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Frontiers of Environmental Science & Engineering

Front. Environ. Sci. Eng.    2019, Vol. 13 Issue (3) : 46     https://doi.org/10.1007/s11783-019-1129-0
REVIEW ARTICLE
Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: A review
Christine C. Nguyen1, Cody N. Hugie2, Molly L. Kile3, Tala Navab-Daneshmand2()
1. Department of Environmental Sciences, Oregon State University, Corvallis, OR 97331, USA
2. School of Chemical, Biological, and Environmental Engineering, Oregon State University, Corvallis, OR 97331, USA
3. School of Biological and Population Health Sciences, Oregon State University, Corvallis, OR 97331, USA
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Abstract

Heavy metals can act as co-selecting agents and promote antibiotic resistance.

Most frequent resistances to heavy metals are observed for zinc and cadmium.

P. aeruginosa and E. coli are commonly resistant to heavy metals and antibiotics.

Heavy metals proliferate antibiotic resistance through co- and cross-resistance.

Heavy metal and antibiotic resistances are common near anthropogenic activities.

Antibiotic resistance in human pathogens can proliferate under selective pressures. Heavy metals in environmental reservoirs may contribute to selecting antibiotic-resistant strains. To determine the associations between heavy metals and antibiotic resistance, a literature review was conducted to systematically collect and categorize evidence for co-occurrence of resistance to heavy metals and antibiotics within human pathogenic bacteria in water, wastewater, and soil. In total, 42 publications adhered to inclusion criteria. Across the reservoirs, zinc and cadmium were the most commonly observed heavy metals associated with resistance to antibiotics. Pseudomonas aeruginosa and Escherichia coli were the most commonly studied bacteria with reported co-occurrence of resistance to several heavy metals and antibiotic classes. As co-selecting agents, prevalence of heavy metals in the environment can proliferate resistance to heavy metals and antibiotics through co-resistance and cross-resistance mechanisms. In comparing different reservoirs, soils and sediments harbor higher heavy metal and antibiotic resistances compared to water environments. Additionally, abiotic factors such as pH can affect the solubility and hence, the availability of heavy metals to bacterial pathogens. Overall, our review demonstrates heavy metals act as co-selecting agents in the proliferation of antibiotic resistance in human pathogens in multiple environmental reservoirs. More studies that include statistical data are needed to further describe the exposure-response relationships between heavy metals and antibiotic resistance in different environmental media. Moreover, integration of culture-based and molecular-based methods in future studies are recommended to better inform our understanding of bacterial co- and cross-resistance mechanisms to heavy metals and antibiotics.

Keywords Zinc      Cadmium      Copper      Lead      E. coli      P. aeruginosa     
This article is part of themed collection: Environmental Antibiotics and Antibiotic Resistance (Xin Yu, Hui Li & Virender K. Sharma)
Corresponding Authors: Tala Navab-Daneshmand   
Issue Date: 18 June 2019
 Cite this article:   
Christine C. Nguyen,Cody N. Hugie,Molly L. Kile, et al. Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: A review[J]. Front. Environ. Sci. Eng., 2019, 13(3): 46.
