [PubMed]
76. Bock LJ, Wand ME, Sutton JM. 2016. Varying activity of chlorhexidine-based disinfectants against Klebsiella pneumoniae clinical isolates and adapted strains. J Hosp Infect 93:42–48 http://dx.doi.org/10.1016/j.jhin.2015.12.019. [PubMed]
77. Liu Q, Zhao H, Han L, Shu W, Wu Q, Ni Y. 2015. Frequency of biocide-resistant genes and susceptibility to chlorhexidine in high-level mupirocin-resistant, methicillin-resistant Staphylococcus aureus (MuH MRSA). Diagn Microbiol Infect Dis 82:278–283 http://dx.doi.org/10.1016/j.diagmicrobio.2015.03.023. [PubMed]
78. Hijazi K, Mukhopadhya I, Abbott F, Milne K, Al-Jabri ZJ, Oggioni MR, Gould IM. 2016. Susceptibility to chlorhexidine amongst multidrug-resistant clinical isolates of Staphylococcus epidermidis from bloodstream infections. Int J Antimicrob Agents 48:86–90 http://dx.doi.org/10.1016/j.ijantimicag.2016.04.015. [PubMed]
79. Conceição T, Coelho C, de Lencastre H, Aires-de-Sousa M. 2015. High prevalence of biocide resistance determinants in Staphylococcus aureus isolates from three African countries. Antimicrob Agents Chemother 60:678–681 http://dx.doi.org/10.1128/AAC.02140-15. [PubMed]
80. Lear JC, Maillard J-Y, Dettmar PW, Goddard PA, Russell AD. 2002. Chloroxylenol- and triclosan-tolerant bacteria from industrial sources. J Ind Microbiol Biotechnol 29:238–242 http://dx.doi.org/10.1038/sj.jim.7000320. [PubMed]
81. Lavilla Lerma L, Benomar N, Gálvez A, Abriouel H. 2013. Prevalence of bacteria resistant to antibiotics and/or biocides on meat processing plant surfaces throughout meat chain production. Int J Food Microbiol 161:97–106 http://dx.doi.org/10.1016/j.ijfoodmicro.2012.11.028. [PubMed]
82. Grande Burgos MJ, Fernández Márquez ML, Pérez Pulido R, Gálvez A, Lucas López R. 2016. Virulence factors and antimicrobial resistance in Escherichia coli strains isolated from hen egg shells. Int J Food Microbiol 238:89–95 http://dx.doi.org/10.1016/j.ijfoodmicro.2016.08.037. [PubMed]
83. 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 http://dx.doi.org/10.3389/fmicb.2016.00638. [PubMed]
84. Sanford JP. 1970. Disinfectants that don’t. Ann Intern Med 72:282–283 http://dx.doi.org/10.7326/0003-4819-72-2-282. [PubMed]
85. Prince J, Ayliffe GAJ. 1972. In-use testing of disinfectants in hospitals. J Clin Pathol 25:586–589 http://dx.doi.org/10.1136/jcp.25.7.586. [PubMed]
86. Bridges K, Lowbury EJL. 1977. Drug resistance in relation to use of silver sulphadiazine cream in a burns unit. J Clin Pathol 30:160–164 http://dx.doi.org/10.1136/jcp.30.2.160. [PubMed]
87. Klasen HJ. 2000. A historical review of the use of silver in the treatment of burns. II. Renewed interest for silver. Burns 26:131–138 http://dx.doi.org/10.1016/S0305-4179(99)00116-3. [PubMed]
88. Reiss I, Borkhardt A, Füssle R, Sziegoleit A, Gortner L. 2000. Disinfectant contaminated with Klebsiella oxytoca as a source of sepsis in babies. Lancet 356:310 http://dx.doi.org/10.1016/S0140-6736(00)02509-5. [PubMed]
89. Weber DJ, Rutala WA, Sickbert-Bennett EE. 2007. Outbreaks associated with contaminated antiseptics and disinfectants. Antimicrob Agents Chemother 51:4217–4224 http://dx.doi.org/10.1128/AAC.00138-07. [PubMed]
90. Aiello AE, Marshall B, Levy SB, Della-Latta P, Larson E. 2004. Relationship between triclosan and susceptibilities of bacteria isolated from hands in the community. Antimicrob Agents Chemother 48:2973–2979 http://dx.doi.org/10.1128/AAC.48.8.2973-2979.2004. [PubMed]
91. Cole EC, Addison RM, Rubino JR, Leese KE, Dulaney PD, Newell MS, Wilkins J, Gaber DJ, Wineinger T, Criger DA. 2003. Investigation of antibiotic and antibacterial agent cross-resistance in target bacteria from homes of antibacterial product users and nonusers. J Appl Microbiol 95:664–676 http://dx.doi.org/10.1046/j.1365-2672.2003.02022.x. [PubMed]
92. Cole EC, Addison RM, Dulaney PD, Leese KE, Madanat HM, Guffey AM. 2011. Investigation of antibiotic and antibacterial susceptibility and resistance in Staphylococcus form the skin of users and non-users of antibacterial wash products in home environments. Int J Microbiol Res 3:90–96 http://dx.doi.org/10.9735/0975-5276.3.2.90-96.
93. Carson RT, Larson E, Levy SB, Marshall BM, Aiello AE. 2008. Use of antibacterial consumer products containing quaternary ammonium compounds and drug resistance in the community. J Antimicrob Chemother 62:1160–1162 http://dx.doi.org/10.1093/jac/dkn332. [PubMed]
94. Alonso-Calleja C, Guerrero-Ramos E, Alonso-Hernando A, Capita R. 2015. Adaptation and cross-adaptation of Escherichia coli ATCC 12806 to several food-grade biocides. Food Control 56:86–94 http://dx.doi.org/10.1016/j.foodcont.2015.03.012.
