Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens

Antibiotics

Volumn 4, Issue 4, 2015, Pages 567-604

  Wales, Andrew D ^a   Davies, Robert H ^a  

^a VETERINARY LABORATORIES AGENCY   (United Kingdom)

Author keywords

Antimicrobial resistance; Biocide; Heavy metal; Zoonoses

Indexed keywords

ANTIBIOTIC AGENT; BIOCIDE; HEAVY METAL;

ADAPTATION; ANIMAL FOOD; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; BACTERIAL GENETICS; BACTERIAL GROWTH; BIOFILM; CAMPYLOBACTER; CO SELECTION; CROSS RESISTANCE; DRUG USE; ENTEROBACTERIACEAE; ENTEROCOCCUS; ESCHERICHIA COLI; FOOD POISONING; GENE EXPRESSION; IMMUNE SYSTEM; LISTERIA; LIVESTOCK; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MICROBIAL COMMUNITY; MINIMUM BACTERICIDAL CONCENTRATION; MINIMUM INHIBITORY CONCENTRATION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; SALMONELLA ENTERICA; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84960416449     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics4040567     Document Type: Review

References (181)

1. SCENIHR. Assessment of the Antibiotic Resistance Effects of Biocides; Scientific Committee on Emerging and Newly Identified Health Risks, European Commission: Brussels, Belgium, 2009; pp. 1-87.
2. Tumah, H.N. Bacterial biocide resistance. J. Chemother. 2009, 21, 5-15.
3. Sheldon, A.T. Antiseptic “resistance”: Real or perceived threat? Clin. Infect. Dis. 2005, 40, 1650-1656.
4. Fraser, C.M., Bergeron, J.A., Mays, A., Aiello, S.E., Eds. Part VI: Pharmacology. In Merck Veterinary Manual; Merck & Co.: Rahway, NJ, USA, 1991; p. 1472.
5. Duffus, J.H. “Heavy metals” a meaningless term? (IUPAC Technical Report). Pure Appl. Chem. 2002, 74, 793-807.
6. Seiler, C.; Berendonk, T.U. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front. Microbiol. 2012, 3, doi:10.3389/fmicb.2012.00399.
7. Barillo, D.J.; Marx, D.E. Silver in medicine: A brief history BC 335 to present. Burns J. Int. Soc. Burn Inj. 2014, 40 (Suppl. S1), S3-S8.
8. Silver, S. Bacterial silver resistance: Molecular biology and uses and misuses of silver compounds. FEMS Microbiol. Rev. 2003, 27, 341-353.
9. Beyth, N.; Houri-Haddad, Y.; Domb, A.; Khan, W.; Hazan, R.; Beyth, N.; Houri-Haddad, Y.; Domb, A.; Khan, W.; Hazan, R. Alternative antimicrobial approach: Nano-antimicrobial materials. Evid. Based Complement. Altern. Med. 2015, 2015, e246012, doi:10.1155/2015/246012.
10. Norwegian Scientific Committee for Food Safety. Zinc and Copper in Pig and Poultry Production—Fate and Effects in the Food Chain and the Environment; Norwegian Food Safety Authority: Oslo, Norway, 2014; p. 128.
11. Hugo, W.B. A brief history of heat, chemical and radiation preservation and disinfection. Int. Biodeterior. Biodegrad. 1995, 36, 197-217.
12. Morente, E.O.; Fernandez-Fuentes, M.A.; Burgos, M.J.G.; Abriouel, H.; Pulido, R.P.; Galvez, A. Biocide tolerance in bacteria. Int. J. Food Microbiol. 2013, 162, 13-25.
13. Cogliani, C.; Goossens, H.; Greko, C. Restricting antimicrobial use in food animals: Lessons from Europe. Microbe 2011, 6, 274-279.
14. Fernandez-Rubio, C.; Ordonez, C.; Abad-Gonzalez, J.; Garcia-Gallego, A.; Honrubia, M.P.; Mallo, J.J.; Balana-Fouce, R. Butyric acid-based feed additives help protect broiler chickens from Salmonella Enteritidis infection. Poult. Sci. 2009, 88, 943-948.
15. Franz, C.; Baser, K.; Windisch, W. Essential oils and aromatic plants in animal feeding—A European perspective. A review. Flavour Fragr. J. 2010, 25, 327-340.
16. Leeson, S.; Namkung, H.; Antongiovanni, M.; Lee, E.H. Effect of butyric acid on the performance and carcass yield of broiler chickens. Poult. Sci. 2005, 84, 1418-1422.
17. Zeng, Z.; Zhang, S.; Wang, H.; Piao, X. Essential oil and aromatic plants as feed additives in nonruminant nutrition: A review. J. Anim. Sci. Biotechnol. 2015, 6, doi:10.1186/s40104-015-0004-5.
18. Dance, D.A.B.; Pearson, A.D.; Seal, D.V.; Lowes, J.A. A hospital outbreak caused by a chlorhexidine and antibiotic-resistant Proteus mirabilis. J. Hosp. Infect. 1987, 10, 10-16.
19. Griffiths, P.A.; Babb, J.R.; Bradley, C.R.; Fraise, A.P. Glutaraldehyde-resistant Mycobacterium chelonae from endoscope washer disinfectors. J. Appl. Microbiol. 1997, 82, 519-526.
20. Sasatsu, M.; Shimizu, K.; Noguchi, N.; Kono, M. Triclosan-resistant Staphylococcus aureus. Lancet 1993, 341, doi:10.1016/0140-6736(93)90526-M.
21. Alexander, D.M.; Jeawon, R.H.; Persad, S. Disinfectant resistance in antibiotic-resistant organisms. S. Afr. J. Sci. 1991, 87, 614-617.
22. Stickler, D.J.; Thomas, B. Antiseptic and antibiotic resistance in Gram-negative bacteria causing urinary tract infection. J. Clin. Pathol. 1980, 33, 288-296.
23. Fraise, A.P. Biocide abuse and antimicrobial resistance—A cause for concern? J. Antimicrob. Chemother. 2002, 49, 11-12.
