Microbial Ecology

, Volume 75, Issue 1, pp 104–112 | Cite as

Plasmid-Mediated Quinolone Resistance (PMQR) Genes and Class 1 Integrons in Quinolone-Resistant Marine Bacteria and Clinical Isolates of Escherichia coli from an Aquacultural Area

  • Alexandra Tomova
  • Larisa Ivanova
  • Alejandro H. Buschmann
  • Henry P. Godfrey
  • Felipe C. Cabello
Environmental Microbiology


Antimicrobial usage in aquaculture selects for antimicrobial-resistant microorganisms in the marine environment. The relevance of this selection to terrestrial animal and human health is unclear. Quinolone-resistance genes qnrA, qnrB, and qnrS were chromosomally located in four randomly chosen quinolone-resistant marine bacteria isolated from an aquacultural area with heavy quinolone usage. In quinolone-resistant uropathogenic clinical isolates of Escherichia coli from a coastal area bordering the same aquacultural region, qnrA was chromosomally located in two E. coli isolates, while qnrB and qnrS were located in small molecular weight plasmids in two other E. coli isolates. Three quinolone-resistant marine bacteria and three quinolone-resistant E. coli contained class 1 integrons but without physical association with PMQR genes. In both marine bacteria and uropathogenic E. coli, class 1 integrons had similar co-linear structures, identical gene cassettes, and similarities in their flanking regions. In a Marinobacter sp. marine isolate and in one E. coli clinical isolate, sequences immediately upstream of the qnrS gene were homologous to comparable sequences of numerous plasmid-located qnrS genes while downstream sequences were different. The observed commonality of quinolone resistance genes and integrons suggests that aquacultural use of antimicrobials might facilitate horizontal gene transfer between bacteria in diverse ecological locations.


Quinolone resistance Aquaculture Class 1 integrons PMQR genes Marine bacteria Uropathogenic clinical isolates 



This work was supported by grants from the Lenfest Ocean Program/Pew Charitable Trusts (FCC and AHB), Basal Program (FB001), Chile (AHB), and by a fellowship from the John Simon Guggenheim Foundation (FCC).


  1. 1.
    Marshall BM, Levy SB (2011) Food animals and antimicrobials: impacts on human health Clin Microbiol Rev 24:718–733. doi: 10.1128/CMR.00002-11 CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Domingues S, Harms K, Fricke WF, Johnsen PJ, Da Silva GJ, Nielsen KM (2012) Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species PLoS Pathog 8:e1002837. doi: 10.1371/journal.ppat.1002837 CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Cabello FC, Godfrey HP, Tomova A, Ivanova L, Dölz H, Millanao A, Buschmann AH (2013) Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health Environ Microbiol 15:1917–1942. doi: 10.1111/1462-2920.1213 CrossRefPubMedGoogle Scholar
  4. 4.
    Cabello FC, Godfrey HP, Buschmann AH, Dölz HJ (2016) Aquaculture as yet another environmental gateway to the development and globalisation of antimicrobial resistance Lancet Infect Dis 16:e127–e133. doi: 10.1016/S1473-3099(16)00100-6 CrossRefPubMedGoogle Scholar
  5. 5.
    Prescott JF (2006) History of antimicrobial usage in agriculture. In: Aarestrup FM (ed) Antimicrobial resistance in bacteria of animal origin. ASM Press, Washington, D.C., pp. 19–27Google Scholar
  6. 6.
    Cantas L, Shah SQ, Cavaco LM, Manaia CM, Walsh F, Popowska M, Garelick H, Bürgmann H, Sørum H (2013) A brief multi-disciplinary review on antimicrobial resistance in medicine and its linkage to the global environmental microbiota Front Microbiol 4:96. doi: 10.3389/fmicb.2013.00096 CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Hastings PJ, Rosenberg SM, Slack A (2004) Antibiotic-induced lateral transfer of antibiotic resistance Trends Microbiol 12:401–404CrossRefPubMedGoogle Scholar
  8. 8.
    Sun M, Chang Z, Van den Brink PJ, Li J, Zhao F, