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Cross-resistance between biocides and antimicrobials
Chapter 28
Cross-resistance between biocides and antimicrobials Chapter outline Classification of biocides Use of biocides in animal farm, agricultural field and fishery sector How biocides work Mechanism of resistance against biocides Intrinsic resistance Acquired resistance
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Cross-resistance, co-resistance and co-regulation between biocides and antimicrobials Cross-resistance Co-resistance Co-regulation References
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Biocides are defined as active substances or a preparation consisting of more than one active substance used to kill or reduce the virulence of pathogens (SCENIHR, 2009). Widespread use of biocides such as triclosan and quaternary ammonium compounds increases the selection of antimicrobial-resistant bacteria such as Escherichia coli and Staphylococcus aureus in the environment (Mcmurry et al., 1998; Russell, 2000; Wesgate et al., 2016). The heavy metal-based biocides (copper, zinc) are commonly used in livestock farms and aquaculture as footbath or antifouling paints in the cages and nets (Thomsen et al., 2008; Burridge et al., 2010). Use of heavy metals can maintain or increase the antimicrobial resistance in certain bacteria. The United States Food and Drug Administration (FDA) and European Union Biocidal Products Regulation make it mandatory for the manufacturers to declare the level of resistance generated in commensal bacteria after use of their biocidal products.
Classification of biocides The biocides belong to several chemical groups such as alcohol, aldehyde, phenols, biguanide, peroxide, organic acids, metallic salts, halogens, etc. (Table 28.1).
Use of biocides in animal farm, agricultural field and fishery sector In commercial animal or poultry farms, biocides are used for cleaning of farm premises, vehicles, utensils and buildings, foot dips at the entry of animal/poultry houses, teat dips, decontamination of carcasses and preservation of eggs or semen. Disinfection of farm premises, buildings, vehicles and utensils are carried out with hydrogen peroxide, acetic acid, sodium dichloroisocyanurate, quaternary ammonium compounds (didecyldimethylammonium chloride, alkyldimethylbenzylammonium chloride), glutaraldehyde, formaldehyde and isopropanol. The farm boots and tools are disinfected with sodium-p-toluene-sulfonchloramide and hydrogen peroxide. Copper sulphate is used for foot dips to prevent or cure foot rot in sheep and cattle, although banned in European countries (Thomsen et al., 2008). Teat dip with quaternary ammonium compounds, iodine (0.25%e1.0%), chlorine-based compounds [chloroisocyanurate, chlorhexidine (>0.5%), chlorine dioxide (0.32%), sodium hypochlorite] and bronopol is a common practice before or after milking to prevent the entry of organisms and to reduce the bacterial count for at least log 3. The organic acids are added in animal feed or silage as preservatives to reduce the concentration of spoilage bacteria. Certain heavy metals such as zinc oxide (2000e3000 ppm)
Antimicrobial Resistance in Agriculture. https://doi.org/10.1016/B978-0-12-815770-1.00028-6 Copyright © 2020 Elsevier Inc. All rights reserved.
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TABLE 28.1 Classification, mechanism of action and usage of biocides. Biocide
Mechanism of action
Usage
Remarks
Alcohols [ethanol (0.1% e99.9%), methanol (0.03%e15%), phenoxyethanol, propanol, propylene glycol, isopropanol (0.1%e77.22%)]
Inhibition of cell wall and nucleic acid synthesis of bacteria; protein denaturation; proton translocation (phenoxyethanol in Escherichia coli)
a. Used as antiseptic/ disinfectant in health care b. Used as preservative in pharmaceutical/ cosmetic industry
Ethanol/isopropanol (70%e90%) is approved by the US FDA for health care settings
Aldehyde [formaldehyde (0.03%e15.7%), glutaraldehyde (2%)]
Lysis of bacterial cell wall as alkylating agent
a. Used as disinfectant in health care b. Used as preservative in pharmaceutical/ cosmetic/paper industry
Glutaraldehyde (2%) is approved by the US FDA for health care settings
Anionic surfactants (diethylamine)
As a part of a preparation it can lyse bacterial cell wall
a. Used as disinfectant in household products b. Used as preservative in pharmaceutical/ cosmetic industry
e
Biguanides (chlorhexidine digluconate, alexidine, polymeric biguanides)
Chlorhexidine specifically inhibits bacterial cytoplasmic membrane-bound ATPase
Used as disinfectant/antiseptic in household products, health care