24. Russell, A.D. Do biocides select for antibiotic resistance? J. Pharm. Pharmacol. 2000, 52, 227-233.
25. Bloomfield, S.F. Significance of biocide usage and antimicrobial resistance in domiciliary environments. J. Appl. Microbiol. 2002, 92, 144S-157S.
26. Gilbert, P.; McBain, A.J. Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin. Microbiol. Rev. 2003, 16, 189-208.
27. Antunes, P.; Mourao, J.; Pestana, N.; Peixe, L. Leakage of emerging clinically relevant multidrug-resistant Salmonella clones from pig farms. J. Antimicrob. Chemother. 2011, 66, 2028-2032.
28. Davies, R.H.; Dalziel, R.; Gibbens, J.C.; Wilesmith, J.W.; Ryan, J.M.B.; Evans, S.J.; Byrne, C.; Paiba, G.A.; Pascoe, S.J.S.; Teale, C.J. National survey for Salmonella in pigs, cattle and sheep at slaughter in Great Britain (1999-2000). J. Appl. Microbiol. 2004, 96, 750-760.
29. EFSA Panel on Biological Hazards (BIOHAZ). Scientific Opinion on monitoring and assessment of the public health risk of “Salmonella Typhimurium-like” strains. EFSA J. 2010, 8, 1826-1874.
30. Cuny, C.; Friedrich, A.; Kozytska, S.; Layer, F.; Nübel, U.; Ohlsen, K.; Strommenger, B.; Walther, B.; Wieler, L.; Witte, W. Emergence of methicillin-resistant Staphylococcus aureus (MRSA) in different animal species. Int. J. Med. Microbiol. 2010, 300, 109-117.
31. Blaak, H.; van Hoek, A.H.; Hamidjaja, R.A.; van der Plaats, R.Q.J.; de Heer, K.L.; de Roda Husman, A.M.; Schets, F.M. Distribution, numbers, and diversity of ESBL-producing E. coli in the poultry farm environment. PLoS ONE 2015, 10, e0135402.
32. Chopra, I.; Hesse, L.; O’Neill, A.J. Exploiting current understanding of antibiotic action for discovery of new drugs. J. Appl. Microbiol. 2002, 92, 4S-15S.
33. Cerf, O.; Carpentier, B.; Sanders, P. Tests for determining in-use concentrations of antibiotics and disinfectants are based on entirely different concepts: “Resistance” has different meanings. Int. J. Food Microbiol. 2010, 136, 247-254.
34. Poole, K. Mechanisms of bacterial biocide and antibiotic resistance. J. Appl. Microbiol. 2002, 92, 55S-64S.
35. Kohanski, M.A.; DePristo, M.A.; Collins, J.J. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 2010, 37, 311-320.
36. Maillard, J.Y. Bacterial target sites for biocide action. J. Appl. Microbiol. 2002, 92, 16S-27S.
37. McDonnell, G.; Russell, A.D. Antiseptics and disinfectants: Activity, action, and resistance. Clin. Microbiol. Rev. 1999, 12, 147-179.
38. Russell, A.D. Biocide use and antibiotic resistance: The relevance of laboratory findings to clinical and environmental situations. Lancet Infect. Dis. 2003, 3, 794-803.
39. Buffet-Bataillon, S.; Tattevin, P.; Bonnaure-Mallet, M.; Jolivet-Gougeon, A. Emergence of resistance to antibacterial agents: The role of quaternary ammonium compounds-a critical review. Int. J. Antimicrob. Agents 2012, 39, 381-389.
40. Davin-Regli, A.; Pagès, J.M. Cross-resistance between biocides and antimicrobials: An emerging question. Rev. Sci. Technol. Off. Int. Epizoot. 2012, 31, 89-104.
41. Carey, D.E.; McNamara, P.J. The impact of triclosan on the spread of antibiotic resistance in the environment. Front. Microbiol. 2015, 5, doi:10.3389/fmicb.2014.00780.
42. Rensch, U.; Klein, G.; Kehrenberg, C. Analysis of triclosan-selected Salmonella enterica mutants of eight serovars revealed increased aminoglycoside susceptibility and reduced growth rates. PLoS ONE 2013, 8, e78310.
43. Suller, M.T.E.; Russell, A.D. Triclosan and antibiotic resistance in Staphylococcus aureus. J. Antimicrob. Chemother. 2000, 46, 11-18.
44. Mavri, A.; Mozina, S.S. Development of antimicrobial resistance in Campylobacter jejuni and Campylobacter coli adapted to biocides. Int. J. Food Microbiol. 2013, 160, 304-312.
45. Medardus, J.J.; Molla, B.Z.; Nicol, M.; Morrow, W.M.; Rajala-Schultz, P.J.; Kazwala, R.; Gebreyes, W.A. In-feed use of heavy metal micronutrients in US swine production systems and its role in persistence of multidrug-resistant Salmonella. Appl. Environ. Microbiol. 2014, 80, 2317-2325.
46. Nicholson, F.A.; Smith, S.R.; Alloway, B.J.; Carlton-Smith, C.; Chambers, B.J. An inventory of heavy metals inputs to agricultural soils in England and Wales. Sci. Total Environ. 2003, 311, 205-219.
47. Berg, J.; Thorsen, M.K.; Holm, P.E.; Jensen, J.; Nybroe, O.; Brandt, K.K. Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivation-independent bacterial community tolerance assay. Environ. Sci. Technol. 2010, 44, 8724-8728.
48. Hao, X.; Luethje, F.L.; Qin, Y.; McDevitt, S.F.; Lutay, N.; Hobman, J.L.; Asiani, K.; Soncini, F.C.; German, N.; Zhang, S.; et al. Survival in amoeba-a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a “copper pathogenicity island”. Appl. Microbiol. Biotechnol. 2015, 99, 5817-5824.
49. Yazdankhah, S.; Rudi, K.; Bernhoft, A. Zinc and copper in animal feed—Development of resistance and co-resistance to antimicrobial agents in bacteria of animal origin. Microb. Ecol. Health Dis. 2014, 25, doi:10.3402/mehd.v25.25862.
