Chapter 12 : Biocides and Resistance

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in

Biocides and Resistance, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817572/9781555813291_Chap12-1.gif /docserver/preview/fulltext/10.1128/9781555817572/9781555813291_Chap12-2.gif


Now the antibiotic resistance is escalating to alarming proportions and the discovery of new antibiotics is waning, a greater reliance on infection prevention has evolved-from fear as well as necessity. Among personal hygiene products, the agents triclocarban and triclosan are the most common biocide components. A major group of commonly used residue producing biocides consists of the quaternary ammonium compounds (QACs) that are also known as cationic detergents. The pathogens and O157 could readily adapt to stable biocide tolerance (30 or more days), and very high triclosan tolerance could be attained in . Importantly, resistance to ciprofloxacin was expressed at clinically significant levels. The reverse phenomenon has also been reported (i.e., strains adapted to antibiotic resistance can demonstrate tolerance to biocides). QACs are widely used as disinfectants in the food industry, and there is concern over the increasing incidence of biocide resistance in food-associated bacteria. The biocide controversy has sparked an increased interest in the undertaking of prospective in situ or microcosm-based studies that would help shed greater insight into the impacts of biocide application as practiced in the community environment. Recent surveys of large numbers of species isolated from a variety of environments have revealed a range in biocide susceptibility, with small frequencies of outliers that exhibit significantly elevated tolerance.

Citation: Marshall B, McMurry L. 2005. Biocides and Resistance, p 174-190. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch12

Key Concept Ranking

Antibacterial Agents
Outer Membrane Proteins
Fatty Acid Biosynthesis
Antiseptics and Disinfectants
Highlighted Text: Show | Hide
Loading full text...

Full text loading...