e
Diamidines (hexamidine)
Lysis of bacterial cytoplasmic membrane
Used as antiseptic
e
Dyes (acridines, triphenylmethane, quinones)
Lysis of bacterial nucleic acids
Used as antiseptic
e
Halogens (sodium hypochlorite, chloramine, povidoneiodine)
Act as oxidizing agent
Used as disinfectant/ antiseptic in household products, health care, water treatment, industrial products, teat dip in livestock farms
Sodium hypochlorite (5.25% e6.15% household bleach diluted, 1:100, z500 ppm available chlorine) is approved by the US FDA for health care settings
Iodophors
Enzymatic interactions with thiol group
Used as disinfectant/ antiseptic in health care
e
Hydrogen peroxide (0.5% e29%)
Act as oxidizing agent
Used as disinfectant in household products, health care, industrial products
Hydrogen peroxide (1%e7.5%) is approved by the US FDA for health care settings
Pentamidine
Inhibition of bacterial nucleic acid synthesis
Used as disinfectant in medical devices (catheter)
e
Metals (silver nitrate, mercury)
Enzymatic interactions with thiol group
a. Used as disinfectant in health care b. Used as preservative in pharmaceutical industry
e
Chelated metal (copper, mercuric chloride, phenyl mercury, thiomersal)
Bacterial nucleotides act as target of chelated metals
Used as disinfectant in health care, livestock farm, aquaculture
e
Limonene
Unknown interaction with bacterial cytoplasmic membrane
Used as disinfectant in household products and industry
e
Organic acids and esters [parabens, propionic acid, potassium sorbate, sodium
Dissipation of proton motive force in cytoplasmic membrane of Gram-positive
a. Used as disinfectant in health care
e
Continued
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TABLE 28.1 Classification, mechanism of action and usage of biocides.dcont’d Biocide
Mechanism of action
Usage
Remarks
benzoate, acetic acid (0.4%e52%)]
bacteria; inhibition of amino acids uptake in Gram-negative bacteria
b. Used as preservative in pharmaceutical/ cosmetic/food industry
Phenolics [triclosan (2,4,40 -trichloro-20 -hydroxydiphenyl ether, 0.5%); dinitrophenol)
Triclosan binds with enoyl-acyl reductase required for bacterial fatty acid synthesis and acts as bacteriostatic agent Dinitrophenol reduces ATP synthesis in bacterial membrane
c. Used as disinfectant in health care, domestic products such as hand washes
e
Isothiazolinone
Reduces active transport and oxidation of glucose in Staphylococcus aureus
Used as disinfectant in personal care products, household products and industrial products
e
Quaternary ammonium compounds (benzalkonium chloride, cetrimide, cetylpyridinium, dequalinium chloride)
Aggregation of bacterial cytoplasmic membrane proteins and destabilization of the membrane
a. Used as disinfectant in health care, household products, teat dip in livestock farm b. Used as preservative in pharmaceutical/ cosmetic/food industry
e
and copper sulphate (125e250 ppm) are added in pig feed to improve the growth, performance and to prevent scour (Hill et al., 2000). Furthermore, chromium, tin, vanadium, nickel and molybdenum are also added in animal or poultry feed. Owing to lack of knowledge about their precise concentration to be used, most of the commercial animal or poultry feeds contain high concentration of the minerals which are not absorbed through the gut and are excreted directly into the environment (Ao and Pierce, 2013). In agricultural field, biocides are used as insecticide, rodenticide, molluscicide and acaricide to control the pest infestation. Bordeaux mixture [CuSO4 and Ca(OH)2] is applied into vineyards and organic potato farming to control vine downy mildew and potato blight, respectively (Gisi et al., 2009). In aquaculture, iodine, halogens, metallic salts, aldehydes, hydrogen peroxide, quaternary ammonium compounds and dyes are used for disinfection of equipments, ponds and waterbodies and fish eggs (Burridge et al., 2010). In the United States, use of many biocides is regulated by Federal Pesticide Law (FIFRA) and Federal Food, Drugs and Cosmetic Act. In Europe, since 2012e13, biocide use is controlled by Biocidal Products Regulation 528/2012 (BPR) in place of Biocidal Products Directive (BPD, 98/8/EC). Few member countries of European Union and Asian countries have their own published lists of authorized substances to be used as biocide. For example, in Taiwan, use of biocides in animals and plants is regulated by Veterinary Drug Administration Law and Pesticide Management Act. Central Insecticide Board and Registration Committee of India have recently published guidelines for the registration of biocides used in paints.