50. Hasman, H.; Kempf, I.; Chidaine, B.; Cariolet, R.; Ersbøll, A.K.; Houe, H.; Hansen, H.C.B.; Aarestrup, F.M. Copper resistance in Enterococcus faecium, mediated by the tcrB gene, is selected by supplementation of pig feed with copper sulfate. Appl. Environ. Microbiol. 2006, 72, 5784-5789.
51. Shelton, N.W.; Jacob, M.E.; Tokach, M.D.; Nelssen, J.L.; Goodband, R.D.; Dritz, S.S.; de Rouchey, J.M.; Amachawadi, R.G.; Shi, X.; Nagaraja, T.G. Effects of copper sulfate, zinc oxide, and neoterramycin on weanling pig growth and antibiotic resistance rate for fecal Escherichia coli. In Kansas State University Swine Day 2009. Report of Progress 1020; Goodband, B., Tokach, M., Dritz, S., de Rouchey, J., Eds.; Kansas State University: Manhattan, KS, USA, 2009; pp. 73-79.
52. Baker-Austin, C.; Wright, M.S.; Stepanauskas, R.; McArthur, J.V. Co-selection of antibiotic and metal resistance. Trends Microbiol. 2006, 14, 176-182.
53. Aarestrup, F.M.; Hasman, H. Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. Vet. Microbiol. 2004, 100, 83-89.
54. Silbergeld, E.K.; Nachman, K. The environmental and public health risks associated with arsenical use in animal feeds. Ann. N. Y. Acad. Sci. 2008, 1140, 346-357.
55. European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Terminology relating to methods for the determination of susceptibility of bacteria to antimicrobial agents. Clin. Microbiol. Infect. 2000, 6, 503-508.
56. Møretrø, T.; Heir, E.; Nesse, L.L.; Vestby, L.K.; Langsrud, S. Control of Salmonella in food related environments by chemical disinfection. Food Res. Int. 2012, 45, 532-544.
57. Suller, M.T.E.; Russell, A.D. Antibiotic and biocide resistance in methicillin-resistant Staphylococcus aureus and vancomycin-resistant enterococcus. J. Hosp. Infect. 1999, 43, 281-291.
58. Capita, R.; Riesco-Peláez, F.; Alonso-Hernando, A.; Alonso-Calleja, C. Exposure of Escherichia coli ATCC 12806 to sublethal concentrations of food-grade biocides influences its ability to form biofilm, resistance to antimicrobials, and ultrastructure. Appl. Environ. Microbiol. 2014, 80, 1268-1280.
59. Lear, J.C.; Maillard, J.Y.; Dettmar, P.W.; Goddard, P.A.; Russell, A.D. Chloroxylenol- and triclosan-tolerant bacteria from industrial sources—Susceptibility to antibiotics and other biocides. Int. Biodeterior. Biodegrad. 2006, 57, 51-56.
60. Tabak, M.; Scher, K.; Hartog, E.; Romling, U.; Matthews, K.R.; Chikindas, M.L.; Yaron, S. Effect of triclosan on Salmonella typhimurium at different growth stages and in biofilms. FEMS Microbiol. Lett. 2007, 267, 200-206.
61. Bednorz, C.; Oelgeschlaeger, K.; Kinnemann, B.; Hartmann, S.; Neumann, K.; Pieper, R.; Bethe, A.; Semmler, T.; Tedin, K.; Schierack, P.; et al. The broader context of antibiotic resistance: Zinc feed supplementation of piglets increases the proportion of multi-resistant Escherichia coli in vivo. Int. J. Med. Microbiol. 2013, 303, 396-403.
62. Condell, O.; Iversen, C.; Cooney, S.; Power, K.A.; Walsh, C.; Burgess, C.; Fanning, S. Efficacy of biocides used in the modern food industry to control Salmonella enterica, and links between biocide tolerance and resistance to clinically relevant antimicrobial compounds. Appl. Environ. Microbiol. 2012, 78, 3087-3097.
63. Russell, A.D. Mechanisms of bacterial resistance to biocides. Int. Biodeterior. Biodegrad. 1995, 36, 247-265.
64. Oggioni, M.R.; Furi, L.; Coelho, J.R.; Maillard, J.Y.; Martinez, J.L. Recent advances in the potential interconnection between antimicrobial resistance to biocides and antibiotics. Expert Rev. Anti Infect. Ther. 2013, 11, 363-366.
65. Gilbert, P.; Allison, D.G.; McBain, A.J. Biofilms in vitro and in vivo: Do singular mechanisms imply cross-resistance? J. Appl. Microbiol. 2002, 92, 98S-110S.
66. McBain, A.J.; Gilbert, P. Biocide tolerance and the harbingers of doom. Int. Biodeterior. Biodegrad. 2001, 47, 55-61.
67. Pagedar, A.; Singh, J.; Batish, V.K. Adaptation to benzalkonium chloride and ciprofloxacin affects biofilm formation potential, efflux pump and haemolysin activity of Escherichia coli of dairy origin. J. Dairy Res. 2012, 79, 383-389.
68. Sheridan, Á.; Lenahan, M.; Condell, O.; Bonilla-Santiago, R.; Sergeant, K.; Renaut, J.; Duffy, G.; Fanning, S.; Nally, J.E.; Burgess, C.M. Proteomic and phenotypic analysis of triclosan tolerant verocytotoxigenic Escherichia coli O157:H19. J. Proteomics 2013, 80, 78-90.
69. Poole, K. Efflux pumps as antimicrobial resistance mechanisms. Ann. Med. 2007, 39, 162-176.
70. Hegstad, K.; Langsrud, S.; Lunestad, B.T.; Scheie, A.A.; Sunde, M.; Yazdankhah, S.P. Does the wide use of quaternary ammonium compounds enhance the selection and spread of antimicrobial resistance and thus threaten our health? Microb. Drug Resist. 2010, 16, 91-104.