1. Adolfsson-Erici, M.,, M. Pettersson,, J. Parkkonen,, and J. Sturve. 2002. Triclosan, a commonly used bactericide found in human milk and in the aquatic environment in Sweden. Chemosphere 46:14851489.
2. Aiello, A. E.,, and E. L. Larson. 2002. What is the evidence for a causal link between hygiene and infections? Lancet Infect. Dis. 2:103110.
3. Aiello, A. E.,, B. Marshall,, S. B. Levy,, P. Della-Latta,, and E. Larson. Submitted for publication.
4. Akimitsu, N.,, H. Hamamoto,, R. Inoue,, M. Shoji,, A. Akamine,, K. Takemori,, N. Hamasaki,, and K. Sekimizu. 1999. Increase in resistance of methicillin-resistant Staphylococcus aureus to beta-lactams caused by mutations conferring resistance to benzalkonium chloride, a disinfectant widely used in hospitals. Antimicrob. Agents Chemother. 43:30423043.
5. Al-Doori, Z.,, D. Morrison,, G. Edwards,, and C. Gemmell. 2003. Susceptibility of MRSA to triclosan. J. Antimicrob. Chemother. 51:185186.
6. al-Masaudi, S. B.,, M. J. Day,, and A. D. Russell. 1991. Effect of some antibiotics and biocides on plasmid transfer in Staphylococcus aureus. J. Appl. Bacteriol. 71:239243.
7.Anon. 2001. Disinfectants in Consumer Products Publication #2001/05E. Health Council of the Netherlands.
8.Anon. 1999. Four pediatric deaths from community-acquired methicillin-resistant Staphylococcus aureus: Minnesota and North Dakota 1997-1999. Morb. Mortal. Wkly. Rep. 48:707710.
9. Baldock, C.,, J. B. Rafferty,, S. E. Sedelnikova,, P. J. Baker,, A. R. Stuitje,, A. R. Slabas,, T. R. Hawkes,, and D. W. Rice. 1996. A mechanism of drug action revealed by structural studies of enoyl reductase. Science 274:21072110.
10. Bamber, A. I.,, and T. J. Neal. 1999. An assessment of triclosan susceptibility in methicillin-resistant and methicillinsensitive Staphylococcus aureus. J. Hosp. Infect. 41:107109.
11. Behr, H.,, M. E. Reverdy,, C. Mabilat,, J. Freney,, and J. Fleurette. 1994. [Relationship between the level of minimal inhibitory concentrations of five antiseptics and the presence of qacA gene in Staphylococcus aureus]. Pathol. Biol. (Paris) 42:438444.
12. Bergler, H.,, P. Wallner,, A. Ebeling,, B. Leitinger,, S. Fuchsbichler,, H. Aschauer,, G. Kollenz,, G. Hogenauer,, and F. Turnowsky. 1994. Protein EnvM is the NADH-dependent enoyl-ACP reductase (FabI) of Escherichia coli. J. Biol. Chem. 269:54935496.
13. Beumer, R.,, S. Bloomfield,, M. Exner,, G. Fara,, K. Nath,, and E. Scott 2003, posting date. Biocide usage and antimicrobial resistance in home settings: an update. International Scientific Forum on Home Hygiene (IFH). [Online.]
14. Beumer, R.,, S. Bloomfield,, M. Exner,, G. Fara,, K. Nath,, and E. Scott 2000, posting date. Microbial Resistance and Biocides. International Scientific Forum onHomeHygiene (IFH). [Online.]
15. Bhargava, H. N.,, and P. A. Leonard. 1996. Triclosan: applications and safety. Am. J. Infect. Control 24:209218.
16. Bjorland, J.,, T. Steinum,, M. Sunde,, S. Waage,, and E. Heir. 2003. Novel plasmid-borne gene qacJ mediates resistance to quaternary ammonium compounds in equine Staphylococcus aureus, Staphylococcus simulans, and Staphylococcus intermedius. Antimicrob. Agents Chemother. 47:30463052.
17. Bjorland, J.,, M. Sunde,, and S. Waage. 2001. Plasmid-borne smr gene causes resistance to quaternary ammonium compounds in bovine Staphylococcus aureus. J. Clin. Microbiol. 39:39994004.
18. Bloomfield, S. F. 2002. Significance of biocide usage and antimicrobial resistance in domiciliary environments. J. Appl. Microbiol. 92:144S157S.
19. Braoudaki, M.,, and A. C. Hilton. 2004. Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J. Clin. Microbiol. 42:7378.