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http://journal.hep.com.cn/fese/EN/10.1007/s11783-019-1129-0
http://journal.hep.com.cn/fese/EN/Y2019/V13/I3/46
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Christine C. Nguyen
Cody N. Hugie
Molly L. Kile
Tala Navab-Daneshmand
Key subjects Web of Science search terms
Antibiotic resistance “antibiotic resist*” OR “drug resist*”
AND
Heavy Metals copper OR Cupr* OR arsen* OR zinc OR mercur* OR (Pb AND lead) OR Plumb* OR Cadmium OR Nickel* OR Chromate* OR Chromium OR Cobalt* OR Silver OR Iron OR Ferr*
AND
Human Pathogenic Bacteria Acinetobacter baumannii OR Campylobacter spp. OR Enterococcus faecium OR Enterobacteriaceae OR Escherichia coli OR Enterobacter spp. OR Klebsiella spp. OR Citrobacter spp. OR Morganella spp. OR Providencia spp. OR Proteus spp. OR Serratia spp. OR Hemophilus influenza OR Helicobacter pylori OR Mycobacterium tuberculosis OR Neisseria gonorrhoeae OR Salmonella spp. OR Pseudomonas aeruginosa OR Shigella spp. OR Staphylococcus aureus OR Streptococcus pneumoniae
Key subjects PubMed search terms
Antibiotic resistance “Drug Resistance, Microbial”[Mesh] OR “antimicrobial drug resistance” OR “antimicrobial drug resistances” OR “microbial drug resistance” OR “microbial drug resistances” OR “antibiotic resistance” OR “antibiotic resistances” OR antimicrobial drug resistance* OR microbial drug resistance* OR antibiotic resistance*
AND
Heavy Metals arsenic OR copper OR zinc OR mercury OR lead OR cadmium OR nickel OR chromium OR cobalt OR silver OR iron
AND
Human Pathogenic Bacteriaa Hemophilus influenzae OR Helicobacter pylori OR Mycobacterium tuberculosis OR Neisseria gonorrhoeae OR Salmonella OR Pseudomonas aeruginosa OR Staphylococcus aureus OR Streptococcus pneumoniae OR Acinetobacter baumannii OR Campylobacter OR Enterococcus faecium OR Enterobacteriaceae OR Escherichia coli OR Enterobacter OR Klebsiella OR Citrobacter OR Morganella OR Providencia OR Proteus OR Serratia OR Hemophilus influenzae OR Helicobacter pylori OR Mycobacterium tuberculosis OR Neisseria gonorrhoeae OR Salmonella OR Pseudomonas aeruginosa OR Staphylococcus aureus OR Streptococcus pneumoniae OR Salmonella typhi OR Shigella
Key subjects Agricultural and Environmental Sciences Database search terms
Antibiotic resistance “antibiotic resist*” OR “drug resist*”
AND
Heavy Metals copper OR Cupr* OR arsen* OR zinc OR mercur* OR Pb OR Plumb* OR Cadmium OR Nickel* OR Chromate* OR Chromium OR Cobalt* OR Silver OR Iron OR Ferr*
AND
Human Pathogenic Bacteria Acinetobacter baumannii OR Campylobacter spp. OR Enterococcus faecium OR Enterobacteriaceae OR Escherichia coli OR Enterobacter spp. OR Klebsiella spp. OR Citrobacter spp. OR Morganella spp. OR Providencia spp. OR Proteus spp. OR Serratia spp. OR Hemophilus influenza OR Helicobacter pylori OR Mycobacterium tuberculosis OR Neisseria gonorrhoeae OR Salmonella spp. OR Pseudomonas aeruginosa OR Salmonella Typhi OR Shigella spp. OR Staphylococcus aureus OR Streptococcus pneumoniae
Tab.1  Combination of key search terms used for the identification of literature on the associations between heavy metals and human pathogenic antibiotic-resistant bacteria in environmental reservoirs
Fig.1  Flowchart summarizing the selection process for the studies included in this systematic review. Boxes with dashed lines depict the articles excluded from the review and their records were not assessed in this manuscript.
Citation Human pathogen(s) Heavy metal(s) Antibiotic classes Relevant findings
Abskharon et al. (2008) E. coli Cd, Co, Cr, Cu, Ni, Pb, Zn Fluoroquinolone, quinolone, vancomycin Associations of resistance between Cr with fluoroquinolone, Pb with vancomycin, Cd with quinolone, Zn with fluoroquinolone and vancomycin
Ali et al. (2017) Salmonella spp. Co, Cr, Cu, Fe, Hg, Ni, Zn Penicillin, polymyxin, teicoplanin Resistances to penicillin and several heavy metal related to contaminated environmental reservoir.
Anssour et al. (2016) Citrobacter spp.
E. coli
Klebsiella spp.
Cd, Hg, Zn Fluoroquinolone, quinolone Resistance to ciprofloxacin can be used as an indicator for MDRa.
Extended spectrum beta-lactamases gene was the most common.
Class 1 integrons associated with ciprofloxacin resistance and aquatic environments.
Prevalence of ARGs Hg-resistant gene (merA).
