Antimicrobial resistance due to the content of potentially toxic metals in soil and fertilizing products

References

• Roca I, Akova M, Baquero F, et al. The global threat of antimicrobial resistance: science for intervention. New Microbes New Infect. 2015;6:1–12.
   Google Scholar
• Baker-Austin C, Wright MS, Stepanauskas R, et al. Co-selection of antibiotic and metal resistance. Trends Microbiol. 2006;14(4):176–182.
   PubMed Web of Science ®Google Scholar
• Knapp CW, McCluskey SM, Singh BK, et al. Antibiotic resistance gene abundances correlate with metal and geochemical conditions in archived Scottish soils. PLoS One. 2011;6(11):e27300.
   PubMed Web of Science ®Google Scholar
• Nies DH. Microbial heavy-metal resistance. Appl Microbiol Biotechnol. 1999;51(6):730–750.
   PubMed Web of Science ®Google Scholar
• Seiler C, Berendonk TU. Heavy metal driven co-selection of antibiotic resistance in soil and water bodies impacted by agriculture and aquaculture. Front Microbiol. 2012;3:399.
   PubMed Web of Science ®Google Scholar
• 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.
   Web of Science ®Google Scholar
• Alonso A, Sanchez P, Martinez JL. Environmental selection of antibiotic resistance genes. Environ Microbiol. 2001;3(1):1–9.
   Web of Science ®Google Scholar
• Summers AO, Wireman J, Vimy MJ, et al. Mercury released from dental “silver” fillings provokes an increase in mercury- and antibiotic-resistant bacteria in oral and intestinal floras of primates. Antimicrob Agents Chemother. 1993;37(4):825–834.
   Web of Science ®Google Scholar
• Stepanauskas R, Glenn TC, Jagoe CH, et al. Elevated microbial tolerance to metals and antibiotics in metal-contaminated industrial environments. Environ Sci Technol. 2005;39(10):3671–3678.
   PubMed Web of Science ®Google Scholar
• Huddleston JR. Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes. Infect Drug Resist. 2014;7:167–176.
   PubMed Web of Science ®Google Scholar
• Nielsen KM, Bøhn T, Townsend JP. Detecting rare gene transfer events in bacterial populations. Front Microbiol. 2014;4:415.
   Web of Science ®Google Scholar
• IFT. Antimicrobial resistance: implications for the food system. USA: Institute of Food Technologists; 2006.
   Google Scholar
• Kahlmeter G. The 2014 Garrod lecture: EUCAST - are we heading towards international agreement? J Antimicrob Chemother. 2015;70(9):2427–2439.
   PubMed Web of Science ®Google Scholar
• Matuschek E, Brown DF, Kahlmeter G. Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin Microbiol Infect. 2014;20(4):O255–O266.
   PubMed Web of Science ®Google Scholar
• Rathnayake IV, Megharaj M, Krishnamurti GS, et al. Heavy metal toxicity to bacteria - are the existing growth media accurate enough to determine heavy metal toxicity? Chemosphere. 2013;90(3):1195–1200.
   Web of Science ®Google Scholar
• Wales AD, Davies RH. Co-selection of resistance to antibiotics, biocides and heavy metals, and its relevance to foodborne pathogens. Antibiotics (Basel). 2015;4(4):567–604.
   Web of Science ®Google Scholar
• Yazdankhah SP, Scheie AA, Høiby EA, et al. Triclosan and antimicrobial resistance in bacteria: an overview. Microb Drug Resist. 2006;12(2):83–90.
   PubMed Web of Science ®Google Scholar
• Kochare T, Tamir B. Assessment of dairy feeds for heavy metals. Am Sci Res J Eng Technol Sci. 2015;11:20–31.
   Google Scholar
• Duffus JH. “Heavy metals” - A meaningless term? (IUPAC technical report). Pure Appl Chem. 2002;74(5):793–807.
   Web of Science ®Google Scholar
• Mortvedt JJ. Heavy metal contaminants in inorganic and organic fertilizers. Ferti Res. 1996;43:55–61.