20. Braoudaki, M.,, and A. C. Hilton. 2004. Low level of crossresistance between triclosan and antibiotics in Escherichia coli K-12 and E. coli O55 compared to E. coli O157. FEMS Microbiol. Lett. 235:305309.
21. Brenwald, N. P.,, and A. P. Fraise. 2003. Triclosan resistance in methicillin-resistant Staphylococcus aureus (MRSA). J. Hosp. Infect. 55:141144.
22. Brooun, A.,, S. Liu,, and K. Lewis. 2000. A dose-response study of antibiotic resistance in Pseudomonas aeruginosa biofilms. J. Antimicrob. Chemother. 44:640646.
23. Bryan, J. L.,, J. Cohran,, and E. L. Larson,. 1994. Handwashing: a ritual revisited., p. 163178. In W. A. Rutala (ed.), Chemical Germicides in Healthcare. Association for Professionals in Infection Control and Epidemiology, Inc., Washington, D.C.
24. Cantrell, F. 2001. The effect of prolonged exposure to triclosan on staphylococci. Presented at the 101st Annual Meeting of the American Society for Microbiology.
25. Chuanchuen, R.,, R. R. Karkhoff-Schweizer,, and H. P. Schweizer. 2003. High-level triclosan resistance in Pseudomonas aeruginosa is solely a result of efflux. Am. J. Infect. Control 31:124127.
26. Cogan, T. A.,, J. Slader,, S. F. Bloomfield,, and T. J. Humphrey. 2002. Achieving hygiene in the domestic kitchen: the effectiveness of commonly used cleaning procedures. J. Appl. Microbiol. 92:885892.
27. Cole, E. C.,, R. M. Addison,, J. R. Rubino,, K. E. Leese,, P. D. Dulaney,, M. S. Newell,, J. Wilkins,, D. J. Gaber,, T. Wineinger,, and D. A. Criger. 2003. Investigation of antibiotic and antibacterial agent cross-resistance in target bacteria from homes of antibacterial product users and nonusers. J. Appl. Microbiol. 95:664676.
28. Cookson, B. D.,, H. Farrelly,, P. Stapleton,, R. P. Garvey,, and M. R. Price. 1991. Transferable resistance to triclosan in MRSA. Lancet 337:15481549.
29. Cullinan, M. P.,, S. M. Hamlet,, B. Westerman,, J. E. Palmer,, M. J. Faddy,, and J. G. Seymour. 2003. Acquisition and loss of Porphyromonas gingivalis, Actinobacillus actinomycetemcomitans and Prevotella intermedia over a 5-year period: effect of a triclosan/copolymer dentifrice. J. Clin. Periodontol. 30:532541.
30. Favero, M. S. 2002. Products containing biocides: perceptions and realities. J. Appl. Microbiol. 92 (Suppl.):72S77S.
31. Fraise, A. P. 2002. Biocide abuse and antimicrobial resistance—a cause for concern? J. Antimicrob. Chemother. 49:1112.
32. Fraise, A. P. 2002. Susceptibility of antibiotic-resistant cocci to biocides. J. Appl. Microbiol. 31:158S162S.
33. Furia, T. E.,, and A. G. Schenkel. 1968. New Broad Spectrum Bacteriostat. Soap and Chemical Specialties 44:4750,116122.
34. Gandhi, I.,, A. D. Sawant,, L. A. Wilson,, and D. G. Ahearn. 1993. Adaptation and growth of Serratia marcescens in contact lens disinfectant solutions containing chlorhexidine gluconate. Appl. Environ. Microbiol. 59:183188.
35. George, A. M.,, and S. B. Levy. 1983. Amplifiable resistance to tetracycline, chloramphenicol, and other antibiotics in Escherichia coli: involvement of a non-plasmid-determined efflux of tetracycline. J. Bacteriol. 155:531540.
36. Gerba, C. P.,, and P. Rusin,. 2001. Relationship between the use of antiseptics/disinfectants and the development of antimicrobial resistance, p. 187194. In W. A. Rutala (ed.), Disinfection, Sterilization and Antisepsis: Principles and Practices in Healthcare Facilities. Association for Professionals in Infection Control and Epidemiology, Washington, D.C.
37. Gilbert, P.,, A. J. McBain,, and S. F. Bloomfield. 2002. Biocide abuse and antimicrobial resistance: being clear about the issues. J. Antimicrob. Chemother. 50:137139; author reply 139-40.