Aviles et al. (1993) P. aeruginosa
Enterobacteriaceae
As, Cd, Cr, Cu, Hg, Ni, Pb Aminoglycoside, amphenicol, cephalosporin, penicillin, quinolone, tetracycline, trimethoprim/sulfamethoxazole Abundance of MDR in P. aeruginosa.
Frequency of strains resistant to As and antibiotics greater in plasmid-harboring bacteria.
Becerra-Castro et al. (2015) E. coli Cu, Zn Aminoglycoside, carbapenem, cephalosporin, fluoroquinolone, penicillin, quinolone, sulfonamide, tetracycline, trimethoprim/sulfamethoxazole MDR in 17% of isolates.
Metal transporter genes associated with MGE/plasmids that convey antibiotic resistance.
Trans-conjugation studies did not corroborate metal resistance because recipient isolate harbored the same metal gene.
Cardonha et al. (2004) E. coli Cu, Hg, Zn Aminoglycoside, amphenicol, carbapenem, cephalosporin, fluoroquinolone, nitrofuran, penicillin, quinolone, tetracycline, trimethoprim/sulfamethoxazole 40% of isolates were MDR and multi-metal resistant.
All 64 tested isolates were resistant to Cu and Zn with associations of resistance to ampicillin, cephalothin, and trimethoprim/sulfamethoxazole.
Choudhury and Kumar (1996) E. coli
P. aeruginosa
Ag, Cd, Co, Cu, Ni, Pb, Zn Aminoglycoside, amphenicol, macrolide, nitrofuran, penicillin, quinolone, sulfonamide, tetracycline, trimethoprim/sulfamethoxazole P. aeruginosa not resistant to Co
Resistance was not plasmid-induced and outer membrane proteins played the dominant role for drug and metal tolerance.
De et al. (2003) Enterobacteriaceae Hg Various antibiotics (not specified) Bacteria were grown in a cocktail of metals and antibiotics. Enterobacteriaceae was able to grow in low to moderate concentrations of Hg, pesticides, and phenol cocktails.
Metal resistance was not plasmid mediated; postulated to relate to chromosomal, horizontal gene transfer or transposable elements.
De Niederhäusern et al. (2013) E. faecium Ag, Cu, Hg, Ni, Pb, Zn Aminoglycoside, amphenicol, macrolide, penicillin, tetracycline, vancomycin, teicoplanin 83.7% of isolates demonstrated resistance to 1 or more antibiotics.
Isolates susceptible to many beta-lactam antibiotics.
Co-occurrence of resistance observed for tetracycline and kanamycin with Cu, Ni, Pb and Zn.
de Vicente et al. (1990) A. baumannii
P. aeruginosa
Ag, As, Cd, Cu, Hg, Ni, Pb, Zn Aminoglycoside, amphenicol, cephalosporin, nitrofuran, penicillin, quinolone, tetracycline Co-occurrence of multiple metal resistance and MDR.
Seawater isolates harbored higher frequencies of resistance, higher MDR potential and were typically more resistant to metals.
Although metal resistance is a trend, it cannot be concluded that heavy metals are a selective pressure due to low concentrations.
Deredjian et al. (2011) P. aeruginosa Cd, Cu, Zn Aminoglycoside, carbapenem, penicillin, tetracycline, trimethoprim/sulfamethoxazole Co-occurrence of resistance to minocycline, trimethoprim-sulfamethoxazole with Zn, Cu, Cd, and Hg.
Zn and Cu can increase imipenem resistance in P. aeruginosa via co-regulation.
No significant differentiation was found between resistance profiles of wastewater and water reservoirs.
Dhakephalkar and Chopade (1994) A. baumannii
Klebsiella spp.
P. aeruginosa
Providencia spp.
Proteus spp.
Cd, Cr, Cu, Zn Aminoglycoside, amphenicol, doxycycline, lincosamide, macrolide, penicillin, quinolone, rifampin, sulfonamide 71% of isolates resistant to beta-lactam antibiotics.
Different minimum inhibitory concentrations comparing pathogenic and non-pathogenic strains.
Resistance to heavy metals and antibiotics more prevalent in environmental isolates compared to clinical isolates.
Cd resistances associated with penicillin and ampicillin.