95. Ciusa ML, Furi L, Knight D, Decorosi F, Fondi M, Raggi C, Coelho JR, Aragones L, Moce L, Visa P, Freitas AT, Baldassarri L, Fani R, Viti C, Orefici G, Martinez JL, Morrissey I, Oggioni MR, BIOHYPO Consortium. 2012. A novel resistance mechanism to triclosan that suggests horizontal gene transfer and demonstrates a potential selective pressure for reduced biocide susceptibility in clinical strains of Staphylococcus aureus. Int J Antimicrob Agents 40:210–220 http://dx.doi.org/10.1016/j.ijantimicag.2012.04.021. [PubMed]
96. Martin DJH, Wesgate RL, Denyer SP, McDonnell G, Maillard J-Y. 2015. Bacillus subtilis vegetative isolate surviving chlorine dioxide exposure: an elusive mechanism of resistance. J Appl Microbiol 119:1541–1551 http://dx.doi.org/10.1111/jam.12963. [PubMed]
97. Bridier A, Le Coq D, del Pilar Sanchez-Vizuete M, Aymerich S, Meylheuc T, Maillard J-Y, Thomas V, Dubois-Brissonnet F, Briandet R. 2012. Biofilms of a Bacillus subtilis endoscope WD isolate that protect Staphylococcus aureus from peracetic acid. PLoS One 7:e44506 http://dx.doi.org/10.1371/journal.pone.0044506. [PubMed]
98. Lear JC, Maillard J-Y, Dettmar PW, Goddard PA, Russell AD. 2006. Chloroxylenol- and triclosan-tolerant bacteria from industrial sources: susceptibility to antibiotics and other biocides. Int Biodeter Biodegrad 57:51–56 http://dx.doi.org/10.1016/j.ibiod.2005.11.002.
99. Fisher CW, Fiorello A, Shaffer D, Jackson M, McDonnell GE. 2012. Aldehyde-resistant mycobacteria bacteria associated with the use of endoscope reprocessing systems. Am J Infect Control 40:880–882 http://dx.doi.org/10.1016/j.ajic.2011.11.004. [PubMed]
100. Alvarado CJ, Stolz SM, Maki DG, Centers for Disease Control (CDC). 1991. Nosocomial infection and pseudoinfection from contaminated endoscopes and bronchoscopes—Wisconsin and Missouri. MMWR Morb Mortal Wkly Rep 40:675–678.
101. Denyer SP, Stewart GSAB. 1998. Mechanisms of action of disinfectants. Int Biodeter Biodegrad 41:261–268 http://dx.doi.org/10.1016/S0964-8305(98)00023-7.
102. Maillard J-Y. 2002. Bacterial target sites for biocide action. J Appl Microbiol 92(Suppl) :16S–27S http://dx.doi.org/10.1046/j.1365-2672.92.5s1.3.x. [PubMed]
103. Denyer SP, Maillard J-Y. 2002. Cellular impermeability and uptake of biocides and antibiotics in Gram-negative bacteria. J Appl Microbiol 92(Suppl) :35S–45S http://dx.doi.org/10.1046/j.1365-2672.92.5s1.19.x. [PubMed]
104. Lambert PA. 2002. Cellular impermeability and uptake of biocides and antibiotics in Gram-positive bacteria and mycobacteria. J Appl Microbiol 92(Suppl) :46S–54S http://dx.doi.org/10.1046/j.1365-2672.92.5s1.7.x. [PubMed]
105. McDonnell G, Russell AD. 1999. Antiseptics and disinfectants: activity, action, and resistance. Clin Microbiol Rev 12:147–179. [PubMed]
106. Leggett MJ, Schwarz JS, Burke PA, Mcdonnell G, Denyer SP, Maillard J-Y. 2015. Resistance to and killing by the sporicidal microbicide peracetic acid. J Antimicrob Chemother 70:773–779 http://dx.doi.org/10.1093/jac/dku445. [PubMed]
107. Munton TJ, Russell AD. 1970. Effect of glutaraldehyde on protoplasts of Bacillus megaterium. J Gen Microbiol 63:367–370 http://dx.doi.org/10.1099/00221287-63-3-367. [PubMed]
108. Ayres HM, Payne DN, Furr JR, Russell AD. 1998. Effect of permeabilizing agents on antibacterial activity against a simple Pseudomonas aeruginosa biofilm. Lett Appl Microbiol 27:79–82 http://dx.doi.org/10.1046/j.1472-765X.1998.00397.x. [PubMed]
109. Codling CE, Jones BV, Mahenthiralingam E, Russell AD, Maillard J-Y. 2004. Identification of genes involved in the susceptibility of Serratia marcescens to polyquaternium-1. J Antimicrob Chemother 54:370–375 http://dx.doi.org/10.1093/jac/dkh351. [PubMed]
110. Walsh SE, Maillard J-Y, Russell AD, Hann AC. 2001. Possible mechanisms for the relative efficacies of ortho-phthalaldehyde and glutaraldehyde against glutaraldehyde-resistant Mycobacterium chelonae. J Appl Microbiol 91:80–92 http://dx.doi.org/10.1046/j.1365-2672.2001.01341.x. [PubMed]
111. McNeil MR, Brennan PJ. 1991. Structure, function and biogenesis of the cell envelope of mycobacteria in relation to bacterial physiology, pathogenesis and drug resistance; some thoughts and possibilities arising from recent structural information. Res Microbiol 142:451–463 http://dx.doi.org/10.1016/0923-2508(91)90120-Y.
112. Broadley SJ, Jenkins PA, Furr JR, Russell AD. 1995. Potentiation of the effects of chlorhexidine diacetate and cetylpyridinium chloride on mycobacteria by ethambutol. J Med Microbiol 43:458–460 http://dx.doi.org/10.1099/00222615-43-6-458. [PubMed]
113. Fraud S, Hann AC, Maillard J-Y, Russell AD. 2003. Effects of ortho-phthalaldehyde, glutaraldehyde and chlorhexidine diacetate on Mycobacterium chelonae and Mycobacterium abscessus strains with modified permeability. J Antimicrob Chemother 51:575–584 http://dx.doi.org/10.1093/jac/dkg099. [PubMed]
114. Svetlíková Z, Skovierová H, Niederweis M, Gaillard J-L, McDonnell G, Jackson M. 2009. Role of porins in the susceptibility of Mycobacterium smegmatis and Mycobacterium chelonae to aldehyde-based disinfectants and drugs. Antimicrob Agents Chemother 53:4015–4018 http://dx.doi.org/10.1128/AAC.00590-09. [PubMed]
115. Tattawasart U, Maillard JY, Furr JR, Russell AD, Russell AD. 2000. Outer membrane changes in Pseudomonas stutzeri resistant to chlorhexidine diacetate and cetylpyridinium chloride. Int J Antimicrob Agents 16:233–238 http://dx.doi.org/10.1016/S0924-8579(00)00206-5.
