Tolerance to multiple metal stressors in emerging non-typhoidal MDR Salmonella serotypes: A relevant role for copper in anaerobic conditions

Journal of Antimicrobial Chemotherapy

Volumn 71, Issue 8, 2016, Pages 2147-2157

  Mourão, Joana ^a   Marçal, Sara ^a   Ramos, Paula ^a   Campos, Joana ^a   Machado, Jorge ^b   Peixe, Luísa ^a   Novais, Carla ^a   Antunes, Patrícia ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b NATIONAL INSTITUTE OF HEALTH DR RICARDO JORGE   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; ARSENIC; CHLORAMPHENICOL; COPPER; COPPER SULFATE; KANAMYCIN; MERCURY; NALIDIXIC ACID; RIFAMPICIN; SILVER; SILVER NITRATE; STREPTOMYCIN; SULFAMETHOXAZOLE; TELLURIUM; TETRACYCLINE; TRIMETHOPRIM; HEAVY METAL;

AEROBIC METABOLISM; ANAEROBIC GROWTH; ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; CLONE; CONTROLLED STUDY; METAL TOLERANCE; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; POLYMERASE CHAIN REACTION; SALMONELLA ENTERICA; SALMONELLA ENTERICA SEROVAR INFANTIS; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA ENTERICA SEROVAR VIRCHOW; SALMONELLA ENTERICA SEROVAR WIEN; SEROTYPE; ANIMAL; ANIMAL HUSBANDRY; BACTERIAL GENE; BACTERIUM CONJUGATION; DRUG EFFECTS; DRUG TOLERANCE; HUMAN; MICROBIAL SENSITIVITY TEST; MULTIDRUG RESISTANCE; PROCEDURES; SALMONELLA;

ANAEROBIOSIS; ANIMAL HUSBANDRY; ANIMALS; CONJUGATION, GENETIC; COPPER; DRUG RESISTANCE, MULTIPLE, BACTERIAL; DRUG TOLERANCE; GENES, BACTERIAL; HUMANS; METALS, HEAVY; MICROBIAL SENSITIVITY TESTS; POLYMERASE CHAIN REACTION; SALMONELLA; SEROGROUP;

EID: 84977576839     PISSN: 03057453     EISSN: 14602091     Source Type: Journal    
DOI: 10.1093/jac/dkw120     Document Type: Article

References (54)

1. Antunes P, Mourão J, Pestana N et al. Leakage of emerging clinically relevant multidrug-resistant Salmonella clones from pig farms. J Antimicrob Chemother 2011; 66: 2028-32.
2. Eng S-K, Pusparajah P, Ab Mutalib N-S et al. Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci 2015; 8: 284-93.
3. Gomes-Neves E, Antunes P, Manageiro V et al. Clinically relevant multidrug resistant Salmonella enterica in swine and meat handlers at the abattoir. Vet Microbiol 2014; 168: 229-33.
4. Medardus JJ, Molla BZ, Nicol M et al. In-feed use of heavymetalmicronutrients in U.S. swine production systems and its role in persistence of multidrug-resistant salmonellae. Appl Environ Microbiol 2014; 80: 2317-25.
5. Mourão J, Machado J, Novais C et al. Characterization of the emerging clinically-relevant multidrug-resistant Salmonella enterica serotype 4, [5], 12:i:- (monophasic variant of S. Typhimurium) clones. Eur J Clin Microbiol Infect Dis 2014; 33: 2249-57.
6. Mourão J, Novais C, Machado J et al. Metal tolerance in emerging clinically relevant multidrug-resistant Salmonella enterica serotype 4, [5], 12:i:- clones circulating in Europe. Int J Antimicrob Agents 2015; 45: 610-6.
7. List of the authorised additives in feedingstuffs (1) published in application of Article 9t (b) of Council Directive 70/524/EEC concerning additives in feedingstuffs of 25 February 2004. Official Journal of the European Union C50/1. http://ec.europa.eu/food/food/animalnutrition/feedadditives/docs/ c_50_en.pdf.
8. Scientific Committee on Emerging and Newly Identified Health Risks (SCENIHR). Opinion on Nanosilver: safety, health and environmental effects and role in antimicrobial resistance. 2014. http://ec.europa.eu/health/ scientific_committees/emerging/docs/scenihr_o_039.pdf.
9. 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.
10. Opinion of the Panel on Animal Feed of the Norwegian Scientific Committee for Food Safety (VKM). Zinc and copper in pig and poultry production- fate and effects in the food chain and the environment. 2014. http://www.english.vkm.no/dav/3b1b6769dd.pdf.
11. 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: 1-7.
12. European Food Safety Authority (EFSA). Opinion of the Scientific Panel on Contaminants in the Food chain on a request from the European Commission on mercury as undesirable substance in feed. EFSA J 2008; 654: 1-76.
13. Bolan NS, Khan MA, Donaldson J et al. Distribution and bioavailability of copper in farm effluent. Sci Total Environ 2003; 309: 225-36.
14. Xiong X, Yanxia L, Wei L et al. Copper content in animal manures and potential risk of soil copper pollution with animal manure use in agriculture. Resour Conserv Recy 2010; 54: 985-90.
15. Zhang F, Li Y, Yang M et al. Content of heavy metals in animal feeds and manures from farms of different scales in northeast China. Int J Environ Res Public Health 2012; 9: 2658-68.
16. European Food Safety Authority (EFSA) and Panel on Additives and Products or Substances used in Animal Feed (FEEDAP). Scientific Opinion on the safety and efficacy of copper compounds (E4) as feed additives for all animal species: cupric sulphate pentahydrate based on a dossier submitted by Manica S.p.A. EFSA J 2012; 10: 2969.
17. Gaze WH, Krone SM, Larsson DG et al. Influence of humans on evolution and mobilization of environmental antibiotic resistome. Emerg Infect Dis 2013; 19: e120871.
18. Baker-Austin C, Wright MS, Stepanauskas R et al. Co-selection of antibiotic and metal resistance. Trends Microbiol 2006; 14: 176-82.
19. Kim EH, Nies DH, McEvoy MM et al. Switch or funnel: how RND-type transport systems control periplasmic metal homeostasis. J Bacteriol 2011; 193: 2381-7.
20. Silver S. Bacterial silver resistance: molecular biology and uses and misuses of silver compounds. FEMS Microbiol Rev 2003; 27: 341-53.
21. Antunes P, Coque TM, Peixe L. Emergence of an IncIg plasmid encoding CMY-2 β-lactamase associated with the international ST19 OXA-30- producing β-lactamase Salmonella Typhimurium multidrug-resistant clone. J Antimicrob Chemother 2010; 65: 2097-100.
22. Antunes P, Machado J, Peixe L. Characterization of antimicrobial resistance and class 1 and 2 integrons in Salmonella enterica isolates from different sources in Portugal. J Antimicrob Chemother 2006; 58: 297-304.
23. Antunes P, Machado J, Peixe L. Dissemination of sul3-containing elements linked to class 1 integrons with an unusual 3' conserved sequence region among Salmonella isolates. Antimicrob Agents Chemother 2007; 51: 1545-8.
24. Antunes P, Mourão J, Alves T et al. Salmonella enterica serotype Bovismorbificans, a new host for CTX-M-9. Int J Antimicrob Agents 2013; 41: 91-3.
25. Antunes P, Mourão J, Machado J et al. First description of qnrS1-IncN plasmid in a ST11 Salmonella Enteritidis clinical isolate from Portugal. Diagn Microbiol Infect Dis 2011; 69: 463-5.
26. Hasman H, Kempf I, Chidaine B et al. Copper resistance in Enterococcus faecium, mediated by the tcrB gene, is selected by supplementation of pig feed with copper sulfate. Appl Environ Microbiol 2006; 72: 5784-9.