Djouadi et al. (2017) Citrobacter spp.
E. coli
Enterobacter spp.
Klebsiella spp.
Proteus spp.
Co, Hg, Pb, Zn Aminoglycoside, amphenicol, cephalosporin, lincosamide, macrolide, penicillin, polymyxin, quinolone, streptogramin, sulfonamide, vancomycin Co-occurrence of resistance for Hg, Pb, Co, and Zn with ampicillin, vancomycin, penicillin among others.
High level of resistance to beta-lactam antibiotics.
Ferreira da Silva et al. (2007) E. coli
Klebsiella spp.
Shigella spp.
Cd, Cr, Hg, Ni, Zn Cephalosporin, fluoroquinolone, penicillin, tetracycline, trimethoprim/sulfamethoxazole Resistances higher in treated wastewater as opposed to raw sewage.
Prevalence of aaA1 and ahfrI found in 10% of isolates.
Hg resistance correlated with tetracycline and sulfamethoxazole/trimethoprim resistance.
Filali et al. (2000) Klebsiella spp.
P. aeruginosa Proteus spp.
Ag, Ca, Cu, Hg, Ni, Zn Amphenicol, cephalosporin, fluoroquinolone, penicillin, rifampin, tetracycline Co-occurrence of resistance to ampicillin, amoxicillin and tetracycline with Cu, Ni, and Zn.
All bacteria multi-resistant to antibiotics and heavy metals.
Habi and Daba (2009) Citrobacter spp.
E. coli
Klebsiella spp.
Cd, Hg, Pb Aminoglycoside, amphenicol, macrolide, tetracycline MDR commonly found.
High Hg and Cd resistances.
Haq et al. (1999) Enterobacter spp.
Klebsiella spp.
Cd, Cr, Pb Aminoglycoside, macrolide, penicillin Resistance associations between Cd, Cr, and Pb with gentamicin and ampicillin.
Hassen et al. (1998) P. aeruginosa Proteus spp.
Providencia spp.
Cd, Cr, Cu, Zn Aminoglycoside, amphenicol, doxycycline, lincosamide, macrolide, penicillin, quinolone, rifampicin, sulfonamide Co-occurrence of resistance to several antibiotics and Cu, Cr and Zn in P. aeruginosa.
Heck et al. (2015) Enterobacter spp.
P. aeruginosa
Cr, Cu Cephalosporin, nitrofuran, penicillin, tetracycline 60% of isolates were MDR with 23% resistant to 6 classes of antibiotics.
Acquisition of MDR phenotypes related to (a) the addition of sewage to compost, (b) the accumulation of non-degrading heavy metals, providing selective pressure.
Hu et al. (2007) Enterobacter spp. Cd, Co, Cu, Pb, Zn Aminoglycoside, macrolide, penicillin, rifampin Co-occurrence of resistance to Cd, Cu, Pb, Zn, and Co with ampicillin, erythromycin, kanamycin and rifampicin.
Mandal et al. (2002) Citrobacter spp.
E. coli
Enterobacter spp.
Klebsiella spp.
Proteus spp.
Salmonella spp.
Cd, Cu, Hg Amphenicol, fluoroquinolone, penicillin, tetracycline Associations of resistance to Hg, Cd, Cu with ampicillin, chloramphenicol, and tetracycline.
Manegabe et al. (2017) Salmonella spp.
Shigella spp.
Pb Amphenicol, fluoroquinolone, penicillin, tetracycline Co-occurrence of resistance for ampicillin, chloramphenicol, and tetracycline with Pb and Cd.
Martins et al. (2014) Citrobacter spp.
E. coli
Enterobacter spp.
P. aeruginosa
Salmonella spp.
Cu, Hg, Zn Aminoglycoside, penicillin, trimethoprim/sulfamethoxazole Tetracycline and Cu resistance via plasmid.
Hg-resistant strains were likely MDR.
40% of all isolates were resistant to at least two antibiotics.
Plasmid pEW32 contained tetA, copA, and copB suggesting resistance to tetracycline and copper.
Prevalence of czcA, copA, copB, and merA in resistant bacteria.
Matyar et al. (2008) E. coli
Enterobacter spp.