116. Fernández-Cuenca F, Tomás M, Caballero-Moyano FJ, Bou G, Martínez-Martínez L, Vila J, Pachón J, Cisneros JM, Rodríguez-Baño J, Pascual Á, Spanish Group of Nosocomial Infections (GEIH) from the Spanish Society of Clinical Microbiology and Infectious Diseases (SEIMC) and the Spanish Network for Research in Infectious Diseases (REIPI), Spanish Group of Nosocomial Infections GEIH from the Spanish Society of Clinical Microbiology and Infectious Diseases SEIMC and the Spanish Network for Research in Infectious Diseases REIPI. 2015. Reduced susceptibility to biocides in Acinetobacter baumannii: association with resistance to antimicrobials, epidemiological behaviour, biological cost and effect on the expression of genes encoding porins and efflux pumps. J Antimicrob Chemother 70:3222–3229. [PubMed]
117. Tattawasart U, Hann AC, Maillard J-Y, Furr JR, Russell AD. 2000. Cytological changes in chlorhexidine-resistant isolates of Pseudomonas stutzeri. J Antimicrob Chemother 45:145–152 http://dx.doi.org/10.1093/jac/45.2.145. [PubMed]
118. Braoudaki M, Hilton AC. 2005. Mechanisms of resistance in Salmonella enterica adapted to erythromycin, benzalkonium chloride and triclosan. Int J Antimicrob Agents 25:31–37 http://dx.doi.org/10.1016/j.ijantimicag.2004.07.016. [PubMed]
119. Pagès JM, James CE, Winterhalter M. 2008. The porin and the permeating antibiotic: a selective diffusion barrier in Gram-negative bacteria. Nat Rev Microbiol 6:893–903 http://dx.doi.org/10.1038/nrmicro1994. [PubMed]
120. Nikaido H. 2003. Molecular basis of bacterial outer membrane permeability revisited. Microbiol Mol Biol Rev 67:593–656 http://dx.doi.org/10.1128/MMBR.67.4.593-656.2003. [PubMed]
121. Gandhi PA, Sawant AD, Wilson LA, Ahearn DG. 1993. Adaptation and growth of Serratia marcescens in contact lens disinfectant solutions containing chlorhexidine gluconate. Appl Environ Microbiol 59:183–188. [PubMed]
122. Brözel VS, Cloete TE. 1994. Resistance of Pseudomonas aeruginosa to isothiazolone. J Appl Bacteriol 76:576–582 http://dx.doi.org/10.1111/j.1365-2672.1994.tb01655.x. [PubMed]
123. Jones MV, Herd TM, Christie HJ. 1989. Resistance of Pseudomonas aeruginosa to amphoteric and quaternary ammonium biocides. Microbios 58:49–61. [PubMed]
124. Méchin L, Dubois-Brissonnet F, Heyd B, Leveau JY. 1999. Adaptation of Pseudomonas aeruginosa ATCC 15442 to didecyldimethylammonium bromide induces changes in membrane fatty acid composition and in resistance of cells. J Appl Microbiol 86:859–866 http://dx.doi.org/10.1046/j.1365-2672.1999.00770.x. [PubMed]
125. Guérin-Méchin L, Dubois-Brissonnet F, Heyd B, Leveau JY. 1999. Specific variations of fatty acid composition of Pseudomonas aeruginosa ATCC 15442 induced by quaternary ammonium compounds and relation with resistance to bactericidal activity. J Appl Microbiol 87:735–742 http://dx.doi.org/10.1046/j.1365-2672.1999.00919.x. [PubMed]
126. Guérin-Méchin L, Dubois-Brissonnet F, Heyd B, Leveau JY. 2000. Quaternary ammonium compound stresses induce specific variations in fatty acid composition of Pseudomonas aeruginosa. Int J Food Microbiol 55:157–159 http://dx.doi.org/10.1016/S0168-1605(00)00189-6.
127. Tkachenko O, Shepard J, Aris VM, Joy A, Bello A, Londono I, Marku J, Soteropoulos P, Peteroy-Kelly MA. 2007. A triclosan-ciprofloxacin cross-resistant mutant strain of Staphylococcus aureus displays an alteration in the expression of several cell membrane structural and functional genes. Res Microbiol 158:651–658 http://dx.doi.org/10.1016/j.resmic.2007.09.003. [PubMed]
128. Boeris PS, Domenech CE, Lucchesi GI. 2007. Modification of phospholipid composition in Pseudomonas putida A ATCC 12633 induced by contact with tetradecyltrimethylammonium. J Appl Microbiol 103:1048–1054 http://dx.doi.org/10.1111/j.1365-2672.2007.03346.x. [PubMed]
129. Bruinsma GM, Rustema-Abbing M, van der Mei HC, Lakkis C, Busscher HJ. 2006. Resistance to a polyquaternium-1 lens care solution and isoelectric points of Pseudomonas aeruginosa strains. J Antimicrob Chemother 57:764–766 http://dx.doi.org/10.1093/jac/dkl011. [PubMed]
130. Lyon BR, Skurray R. 1987. Antimicrobial resistance of Staphylococcus aureus: genetic basis. Microbiol Rev 51:88–134. [PubMed]
131. Tennent JM, Lyon BR, Midgley M, Jones IG, Purewal AS, Skurray RA. 1989. Physical and biochemical characterization of the qacA gene encoding antiseptic and disinfectant resistance in Staphylococcus aureus. J Gen Microbiol 135:1–10. [PubMed]
132. Littlejohn TG, Paulsen IT, Gillespie MT, Tennent JM, Midgley M, Jones IG, Purewal AS, Skurray RA. 1992. Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol Lett 74:259–265 http://dx.doi.org/10.1111/j.1574-6968.1992.tb05376.x. [PubMed]
133. Leelaporn A, Paulsen IT, Tennent JM, Littlejohn TG, Skurray RA. 1994. Multidrug resistance to antiseptics and disinfectants in coagulase-negative staphylococci. J Med Microbiol 40:214–220 http://dx.doi.org/10.1099/00222615-40-3-214. [PubMed]
134. Heir E, Sundheim G, Holck AL. 1998. The Staphylococcus qacH gene product: a new member of the SMR family encoding multidrug resistance. FEMS Microbiol Lett 163:49–56 http://dx.doi.org/10.1111/j.1574-6968.1998.tb13025.x. [PubMed]
135. Heir E, Sundheim G, Holck AL. 1999. The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J Appl Microbiol 86:378–388 http://dx.doi.org/10.1046/j.1365-2672.1999.00672.x. [PubMed]
136. Rouch DA, Cram DS, DiBerardino D, Littlejohn TG, Skurray RA. 1990. Efflux-mediated antiseptic resistance gene qacA from Staphylococcus aureus: common ancestry with tetracycline- and sugar-transport proteins. Mol Microbiol 4:2051–2062 http://dx.doi.org/10.1111/j.1365-2958.1990.tb00565.x. [PubMed]