38. Goldstein, F. W.,, C. Soria,, A. Ly,, and M. D. Kitzis. 2004. Very high prevalence of resistance to tricolsan and other antiseptics among French glycopeptide-intermediate S. aureus (GISA). Presented at the 44th Interscience Conference on Antimicrobial Agents and Chemotherapy, Washington, D.C.
39. Haines, K. A.,, D. A. Klein,, G. McDonnell,, and D. Pretzer. 1997. Could antibiotic-resistant pathogens be cross-resistant to hard-surface disinfectants? Am. J. Infect. Control 25:439441.
40. Hay, A. G.,, P. M. Dees,, and G. S. Sayler. 2001. Growth of a bacterial consortium on triclosan. FEMS Microbiol. Ecol. 36:105112.
41. Heath, R. J.,, J. Li,, G. E. Roland,, and C. O. Rock. 2000. Inhibition of the Staphylococcus aureus NADPH-dependent enoyl-acyl carrier protein reductase by triclosan and hexachlorophene. J. Biol. Chem. 275:46544659.
42. Heath, R. J.,, N. Su,, C. K. Murphy,, and C. O. Rock. 2000. The enoyl-[acyl-carrier-protein] reductases FabI and FabL from Bacillus subtilis. J. Biol. Chem. 275:4012840133.
43. Heath, R. J.,, Y. T. Yu,, M. A. Shapiro,, E. Olson,, and C. O. Rock. 1998. Broad spectrum antimicrobial biocides target the FabI component of fatty acid synthesis. J. Biol. Chem. 273: 3031630320.
44. Heir, E.,, G. Sundheim,, and A. L. Holck. 1999. Identification and characterization of quaternary ammonium compound resistant staphylococci from the food industry. Int J. Food Microbiol. 48:211219.
45. Heir, E.,, G. Sundheim,, and A. L. Holck. 1999. The qacG gene on plasmid pST94 confers resistance to quaternary ammonium compounds in staphylococci isolated from the food industry. J. Appl. Microbiol. 86:378388.
46. Heir, E.,, G. Sundheim,, and A. L. Holck. 1995. Resistance to quaternary ammonium compounds in Staphylococcus spp. isolated from the food industry and nucleotide sequence of the resistance plasmid pST827. J. Appl. Bacteriol. 79:149156.
47. Heir, E.,, G. Sundheim,, and A. L. Holck. 1998. The Staphylococcus qacH gene product: a new member of the SMR family encoding multidrug resistance. FEMS Microbiol. Lett. 163:4956.
48. Hoang, T. T.,, and H. P. Schweizer. 1999. Characterization of Pseudomonas aeruginosa enoyl-acyl carrier protein reductase (FabI): a target for the antimicrobial triclosan and its role in acylated homoserine lactone synthesis. J. Bacteriol. 181:54895497.
49. Hovander, L.,, T. Malmberg,, M. Athanasiadou,, I. Athanassiadis,, S. Rahm,, A. Bergman,, and E. K. Wehler. 2002. Identification of hydroxylated PCB metabolites and other phenolic halogenated pollutants in human blood plasma. Arch. Environ. Contam. Toxicol. 42:105117.
50. Hundt, K.,, D. Martin,, E. Hammer,, U. Jonas,, M. K. Kindermann,, and F. Schauer. 2000. Transformation of triclosan by Trametes versicolor and Pycnoporus cinnabarinus. Appl. Environ. Microbiol. 66:41574160.
51. Ishikawa, S.,, F. Matsumura,, F. Yoshizako,, and T. Tsuchido. 2002. Characterization of a cationic surfactant-resistant mutant isolated spontaneously from Escherichia coli. J. Appl. Microbiol. 92:261268.
52. Jones, R. D. 1999. Bacterial resistance and topical antimicrobial wash products. Am. J. Infect. Control 27:351363.
53. Jones, R. D.,, H. B. Jampani,, J. L. Newman,, and A. S. Lee. 2000. Triclosan: a review of effectiveness and safety in health care settings. Am. J. Infect. Control 28:184196.
54. Josephson, K. L.,, J. R. Rubino,, and I. L. Pepper. 1997. Characterization and quantification of bacterial pathogens and indicator organisms in household kitchens with and without the use of a disinfectant cleaner. J. Appl. Microbiol. 83:737750.
55. Joynson, J. A.,, B. Forbes,, and R. J. Lambert. 2002. Adaptive resistance to benzalkonium chloride, amikacin and tobramycin: the effect on susceptibility to other antimicrobials. J. Appl. Microbiol. 93:96107.