P. aeruginosa
Salmonella spp.
Cd, Cr, Cu, Pb Aminoglycoside, penicillin, trimethoprim/sulfamethoxazole 16-20% of bacteria were MDR.
Correlation of resistance to metals to MDR.
Mirzaei et al. (2013) Serratia spp. Hg Aminoglycoside, penicillin, tetracycline MDR was more common in bacteria that had metal resistances.
Increase in mercury levels increased antibiotic resistance.
Mourão et al. (2016) Salmonella spp.
Shigella spp.
Pb Amphenicol, fluoroquinolone, penicillin, tetracycline Selective pressure of environment selects for tolerance genes.
Co-occurrence of resistance for Cu and Ag with amoxicillin, sulfamethoxazole, trimethoprim and nalidixic acid.
Oyetibo et al. (2010) P. aeruginosa Cd, Co, Cr, Hg, Ni, Pb Aminoglycoside, amphenicol, cephalosporin, fluoroquinolone, penicillin, quinolone, trimethoprim/sulfamethoxazole Sediments harbor more resistance to heavy metals and antibiotic as well as higher MDR compared to water.
Co-occurrence of resistance to Cr, Pb, Cd, Ni and several antibiotics including septrin and chloramphenicol.
Pathak and Gopal (1994) Citrobacter spp.
Enterobacter spp.
Klebsiella spp.
Cd, Cr, Co, Cu, Hg, Fe, Ni, Pb, Zn Aminoglycoside, amphenicol, cephalosporin, penicillin, quinolone, sulfonamide, tetracycline MDR Isolates had more metal resistances.
Co-occurrence of resistance to ampicillin, streptomycin with Fe, Zn, Cu and Cd.
Patra et al. (2012) E. coli Cd Aminoglycoside, fluoroquinolone, penicillin, polymyxin Resistances to Cd associated with resistance to ciprofloxacin, gentamycin, amikacin, and tobramycin.
E. coli lost resistance to Cd and antibiotics through treatment in sewage-fed fish stabilization ponds.
Roane and Kellogg (1996) Enterobacter spp. Cd, Pb Cephalosporin, macrolide, penicillin Co-occurrence of resistance to Cd and Pb with cephalothin, erythromycin, penicillin.
Variable levels of contamination can be dependent on solubility of metals which can be derived by abiotic factors such as soil pH and texture.
Isolate showed Pb-resistance but no Pb contamination in soil, suggesting gene transfer.
Schneider and Schweisfurth (1991) Enterobacteriaceae Cd, Co, Hg, Zn Aminoglycoside, carbapenem, cephalosporin, fluoroquinolone, penicillin, tetracycline, trimethoprim/sulfamethoxazole Co-occurrence of resistance for ampicillin, augmentin, and tetracycline with Zn and Hg.
Seginkova and Kralikova (1993) E. coli
Salmonella spp.
Ag, As, Cd, Hg, Ni, Pb Aminoglycoside, amphenicol, penicillin, sulfonamide, tetracycline Co-occurrence of resistance for ampicillin with Ni, Pb, Ag, and Cd, carbenicillin with Ni, Pb, Ag, and Cd, streptomycin with Ni, Pb, Ag, and Cd.
Resistances occurred close to anthropogenic sources.
Sepahy et al. (2015) Citrobacter spp.
E. coli
Enterobacter spp.
Klebsiella spp.
Cd, Cr, Hg, Ni Aminoglycoside, amphenicol, cephalosporin, nitrofuran, penicillin, sulfonamide, tetracycline Resistances found to cd and ampicillin. Statistically significant findings that Industrial wastewater had higher resistances to heavy metals and antibiotics compared to domestic wastewater.
Silveira et al. (2014) E. faecium Cu Amphenicol, fluoroquinolone, macrolide, penicillin, tetracycline, vancomycin 62% of isolates were resistant to Cu.
Co-occurrence of resistance to Cu with vancomycin, gentamicin, and ampicillin resistance in E. faecium.
Prevalence of tcrB and cueB encoding resistance to erythromycin and tetracycline.