137. Huet AA, Raygada JL, Mendiratta K, Seo SM, Kaatz GW. 2008. Multidrug efflux pump overexpression in Staphylococcus aureus after single and multiple in vitro exposures to biocides and dyes. Microbiology 154:3144–3153 http://dx.doi.org/10.1099/mic.0.2008/021188-0. [PubMed]
138. Schindler BD, Kaatz GW. 2016. Multidrug efflux pumps of Gram-positive bacteria. Drug Resist Updat 27:1–13 http://dx.doi.org/10.1016/j.drup.2016.04.003. [PubMed]
139. Santos Costa S, Viveiros M, Rosato AE, Melo-Cristino J, Couto I. 2015. Impact of efflux in the development of multidrug resistance phenotypes in Staphylococcus aureus. BMC Microbiol 15:232 http://dx.doi.org/10.1186/s12866-015-0572-8. [PubMed]
140. Chuanchuen R, Beinlich K, Hoang TT, Becher A, Karkhoff-Schweizer RR, Schweizer HP. 2001. Cross-resistance 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 45:428–432 http://dx.doi.org/10.1128/AAC.45.2.428-432.2001. [PubMed]
141. Chuanchuen R, Narasaki CT, Schweizer HP. 2002. The MexJK efflux pump of Pseudomonas aeruginosa requires OprM for antibiotic efflux but not for efflux of triclosan. J Bacteriol 184:5036–5044 http://dx.doi.org/10.1128/JB.184.18.5036-5044.2002. [PubMed]
142. Mima T, Joshi S, Gomez-Escalada M, Schweizer HP. 2007. Identification and characterization of TriABC-OpmH, a triclosan efflux pump of Pseudomonas aeruginosa requiring two membrane fusion proteins. J Bacteriol 189:7600–7609 http://dx.doi.org/10.1128/JB.00850-07. [PubMed]
143. Schweizer HP. 1998. Intrinsic resistance to inhibitors of fatty acid biosynthesis in Pseudomonas aeruginosa is due to efflux: application of a novel technique for generation of unmarked chromosomal mutations for the study of efflux systems. Antimicrob Agents Chemother 42:394–398. [PubMed]
144. Chuanchuen R, Karkhoff-Schweizer RR, Schweizer HP. 2003. High-level triclosan resistance in Pseudomonas aeruginosa is solely a result of efflux. Am J Infect Control 31:124–127 http://dx.doi.org/10.1067/mic.2003.11. [PubMed]
145. Morita Y, Murata T, Mima T, Shiota S, Kuroda T, Mizushima T, Gotoh N, Nishino T, Tsuchiya T. 2003. Induction of mexCD-oprJ operon for a multidrug efflux pump by disinfectants in wild-type Pseudomonas aeruginosa PAO1. J Antimicrob Chemother 51:991–994 http://dx.doi.org/10.1093/jac/dkg173. [PubMed]
146. Moken MC, McMurry LM, Levy SB. 1997. Selection of multiple-antibiotic-resistant (mar) mutants of Escherichia coli by using the disinfectant pine oil: roles of the mar and acrAB loci. Antimicrob Agents Chemother 41:2770–2772. [PubMed]
147. Nishino K, Yamaguchi A. 2001. Analysis of a complete library of putative drug transporter genes in Escherichia coli. J Bacteriol 183:5803–5812 http://dx.doi.org/10.1128/JB.183.20.5803-5812.2001. [PubMed]
148. Lomovskaya O, Lewis K. 1992. Emr, an Escherichia coli locus for multidrug resistance. Proc Natl Acad Sci USA 89:8938–8942 http://dx.doi.org/10.1073/pnas.89.19.8938. [PubMed]
149. Davin-Regli A, Bolla JM, James CE, Lavigne JP, Chevalier J, Garnotel E, Molitor A, Pagès JM. 2008. Membrane permeability and regulation of drug “influx and efflux” in enterobacterial pathogens. Curr Drug Targets 9:750–759 http://dx.doi.org/10.2174/138945008785747824. [PubMed]
150. Randall LP, Cooles SW, Coldham NG, Penuela EG, Mott AC, Woodward MJ, Piddock LJ, Webber MA. 2007. Commonly used farm disinfectants can select for mutant Salmonella enterica serovar Typhimurium with decreased susceptibility to biocides and antibiotics without compromising virulence. J Antimicrob Chemother 60:1273–1280 http://dx.doi.org/10.1093/jac/dkm359. [PubMed]
151. Webber MA, Randall LP, Cooles S, Woodward MJ, Piddock LJ. 2008. Triclosan resistance in Salmonella enterica serovar Typhimurium. J Antimicrob Chemother 62:83–91 http://dx.doi.org/10.1093/jac/dkn137. [PubMed]
152. Rajamohan G, Srinivasan VB, Gebreyes WA. 2010. Novel role of Acinetobacter baumannii RND efflux transporters in mediating decreased susceptibility to biocides. J Antimicrob Chemother 65:228–232 http://dx.doi.org/10.1093/jac/dkp427. [PubMed]
153. Piddock LJ. 2006. Clinically relevant chromosomally encoded multidrug resistance efflux pumps in bacteria. Clin Microbiol Rev 19:382–402 http://dx.doi.org/10.1128/CMR.19.2.382-402.2006. [PubMed]
154. Noguchi N, Suwa J, Narui K, Sasatsu M, Ito T, Hiramatsu K, Song JH. 2005. Susceptibilities to antiseptic agents and distribution of antiseptic-resistance genes qacA/B and smr of methicillin-resistant Staphylococcus aureus isolated in Asia during 1998 and 1999. J Med Microbiol 54:557–565 http://dx.doi.org/10.1099/jmm.0.45902-0. [PubMed]
155. Sánchez MB, Decorosi F, Viti C, Oggioni MR, Martínez JL, Hernández A. 2015. Predictive studies suggest that the risk for the selection of antibiotic resistance by biocides is likely low in Stenotrophomonas maltophilia. PLoS One 10:e0132816 http://dx.doi.org/10.1371/journal.pone.0132816. [PubMed]
156. Poole K. 2007. Efflux pumps as antimicrobial resistance mechanisms. Ann Med 39:162–176 http://dx.doi.org/10.1080/07853890701195262. [PubMed]
157. Brown MH, Paulsen IT, Skurray RA. 1999. The multidrug efflux protein NorM is a prototype of a new family of transporters. Mol Microbiol 31:394–395 http://dx.doi.org/10.1046/j.1365-2958.1999.01162.x. [PubMed]
158. Borges-Walmsley MI, Walmsley AR. 2001. The structure and function of drug pumps. Trends Microbiol 9:71–79 http://dx.doi.org/10.1016/S0966-842X(00)01920-X. [PubMed]
159. Poole K. 2001. Multidrug resistance in Gram-negative bacteria. Curr Opin Microbiol 4:500–508 http://dx.doi.org/10.1016/S1369-5274(00)00242-3.