56. Junker, L. M.,, and A. G. Hay. 2004. Effects of triclosan incorporation into ABS plastic on biofilm communities. J. Antimicrob. Chemother. 53:989996.
57. Kalyon, B. D.,, and U. Olgun. 2001. Antibacterial efficacy of polymers containing triclosan and other antimicrobial additives: REPLY. Amer. J. Infect. Cont. 29:429430.
58. Kuo, M. R.,, H. R. Morbidoni,, D. Alland,, S. F. Sneddon,, B. B. Gourlie,, M. M. Staveski,, M. Leonard,, J. S. Gregory,, A. D. Janjigian,, C. Yee,, J. M. Musser,, B. Kreiswirth,, H. Iwamoto,, R. Perozzo,, W. R. Jacobs, Jr.,, J. C. Sacchettini,, and D. A. Fidock. 2003. Targeting tuberculosis and malaria through inhibition of enoyl reductase: compound activity and structural data. J. Biol. Chem. 278:2085120859.
59. Langsrud, S.,, G. Sundheim,, and R. Borgmann-Strahsen. 2003. Intrinsic and acquired resistance to quaternary ammonium compounds in food-related Pseudomonas spp. J. Appl. Microbiol. 95:874882.
60. Langsrud, S.,, G. Sundheim,, and A. L. Holck. 2004. Crossresistance to antibiotics of Escherichia coli adapted to benzalkonium chloride or exposed to stress-inducers. J. Appl. Microbiol. 96:201208.
61. Larson, E.,, A. Aiello,, L. V. Lee,, P. Della-Latta,, C. Gomez- Duarte,, and S. Lin. 2003. Short- and long-term effects of handwashing with antimicrobial or plain soap in the community. J. Commun. Hlth. 28:139150.
62. Larson, E. L.,, S. X. Lin,, C. Gomez-Pichardo,, and P. Della- Latta. 2004. Effect of antibacterial home cleaning and handwashing products on infectious disease symptoms: a randomized, double-blind trial. Ann. Intern. Med. 140:321329.
63. Leelaporn, A.,, I. T. Paulsen,, J. M. Tennent,, T. G. Littlejohn,, and R. A. Skurray. 1994. Multidrug resistance to antiseptics and disinfectants in coagulase-negative staphylococci. J. Med. Microbiol. 40:214220.
64. Levy, C. W.,, A. Roujeinikova,, S. Sedelnikova,, P. J. Baker,, A. R. Stuitje,, A. R. Slabas,, D. W. Rice,, and J. B. Rafferty. 1999. Molecular basis of triclosan activity. Nature 398:383384.
65. Levy, S. B. 2002. Active efflux, a common mechanism for biocide and antibiotic resistance. J. Appl. Microbiol. 92:65S71S.
66. Levy, S. B. 2001. Antibacterial household products: cause for concern. Emerg. Infect. Dis. 7:512515.
67. Levy, S. B. 2000. Antibiotic and antiseptic resistance: impact on public health. Pediatr. Infect. Dis. J. 19:S120S122.
68. Levy, S. B. 2002. The Antibiotic Paradox: How the Misuse of Antibiotics Destroys Their Curative Powers. Perseus Publishing, Cambridge, Mass.
69. Levy, S. B. 2002. Antimicrobial consumer products: where’s the benefit? What’s the risk? Arch. Dermatol. 138:10871088.
70. Littlejohn, T. G.,, I. T. Paulsen,, M. T. Gillespie,, J. M. Tennent,, M. Midgley,, I. G. Jones,, A. S. Purewal,, and R. A. Skurray. 1992. Substrate specificity and energetics of antiseptic and disinfectant resistance in Staphylococcus aureus. FEMS Microbiol. Lett. 74:259265.
71. Loughlin, M. F.,, M. V. Jones,, and P. A. Lambert. 2002. Pseudomonas aeruginosa cells adapted to benzalkonium chloride show resistance to other membrane-active agents but not to clinically relevant antibiotics. J. Antimicrob. Chemother. 49: 631639.
72. Luby, S. P.,, M. Agboatwalla,, J. Painter,, A. Altaf,, W. L. Billhimer,, and R. M. Hoekstra. 2004. Effect of intensive handwashing promotion on childhood diarrhea in high-risk communities in Pakistan: a randomized controlled trial. J. Am. Med. Assoc. 291:25472554.
73. Marshall, B. M.,, E. Robleto,, T. Dumont,, W. Billhimer,, K. Wiandt,, B. Keswick,, and S. B. Levy. 2003. The frequency of bacteria and antibiotic resistance in homes that use and do not use surface antibacterial agents. Presented at the Annual 103rd Meeting of the American Society for Microbiology, Washington, D.C.