How biocides work Unlike the antimicrobials, the biocides use vivid mechanisms by which it can kill the organisms or inhibit their growth (Table 28.1, Meyer and Cookson, 2010).
Mechanism of resistance against biocides Since 1950, resistance to biocides was reported in bacterial strains (Davin-Regli and Pagès, 2012). The clinical isolates of E. coli, S. aureus, Mycobacterium chelonae, Burkholderia cepacia and Pseudomonas aeruginosa were detected to be associated with reduced susceptibility to the biocides such as quaternary ammonium compounds, triclosan, paraben, and
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glutaraldehyde (Greenberg and Demple, 1989; Bamber and Neal, 1999; Manzoor et al., 1999; Fraud et al., 2001; Hutchinson et al., 2004; Romão et al., 2005). Intrinsic and acquired resistance mechanisms against biocides are observed in clinical bacterial isolates.
Intrinsic resistance Modification of outer membrane proteins and phospholipids/lipopolysaccharide (LPS) structure in bacterial cell wall is associated with reduced permeability of biocides into the bacterial cell (Guerin-Mechin et al., 2000; Braoudaki and Hilton, 2005). Change in LPS structure increases positive charge of the bacterial outer membrane and the electrostatic repulsion prevents the entry of positively charged quaternary ammonium compounds (Bruinsma et al., 2006). Recent study elucidates the role of UDP-glucose 4-epimerase (galE) in increasing the positive charge of LPS in Gram-negative bacteria (E. coli), which repulses the positively charged biocides (quaternary ammonium compounds) (Tansirichaiya et al., 2018). Sugar composition of mycobacterial cell wall also reduces the penetration of biocides (Walsh and Fanning, 2008). In Gram-negative bacteria, reduced synthesis of porins is also detected to decrease the entry of biocides (Nikaido, 2003). Expression of efflux pumps such as QacA-D, Smr, QacG and QacH in S. aureus, MexAB-OprM, MexCD-OprJ, MexEF-OprN and MexJK in P. aeruginosa and AcrAB-TolC, AcrEF-TolC and EmrE in E. coli is associated with reduced intracellular concentration and resistance to quaternary ammonium compounds, triclosan, phenolic parabens and intercalating agents (Littlejohn et al., 1992; Heir et al., 1999; Nishino and Yamaguchi, 2001; Morita et al., 2003). Exposure to biocide (triclosan) in Stenotrophomonas maltophilia can also induce efflux pump which helps in expulsion of antibiotics (quinolones) (Hernández et al., 2011). Resistance to parabens, aldehydes, heavy metals and peroxygens is associated with enzymatic modification of biocides. For example, modification of the enzyme (enoyl-acyl reductase) structure produces reduced susceptibility to triclosan in S. aureus (Heath et al., 2000). In Gram-negative bacteria (E. coli), triclosan inhibits FabI-dependent fatty acid synthesis and FabI mutant bacteria are intrinsically triclosan resistant (Zhu et al., 2010).
Acquired resistance Acquisition of mobile genetic elements (transposons, plasmids) encoding the resistance factors can induce acquired resistance to biocides in bacteria. Experimental introduction of genetic inserts containing fabI causes overexpression of enoyl-acyl reductase in E. coli and reduces the inhibitory effect of triclosan (Tansirichaiya et al., 2018).
Cross-resistance, co-resistance and co-regulation between biocides and antimicrobials Cross-resistance Use of biocides at suboptimal concentration for a prolonged period can induce multiple drug-resistant bacteria. Few biocides and antibiotics share common mechanism such as disruption of bacterial membrane integrity, inhibition of synthesis of enzymes and nucleic acids. For survival, the bacteria use similar defence mechanisms which may confer cross-resistance against structurally unrelated molecules. The efflux pump (MdrL) detected in Listeria is active to expel both the antibiotics (cefotaxime, clindamycin, erythromycin and josamycin) and metals (zinc, cobalt and chromium) from the bacterial cell (Mata et al., 2000). Presence of zinc can select a resistant phenotype of Listeria which confers co-resistance to any of the stated antibiotics. Oethinger et al. (1998) observed the association between cyclohexane tolerance and fluoroquinolones resistance in clinical isolates of E. coli. Salmonella serovars isolated from animals showed cross-resistance to multiple antibiotics and biocides (ethidium bromide, cetrimide, cyclohexane, triclosan, acridine orange) (Randall et al., 2001). Other studies also observed cross-resistance to antibiotics and disinfectants in E. coli strains associated with overexpression of AcrAB efflux pump (Ma et al., 1996; Moken et al., 1997). Exposure to quaternary ammonium compounds and tar oil phenol in Salmonella serovars of poultry caused overexpression of efflux pumps (AcrAB, TolC) and reduced susceptibility to multiple antibiotics (Baucheron et al., 2005). Exposure to biocide also increased expression of antibiotic resistance genes in clinical isolates of S. aureus (Huet et al., 2008).