Soltan (2001) P. aeruginosa Cd, Hg, Pb, Zn Aminoglycoside, amphenicol, fluoroquinolone, penicillin, rifampin, tetracycline P. aeruginosa co-occurrence of resistance for ofloxacin with Pb, Zn, Cd, and Hg, and amikacin with Zn, Cd, and Hg.
Turki et al. (2012) Salmonella spp. Hg Aminoglycoside, amphenicol, carbapenem, cephalosporin, penicillin, quinolone, sulfonamide, tetracycline, trimethoprim/sulfamethoxazole Salmonella strains resistant to Hg and multiple antibiotics including ciprofloxacin, nalidixic acid, ofloxacin, and streptomycin.
Verma et al. (2004) E. coli As, Cd, Co, Cr, Hg, Ni, Zn Aminoglycoside, cephalosporin, penicillin, polymyxin, sulfonamide, tetracycline CR prevalent in the environment.
Isolates resistant to Cu, As, Cd, Ni, Zn, Co, Hg, and bacitracin
Vignaroli et al. (2018) E. faecium Cd, Cu Macrolide, streptogramin,
tetracycline
Sediment resuspension from wave motion can induce higher concentrations of antibiotic resistance in overlaying waters.
Heavy metals are more stable in marine sediments than antibiotics.
Prevalence of erm(B), tet(M), and cadA encoding resistance to erythromycin, tetracycline and cadmium.
Wnorowski (1993) Enterobacteriaceae Ag, Cd, Cu, Ni Cephalosporin, penicillin, sulfonamide, tetracycline Sewage effluents can increase the number of antibiotic resistances and tolerance to heavy metals.
70% of the samples were MDR.
Co-occurrence of resistance to ampicillin with Ni, Ag, Cu, and Cd.
Yilmaz et al. (2013) S. aureus Ag, Cr Aminoglycoside, carbapenem, cephalosporin, fluoroquinolone, penicillin, quinolone, trimethoprim/sulfamethoxazole Resistances suggested as chromosomal-based, and not plasmid-mediated.
Co-occurrence of resistance to ampicillin, gentamicin with Ag and Ni.
Zeng et al. (2009) P. aeruginosa Cd, Co, Cu, Pb, Zn Aminoglycoside, amphenicol, macrolide, penicillin, quinolone, polymyxin Contamination in surface soil with Cd correlated to resistance to Cd, Zn, Cu, Pb, Co and several antibiotics such as amikacin, ampicillin, and chloramphenicol.
(Zeng et al., 2010) P. aeruginosa Cd, Co, Cu, Hg, Pb, Zn Aminoglycoside, amphenicol, macrolide, penicillin, polymyxin, quinolone, tetracycline Co-occurrence of resistance to Cd, Cu, Co, Pb, and Hg with ampicillin, erythromycin and penicillin.
Resistance was not plasmid-mediated.
Tab.2  Findings for studies included in this systematics review that assessed the impact of heavy metals on the proliferation of antibiotic resistant human pathogens (n = 42). Heavy metals and antibiotic classes demonstrated are for cases with reported resistance
Citation Country Environmental reservoir
Abskharon et al. (2008) Egypt Wastewater (sewage)
Ali et al. (2017) Pakistan Water (freshwater)
Anssour et al. (2016) Algeria Wastewater (industry)
Aviles et al. (1993) Spain Water (seawater, sediment)
Becerra-Castro et al. (2015) Portugal Wastewater (sewage)
Cardonha et al. (2004) Brazil Water (seawater), wastewater (sewage)
Choudhury and Kumar (1996) India Water (seawater, sediment)
De et al. (2003) India Water (seawater)
De Niederhäusern et al. (2013) Italy Water (freshwater)
de Vicente et al. (1990) Spain Water (freshwater, seawater)
Deredjian et al. (2011) France Water (freshwater), wastewater (industry)
Dhakephalkar and Chopade (1994) India Water (freshwater), wastewater (sewage), soil (surface soil)
Djouadi et al. (2017) Algeria Water (freshwater)
Ferreira da Silva et al. (2007) Portugal Wastewater (sewage)
Filali et al. (2000) Morocco Wastewater (sewage)
Habi and Daba (2009) Algeria Water (freshwater)
Haq et al. (1999) Pakistan Wastewater (sewage)
Hassen et al. (1998) Tunisia Wastewater (sewage)
Heck et al. (2015) Portugal Soil (compost)
Hu et al. (2007) China Soil (surface soil)
Mandal et al. (2002) India Water (freshwater)