74. McBain, A. J.,, R. G. Bartolo,, C. E. Catrenich,, D. Charbonneau,, R. G. Ledder,, and P. Gilbert. 2003. Effects of a chlorhexidine gluconate-containing mouthwash on the vitality and antimicrobial susceptibility of in vitro oral bacterial ecosystems. Appl. Environ. Microbiol. 69:47704776.
75. McBain, A. J.,, R. G. Bartolo,, C. E. Catrenich,, D. Charbonneau,, R. G. Ledder,, and P. Gilbert. 2003. Effects of triclosancontaining rinse on the dynamics and antimicrobial susceptibility of in vitro plaque ecosystems. Antimicrob. Agents Chemother. 47:35313538.
76. McBain, A. J.,, R. G. Bartolo,, C. E. Catrenich,, D. Charbonneau,, R. G. Ledder,, B. B. Price,, and P. Gilbert. 2003. Exposure of sink drain microcosms to triclosan: population dynamics and antimicrobial susceptibility. Appl. Environ. Microbiol. 69:54335422.
77. McBain, A. J.,, R. G. Ledder,, L. E. Moore,, C. E. Catrenich,, and P. Gilbert. 2004. Effects of quaternary-ammonium-based formulations on bacterial community dynamics and antimicrobial suseptibility. Appl. Environ. Microbiol. 70:34493456.
78. McBain, A. J.,, R. G. Ledder,, P. Sreenivasan,, and P. Gilbert. 2004. Selection for high-level resistance by chronic triclosan exposure is not universal. J. Antimicrob. Chemother. 53:772777.
79. McDonnell, G.,, and A. D. Russell. 1999. Antiseptics and disinfectants: activity, action, and resistance. Clin. Microbiol. Rev. 12:147179.
80. McMurry, L. M.,, P. F. McDermott,, and S. B. Levy. 1999. Genetic evidence that InhA of Mycobacterium smegmatis is a target for triclosan. Antimicrob. Agents. Chemother. 43:711713.
81. McMurry, L. M.,, M. Oethinger,, and S. B. Levy. 1998. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol. Lett. 166:305309.
82. McMurry, L. M.,, M. Oethinger,, and S. B. Levy. 1998. Triclosan targets lipid synthesis. Nature 394:531532.
83. Meade, M. J.,, R. L. Waddell,, and T. M. Callahan. 2001. Soil bacteria Pseudomonas putida and Alcaligenes xylosoxidans subsp. denitrificans inactivate triclosan in liquid and solid substrates. FEMS Microbiol. Lett. 204:4548.
84. Miyazaki, T.,, T. Yamagishi,, and M. Matsumoto. 1984. Residues of 4-chloro-1-(2,4-dichlorophenoxy)-2 methoxy-benzene (triclosan methyl) in aquatic biota. Contam. Toxicol. 32:227232.
85. Moken, M. C.,, L. M. McMurry,, and S. B. Levy. 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. 41:27702772.
86. Nishihara, T.,, T. Okamoto,, and N. Nishiyama. 2000. Biodegradation of didecyldimethylammonium chloride by Pseudomonas fluorescens TN4 isolated from activated sludge. J. Appl. Microbiol. 88:641647.
87. Nishiyama, N.,, Y. Toshima,, and Y. Ikeda. 1995. Biodegradation of alkyltrimethylammonium salts in activated sludge. Chemosphere 30:593603.
88. Noguchi, N.,, M. Hase,, M. Kitta,, M. Sasatsu,, K. Deguchi,, and M. Kono. 1999. Antiseptic susceptibility and distribution of antiseptic-resistance genes in methicillin-resistant Staphylococcus aureus. FEMS Microbiol. Lett. 172:247253.
89. Noguchi, N.,, M. Tamura,, K. Narui,, K. Wakasugi,, and M. Sasatsu. 2002. Frequency and genetic characterization of multidrug- resistant mutants of Staphylococcus aureus after selection with individual antiseptics and fluoroquinolones. Biolog. Pharmaceut. Bull. 25:11291132.
90. Parikh, S. L.,, G. Xiao,, and P. J. Tonge. 2000. Inhibition of InhA, the enoyl reductase from Mycobacterium tuberculosis, by triclosan and isoniazid. Biochemistry 39:76457650.
91. Patrauchan, M. A.,, and P. J. Oriel. 2003. Degradation of benzyldimethylalkylammonium chloride by Aeromonas hydrophila sp. J. Appl. Microbiol. 94:266272.
92. Paulsen, I. T.,, T. G. Littlejohn,, P. Radstrom,, L. Sundstrom,, O. Skold,, G. Swedberg,, and R. A. Skurray. 1993. The 3′ conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants. Antimicrob. Agents Chemother. 37:761768.