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Co-resistance Biofilm is one of the defence mechanisms which induce co-resistance in bacteria to both biocides and antibiotics. Resistance in biofilm-producing bacteria is associated with decreased metabolism, reduced penetration of biocide/antibiotic through extracellular polymeric matrix, enzymatic inactivation and the induction of multidrug-resistant operons (marA) and efflux pumps (acrB) (Huang et al., 1995; Maira-Litran et al., 2000; Pan et al., 2006; Tabak et al., 2007). The diffusion of biocides through extracellular matrix is the major contributing factor identified to produce resistance against biocides in Pseudomonas-associated biofilms (Bridier et al., 2011). During exposure to metal-based biocides, the metals are chelated with the bacterial dead cells and metabolism end products to generate the biofilm matrix. This kind of matrix prevents further entry of metal ions into the deeper part of the structure (Harrison et al., 2007). In Gram-negative bacteria (E. coli, Salmonella) mar and soxS regulons induce the overlapping genes associated with co-resistance to multiple antibiotics (ampicillin, nalidixic acid, chloramphenicol and tetracycline) and biocides (paraquat, organic solvent) (Poole, 2007). Some biocide/metal resistance genes (mer, qac) are present in the same mobile genetic elements (Tn21, Tn5045, class 1 integron) of bacteria along with antimicrobial resistance genes which may produce co-resistance even in absence of the antibiotic selection pressure (Liebert et al., 1999; Levy and Marshall, 2004; Petrova et al., 2011). The transposon (Tn21) present in Salmonella typhimurium carried mercury resistance gene along with resistance factors against sulfonamide, quaternary ammonium compounds, streptomycin, spectinomycin and penicillin (Summers et al., 1993). A correlation between presence of heavy metal and antibiotic resistance in bacteria even in absence and weakly presence of antibiotic selection pressure was noted since 1970 (Timoney et al., 1978; Ji et al., 2012). Co-resistance of heavy metals (zinc, cadmium and copper) and antibiotics (b-lactams, erythromycin, kanamycin, novobiocin, ofloxacin and sulphanilamide) was reported in B. cepacia associated with DsbA-DsbB system and copper-resistant soil bacteria (Hayashi et al., 2000; Berg et al., 2005). Multidrug-resistant plasmid/transposon was detected in the bacteria possessing the genes for various antibiotics, heavy metals and other biocides, and the plasmids are carried by the bacteria with a fitness cost (Ghosh et al., 2000). The minimal selective concentration (MSC) of a drug or heavy metal is defined as the concentration in which advantage of being resistant is equal to the fitness cost of the bacteria. If the antibiotic or heavy metal is maintained in the concentration higher than MSC, more resistant bacteria emerge in the nature. Moreover, when an individual element (antibiotic or metal biocide) is not present in sufficient concentration (below MSC level) in the environment to select resistant bacteria, their combined concentration can do the same. Experimentally, various concentrations of arsenic, tetracycline and trimethoprim result in selection and maintenance of multidrug-resistant plasmid in Klebsiella pneumoniae and E. coli (Gullberg et al., 2014). However, the network constructed with the sequences of antibiotic/metal/biocide resistance genes revealed limited connections between the heavy metal and antibiotic resistance genes (Pal et al., 2015).
Co-regulation Exposure to heavy metals can alter the expression of antibiotic resistance genes in bacteria, which is known as co-regulation. In presence of zinc, a two-component regulatory system (cscRS) is activated in P. aeruginosa, which encodes an efflux pump (RND) to confer resistance against zinc, cadmium and cobalt. Simultaneously the regulatory system also reduces expression of a porin (OprD) used by the antibiotic (imipenem) to enter the cell (Caille et al., 2007). The two-component regulatory system encodes the efflux pump through the transcription of the czcCBA operon. Mutation in czcS operon (GTG to TTG) in zinc-exposed P. aeruginosa was correlated with reduced expression of OprD (Perron et al., 2004).