   Web of Science ®Google Scholar
• Fraise AP, Maillard J-Y SS. Principles and practice of disinfection, preservation and sterilization. Chichester, West Sussex: John Wiley & Sons; 2012.
   Google Scholar
• Lemire JA, Harrison JJ, Turner RJ. Antimicrobial activity of metals: mechanisms, molecular targets and applications. Nat Rev Microbiol. 2013;11(6):371–384.
   PubMed Web of Science ®Google Scholar
• Silver S, Phung LT. Bacterial heavy metal resistance: new surprises. Annu Rev Microbiol. 1996;50:753–789.
   PubMed Web of Science ®Google Scholar
• Harrison JJ, Ceri H, Turner RJ. Multimetal resistance and tolerance in microbial biofilms. Nat Rev Microbiol. 2007;5(12):928–938.
   PubMed Web of Science ®Google Scholar
• Teitzel GM, Parsek MR. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl Environ Microbiol. 2003;69(4):2313–2320.
   PubMed Web of Science ®Google Scholar
• Schiering N, Kabsch W, Moore MJ, et al. Structure of the detoxification catalyst mercuric ion reductase from Bacillus sp. strain RC607. Nature. 1991;352(6331): 168–172.
   Web of Science ®Google Scholar
• Nies DH, Silver S. Ion efflux systems involved in bacterial metal resistances. J Ind Microbiol. 1995;14(2):186–199.
   PubMedGoogle Scholar
• Pal C, Bengtsson-Palme J, Rensing C, et al. BacMet: antibacterial biocide and metal resistance genes database. Nucleic Acids Res. 2014;42(Databaseissue):D737–D743.
   Google Scholar
• Herland BJ, Taylor D, Wither K. The distribution of mercury and other trace metals in the sediments of the Mersey Estuary over 25 years 1974–1998. Sci Total Environ. 2000;253:45–62.
   Web of Science ®Google Scholar
• Giller KE, Witter E, Mcgrath SP. Toxicity of heavy metals to microorganisms and microbial processes in agricultural soils: a review. Soil Biol Biochem. 1998;30:1389–1414.
   Web of Science ®Google Scholar
• Roane TM, Kellogg ST. Characterization of bacterial communities in heavy metal contaminated soils. Can J Microbiol. 1996;42(6):593–603.
   PubMed Web of Science ®Google Scholar
• Xie Y, Fan J, Zhu W, et al. Effect of heavy metals pollution on soil microbial diversity and Bermudagrass genetic variation. Front Plant Sci. 2016;7:755.
   PubMed Web of Science ®Google Scholar
• Hobman JL, Crossman LC. Bacterial antimicrobial metal ion resistance. J Med Microbiol. 2015;64(Pt 5):471–497.
   PubMedGoogle Scholar
• Pikkemaat MG, Yassin H, van der Fels-Klerx HJ, et al. Antibiotic residues and resistance in the environment, RIKILT report 2016.009. The Netherlands: RIKILT Wageningen UR (University & Research centre); 2016.
   Google Scholar
• Qian M, Wu H, Wang J, et al. Occurrence of trace elements and antibiotics in manure-based fertilizers from the Zhejiang Province of China. Sci Total Environ. 2016;559:174–181.
   PubMed Web of Science ®Google Scholar
• Lin H, Sun W, Zhang Z, et al. Effects of manure and mineral fertilization strategies on soil antibiotic resistance gene levels and microbial community in a paddy-upland rotation system. Environ Pollut. 2016;211:332–337.
   Web of Science ®Google Scholar
• Li Y, Liu B, Zhang X, et al. Effects of Cu exposure on enzyme activities and selection for microbial tolerances during swine-manure composting. J Hazard Mater. 2015;283:512–518.
   Web of Science ®Google Scholar
• Riber L, Poulsen PH, Al-Soud WA, et al. Exploring the immediate and long-term impact on bacterial communities in soil amended with animal and urban organic waste fertilizers using pyrosequencing and screening for horizontal transfer of antibiotic resistance. FEMS Microbiol Ecol. 2014;90(1):206–224.