71. Huet, A.A.; Raygada, J.L.; Mendiratta, K.; Seo, S.M.; Kaatz, G.W. Multidrug efflux pump overexpression in Staphylococcus aureus after single and multiple in vitro exposures to biocides and dyes. Microbiol. SGM 2008, 154, 3144-3153.
72. Putman, M.; van Veen, H.W.; Konings, W.N. Molecular properties of bacterial multidrug transporters. Microbiol. Mol. Biol. Rev. 2000, 64, 672-693.
73. Oethinger, M.; Kern, W.V.; Jellen-Ritter, A.S.; McMurry, L.M.; Levy, S.B. Ineffectiveness of topoisomerase mutations in mediating clinically significant fluoroquinolone resistance in Escherichia coli in the absence of the AcrAB efflux pump. Antimicrob. Agents Chemother. 2000, 44, 10-13.
74. Jaglic, Z.; Cervinkova, D. Genetic basis of resistance to quaternary ammonium compounds—The qac genes and their role: A review. Vet. Med. 2012, 57, 275-281.
75. Gilbert, P.; McBain, A.J.; Bloomfield, S.F. Biocide abuse and antimicrobial resistance: Being clear about the issues. J. Antimicrob. Chemother. 2002, 50, 137-139.
76. Langsrud, S.; Sundheim, G.; Holck, A.L. Cross-resistance to antibiotics of Escherichia coli adapted to benzalkonium chloride or exposed to stress-inducers. J. Appl. Microbiol. 2004, 96, 201-208.
77. Trias, J.; Benz, R. Permeability of the cell wall of Mycobacterium smegmatis. Mol. Microbiol. 1994, 14, 283-290.
78. Karatzas, K.A.G.; Randall, L.P.; Webber, M.; Piddock, L.J.V.; Humphrey, T.J.; Woodward, M.J.; Coldham, N.G. Phenotypic and proteomic characterization of multiply antibiotic-resistant variants of Salmonella enterica serovar Typhimurium selected following exposure to disinfectants. Appl. Environ. Microbiol. 2008, 74, 1508-1516.
79. Grkovic, S.; Brown, M.H.; Skurray, R.A. Regulation of bacterial drug export systems. Microbiol. Mol. Biol. Rev. 2002, 66, 671-701.
80. Oethinger, M.; Podglajen, I.; Kern, W.V.; Levy, S.B. Overexpression of the marA or soxS regulatory gene in clinical topoisomerase mutants of Escherichia coli. Antimicrob. Agents Chemother. 1998, 42, 2089-2094.
81. Hao, Z.; Lou, H.; Zhu, R.; Zhu, J.; Zhang, D.; Zhao, B.S.; Zeng, S.; Chen, X.; Chan, J.; He, C.; et al. The multiple antibiotic resistance regulator MarR is a copper sensor in Escherichia coli. Nat. Chem. Biol. 2014, 10, 21-28.
82. Lee, H.H.; Molla, M.N.; Cantor, C.R.; Collins, J.J. Bacterial charity work leads to population-wide resistance. Nature 2010, 467, 82-85.
83. Threlfall, E.J. Epidemic Salmonella typhimurium DT 104—A truly international multiresistant clone. J. Antimicrob. Chemother. 2000, 46, 7-10.
84. Ciric, L.; Mullany, P.; Roberts, A.P. Antibiotic and antiseptic resistance genes are linked on a novel mobile genetic element: Tn6087. J. Antimicrob. Chemother. 2011, 66, 2235-2239.
85. Carattoli, A. Importance of integrons in the diffusion of resistance. Vet. Res. 2001, 32, doi:10.1051/vetres:2001122.
86. Paulsen, I.T.; Littlejohn, T.G.; Rådström, P.; Sundström, L.; Sköld, O.; Swedberg, G.; Skurray, R.A. The 3’-conserved segment of integrons contains a gene associated with multidrug resistance to antiseptics and disinfectants. Antimicrob. Agents Chemother. 1993, 37, 761-768.
87. Agga, G.E.; Scott, H.M.; Amachawadi, R.G.; Nagaraja, T.G.; Vinasco, J.; Bai, J.; Norby, B.; Renter, D.G.; Dritz, S.S.; Nelssen, J.L.; et al. Effects of chlortetracycline and copper supplementation on antimicrobial resistance of fecal Escherichia coli from weaned pigs. Prev. Vet. Med. 2014, 114, 231-246.
88. Gullberg, E.; Albrecht, L.M.; Karlsson, C.; Sandegren, L.; Andersson, D.I. Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. MBIO 2014, 5, doi:10.1128/mBio.01918-14.
89. Randall, L.P.; Cooles, S.W.; Piddock, L.J.V.; Woodward, M.J. Effect of triclosan or a phenolic farm disinfectant on the selection of antibiotic-resistant Salmonella enterica. J. Antimicrob. Chemother. 2004, 54, 621-627.
90. Kastbjerg, V.G.; Hein-Kristensen, L.; Gram, L. Triclosan-induced aminoglycoside-tolerant Listeria monocytogenes isolates can appear as small-colony variants. Antimicrob. Agents Chemother. 2014, 58, 3124-3132.
91. Guo, M.T.; Yuan, Q.B.; Yang, J. Distinguishing effects of ultraviolet exposure and chlorination on the horizontal transfer of antibiotic resistance genes in municipal wastewater. Environ. Sci. Technol. 2015, 49, 5771-5778.
92. Rensing, C.; Grass, G. Escherichia coli mechanisms of copper homeostasis in a changing environment. FEMS Microbiol. Rev. 2003, 27, 197-213.
93. Beard, S.J.; Ciccognani, D.T.; Hughes, M.N.; Poole, R.K. Metal ion-catalysed hydrolysis of ampicillin in microbiological growth media. FEMS Microbiol. Lett. 1992, 96, 207-211.
94. Hölzel, C.S.; Müller, C.; Harms, K.S.; Mikolajewski, S.; Schäfer, S.; Schwaiger, K.; Bauer, J. Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance. Environ. Res. 2012, 113, 21-27.