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Cross-resistance between biocides and antimicrobials Chapter outline Classification of biocides Use of biocides in animal farm, agricultural field and fishery sector How biocides work Mechanism of resistance against biocides Intrinsic resistance Acquired resistance
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Cross-resistance, co-resistance and co-regulation between biocides and antimicrobials Cross-resistance Co-resistance Co-regulation References
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Biocides are defined as active substances or a preparation consisting of more than one active substance used to kill or reduce the virulence of pathogens (SCENIHR, 2009). Widespread use of biocides such as triclosan and quaternary ammonium compounds increases the selection of antimicrobial-resistant bacteria such as Escherichia coli and Staphylococcus aureus in the environment (Mcmurry et al., 1998; Russell, 2000; Wesgate et al., 2016). The heavy metal-based biocides (copper, zinc) are commonly used in livestock farms and aquaculture as footbath or antifouling paints in the cages and nets (Thomsen et al., 2008; Burridge et al., 2010). Use of heavy metals can maintain or increase the antimicrobial resistance in certain bacteria. The United States Food and Drug Administration (FDA) and European Union Biocidal Products Regulation make it mandatory for the manufacturers to declare the level of resistance generated in commensal bacteria after use of their biocidal products.
Classification of biocides The biocides belong to several chemical groups such as alcohol, aldehyde, phenols, biguanide, peroxide, organic acids, metallic salts, halogens, etc. (Table 28.1).
Use of biocides in animal farm, agricultural field and fishery sector In commercial animal or poultry farms, biocides are used for cleaning of farm premises, vehicles, utensils and buildings, foot dips at the entry of animal/poultry houses, teat dips, decontamination of carcasses and preservation of eggs or semen. Disinfection of farm premises, buildings, vehicles and utensils are carried out with hydrogen peroxide, acetic acid, sodium dichloroisocyanurate, quaternary ammonium compounds (didecyldimethylammonium chloride, alkyldimethylbenzylammonium chloride), glutaraldehyde, formaldehyde and isopropanol. The farm boots and tools are disinfected with sodium-p-toluene-sulfonchloramide and hydrogen peroxide. Copper sulphate is used for foot dips to prevent or cure foot rot in sheep and cattle, although banned in European countries (Thomsen et al., 2008). Teat dip with quaternary ammonium compounds, iodine (0.25%e1.0%), chlorine-based compounds [chloroisocyanurate, chlorhexidine (>0.5%), chlorine dioxide (0.32%), sodium hypochlorite] and bronopol is a common practice before or after milking to prevent the entry of organisms and to reduce the bacterial count for at least log 3. The organic acids are added in animal feed or silage as preservatives to reduce the concentration of spoilage bacteria. Certain heavy metals such as zinc oxide (2000e3000 ppm)
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TABLE 28.1 Classification, mechanism of action and usage of biocides. Biocide
Mechanism of action
Usage
Remarks
Alcohols [ethanol (0.1% e99.9%), methanol (0.03%e15%), phenoxyethanol, propanol, propylene glycol, isopropanol (0.1%e77.22%)]
Inhibition of cell wall and nucleic acid synthesis of bacteria; protein denaturation; proton translocation (phenoxyethanol in Escherichia coli)
a. Used as antiseptic/ disinfectant in health care b. Used as preservative in pharmaceutical/ cosmetic industry
Ethanol/isopropanol (70%e90%) is approved by the US FDA for health care settings
Aldehyde [formaldehyde (0.03%e15.7%), glutaraldehyde (2%)]
Lysis of bacterial cell wall as alkylating agent
a. Used as disinfectant in health care b. Used as preservative in pharmaceutical/ cosmetic/paper industry
Glutaraldehyde (2%) is approved by the US FDA for health care settings
Anionic surfactants (diethylamine)
As a part of a preparation it can lyse bacterial cell wall
a. Used as disinfectant in household products b. Used as preservative in pharmaceutical/ cosmetic industry
e
Biguanides (chlorhexidine digluconate, alexidine, polymeric biguanides)
Chlorhexidine specifically inhibits bacterial cytoplasmic membrane-bound ATPase
Used as disinfectant/antiseptic in household products, health care
e
Diamidines (hexamidine)
Lysis of bacterial cytoplasmic membrane
Used as antiseptic
e