   Web of Science ®Google Scholar
• Ji X, Shen Q, Liu F, et al. Antibiotic resistance gene abundances associated with antibiotics and heavy metals in animal manures and agricultural soils adjacent to feedlots in Shanghai; China. J Hazard Mater. 2012;235–236:178–185.
   PubMed Web of Science ®Google Scholar
• Rahube TO, Yost CK. Characterization of a mobile and multiple resistance plasmid isolated from swine manure and its detection in soil after manure application. J Appl Microbiol. 2012;112(6):1123–1133.
   PubMed Web of Science ®Google Scholar
• Holzel CS, Muller C, Harms KS, et al. Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance. Environ Res. 2012;113:21–27.
   PubMed Web of Science ®Google Scholar
• Caldini G, Cenci G, Morozzi G. Resistotype heterogeneity of Escherichia coli strains isolated from humans, animals and sewage waters. Zentralbl Bakteriol Mikrobiol Hyg B. 1987;184(3–4):206–213.
   Google Scholar
• Collignon PC, Conly JM, Andremont A, World Health Organization Advisory Group BMoISoAR, et al. World Health Organization ranking of antimicrobials according to their importance in human medicine: a critical step for developing risk management strategies to control antimicrobial resistance from food animal production. Clin Infect Dis. 2016;63(8):1087–1093.
   PubMed Web of Science ®Google Scholar
• Anssour L, Messai Y, Estepa V, et al. Characteristics of ciprofloxacin-resistant Enterobacteriaceae isolates recovered from wastewater of an Algerian hospital. J Infect Dev Ctries. 2016;10(7):728–734.
   Web of Science ®Google Scholar
• Gao P, He S, Huang S, et al. Impacts of coexisting antibiotics, antibacterial residues, and heavy metals on the occurrence of erythromycin resistance genes in urban wastewater. Appl Microbiol Biotechnol. 2015;99(9):3971–3980.
   PubMed Web of Science ®Google Scholar
• Heck K, De Marco EG, Duarte MW, et al. Pattern of multiresistant to antimicrobials and heavy metal tolerance in bacteria isolated from sewage sludge samples from a composting process at a recycling plant in southern Brazil. Environ Monit Assess. 2015;187(6):328.
   Web of Science ®Google Scholar
• Varela AR, Andre´ S, Nunes OC, et al. Insights into the relationship between antimicrobial residues and bacterial populations in a hospital-urban wastewater treatment plant system. Water Res. 2014;54:327–336.
   Web of Science ®Google Scholar
• Martins VV, Zanetti MO, Pitondo-Silva A, et al. Aquatic environments polluted with antibiotics and heavy metals: a human health hazard. Environ Sci Pollut Res Int. 2014;21(9):5873–5878.
   Web of Science ®Google Scholar
• Filali BK, Taoufik J, Zeroual Y, et al. Waste water bacterial isolates resistant to heavy metals and antibiotics. Curr Microbiol. 2000;41(3):151–156.
   PubMed Web of Science ®Google Scholar
• Dhakephalkar PK, Chopade BA. High levels of multiple metal resistance and its correlation to antibiotic resistance in environmental isolates of Acinetobacter. Biometals. 1994;7(1):67–74.
   Web of Science ®Google Scholar
• Silveira E, Freitas AR, Antunes P, et al. Co-transfer of resistance to high concentrations of copper and first-line antibiotics among Enterococcus from different origins (humans, animals, the environment and foods) and clonal lineages. J Antimicrob Chemother. 2014;69(4):899–906.
   PubMed Web of Science ®Google Scholar
• Hasman H, Aarestrup FM. Relationship between copper, glycopeptide, and macrolide resistance among Enterococcus faecium strains isolated from pigs in Denmark between 1997 and 2003. Antimicrob Agents Chemother. 2005;49(1):454–456.