95. Mukherjee, G.; Ghosh, T. Metal ion interaction with penicillins—Part VII: Mixed-ligand complex formation of cobalt (II), nickel (II), copper (II), and zinc (II) with ampicillin and nucleic bases. J. Inorg. Biochem. 1995, 59, 827-833.
96. Rutala, W.A.; Stiegel, M.M.; Sarubbi, F.A.; Weber, D.J. Susceptibility of antibiotic-susceptible and antibiotic-resistant hospital bacteria to disinfectants. Infect. Control Hosp. Epidemiol. 1997, 18, 417-421.
97. McLaren, I.; Wales, A.; Breslin, M.; Davies, R. Evaluation of commonly-used farm disinfectants in wet and dry models of Salmonella farm contamination. Avian Pathol. 2011, 40, 33-42.
98. Holman, D.B.; Chénier, M.R. Temporal changes and the effect of subtherapeutic concentrations of antibiotics in the gut microbiota of swine. FEMS Microbiol. Ecol. 2014, 90, 599-608.
99. Stepanauskas, R.; Glenn, T.C.; Jagoe, C.H.; Tuckfield, R.C.; Lindell, A.H.; King, C.J.; McArthur, J.V. Coselection for microbial resistance to metals and antibiotics in freshwater microcosms. Environ. Microbiol. 2006, 8, 1510-1514.
100. Tandukar, M.; Oh, S.; Tezel, U.; Konstantinidis, K.T.; Pavlostathis, S.G. Long-term exposure to benzalkonium chloride disinfectants results in change of microbial community structure and increased antimicrobial resistance. Environ. Sci. Technol. 2013, 47, 9730-9738.
101. Yazdankhah, S.P.; Scheie, A.A.; Høiby, E.A.; Lunestad, B.T.; Heir, E.; Fotland, T.Ø.; Naterstad, K.; Kruse, H. Triclosan and antimicrobial resistance in bacteria: An overview. Microb. Drug Resist. 2006, 12, 83-90.
102. Buffet-Bataillon, S.; Branger, B.; Cormier, M.; Bonnaure-Mallet, M.; Jolivet-Gougeon, A. Effect of higher minimum inhibitory concentrations of quaternary ammonium compounds in clinical E. coli isolates on antibiotic susceptibilities and clinical outcomes. J. Hosp. Infect. 2011, 79, 141-146.
103. Buffet-Bataillon, S.; le Jeune, A.; le Gall-David, S.; Bonnaure-Mallet, M.; Jolivet-Gougeon, A. Molecular mechanisms of higher MICs of antibiotics and quaternary ammonium compounds for Escherichia coli isolated from bacteraemia. J. Antimicrob. Chemother. 2012, 67, 2837-2842.
104. Willinghan, E.M.; Sander, J.E.; Thayer, S.G.; Wilson, J.L. Investigation of bacterial resistance to hatchery disinfectants. Avian Dis. 1996, 40, 510-515.
105. Martin, H.; Maris, P. Resistance of 310 Gram-positive strains isolated from milking cow udders. Vet. Res. 1995, 26, 43-56.
106. Lear, J.C.; Maillard, J.Y.; Dettmar, P.W.; Goddard, P.A.; Russell, A.D. Chloroxylenol- and triclosan-tolerant bacteria from industrial sources. J. Ind. Microbiol. Biotechnol. 2002, 29, 238-242.
107. Braoudaki, M.; Hilton, A.C. Adaptive resistance to biocides in Salmonella enterica and Escherichia coli O157 and cross-resistance to antimicrobial agents. J. Clin. Microbiol. 2004, 42, 73-78.
108. Ledder, R.G.; Gilbert, P.; Willis, C.; McBain, A.J. Effects of chronic triclosan exposure upon the antimicrobial susceptibility of 40 ex-situ environmental and human isolates. J. Appl. Microbiol. 2006, 100, 1132-1140.
109. McBain, A.J.; Ledder, R.G.; Sreenivasan, P.; Gilbert, P. Selection for high-level resistance by chronic triclosan exposure is not universal. J. Antimicrob. Chemother. 2004, 53, 772-777.
110. Sheridan, À.; Lenahan, M.; Duffy, G.; Fanning, S.; Burgess, C. The potential for biocide tolerance in Escherichia coli and its impact on the response to food processing stresses. Food Control 2012, 26, 98-106.
111. Karatzas, K.A.G.; Webber, M.A.; Jorgensen, F.; Woodward, M.J.; Piddock, L.J.V.; Humphrey, T.J. Prolonged treatment of Salmonella enterica serovar Typhimurium with commercial disinfectants selects for multiple antibiotic resistance, increased efflux and reduced invasiveness. J. Antimicrob. Chemother. 2007, 60, 947-955.
112. Alonso-Hernando, A.; Capita, R.; Prieto, M.; Alonso-Calleja, C. Comparison of antibiotic resistance patterns in Listeria monocytogenes and Salmonella enterica strains pre-exposed and exposed to poultry decontaminants. Food Control 2009, 20, 1108-1111.
113. Soumet, C.; Fourreau, E.; Legrandois, P.; Maris, P. Resistance to phenicol compounds following adaptation to quaternary ammonium compounds in Escherichia coli. Vet. Microbiol. 2012, 158, 147-152.
114. EFSA Panel on Biological Hazards (BIOHAZ). Assessment of the possible effect of the four antimicrobial treatment substances on the emergence of antimicrobial resistanc. EFSA J. 2008, 6, doi:10.2903/j.efsa.2008.659.
115. Potenski, C.J.; Gandhi, M.; Matthews, K.R. Exposure of Salmonella Enteritidis to chlorine or food preservatives increases susceptibility to antibiotics Corrigendum: The correct title is “Exposure of Salmonella Enteritidis to chlorine or food preservatives decreases susceptibility to antibiotics”. FEMS Microbiol. Lett. 2003, 220, 181-186.
116. Pumbwe, L.; Skilbeck, C.A.; Wexler, H.M. 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. 2007, 60, 1288-1297.