Dyes (acridines, triphenylmethane, quinones)
Lysis of bacterial nucleic acids
Used as antiseptic
e
Halogens (sodium hypochlorite, chloramine, povidoneiodine)
Act as oxidizing agent
Used as disinfectant/ antiseptic in household products, health care, water treatment, industrial products, teat dip in livestock farms
Sodium hypochlorite (5.25% e6.15% household bleach diluted, 1:100, z500 ppm available chlorine) is approved by the US FDA for health care settings
Iodophors
Enzymatic interactions with thiol group
Used as disinfectant/ antiseptic in health care
e
Hydrogen peroxide (0.5% e29%)
Act as oxidizing agent
Used as disinfectant in household products, health care, industrial products
Hydrogen peroxide (1%e7.5%) is approved by the US FDA for health care settings
Pentamidine
Inhibition of bacterial nucleic acid synthesis
Used as disinfectant in medical devices (catheter)
e
Metals (silver nitrate, mercury)
Enzymatic interactions with thiol group
a. Used as disinfectant in health care b. Used as preservative in pharmaceutical industry
e
Chelated metal (copper, mercuric chloride, phenyl mercury, thiomersal)
Bacterial nucleotides act as target of chelated metals
Used as disinfectant in health care, livestock farm, aquaculture
e
Limonene
Unknown interaction with bacterial cytoplasmic membrane
Used as disinfectant in household products and industry
e
Organic acids and esters [parabens, propionic acid, potassium sorbate, sodium
Dissipation of proton motive force in cytoplasmic membrane of Gram-positive
a. Used as disinfectant in health care
e
Continued
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TABLE 28.1 Classification, mechanism of action and usage of biocides.dcont’d Biocide
Mechanism of action
Usage
Remarks
benzoate, acetic acid (0.4%e52%)]
bacteria; inhibition of amino acids uptake in Gram-negative bacteria
b. Used as preservative in pharmaceutical/ cosmetic/food industry
Phenolics [triclosan (2,4,40 -trichloro-20 -hydroxydiphenyl ether, 0.5%); dinitrophenol)
Triclosan binds with enoyl-acyl reductase required for bacterial fatty acid synthesis and acts as bacteriostatic agent Dinitrophenol reduces ATP synthesis in bacterial membrane
c. Used as disinfectant in health care, domestic products such as hand washes
e
Isothiazolinone
Reduces active transport and oxidation of glucose in Staphylococcus aureus
Used as disinfectant in personal care products, household products and industrial products
e
Quaternary ammonium compounds (benzalkonium chloride, cetrimide, cetylpyridinium, dequalinium chloride)
Aggregation of bacterial cytoplasmic membrane proteins and destabilization of the membrane
a. Used as disinfectant in health care, household products, teat dip in livestock farm b. Used as preservative in pharmaceutical/ cosmetic/food industry
e
and copper sulphate (125e250 ppm) are added in pig feed to improve the growth, performance and to prevent scour (Hill et al., 2000). Furthermore, chromium, tin, vanadium, nickel and molybdenum are also added in animal or poultry feed. Owing to lack of knowledge about their precise concentration to be used, most of the commercial animal or poultry feeds contain high concentration of the minerals which are not absorbed through the gut and are excreted directly into the environment (Ao and Pierce, 2013). In agricultural field, biocides are used as insecticide, rodenticide, molluscicide and acaricide to control the pest infestation. Bordeaux mixture [CuSO4 and Ca(OH)2] is applied into vineyards and organic potato farming to control vine downy mildew and potato blight, respectively (Gisi et al., 2009). In aquaculture, iodine, halogens, metallic salts, aldehydes, hydrogen peroxide, quaternary ammonium compounds and dyes are used for disinfection of equipments, ponds and waterbodies and fish eggs (Burridge et al., 2010). In the United States, use of many biocides is regulated by Federal Pesticide Law (FIFRA) and Federal Food, Drugs and Cosmetic Act. In Europe, since 2012e13, biocide use is controlled by Biocidal Products Regulation 528/2012 (BPR) in place of Biocidal Products Directive (BPD, 98/8/EC). Few member countries of European Union and Asian countries have their own published lists of authorized substances to be used as biocide. For example, in Taiwan, use of biocides in animals and plants is regulated by Veterinary Drug Administration Law and Pesticide Management Act. Central Insecticide Board and Registration Committee of India have recently published guidelines for the registration of biocides used in paints.