93. Pearce, H.,, S. Messager,, and J. Y. Maillard. 1999. Effect of biocides commonly used in the hospital environment on the transfer of antibiotic-resistance genes in Staphylococcus aureus. J. Hosp. Infect. 43:101107.
94. Price, C. T.,, V. K. Singh,, R. K. Jayaswal,, B. J. Wilkinson,, and J. E. Gustafson. 2002. Pine oil cleaner-resistant Staphylococcus aureus: reduced susceptibility to vancomycin and oxacillin and involvement of SigB. Appl. Environ. Microbiol. 68:54175421.
95. Randall, L. P.,, S. W. Cooles,, L. J. Piddock,, and M. J. Woodward. 2004. Effect of triclosan or a phenolic farm disinfectant on the selection of antibiotic-resistant Salmonella enterica. J. Antimicrob. Chemother. 54:621627.
96. Randall, L. P.,, and M. J. Woodward. 2002. The multiple antibiotic resistance (mar) locus and its significance. Res. Vet. Sci. 72:8793.
97. Regos, J.,, and H. R. Hitz. 1974. Investigations on the mode of action of Triclosan, a broad spectrum antimicrobial agent. Zbl. Bakt. Hyg. 226:390401.
98. Reynolds, H. S.,, P. K. Sreenivasan,, R. Subramanyam,, V. I. Haraszthy,, D. Cummins,, and J. J. Zambon. 2003. Media and method-dependent variations in minimal inhibitory concentrations of triclosan and 2-t-butyl-5-(4-t-butylphenyl)-phenol. Presented at the Annual Meeting of the American Society for Microbiology, Washington D.C.
99. Russell, A. D. 2002. Introduction of biocides into clinical practice and the impact on antibiotic-resistant bacteria. Symp. Ser. Soc. Appl. Microbiol. 31:121S135S.
100. Russell, A. D.,, U. Tattawasart,, J. Y. Maillard,, and J. R. Furr. 1998. Possible link between bacterial resistance and use of antibiotics and biocides. Antimicrob. Agents Chemother. 42:2151.
101. Sanchez, P.,, E. Moreno,, and J. L. Martinez. 2005. The biocide triclosan selects Stenotrophomonas maltophilia mutants that overproduce the SmeDEF multidrug efflux pump. Antimicrob. Agents Chemother. 49:781782.
102. Saunders, K. A.,, J. Greenman,, and C. McKenzie. 2000. Ecological effects of triclosan and triclosan monophosphate on defined mixed cultures of oral species grown in continuous culture. J. Antimicrob. Chemother. 45:447452.
103. Schweizer, H. P. 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. 42:394398.
104. Sharma, S.,, T. N. Ramya,, A. Surolia,, and N. Surolia. 2003. Triclosan as a systemic antibacterial agent in a mouse model of acute bacterial challenge. Antimicrob. Agents Chemother. 47:38593866.
105. Shimizu, M.,, K. Okuzumi,, A. Yoneyama,, T. Kunisada,, M. Araake,, H. Ogawa,, and S. Kimura. 2002. In vitro antiseptic susceptibility of clinical isolates from nosocomial infections. Dermatol. 204(Suppl. 1):2127.
106. Sidhu, M. S.,, E. Heir,, T. Leegaard,, K. Wiger,, and A. Holck. 2002. Frequency of disinfectant resistance genes and genetic linkage with beta-lactamase transposon Tn552 among clinical staphylococci. Antimicrob. Agents Chemother. 46:27972803.
107. Sidhu, M. S.,, E. Heir,, H. Sorum,, and A. Holck. 2001. Genetic linkage between resistance to quaternary ammonium compounds and beta-lactam antibiotics in food-related Staphylococcus spp. Microb. Drug Resist. 7:36371.
108. Sidhu, M. S.,, S. Langsrud,, and A. Holck. 2001. Disinfectant and antibiotic resistance of lactic acid bacteria isolated from the food industry. Microb. Drug. Resist. 7:7383.
109. Sidhu, M. S.,, H. Sorum,, and A. Holck. 2002. Resistance to quaternary ammonium compounds in food-related bacteria. Microb. Drug Resist. 8:393399.