160. Poole K. 2002. Outer membranes and efflux: the path to multidrug resistance in Gram-negative bacteria. Curr Pharm Biotechnol 3:77–98 http://dx.doi.org/10.2174/1389201023378454. [PubMed]
161. Buffet-Bataillon S, Tattevin P, Maillard J-Y, Bonnaure-Mallet M, Jolivet-Gougeon A. 2016. Efflux pump induction by quaternary ammonium compounds and fluoroquinolone resistance in bacteria. Future Microbiol 11:81–92 http://dx.doi.org/10.2217/fmb.15.131. [PubMed]
162. Bailey AM, Constantinidou C, Ivens A, Garvey MI, Webber MA, Coldham N, Hobman JL, Wain J, Woodward MJ, Piddock LJ. 2009. Exposure of Escherichia coli and Salmonella enterica serovar Typhimurium to triclosan induces a species-specific response, including drug detoxification. J Antimicrob Chemother 64:973–985 http://dx.doi.org/10.1093/jac/dkp320. [PubMed]
163. Randall LP, Cooles SW, Coldham NG, Penuela EG, Mott AC, Woodward MJ, Piddock LJ, Webber MA. 2007. Commonly used farm disinfectants can select for mutant Salmonella enterica serovar Typhimurium with decreased susceptibility to biocides and antibiotics without compromising virulence. J Antimicrob Chemother 60:1273–1280 http://dx.doi.org/10.1093/jac/dkm359. [PubMed]
164. Webber MA, Randall LP, Cooles S, Woodward MJ, Piddock LJ. 2008. Triclosan resistance in Salmonella enterica serovar Typhimurium. J Antimicrob Chemother 62:83–91 http://dx.doi.org/10.1093/jac/dkn137. [PubMed]
165. Buckley AM, Webber MA, Cooles S, Randall LP, La Ragione RM, Woodward MJ, Piddock LJ. 2006. The AcrAB-TolC efflux system of Salmonella enterica serovar Typhimurium plays a role in pathogenesis. Cell Microbiol 8:847–856 http://dx.doi.org/10.1111/j.1462-5822.2005.00671.x. [PubMed]
166. Sánchez P, Moreno E, Martinez JL. 2005. The biocide triclosan selects Stenotrophomonas maltophilia mutants that overproduce the SmeDEF multidrug efflux pump. Antimicrob Agents Chemother 49:781–782 http://dx.doi.org/10.1128/AAC.49.2.781-782.2005. [PubMed]
167. Pumbwe L, Randall LP, Woodward MJ, Piddock LJV. 2004. Expression of the efflux pump genes cmeB, cmeF and the porin gene porA in multiple-antibiotic-resistant Campylobacter jejuni. J Antimicrob Chemother 54:341–347 http://dx.doi.org/10.1093/jac/dkh331. [PubMed]
168. Demple B. 1996. Redox signaling and gene control in the Escherichia coli soxRS oxidative stress regulon: a review. Gene 179:53–57 http://dx.doi.org/10.1016/S0378-1119(96)00329-0.
169. Hutchinson J, Runge W, Mulvey M, Norris G, Yetman M, Valkova N, Villemur R, Lepine F. 2004. Burkholderia cepacia infections associated with intrinsically contaminated ultrasound gel: the role of microbial degradation of parabens. Infect Control Hosp Epidemiol 25:291–296 http://dx.doi.org/10.1086/502394. [PubMed]
170. Valkova N, Lépine F, Valeanu L, Dupont M, Labrie L, Bisaillon JG, Beaudet R, Shareck F, Villemur R. 2001. Hydrolysis of 4-hydroxybenzoic acid esters (parabens) and their aerobic transformation into phenol by the resistant Enterobacter cloacae strain EM. Appl Environ Microbiol 67:2404–2409 http://dx.doi.org/10.1128/AEM.67.6.2404-2409.2001. [PubMed]
171. Kümmerle N, Feucht HH, Kaulfers PM. 1996. Plasmid-mediated formaldehyde resistance in Escherichia coli: characterization of resistance gene. Antimicrob Agents Chemother 40:2276–2279. [PubMed]
172. Gomez Escalada M, Russell AD, Maillard J-Y, Ochs D. 2005. Triclosan- bacteria interactions: single or multiple target sites? Lett Appl Microbiol 41:476–481. [PubMed]
173. Wu VCH. 2008. A review of microbial injury and recovery methods in food. Food Microbiol 25:735–744 http://dx.doi.org/10.1016/j.fm.2008.04.011. [PubMed]
174. Lambert RJW, van der Ouderaa M-LH. 1999. An investigation into the differences between the Bioscreen and the traditional plate count disinfectant test methods. J Appl Microbiol 86:689–694 http://dx.doi.org/10.1046/j.1365-2672.1999.00712.x. [PubMed]
175. Brown MRW, Williams P. 1985. Influence of substrate limitation and growth phase on sensitivity to antimicrobial agents. J Antimicrob Chemother 15(Suppl A) :7–14 http://dx.doi.org/10.1093/jac/15.suppl_A.7. [PubMed]
176. Wright NE, Gilbert P. 1987. Influence of specific growth rate and nutrient limitation upon the sensitivity of Escherichia coli towards chlorhexidine diacetate. J Appl Bacteriol 62:309–314 http://dx.doi.org/10.1111/j.1365-2672.1987.tb04925.x. [PubMed]
177. Gomez Escalada M, Harwood JL, Maillard J-Y, Ochs D. 2005. Triclosan inhibition of fatty acid synthesis and its effect on growth of E. coli and Ps. aeruginosa. J Antimicrob Chemother 55:879–882 http://dx.doi.org/10.1093/jac/dki123. [PubMed]