How biocides work Unlike the antimicrobials, the biocides use vivid mechanisms by which it can kill the organisms or inhibit their growth (Table 28.1, Meyer and Cookson, 2010).
Mechanism of resistance against biocides Since 1950, resistance to biocides was reported in bacterial strains (Davin-Regli and Pagès, 2012). The clinical isolates of E. coli, S. aureus, Mycobacterium chelonae, Burkholderia cepacia and Pseudomonas aeruginosa were detected to be associated with reduced susceptibility to the biocides such as quaternary ammonium compounds, triclosan, paraben, and
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glutaraldehyde (Greenberg and Demple, 1989; Bamber and Neal, 1999; Manzoor et al., 1999; Fraud et al., 2001; Hutchinson et al., 2004; Romão et al., 2005). Intrinsic and acquired resistance mechanisms against biocides are observed in clinical bacterial isolates.
Intrinsic resistance Modification of outer membrane proteins and phospholipids/lipopolysaccharide (LPS) structure in bacterial cell wall is associated with reduced permeability of biocides into the bacterial cell (Guerin-Mechin et al., 2000; Braoudaki and Hilton, 2005). Change in LPS structure increases positive charge of the bacterial outer membrane and the electrostatic repulsion prevents the entry of positively charged quaternary ammonium compounds (Bruinsma et al., 2006). Recent study elucidates the role of UDP-glucose 4-epimerase (galE) in increasing the positive charge of LPS in Gram-negative bacteria (E. coli), which repulses the positively charged biocides (quaternary ammonium compounds) (Tansirichaiya et al., 2018). Sugar composition of mycobacterial cell wall also reduces the penetration of biocides (Walsh and Fanning, 2008). In Gram-negative bacteria, reduced synthesis of porins is also detected to decrease the entry of biocides (Nikaido, 2003). Expression of efflux pumps such as QacA-D, Smr, QacG and QacH in S. aureus, MexAB-OprM, MexCD-OprJ, MexEF-OprN and MexJK in P. aeruginosa and AcrAB-TolC, AcrEF-TolC and EmrE in E. coli is associated with reduced intracellular concentration and resistance to quaternary ammonium compounds, triclosan, phenolic parabens and intercalating agents (Littlejohn et al., 1992; Heir et al., 1999; Nishino and Yamaguchi, 2001; Morita et al., 2003). Exposure to biocide (triclosan) in Stenotrophomonas maltophilia can also induce efflux pump which helps in expulsion of antibiotics (quinolones) (Hernández et al., 2011). Resistance to parabens, aldehydes, heavy metals and peroxygens is associated with enzymatic modification of biocides. For example, modification of the enzyme (enoyl-acyl reductase) structure produces reduced susceptibility to triclosan in S. aureus (Heath et al., 2000). In Gram-negative bacteria (E. coli), triclosan inhibits FabI-dependent fatty acid synthesis and FabI mutant bacteria are intrinsically triclosan resistant (Zhu et al., 2010).
Acquired resistance Acquisition of mobile genetic elements (transposons, plasmids) encoding the resistance factors can induce acquired resistance to biocides in bacteria. Experimental introduction of genetic inserts containing fabI causes overexpression of enoyl-acyl reductase in E. coli and reduces the inhibitory effect of triclosan (Tansirichaiya et al., 2018).
Cross-resistance, co-resistance and co-regulation between biocides and antimicrobials Cross-resistance Use of biocides at suboptimal concentration for a prolonged period can induce multiple drug-resistant bacteria. Few biocides and antibiotics share common mechanism such as disruption of bacterial membrane integrity, inhibition of synthesis of enzymes and nucleic acids. For survival, the bacteria use similar defence mechanisms which may confer cross-resistance against structurally unrelated molecules. The efflux pump (MdrL) detected in Listeria is active to expel both the antibiotics (cefotaxime, clindamycin, erythromycin and josamycin) and metals (zinc, cobalt and chromium) from the bacterial cell (Mata et al., 2000). Presence of zinc can select a resistant phenotype of Listeria which confers co-resistance to any of the stated antibiotics. Oethinger et al. (1998) observed the association between cyclohexane tolerance and fluoroquinolones resistance in clinical isolates of E. coli. Salmonella serovars isolated from animals showed cross-resistance to multiple antibiotics and biocides (ethidium bromide, cetrimide, cyclohexane, triclosan, acridine orange) (Randall et al., 2001). Other studies also observed cross-resistance to antibiotics and disinfectants in E. coli strains associated with overexpression of AcrAB efflux pump (Ma et al., 1996; Moken et al., 1997). Exposure to quaternary ammonium compounds and tar oil phenol in Salmonella serovars of poultry caused overexpression of efflux pumps (AcrAB, TolC) and reduced susceptibility to multiple antibiotics (Baucheron et al., 2005). Exposure to biocide also increased expression of antibiotic resistance genes in clinical isolates of S. aureus (Huet et al., 2008).