   PubMed Web of Science ®Google Scholar
• Hasman H. The tcrB gene is part of the tcrYAZB operon conferring copper resistance in Enterococcus faecium and Enterococcus faecalis. Microbiology. 2005;151(Pt 9):3019–3025.
   Google Scholar
• Borgen K, Simonsen GS, Sundsfjord A, et al. Continuing high prevalence of VanA-type vancomycin-resistant enterococci on Norwegian poultry farms three years after avoparcin was banned. J Appl Microbiol. 2000;89(3):478–485.
   Web of Science ®Google Scholar
• Borgen K, Sørum M, Kruse H, et al. Persistence of vancomycin-resistant enterococci (VRE) on Norwegian broiler farms. FEMS Microbiol Lett. 2000;191(2):255–258.
   Web of Science ®Google Scholar
• Borgen K, Sørum M, Wasteson Y, et al. VanA-type vancomycin-resistant enterococci (VRE) remain prevalent in poultry carcasses 3 years after avoparcin was banned. Int J Food Microbiol. 2001;64(1–2):89–94.
   Web of Science ®Google Scholar
• Sørum M, Holstad G, Lillehaug A, et al. Prevalence of vancomycin resistant enterococci on poultry farms established after the ban of avoparcin. Avian Dis. 2004;48(4):823–828.
   Web of Science ®Google Scholar
• NORM/NORM-VET. Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway. Tromsø/Oslo, Norway; 2012. ISSN:1502-2307 (print)/1890-9965 (electronic). 2011.
   Google Scholar
• NORM/NORM-VET. Usage of antimicrobial agents and occurrence of antimicrobial resistance in Norway. Tromsø/Oslo, Norway; 2014. ISSN:1502-2307 (print)/1890-9965 (electronic). 2013.
   Google Scholar
• VKM. Zinc and copper in pig and poultry production – fate and effects in the food chain and the environment. Norwegian Scientific Committee for Food Safety. ISBN 978-82-8259-093-8; 2014. Contract No: 13-603 Final.
   Google Scholar
• Jensen J, Larsen MM, Bak J. National monitoring study in Denmark finds increased and critical levels of copper and zinc in arable soils fertilized with pig slurry. Environ Pollut. 2016;214:334–340.
   PubMed Web of Science ®Google Scholar
• Song J, Rensing C, Holm PE, et al. Comparison of metals and tetracycline as selective agents for development of tetracycline resistant bacterial communities in agricultural soil. Environ Sci Technol. 2017;7;51(5):3040–3047.
   Web of Science ®Google Scholar
• Cavaco LM, Hasman H, Aarestrup FM. Zinc resistance of Staphylococcus aureus of animal origin is strongly associated with methicillin resistance. Vet Microbiol. 2011;150(3–4):344–348.
   Web of Science ®Google Scholar
• Kaur S, Kamli MR, Ali A. Role of arsenic and its resistance in nature. Can J Microbiol. 2011;57(10):769–774.
   Web of Science ®Google Scholar
• Kotas J, Stasicka Z. Chromium occurrence in the environment and methods of its speciation. Environ Pollut. 2000;107(3):263–283.
   PubMed Web of Science ®Google Scholar
• Wise SS, Holmes AL, Ketterer ME, et al. Chromium is the proximate clastogenic species for lead chromate-induced clastogenicity in human bronchial cells. Mutat Res. 2004;560(1):79–89.
   Web of Science ®Google Scholar
• Ackerley DF, Barak Y, Lynch SV, et al. Effect of chromate stress on Escherichia coli K-12. J Bacteriol. 2006;188(9):3371–3381.
   Web of Science ®Google Scholar
• Tchounwou PB, Yedjou CG, Patlolla AK, et al. Heavy metal toxicity and the environment. EXS. 2012;101:133–164.
   PubMedGoogle Scholar
• Clarkson TW, Magos L. The toxicology of mercury and its chemical compounds. Crit Rev Toxicol. 2006;36(8):609–662.
   PubMed Web of Science ®Google Scholar
• Macomber L, Hausinger RP. Mechanisms of nickel toxicity in microorganisms. Metallomics. 2011;3(11):1153–1162.