178. McMurry LM, Oethinger M, Levy SB. 1998. Triclosan targets lipid synthesis. Nature 394:531–532 http://dx.doi.org/10.1038/28970. [PubMed]
179. Levy CW, Roujeinikova A, Sedelnikova S, Baker PJ, Stuitje AR, Slabas AR, Rice DW, Rafferty JB. 1999. Molecular basis of triclosan activity. Nature 398:383–384 http://dx.doi.org/10.1038/18803. [PubMed]
180. Webber MA, Coldham NG, Woodward MJ, Piddock LJV. 2008. Proteomic analysis of triclosan resistance in Salmonella enterica serovar Typhimurium. J Antimicrob Chemother 62:92–97 http://dx.doi.org/10.1093/jac/dkn138. [PubMed]
181. Curiao T, Marchi E, Grandgirard D, León-Sampedro R, Viti C, Leib SL, Baquero F, Oggioni MR, Martinez JL, Coque TM. 2016. Multiple adaptive routes of Salmonella enterica Typhimurium to biocide and antibiotic exposure. BMC Genomics 17:491 http://dx.doi.org/10.1186/s12864-016-2778-z. [PubMed]
182. Seaman PF, Ochs D, Day MJ. 2007. Small-colony variants: a novel mechanism for triclosan resistance in methicillin-resistant Staphylococcus aureus. J Antimicrob Chemother 59:43–50 http://dx.doi.org/10.1093/jac/dkl450. [PubMed]
183. Abdel-Malek SM, Al-Adham IS, Winder CL, Buultjens TE, Gartland KM, Collier PJ. 2002. Antimicrobial susceptibility changes and T-OMP shifts in pyrithione-passaged planktonic cultures of Pseudomonas aeruginosa PAO1. J Appl Microbiol 92:729–736 http://dx.doi.org/10.1046/j.1365-2672.2002.01575.x. [PubMed]
184. Parikh SL, Xiao G, Tonge PJ. 2000. Inhibition of InhA, the enoyl reductase from Mycobacterium tuberculosis, by triclosan and isoniazid. Biochemistry 39:7645–7650 http://dx.doi.org/10.1021/bi0008940. [PubMed]
185. Chen Y, Pi B, Zhou H, Yu Y, Li L. 2009. Triclosan resistance in clinical isolates of Acinetobacter baumannii. J Med Microbiol 58:1086–1091 http://dx.doi.org/10.1099/jmm.0.008524-0. [PubMed]
186. Zhu L, Lin J, Ma J, Cronan JE, Wang H. 2010. Triclosan resistance of Pseudomonas aeruginosa PAO1 is due to FabV, a triclosan-resistant enoyl-acyl carrier protein reductase. Antimicrob Agents Chemother 54:689–698 http://dx.doi.org/10.1128/AAC.01152-09. [PubMed]
187. Heath RJ, Li J, Roland GE, Rock CO. 2000. Inhibition of the Staphylococcus aureus NADPH-dependent enoyl-acyl carrier protein reductase by triclosan and hexachlorophene. J Biol Chem 275:4654–4659 http://dx.doi.org/10.1074/jbc.275.7.4654. [PubMed]
188. Slater-Radosti C, Van Aller G, Greenwood R, Nicholas R, Keller PM, DeWolf WE Jr, Fan F, Payne DJ, Jaworski DD. 2001. Biochemical and genetic characterization of the action of triclosan on Staphylococcus aureus. J Antimicrob Chemother 48:1–6 http://dx.doi.org/10.1093/jac/48.1.1. [PubMed]
189. Massengo-Tiassé RP, Cronan JE. 2008. Vibrio cholerae FabV defines a new class of enoyl-acyl carrier protein reductase. J Biol Chem 283:1308–1316 http://dx.doi.org/10.1074/jbc.M708171200. [PubMed]
190. Webber MA, Whitehead RN, Mount M, Loman NJ, Pallen MJ, Piddock LJV. 2015. Parallel evolutionary pathways to antibiotic resistance selected by biocide exposure. J Antimicrob Chemother 70:2241–2248 http://dx.doi.org/10.1093/jac/dkv109. [PubMed]
191. Roujeinikova A, Levy CW, Rowsell S, Sedelnikova S, Baker PJ, Minshull CA, Mistry A, Colls JG, Camble R, Stuitje AR, Slabas AR, Rafferty JB, Pauptit RA, Viner R, Rice DW. 1999. Crystallographic analysis of triclosan bound to enoyl reductase. J Mol Biol 294:527–535 http://dx.doi.org/10.1006/jmbi.1999.3240. [PubMed]
192. Stewart MJ, Parikh S, Xiao G, Tonge PJ, Kisker C. 1999. Structural basis and mechanism of enoyl reductase inhibition by triclosan. J Mol Biol 290:859–865 http://dx.doi.org/10.1006/jmbi.1999.2907. [PubMed]
193. Heath RJ, Rubin JR, Holland DR, Zhang E, Snow ME, Rock CO. 1999. Mechanism of triclosan inhibition of bacterial fatty acid synthesis. J Biol Chem 274:11110–11114 http://dx.doi.org/10.1074/jbc.274.16.11110. [PubMed]
194. McCay PH, Ocampo-Sosa AA, Fleming GTA. 2010. Effect of subinhibitory concentrations of benzalkonium chloride on the competitiveness of Pseudomonas aeruginosa grown in continuous culture. Microbiology 156:30–38 http://dx.doi.org/10.1099/mic.0.029751-0. [PubMed]
195. Casado Muñoz MC, Benomar N, Ennahar S, Horvatovich P, Lavilla Lerma L, Knapp CW, Gálvez A, Abriouel H. 2016. Comparative proteomic analysis of a potentially probiotic Lactobacillus pentosus MP-10 for the identification of key proteins involved in antibiotic resistance and biocide tolerance. Int J Food Microbiol 222:8–15 http://dx.doi.org/10.1016/j.ijfoodmicro.2016.01.012. [PubMed]