27. Randall CP, Oyama LB, Bostock JM et al. The silver cation (Ag+): antistaphylococcal activity, mode of action and resistance studies. J Antimicrob Chemother 2013; 68: 131-8.
28. Williams JR, Morgan AG, Rouch DA et al. Copper-resistant enteric bacteria from United Kingdom and Australian piggeries. Appl Environ Microbiol 1993; 59: 2531-7.
29. Carattoli A, Bertini A, Villa L et al. Identification of plasmids by PCR-based replicon typing. J Microbiol Methods 2005; 63: 219-28.
30. Garcia-Fernandez A, Fortini D, Veldman K et al. Characterization of plasmids harbouring qnrS1, qnrB2 and qnrB19 genes in Salmonella. J Antimicrob Chemother 2009; 63: 274-81.
31. Pornsukarom S, Patchanee P, Erdman M et al. Comparative phenotypic and genotypic analyses of Salmonella Rissen that originated from food animals in Thailand and United States. Zoonoses Public Health 2015; 62: 151-8.
32. Hölzel CS, Muller C, Harms KS et al. Heavy metals in liquid pig manure in light of bacterial antimicrobial resistance. Environ Res 2012; 113: 21-7.
33. 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: 178-85.
34. Zhu YG, Johnson TA, Su JQ et al. Diverse and abundant antibiotic resistance genes in Chinese swine farms. Proc Natl Acad Sci USA 2013; 110: 3435-40.
35. European Food Safety Authority (EFSA) and European Food Safety Authority and European Centre for Disease Prevention and Control (ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2013. EFSA J 2015; 13: 3991.
36. Hoffmann M, Zhao S, Pettengill J et al. Comparative genomic analysis and virulence differences in closely related Salmonella enterica serotype Heidelberg isolates from humans, retail meats, and animals. Genome Biol Evol 2014; 6: 1046-68.
37. Gerber P, Opio C, Steinfeld H. Poultry production and the environment- a review. In: Proceedings of the International Conference Poultry in the Twenty-First Century: Avian Influenza and Beyond, Bangkok, Thailand, 2007. 379-405. Food and Agriculture Organization of the United Nations.
38. Carattoli A. Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother 2009; 53: 2227-38.
39. Garcia-Fernandez A, Carattoli A. Plasmid double locus sequence typing for IncHI2 plasmids, a subtyping scheme for the characterization of IncHI2 plasmids carrying extended-spectrum β-lactamase and quinolone resistance genes. J Antimicrob Chemother 2010; 65: 1155-61.
40. Hao X, Luthje FL, Qin Y et al. Survival in amoeba-a major selection pressure on the presence of bacterial copper and zinc resistance determinants? Identification of a "copper pathogenicity island". Appl Microbiol Biotechnol 2015; 99: 5817-24.
41. Moreno Switt AI, den Bakker HC, Cummings CA et al. Identification and characterization of novel Salmonella mobile elements involved in the dissemination of genes linked to virulence and transmission. PLoS One 2012; 7: e41247.
42. Qin Y, Hasman H, Aarestrup FM et al. Genome sequences of three highly copper-resistant Salmonella enterica subsp. I serovar Typhimurium strains isolated from pigs in Denmark. Genome Announc 2014; 2: e01334-14.
43. Peters JE, Fricker AD, Kapili BJ et al. Heteromeric transposase elements: generators of genomic islands across diverse bacteria. Mol Microbiol 2014; 93: 1084-92.
44. Liebert CA, Wireman J, Smith T et al. Phylogeny of mercury resistance (mer) operons of Gram-negative bacteria isolated from the fecal flora of primates. Appl Environ Microbiol 1997; 63: 1066-76.
45. Boyd ES, Barkay T. The mercury resistance operon: from an origin in a geothermal environment to an efficient detoxification machine. Front Microbiol 2012; 3: 349.
46. Berg J, Thorsen MK, Holm PE et al. Cu exposure under field conditions coselects for antibiotic resistance as determined by a novel cultivationindependent bacterial community tolerance assay. Environ Sci Technol 2010; 44: 8724-8.
47. 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: e27300.
48. Gullberg E, Albrecht LM, Karlsson C et al. Selection of a multidrug resistance plasmid by sublethal levels of antibiotics and heavy metals. MBio 2014; 5: e01918-14.
49. Aarestrup FM, Hasman H. Susceptibility of different bacterial species isolated from food animals to copper sulphate, zinc chloride and antimicrobial substances used for disinfection. Vet Microbiol 2004; 100: 83-9.
50. Mourão J, Rae J, Silveira E et al. Relevance of tcrYAZB operon acquisition for Enterococcus survival at high copper concentrations under anaerobic conditions. J Antimicrob Chemother 2016; 71: 560-3.
51. Porcheron G, Garenaux A, Proulx J et al. Iron, copper, zinc, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the different metal transport systems for virulence. Front Cell Infect Microbiol 2013; 3: 90.
52. Maillard JY, Hartemann P. Silver as an antimicrobial: facts and gaps in knowledge. Crit Rev Microbiol 2013; 39: 373-83.
53. Mijnendonckx K, Leys N, Mahillon J et al. Antimicrobial silver: uses, toxicity and potential for resistance. Biometals 2013; 26: 609-21.
54. Achard ME, Tree JJ, Holden JA et al. The multi-copper-ion oxidase CueO of Salmonella enterica serovar Typhimurium is required for systemic virulence. Infect Immun 2010; 78: 2312-9.