117. McMurry, L.M.; Oethinger, M.; Levy, S.B. Overexpression of marA, soxS, or acrAB produces resistance to triclosan in laboratory and clinical strains of Escherichia coli. FEMS Microbiol. Lett. 1998, 166, 305-309.
118. Braoudaki, M.; Hilton, A.C. Mechanisms of resistance in Salmonella enterica adapted to erythromycin, benzalkonium chloride and triclosan. Int. J. Antimicrob. Agents 2005, 25, 31-37.
119. Whitehead, R.N.; Overton, T.W.; Kemp, C.L.; Webber, M.A. Exposure of Salmonella enterica serovar Typhimurium to high level biocide challenge can select multidrug resistant mutants in a single step. PLoS ONE 2011, 6, e22833.
120. Fernández-Fuentes, M.A.; Morente, E.O.; Abriouel, H.; Pulido, R.P.; Gálvez, A. Antimicrobial resistance determinants in antibiotic and biocide-resistant gram-negative bacteria from organic foods. Food Control 2014, 37, 9-14.
121. Thorrold, C.A.; Letsoalo, M.E.; Duse, A.G.; Marais, E. Efflux pump activity in fluoroquinolone and tetracycline resistant Salmonella and E. coli implicated in reduced susceptibility to household antimicrobial cleaning agents. Int. J. Food Microbiol. 2007, 113, 315-320.
122. Yamamoto, T.; Tamura, Y.; Yokota, T. Antiseptic and antibiotic resistance plasmid in Staphylococcus aureus that possesses ability to confer chlorhexidine and acrinol resistance. Antimicrob. Agents Chemother. 1988, 32, 932-935.
123. Cervinkova, D.; Babak, V.; Marosevic, D.; Kubikova, I.; Jaglic, Z. The role of the qacA gene in mediating resistance to quaternary ammonium compounds. Microb. Drug Resist. 2012, 19, 160-167.
124. Berg, J.; Tom-Petersen, A.; Nybroe, O. Copper amendment of agricultural soil selects for bacterial antibiotic resistance in the field. Lett. Appl. Microbiol. 2005, 40, 146-151.
125. Cavaco, L.M.; Hasman, H.; Stegger, M.; Andersen, P.S.; Skov, R.; Fluit, A.C.; Ito, T.; Aarestrup, F.M. Cloning and occurrence of czrC, a gene conferring cadmium and zinc resistance in methicillin-resistant Staphylococcus aureus CC398 isolates. Antimicrob. Agents Chemother. 2010, 54, 3605-3608.
126. Vahjen, W.; Pietruszyńska, D.; Starke, I.C.; Zentek, J. High dietary zinc supplementation increases the occurrence of tetracycline and sulfonamide resistance genes in the intestine of weaned pigs. Gut Pathog. 2015, 7, doi:10.1186/s13099-015-0071-3.
127. Solioz, M.; Stoyanov, J.V. Copper homeostasis in Enterococcus hirae. FEMS Microbiol. Rev. 2003, 27, 183-195.
128. Çardak, M.; Altug, G. Species distribution and heavy metal resistance of Enterobacteriaceae members isolated from Istanbul Strait. Fresenius Environ. Bull. 2014, 23, 2620-2626.
129. Hasman, H.; Aarestrup, F.M. tcrB a gene conferring transferable copper resistance in Enterococcus faecium: Occurrence, transferability, and linkage to macrolide and glycopeptide resistance. Antimicrob. Agents Chemother. 2002, 46, 1410-1416.
130. Klare, I.; Heier, H.; Claus, H.; Reissbrodt, R.; Witte, W. vanA-mediated high-level glycopeptide resistance in Enterococcus faecium from animal husbandry. FEMS Microbiol. Lett. 1995, 125, 165-172.
131. Becerril, R.; Nerin, C.; Gomez-Lus, R. Evaluation of bacterial resistance to essential oils and antibiotics after exposure to oregano and cinnamon essential oils. Foodborne Pathog. Dis. 2012, 9, 699-705.
132. Fadli, M.; Chevalier, J.; Hassani, L.; Mezrioui, N.E.; Pages, J.M. Natural extracts stimulate membrane-associated mechanisms of resistance in Gram-negative bacteria. Lett. Appl. Microbiol. 2014, 58, 472-477.
133. McMahon, M.A.S.; Blair, I.S.; Moore, J.E.; McDowell, D.A. Habituation to sub-lethal concentrations of tea tree oil (Melaleuca alternifolia) is associated with reduced susceptibility to antibiotics in human pathogens. J. Antimicrob. Chemother. 2007, 59, 125-127.
134. Oosterik, L.H.; Peeters, L.; Mutuku, I.; Goddeeris, B.M.; Butaye, P. Susceptibility of Avian Pathogenic Escherichia coli from laying hens in Belgium to antibiotics and disinfectants and integron prevalence. Avian Dis. 2014, 58, 271-278.
135. Zou, L.; Meng, J.; McDermott, P.F.; Wang, F.; Yang, Q.; Cao, G.; Hoffmann, M.; Zhao, S. Presence of disinfectant resistance genes in Escherichia coli isolated from retail meats in the USA. J. Antimicrob. Chemother. 2014, 69, 2644-2649.
136. Randall, L.P.; Clouting, C.S.; Gradel, K.O.; Clifton-Hadley, F.A.; Davies, R.D.; Woodward, M.J. Farm disinfectants select for cyclohexane resistance, a marker of multiple antibiotic resistance, in Escherichia coli. J. Appl. Microbiol. 2005, 98, 556-563.
137. Braoudaki, M.; Hilton, A.C. 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. 2004, 235, 305-309.
138. Gradel, K.O.; Randall, L.; Sayers, A.R.; Davies, R.H. Possible associations between Salmonella persistence in poultry houses and resistance to commonly used disinfectants and a putative role of mar. Vet. Microbiol. 2005, 107, 127-138.
139. Gantzhorn, M.R.; Pedersen, K.; Olsen, J.E.; Thomsen, L.E. Biocide and antibiotic susceptibility of Salmonella isolates obtained before and after cleaning at six Danish pig slaughterhouses. Int. J. Food Microbiol. 2014, 181, 53-59.