110. Singer, H.,, S. Muller,, C. Tixier,, and L. Pillonel. 2002. Triclosan: occurrence and fate of a widely used biocide in the aquatic environment: field measurements in wastewater treatment plants, surface waters, and lake sediments. Environ. Sci. Technol. 36:49985004.
111. Sivaji, Y.,, and A. Mandal. 1987. Antibiotic resistance & serotypic variations in Escherichia coli induced by disinfectants. Indian J. Med. Res. 86:165172.
112. Sreenivasan, P.,, and A. Gaffar. 2002. Antiplaque biocides and bacterial resistance: a review. J. Clin. Periodon. 29:965974.
113. Suller, M.T.,, and A. D. Russell. 1999. Antibiotic and biocide resistance in methicillin-resistant Staphylococcus aureus and vancomycin- resistant enterococcus. J. Hosp. Infect. 43:281291.
114. Suller, M. T.,, and A. D. Russell. 2000. Triclosan and antibiotic resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 46:118.
115. Sullivan, A.,, B. Wretlind,, and C. E. Nord. 2003. Will triclosan in toothpaste select for resistant oral streptococci? Clin. Microbiol. Infect. 9:306309.
116. Surolia, N.,, and A. Surolia. 2001. Triclosan offers protection against blood stages of malaria by inhibiting enoyl-ACP reductase of Plasmodium falciparum. Nat. Med. 7:167173.
117. Sutton, L.,, and G. A. Jacoby. 1978. Plasmid-determined resistance to hexachlorophene in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 13:634636.
118. Tabata, A.,, H. Nagamune,, T. Maeda,, K. Murakami,, Y. Miyake,, and H. Kourai. 2003. Correlation between resistance of Pseudomonas aeruginosa to quaternary ammonium compounds and expression of outer membrane protein OprR. Antimicrob. Agents Chemother. 47:20932099.
119. Tan, L.,, N. H. Nielsen,, D. C. Young,, Z. Trizna, and A. M. A. Council on Scientific Affairs. 2002. Use of antimicrobial agents in consumer products. Arch. Dermatol. 138:10821086.
120. Tennent, J. M.,, B. R. Lyon,, M. T. Gillespie,, J. W. May,, and R. A. Skurray. 1985. Cloning and expression of Staphylococcus aureus plasmid-mediated quaternary ammonium resistance in Escherichia coli. Antimicrob. Agents Chemother. 27:7983.
121. Villalain, J.,, C. R. Mateo,, F. J. Aranda,, S. Shapiro,, and V. Micol. 2001. Membranotropic effects of the antibacterial agent Triclosan. Arch. Biochem. Biophys. 390:128136.
122. Vischer, W. A.,, and J. Regos. 1974. Antimicrobial spectrum of Triclosan, a broad-spectrum antimicrobial agent for topical application. Zentralbl. Bakteriol. 226:376389.
123. Walsh, S. E.,, J. Y. Maillard,, A. D. Russell,, C. E. Catrenich,, D. L. Charbonneau,, and R. G. Bartolo. 2003. Development of bacterial resistance to several biocides and effects on antibiotic susceptibility. J. Hosp. Infect. 55:98107.
124. Webber, M. A.,, and L. J. Piddock. 2003. The importance of efflux pumps in bacterial antibiotic resistance. J. Antimicrob. Chemother. 51:911.
125. White, D. G.,, J. D. Goldman,, B. Demple,, and S. B. Levy. 1997. Role of the acrAB locus in organic solvent tolerance mediated by expression of marA, soxS, or robA in Escherichia coli. J. Bacteriol. 179:61226126.


Generic image for table
Table 1

Biocides and their mechanisms of action

Compiled from references , and .

Citation: Marshall B, McMurry L. 2005. Biocides and Resistance, p 174-190. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch12
Generic image for table
Table 2

In vitro biocide adaptation/mutation and cross-resistance to unrelated biocides and antibiotics

Partially or fully resistant to one or more of the stated agents.

QAC, quaternary ammonium compounds.

MRSA, methicillin-resistant

Citation: Marshall B, McMurry L. 2005. Biocides and Resistance, p 174-190. In White D, Alekshun M, McDermott P (ed), Frontiers in Antimicrobial Resistance. ASM Press, Washington, DC. doi: 10.1128/9781555817572.ch12

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error