Association between heavy metals and antibiotic-resistant human pathogens in environmental reservoirs: A review

doi:10.1007/s11783-019-1129-0

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

Corresponding Author(s): 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.

URL:

https://academic.hep.com.cn/fese/EN/10.1007/s11783-019-1129-0
https://academic.hep.com.cn/fese/EN/Y2019/V13/I3/46

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 MDR^a. 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

1	R N Abskharon, S H Hassan, S M Gad El-Rab, A A Shoreit (2008). Heavy metal resistant of E. coli isolated from wastewater sites in Assiut City, Egypt. Bulletin of Environmental Contamination and Toxicology, 81(3): 309–315 https://doi.org/10.1007/s00128-008-9494-6 pmid: 18584108
2	N M Ali, S A Mazhar, B Mazhar, A Imtiaz, S Andleeb (2017). Antibacterial activity of different plant extracts and antibiotics on pathogenic bacterial isolates from wheat field water. Pakistan Journal of Pharmaceutical Sciences, 30(4): 1321–1325 pmid: 29039332
3	L Anssour, Y Messai, V Estepa, C Torres, R Bakour (2016). Characteristics of ciprofloxacin-resistant Enterobacteriaceae isolates recovered from wastewater of an Algerian hospital. Journal of Infection in Developing Countries, 10(07): 728–734 https://doi.org/10.3855/jidc.6727 pmid: 27482804
4	N J Ashbolt, A Amézquita, T Backhaus, P Borriello, K K Brandt, P Collignon, A Coors, R Finley, W H Gaze, T Heberer, J R Lawrence, D G Larsson, S A McEwen, J J Ryan, J Sch�nfeld, P Silley, J R Snape, C Van den Eede, E Topp (2013). Human Health Risk Assessment (HHRA) for environmental development and transfer of antibiotic resistance. Environmental Health Perspectives, 121(9): 993–1001 https://doi.org/10.1289/ehp.1206316 pmid: 23838256
5	M Aviles, J C Codina, A Perez-Garcia, F Cazorla, P Romero, A De Vicente (1993). Occurrence of Resistance to Antibiotics and Metals and of Plasmids in Bacterial Strains Isolated from Marine Environments. Oxford, UK: Pergamon Press
6	M Ayrapetyan, T C Williams, J D Oliver (2015). Bridging the gap between viable but non-culturable and antibiotic persistent bacteria. Trends in Microbiology, 23(1): 7–13 https://doi.org/10.1016/j.tim.2014.09.004 pmid: 25449050
7	C Baker-Austin, M S Wright, R Stepanauskas, J V McArthur (2006). Co-selection of antibiotic and metal resistance. Trends in Microbiology, 14(4): 176–182 https://doi.org/10.1016/j.tim.2006.02.006 pmid: 16537105
8	A W Bauer, W M Kirby, J C Sherris, M Turck (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45(4_ts): 493–496 https://doi.org/10.1093/ajcp/45.4_ts.493 pmid: 5325707
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 pmid: 15492936
11	CDC (2013). Antibiotic Resistace Threats in the United States. Center for Disease Control and Prevention: U.S. Department of Health and Human Services
12	P Chen, C Chen, X Li (2018). Transport of antibiotic resistance plasmids in porous media and the influence of surfactants. Frontiers of Environmental Science & Engineering, 12(2): 5 https://doi.org/10.1007/s11783-017-0986-7
13	S Chernousova, M Epple (2013). Silver as antibacterial agent: Ion, nanoparticle, and metal. Angewandte Chemie (International ed. In English), 52(6): 1636–1653 https://doi.org/10.1002/anie.201205923 pmid: 23255416
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 pmid: 8783519
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 https://doi.org/10.1016/j.ijmm.2013.02.009 pmid: 23499305
16	J Davies, D Davies (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews: MMBR, 74(3): 417–433 https://doi.org/10.1128/MMBR.00016-10 pmid: 20805405
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
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