140. Chuanchuen, R.; Pathanasophon, P.; Khemtong, S.; Wannaprasat, W.; Padungtod, P. Susceptibilities to antimicrobials and disinfectants in Salmonella isolates obtained from poultry and swine in Thailand. J. Vet. Med. Sci. 2008, 70, 595-601.
141. Copitch, J.L.; Whitehead, R.N.; Webber, M.A. Prevalence of decreased susceptibility to triclosan in Salmonella enterica isolates from animals and humans and association with multiple drug resistance. Int. J. Antimicrob. Agents 2010, 36, 247-251.
142. Randall, L.P.; Cooles, S.W.; Sayers, A.R.; Woodward, M.J. Association between cyclohexane resistance in Salmonella of different serovars and increased resistance to multiple antibiotics, disinfectants and dyes. J. Med. Microbiol. 2001, 50, 919-924.
143. Guo, W.; Cui, S.; Xu, X.; Wang, H. Resistant mechanism study of benzalkonium chloride selected Salmonella Typhimurium mutants. Microb. Drug Resist. 2014, 20, 11-16.
144. Randall, L.P.; Cooles, S.W.; Coldham, N.G.; Penuela, E.G.; Mott, A.C.; Woodward, M.J.; Piddock, L.J.V.; Webber, M.A. 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. 2007, 60, 1273-1280.
145. Randall, L.P.; Bagnall, M.C.; Karatzas, K.A.; Coldham, N.C.; Piddock, L.J.V.; Woodward, M.J. Fitness and dissemination of disinfectant-selected multiple-antibiotic-resistant (MAR) strains of Salmonella enterica serovar Typhimurium in chickens. J. Antimicrob. Chemother. 2008, 61, 156-162.
146. Birošová, L.; Mikulášová, M. Development of triclosan and antibiotic resistance in Salmonella enterica serovar Typhimurium. J. Med. Microbiol. 2009, 58, 436-441.
147. Geornaras, I.; Yang, H.; Moschonas, G.; Nunnelly, M.C.; Belk, K.E.; Nightingale, K.K.; Woerner, D.R.; Smith, G.C.; Sofos, J.N. Efficacy of chemical interventions against Escherichia coli O157:H7 and multidrug-resistant and antibiotic-susceptible Salmonella on inoculated beef trimmings. J. Food Prot. 2012, 75, 1960-1967.
148. Capita, R. Variation in Salmonella resistance to poultry chemical decontaminants, based on serotype, phage type, and antibiotic resistance patterns. J. Food Prot. 2007, 70, 1835-1843.
149. Molina-González, D.; Alonso-Calleja, C.; Alonso-Hernando, A.; Capita, R. Effect of sub-lethal concentrations of biocides on the susceptibility to antibiotics of multi-drug resistant Salmonella enterica strains. Food Control 2014, 40, 329-334.
150. Mourão, J.; Novais, C.; Machado, J.; Peixe, L.; Antunes, P. Metal tolerance in emerging clinically relevant multidrug-resistant Salmonella enterica serotype 4,[5],12:i:—Clones circulating in Europe. Int. J. Antimicrob. Agents 2015, 45, 610-616.
151. Hasman, H.; Moodley, A.; Guardabassi, L.; Stegger, M.; Skov, R.L.; Aarestrup, F.M. Spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet. Microbiol. 2010, 141, 326-331.
152. Aarestrup, F.M.; Cavaco, L.; Hasman, H. Decreased susceptibility to zinc chloride is associated with methicillin resistant Staphylococcus aureus CC398 in Danish swine. Vet. Microbiol. 2010, 142, 455-457.
153. Moodley, A.; Nielsen, S.S.; Guardabassi, L. Author’s response: Critique of paper on “Effects of tetracycline and zinc on selection of methicillin-resistant Staphylococcus aureus (MRSA) sequence type 398 in pigs”. Vet. Microbiol. 2014, 173, 401-402.
154. Moodley, A.; Nielsen, S.S.; Guardabassi, L. Effects of tetracycline and zinc on selection of methicillin-resistant Staphylococcus aureus (MRSA) sequence type 398 in pigs. Vet. Microbiol. 2011, 152, 420-423.
155. Slifierz, M.J.; Friendship, R.; Weese, J.S. Zinc oxide therapy increases prevalence and persistence of methicillin-resistant Staphylococcus aureus in pigs: A randomized controlled trial. Zoonoses Public Health 2015, 62, 301-308.
156. Slifierz, M.J.; Friendship, R.M.; Weese, J.S. Methicillin-resistant Staphylococcus aureus in commercial swine herds is associated with disinfectant and zinc usage. Appl. Environ. Microbiol. 2015, 81, 2690-2695.
157. Millar, M.R.; Griffin, N.; Keyworth, N. Pattern of antibiotic and heavy-metal ion resistance in recent hospital isolates of Staphylococcus aureus. Epidemiol. Infect. 1987, 99, 343-347.
158. Poston, S.M.; Li Saw Hee, F.L. Genetic characterisation of resistance to metal ions in methicillin-resistant Staphylococcus aureus: Elimination of resistance to cadmium, mercury and tetracycline with loss of methicillin resistance. J. Med. Microbiol. 1991, 34, 193-201.
159. Townsend, D.E.; Grubb, W.B.; Ashdown, N. Genetics of drug resistance in methicillin-resistant Staphylococcus aureus from Australian hospitals. J. Hosp. Infect. 1983, 4, 331-337.
160. Gómez-Sanz, E.; Kadlec, K.; Feßler, A.T.; Zarazaga, M.; Torres, C.; Schwarz, S. Novel erm(T)-carrying multiresistance plasmids from porcine and human isolates of methicillin-resistant Staphylococcus aureus ST398 that also harbor cadmium and copper resistance determinants. Antimicrob. Agents Chemother. 2013, 57, 3275-3282.
161. Bae, D.; Mezal, E.H.; Smiley, R.D.; Cheng, C.M.; Khan, A.A. The sub-species characterization and antimicrobial resistance of Listeria monocytogenes isolated from domestic and imported food products from 2004 to 2011. Food Res. Int. 2014, 64, 656-663.