196. Casado Muñoz MC, Benomar N, Lavilla Lerma L, Knapp CW, Gálvez A, Abriouel H. 2016. Biocide tolerance, phenotypic and molecular response of lactic acid bacteria isolated from naturally-fermented Aloreña table to different physico-chemical stresses. Food Microbiol 60:1–12 http://dx.doi.org/10.1016/j.fm.2016.06.013. [PubMed]
197. Jang H-J, Chang MW, Toghrol F, Bentley WE. 2008. Microarray analysis of toxicogenomic effects of triclosan on Staphylococcus aureus. Appl Microbiol Biotechnol 78:695–707 http://dx.doi.org/10.1007/s00253-008-1349-x. [PubMed]
198. Cerf O, Carpentier B, Sanders P. 2010. Tests for determining in-use concentrations of antibiotics and disinfectants are based on entirely different concepts: “resistance” has different meanings. Int J Food Microbiol 136:247–254 http://dx.doi.org/10.1016/j.ijfoodmicro.2009.10.002. [PubMed]
199. Russell AD, McDonnell G. 2000. Concentration: a major factor in studying biocidal action. J Hosp Infect 44:1–3 http://dx.doi.org/10.1053/jhin.1999.0654. [PubMed]
200. Koutsolioutsou A, Peña-Llopis S, Demple B. 2005. Constitutive soxR mutations contribute to multiple-antibiotic resistance in clinical Escherichia coli isolates. Antimicrob Agents Chemother 49:2746–2752 http://dx.doi.org/10.1128/AAC.49.7.2746-2752.2005. [PubMed]
201. Mokgatla RM, Gouws PA, Brözel VS. 2002. Mechanisms contributing to hypochlorous acid resistance of a Salmonella isolate from a poultry-processing plant. J Appl Microbiol 92:566–573 http://dx.doi.org/10.1046/j.1365-2672.2002.01565.x. [PubMed]
202. Allen MJ, White GF, Morby AP. 2006. The response of Escherichia coli to exposure to the biocide polyhexamethylene biguanide. Microbiology 152:989–1000 http://dx.doi.org/10.1099/mic.0.28643-0. [PubMed]
203. Slade D, Radman M. 2011. Oxidative stress resistance in Deinococcus radiodurans. Microbiol Mol Biol Rev 75:133–191 http://dx.doi.org/10.1128/MMBR.00015-10. [PubMed]
204. Daniels C, Ramos JL. 2009. Adaptive drug resistance mediated by root-nodulation-cell division efflux pumps. Clin Microbiol Infect 15(Suppl 1) :32–36 http://dx.doi.org/10.1111/j.1469-0691.2008.02693.x. [PubMed]
205. Maseda H, Hashida Y, Konaka R, Shirai A, Kourai H. 2009. Mutational upregulation of a resistance-nodulation-cell division-type multidrug efflux pump, SdeAB, upon exposure to a biocide, cetylpyridinium chloride, and antibiotic resistance in Serratia marcescens. Antimicrob Agents Chemother 53:5230–5235 http://dx.doi.org/10.1128/AAC.00631-09. [PubMed]
206. Walsh C, Fanning S. 2008. Antimicrobial resistance in foodborne pathogens: a cause for concern? Curr Drug Targets 9:808–815 http://dx.doi.org/10.2174/138945008785747761. [PubMed]
207. Li XZ, Nikaido H. 2009. Efflux-mediated drug resistance in bacteria: an update. Drugs 69:1555–1623 http://dx.doi.org/10.2165/11317030-000000000-00000. [PubMed]
208. Oethinger M, Kern WV, Goldman JD, Levy SB. 1998. Association of organic solvent tolerance and fluoroquinolone resistance in clinical isolates of Escherichia coli. J Antimicrob Chemother 41:111–114 http://dx.doi.org/10.1093/jac/41.1.111. [PubMed]
209. Pomposiello PJ, Bennik MH, Demple B. 2001. Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate. J Bacteriol 183:3890–3902 http://dx.doi.org/10.1128/JB.183.13.3890-3902.2001. [PubMed]
210. Fraise AP. 2002. Biocide abuse and antimicrobial resistance: a cause for concern? J Antimicrob Chemother 49:11–12 http://dx.doi.org/10.1093/jac/49.1.11. [PubMed]
211. Langsrud S, Sidhu MS, Heir E, Holck AL. 2003. Bacterial disinfectant resistance: a challenge for the food industry. Int Biodeter Biodegrad 51:283–290 http://dx.doi.org/10.1016/S0964-8305(03)00039-8.
212. Braoudaki M, Hilton AC. 2004. Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J Clin Microbiol 42:73–78 http://dx.doi.org/10.1128/JCM.42.1.73-78.2004. [PubMed]
213. Braoudaki M, Hilton AC. 2004. Low level of cross-resistance between triclosan and antibiotics in Escherichia coli K-12 and E. coli O55 compared to E. coli O157. FEMS Microbiol Lett 235:305–309 http://dx.doi.org/10.1111/j.1574-6968.2004.tb09603.x. [PubMed]
214. Gilbert P, McBain AJ. 2003. Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin Microbiol Rev 16:189–208 http://dx.doi.org/10.1128/CMR.16.2.189-208.2003. [PubMed]
215. Russell AD. 2004. Bacterial adaptation and resistance to antiseptics, disinfectants and preservatives is not a new phenomenon. J Hosp Infect 57:97–104 http://dx.doi.org/10.1016/j.jhin.2004.01.004. [PubMed]
216. Alonso-Hernando A, Capita R, Prieto M, Alonso-Calleja C. 2009. Comparison of antibiotic resistance patterns in Listeria monocytogenes and Salmonella enterica strains pre-exposed and exposed to poultry decontaminants. Food Control 20:1108–1111 http://dx.doi.org/10.1016/j.foodcont.2009.02.011.