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Co-resistance Biofilm is one of the defence mechanisms which induce co-resistance in bacteria to both biocides and antibiotics. Resistance in biofilm-producing bacteria is associated with decreased metabolism, reduced penetration of biocide/antibiotic through extracellular polymeric matrix, enzymatic inactivation and the induction of multidrug-resistant operons (marA) and efflux pumps (acrB) (Huang et al., 1995; Maira-Litran et al., 2000; Pan et al., 2006; Tabak et al., 2007). The diffusion of biocides through extracellular matrix is the major contributing factor identified to produce resistance against biocides in Pseudomonas-associated biofilms (Bridier et al., 2011). During exposure to metal-based biocides, the metals are chelated with the bacterial dead cells and metabolism end products to generate the biofilm matrix. This kind of matrix prevents further entry of metal ions into the deeper part of the structure (Harrison et al., 2007). In Gram-negative bacteria (E. coli, Salmonella) mar and soxS regulons induce the overlapping genes associated with co-resistance to multiple antibiotics (ampicillin, nalidixic acid, chloramphenicol and tetracycline) and biocides (paraquat, organic solvent) (Poole, 2007). Some biocide/metal resistance genes (mer, qac) are present in the same mobile genetic elements (Tn21, Tn5045, class 1 integron) of bacteria along with antimicrobial resistance genes which may produce co-resistance even in absence of the antibiotic selection pressure (Liebert et al., 1999; Levy and Marshall, 2004; Petrova et al., 2011). The transposon (Tn21) present in Salmonella typhimurium carried mercury resistance gene along with resistance factors against sulfonamide, quaternary ammonium compounds, streptomycin, spectinomycin and penicillin (Summers et al., 1993). A correlation between presence of heavy metal and antibiotic resistance in bacteria even in absence and weakly presence of antibiotic selection pressure was noted since 1970 (Timoney et al., 1978; Ji et al., 2012). Co-resistance of heavy metals (zinc, cadmium and copper) and antibiotics (b-lactams, erythromycin, kanamycin, novobiocin, ofloxacin and sulphanilamide) was reported in B. cepacia associated with DsbA-DsbB system and copper-resistant soil bacteria (Hayashi et al., 2000; Berg et al., 2005). Multidrug-resistant plasmid/transposon was detected in the bacteria possessing the genes for various antibiotics, heavy metals and other biocides, and the plasmids are carried by the bacteria with a fitness cost (Ghosh et al., 2000). The minimal selective concentration (MSC) of a drug or heavy metal is defined as the concentration in which advantage of being resistant is equal to the fitness cost of the bacteria. If the antibiotic or heavy metal is maintained in the concentration higher than MSC, more resistant bacteria emerge in the nature. Moreover, when an individual element (antibiotic or metal biocide) is not present in sufficient concentration (below MSC level) in the environment to select resistant bacteria, their combined concentration can do the same. Experimentally, various concentrations of arsenic, tetracycline and trimethoprim result in selection and maintenance of multidrug-resistant plasmid in Klebsiella pneumoniae and E. coli (Gullberg et al., 2014). However, the network constructed with the sequences of antibiotic/metal/biocide resistance genes revealed limited connections between the heavy metal and antibiotic resistance genes (Pal et al., 2015).
Co-regulation Exposure to heavy metals can alter the expression of antibiotic resistance genes in bacteria, which is known as co-regulation. In presence of zinc, a two-component regulatory system (cscRS) is activated in P. aeruginosa, which encodes an efflux pump (RND) to confer resistance against zinc, cadmium and cobalt. Simultaneously the regulatory system also reduces expression of a porin (OprD) used by the antibiotic (imipenem) to enter the cell (Caille et al., 2007). The two-component regulatory system encodes the efflux pump through the transcription of the czcCBA operon. Mutation in czcS operon (GTG to TTG) in zinc-exposed P. aeruginosa was correlated with reduced expression of OprD (Perron et al., 2004).
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