162. Ortiz, S.; Lopez, P.; Lopez, V.; Martinez-Suarez, J.V. Antibiotic susceptibility in benzalkonium chloride-resistant and -susceptible Listeria monocytogenes strains. Foodborne Pathog. Dis. 2014, 11, 517-519.
163. Aarestrup, F.M.; Knöchel, S.; Hasman, H. Antimicrobial susceptibility of Listeria monocytogenes from food products. Foodborne Pathog. Dis. 2007, 4, 216-221.
164. Rakic-Martinez, M.; Drevets, D.A.; Dutta, V.; Katic, V.; Kathariou, S. Listeria monocytogenes strains selected on ciprofloxacin or the disinfectant benzalkonium chloride exhibit reduced susceptibility to ciprofloxacin, gentamicin, benzalkonium chloride, and other toxic compounds. Appl. Environ. Microbiol. 2011, 77, 8714-8721.
165. Romanova, N.A.; Wolffs, P.F.G.; Brovko, L.Y.; Griffiths, M.W. Role of efflux pumps in adaptation and resistance of Listeria monocytogenes to benzalkonium chloride. Appl. Environ. Microbiol. 2006, 72, 3498-3503.
166. Christensen, E.G.; Gram, L.; Kastbjerg, V.G. Sublethal triclosan exposure decreases susceptibility to gentamicin and other aminoglycosides in Listeria monocytogenes. Antimicrob. Agents Chemother. 2011, 55, 4064-4071.
167. López-Alonso, V.; Ortiz, S.; Martinez-Suárez, J.V. Genome sequences of five disinfectant-resistant Listeria monocytogenes strains from two Iberian pork-processing plants. Genome Announc. 2015, 3, e00077-15.
168. Mavri, A.; Kurinčić, M.; Možina, S.S. The prevalence of antibiotic and biocide resistance among Campylobacter coli and Campylobacter jejuni from different sources. Food Technol. Biotechnol. 2012, 50, 371-376.
169. Randall, L.P.; Ridley, A.M.; Cooles, S.W.; Sharma, M.; Sayers, A.R.; Pumbwe, L.; Newell, D.G.; Piddock, L.J.V.; Woodward, M.J. Prevalence of multiple antibiotic resistance in 443 Campylobacter spp. isolated from humans and animals. J. Antimicrob. Chemother. 2003, 52, 507-510.
170. Sundsfjord, A.; Willems, R. Enterococcus research: Recent developments and clinical challenges. Clin. Microbiol. Infect. 2010, 16, 525-526.
171. Schwaiger, K.; Harms, K.S.; Bischoff, M.; Preikschat, P.; Mölle, G.; Bauer-Unkauf, I.; Lindorfer, S.; Thalhammer, S.; Bauer, J.; Hölzel, C.S. Insusceptibility to disinfectants in bacteria from animals, food and humans—Is there a link to antimicrobial resistance? Front. Microbiol. 2014, 5, doi:10.3389/fmicb.2014.00088.
172. Pasquaroli, S.; di Cesare, A.; Vignaroli, C.; Conti, G.; Citterio, B.; Biavasco, F. Erythromycin- and copper-resistant Enterococcus hirae from marine sediment and co-transfer of erm(B) and tcrB to human Enterococcus faecalis. Diagn. Microbiol. Infect. Dis. 2014, 80, 26-28.
173. Aarestrup, F.M.; Hasman, H.; Jensen, L.B.; Moreno, M.; Herrero, I.A.; Domínguez, L.; Finn, M.; Franklin, A. Antimicrobial resistance among enterococci from pigs in three European countries. Appl. Environ. Microbiol. 2002, 68, 4127-4129.
174. Zhang, S.; Wang, D.; Wang, Y.; Hasman, H.; Aarestrup, F.M.; Alwathnani, H.A.; Zhu, Y.-G.; Rensing, C. Genome sequences of copper resistant and sensitive Enterococcus faecalis strains isolated from copper-fed pigs in Denmark. Stand. Genomic Sci. 2015, 10, doi:10.1186/s40793-015-0021-1.
175. Fard, R.M.N.; Heuzenroeder, M.W.; Barton, M.D. Antimicrobial and heavy metal resistance in commensal enterococci isolated from pigs. Vet. Microbiol. 2011, 148, 276-282.
176. Amachawadi, R.G.; Scott, H.M.; Aperce, C.; Vinasco, J.; Drouillard, J.S.; Nagaraja, T.G. Effects of in-feed copper and tylosin supplementations on copper and antimicrobial resistance in faecal enterococci of feedlot cattle. J. Appl. Microbiol. 2015, 118, 1287-1297.
177. Biswal, B.K.; Khairallah, R.; Bibi, K.; Mazza, A.; Gehr, R.; Masson, L.; Frigon, D. Impact of UV and peracetic acid disinfection on the prevalence of virulence and antimicrobial resistance genes in uropathogenic Escherichia coli in wastewater effluents. Appl. Environ. Microbiol. 2014, 80, 3656-3666.
178. Tuckfield, R.C.; McArthur, J.V. Spatial analysis of antibiotic resistance along metal contaminated streams. Microb. Ecol. 2007, 55, 595-607.
179. Hernández, A.; Ruiz, F.M.; Romero, A.; Martinez, J.L. The binding of triclosan to SmeT, the repressor of the multidrug efflux pump SmeDEF, induces antibiotic resistance in Stenotrophomonas maltophilia. PLOS Pathog. 2011, 7, e1002103.
180. Suling, W.J.; O’Leary, W.M. Effect of surfactants on antibiotic resistance. Antimicrob. Agents Chemother. 1975, 8, 334-343.
181. Zanini, S.F.; Silva-Angulo, A.B.; Rosenthal, A.; Aliaga, D.R.; Martinez, A. Influence of the treatment of Listeria monocytogenes and Salmonella enterica serovar Typhimurium with citral on the efficacy of various antibiotics. Foodborne Pathog. Dis. 2014, 11, 265-271.