217. Weber DJ, Rutala WA. 2006. Use of germicides in the home and the healthcare setting: is there a relationship between germicide use and antibiotic resistance? Infect Control Hosp Epidemiol 27:1107–1119 http://dx.doi.org/10.1086/507964. [PubMed]
218. Pumbwe L, Skilbeck CA, Wexler HM. 2007. Induction of multiple antibiotic resistance in Bacteroides fragilis by benzene and benzene-derived active compounds of commonly used analgesics, antiseptics and cleaning agents. J Antimicrob Chemother 60:1288–1297 http://dx.doi.org/10.1093/jac/dkm363. [PubMed]
219. Lara HH, Ayala-Nunez NV, Turrent LDCI, Padilla CR. 2010. Bactericidal effect of silver nanoparticles against multidrug-resistant bacteria. World J Microbiol Biotechnol 26:615–621 http://dx.doi.org/10.1007/s11274-009-0211-3.
220. Peyrat MB, Soumet C, Maris P, Sanders P. 2008. Phenotypes and genotypes of Campylobacter strains isolated after cleaning and disinfection in poultry slaughterhouses. Vet Microbiol 128:313–326 http://dx.doi.org/10.1016/j.vetmic.2007.10.021. [PubMed]
221. Gilbert P, McBain AJ, Bloomfield SF. 2002. Biocide abuse and antimicrobial resistance: being clear about the issues. J Antimicrob Chemother 50:137–139, author reply 139–140 http://dx.doi.org/10.1093/jac/dkf071. [PubMed]
222. Lear JC, Maillard J-Y, Dettmar PW, Goddard PA, Russell AD. 2006. Chloroxylenol- and triclosan-tolerant bacteria from industrial sources: susceptibility to antibiotics and other biocides. Int Biodeter Biodegrad 57:51–56 http://dx.doi.org/10.1016/j.ibiod.2005.11.002.
223. Knapp L, Amézquita A, McClure P, Stewart S, Maillard J-Y. 2015. Development of a protocol for predicting bacterial resistance to microbicides. Appl Environ Microbiol 81:2652–2659 http://dx.doi.org/10.1128/AEM.03843-14. [PubMed]
224. Sundheim G, Langsrud S, Heir E, Holck AL. 1998. Bacterial resistance to disinfectants containing quaternary ammonium compounds. Int Biodeter Biodegrad 41:235–239 http://dx.doi.org/10.1016/S0964-8305(98)00027-4.
225. International Organization for Standardization. 2006. ISO: 20776-1. Clinical laboratory testing and in vitro diagnostic test systems: susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices. Part 1. Reference method for testing the in vitro activity of antimicrobial agents against rapidly growing aerobic bacteria involved in infectious diseases. British Standard Institute, London, United Kingdom.
226. European Committee on Antimicrobial Susceptibility Testing (EUCAST). 2014. Breakpoint tables for interpretation of MICs and zone diameters. Version 4.0. 2014. http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_6.0_Breakpoint_table.pdf. Accessed January 2017.
227. Andrews JM, BSAC Working Party on Susceptibility Testing. 2009. BSAC standardized disc susceptibility testing method (version 8). J Antimicrob Chemother 64:454–489 http://dx.doi.org/10.1093/jac/dkp244. [PubMed]
228. Saleh S, Haddadin RNS, Baillie S, Collier PJ. 2011. Triclosan: an update. Lett Appl Microbiol 52:87–95 http://dx.doi.org/10.1111/j.1472-765X.2010.02976.x. [PubMed]
229. Gradel KO, Randall L, Sayers AR, Davies RH. 2005. Possible associations between Salmonella persistence in poultry houses and resistance to commonly used disinfectants and a putative role of mar. Vet Microbiol 107:127–138 http://dx.doi.org/10.1016/j.vetmic.2005.01.013. [PubMed]
230. Chuanchuen R, Pathanasophon P, Khemtong S, Wannaprasat W, Padungtod P. 2008. Susceptibilities to antimicrobials and disinfectants in Salmonella isolates obtained from poultry and swine in Thailand. J Vet Med Sci 70:595–601 http://dx.doi.org/10.1292/jvms.70.595. [PubMed]
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/content/journal/microbiolspec/10.1128/microbiolspec.ARBA-0006-2017
2018-04-19
2019-10-21

Abstract:

Biocides and formulated biocides are used worldwide for an increasing number of applications despite tightening regulations in Europe and in the United States. One concern is that such intense usage of biocides could lead to increased bacterial resistance to a product and cross-resistance to unrelated antimicrobials including chemotherapeutic antibiotics. Evidence to justify such a concern comes mostly from the use of health care-relevant bacterial isolates, although the number of studies of the resistance characteristics of veterinary isolates to biocides have increased the past few years. One problem remains the definition of “resistance” and how to measure resistance to a biocide. This has yet to be addressed globally, although the measurement of resistance is becoming more pressing, with regulators both in Europe and in the United States demanding that manufacturers provide evidence that their biocidal products will not impact on bacterial resistance. Alongside evidence of potential antimicrobial cross-resistance following biocide exposure, our understanding of the mechanisms of bacterial resistance and, more recently, our understanding of the effect of biocides to induce a mechanism(s) of resistance in bacteria has improved. This article aims to provide an understanding of the development of antimicrobial resistance in bacteria following a biocide exposure. The sections provide evidence of the occurrence of bacterial resistance and its mechanisms of action and debate how to measure bacterial resistance to biocides. Examples pertinent to the veterinary field are used where appropriate.

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Figures

Image of FIGURE 1
FIGURE 1

Diagrammatic comparison of the five families of efflux pumps (reproduced from reference 153 ). MATE, multidrug and toxic compound extrusion; MFS, major facilitator superfamily; SMR, •••; RND, resistance-nodulation-division; ABC, ATP-binding cassette.

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.ARBA-0006-2017
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Image of FIGURE 2
FIGURE 2

Schematic map of mutations in the () and () genes. Mutations in are reported on a schematic map. Mutations detected in clinical isolates are mapped above the sequence, while mutations selected are shown below the sequence. (Reproduced from reference 95 .)

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.ARBA-0006-2017
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Tables

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TABLE 1

Levels of biocide interactions with a bacterial cell

Source: microbiolspec April 2018 vol. 6 no. 2 doi:10.1128/microbiolspec.ARBA-0006-2017

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