   PubMed Web of Science ®Google Scholar
• Imlay JA. Pathways of oxidative damage. Annu Rev Microbiol. 2003;57:395–418.
   PubMed Web of Science ®Google Scholar
• Phan TN, Buckner T, Sheng J, et al. Physiologic actions of zinc related to inhibition of acid and alkali production by oral streptococci in suspensions and biofilms. Oral Microbiol Immunol. 2004;19(1):31–38.
   Google Scholar
• Carlin A, Shi W, Dey S, et al. The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol. 1995;177(4):981–986.
   PubMed Web of Science ®Google Scholar
• Rosen BP. Biochemistry of arsenic detoxification. FEBS Lett. 2002;529(1):86–92.
   PubMed Web of Science ®Google Scholar
• Silver S. Genes for all metals–a bacterial view of the periodic table. The 1996 Thom award lecture. J Ind Microbiol Biotechnol. 1998;20(1):1–12.
   PubMed Web of Science ®Google Scholar
• Kruger MC, Bertin PN, Heipieper HJ, et al. Bacterial metabolism of environmental arsenic–mechanisms and biotechnological applications. Appl Microbiol Biotechnol. 2013;97(9):3827–3841.
   Web of Science ®Google Scholar
• Viti C, Marchi E, Decorosi F, et al. Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol Rev. 2014;38(4):633–659.
   PubMed Web of Science ®Google Scholar
• Amachawadi RG, Shelton NW, Shi X, et al. Selection of fecal enterococci exhibiting tcrB-mediated copper resistance in pigs fed diets supplemented with copper. Appl Environ Microbiol. 2011;77(16):5597–5603.
   Web of Science ®Google Scholar
• Freitas AR, Coque TM, Novais C, et al. Human and swine hosts share vancomycin-resistant Enterococcus faecium CC17 and CC5 and Enterococcus faecalis CC2 clonal clusters harboring Tn1546 on indistinguishable plasmids. J Clin Microbiol. 2011;49(3):925–931.
   Web of Science ®Google Scholar
• Jacob ME, Fox JT, Nagaraja TG, et al. Effects of feeding elevated concentrations of copper and zinc on the antimicrobial susceptibilities of fecal bacteria in feedlot cattle. Foodborne Pathog Dis. 2010;7(6):643–648.
   PubMed Web of Science ®Google Scholar
• Aarestrup FM, Hasman H, Jensen LB, et al. Antimicrobial resistance among enterococci from pigs in three European countries. Appl Environ Microbiol. 2002;68(8):4127–4129.
   PubMed Web of Science ®Google Scholar
• Jaroslawiecka A, Piotrowska-Seget Z. Lead resistance in micro-organisms. Microbiology. 2014;160(Pt 1):12–25.
   PubMedGoogle Scholar
• Naik MM, Dubey SK. Lead resistant bacteria: lead resistance mechanisms, their applications in lead bioremediation and biomonitoring. Ecotoxicol Environ Saf. 2013;98:1–7.
   PubMed Web of Science ®Google Scholar
• Foster TJ. The genetics and biochemistry of mercury resistance. Crit Rev Microbiol. 1987;15(2):117–140.
   Web of Science ®Google Scholar
• Khesin RB, Karasyova EV. Mercury-resistant plasmids in bacteria from a mercury and antimony deposit area. Mol Gen Genet. 1984;197(2):280–285.
   Google Scholar
• Silver S, Phung LT. A bacterial view of the periodic table: genes and proteins for toxic inorganic ions. J Ind Microbiol Biotechnol. 2005;32(11–12):587–605.
   PubMed Web of Science ®Google Scholar
• Zscheck KK, Murray BE. Genes involved in the regulation of beta-lactamase production in enterococci and staphylococci. Antimicrob Agents Chemother. 1993;37(9):1966–1970.
   PubMed Web of Science ®Google Scholar
• Bednorz C, Oelgeschlager K, Kinnemann B, 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(6–7):396–403.
   Web of Science ®Google Scholar