Manegabe et al. (2017) Republic of Congo Water (freshwater, sediment)
Martins et al. (2014) Brazil Water (freshwater)
Matyar et al. (2008) Turkey Water (seawater, sediment)
Mirzaei et al. (2013) Iran Water (freshwater, sediment)
Mourão et al. (2016) Portugal Water (freshwater)
Oyetibo et al. (2010) Nigeria Wastewater (sewage)
Pathak and Gopal (1994) India Water (freshwater)
Patra et al. (2012) South Africa Wastewater (sewage)
Roane and Kellogg (1996) Idaho, US Soil (surface soil)
Schneider and Schweisfurth (1991) Germany Water (freshwater)
Seginkova and Kralikova (1993) Slovakia Water (freshwater), wastewater (sewage)
Sepahy et al. (2015) Iran Wastewater (sewage)
Silveira et al. (2014) Portugal Water (freshwater), wastewater (sewage)
Soltan (2001) Egypt Water (freshwater), wastewater (sewage)
Turki et al. (2012) Tunisia Wastewater(sewage), soil (surface soil)
Verma et al. (2004) India Wastewater (industry)
Vignaroli et al. (2018) Italy Water (seawater, sediment)
Wnorowski (1993) South Africa Water (freshwater)
Yilmaz et al. (2013) Turkey Water (freshwater)
Zeng et al. (2009) China Soil (surface soil)
Zeng et al. (2010) China Soil (surface soil)
Tab.3  Descriptive information for the 42 studies included in this systematic review
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9 C Becerra-Castro, R A Machado, I Vaz-Moreira, C M Manaia (2015). Assessment of copper and zinc salts as selectors of antibiotic resistance in Gram-negative bacteria. The Science of the Total Environment, 530-531: 367–372
https://doi.org/10.1016/j.scitotenv.2015.05.102 pmid: 26057541
10 A M Cardonha, R H Vieira, D P Rodrigues, A Macrae, G Peirano, G N Teophilo (2004). Fecal pollution in water from storm sewers and adjacent seashores in Natal, Rio Grande do Norte, Brazil. International Microbiology: The Official Journal of the Spanish Society for Microbiology, 7(3): 213–218
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13 S Chernousova, M Epple (2013). Silver as antibacterial agent: Ion, nanoparticle, and metal. Angewandte Chemie (International ed. In English), 52(6): 1636–1653
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14 P Choudhury, R Kumar (1996). Association of metal tolerance with multiple antibiotic resistance of enteropathogenic organisms isolated from coastal region of deltaic Sunderbans. The Indian Journal of Medical Research, 104: 148–151
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15 G Cox, G D Wright (2013). Intrinsic antibiotic resistance: Mechanisms, origins, challenges and solutions. International Journal of Medical Microbiology: IJMM, 303(6-7): 287–292
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16 J Davies, D Davies (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews: MMBR, 74(3): 417–433
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17 J De, N Ramaiah, A Mesquita, X N Verlekar (2003). Tolerance to various toxicants by marine bacteria highly resistant to mercury. Marine Biotechnology (New York, N.Y.), 5(2): 185–193
https://doi.org/10.1007/s10126-002-0061-6 pmid: 12876655
18 S De Niederhäusern, M Bondi, I Anacarso, R Iseppi, C Sabia, F Bitonte, P Messi (2013). Antibiotics and heavy metals resistance and other biological characters in Enterococci isolated from surface water of Monte Cotugno Lake (Italy). Journal of Environmental Science and Health. Part A, Toxic/Hazardous Substances & Environmental Engineering, 48(8): 939–946
https://doi.org/10.1080/10934529.2013.762739 pmid: 23485245
19 A de Vicente, M Avilés, J C Codina, J J Borrego, P Romero (1990). Resistance to antibiotics and heavy metals of Pseudomonas aeruginosa isolated from natural waters. The Journal of Applied Bacteriology, 68(6): 625–632
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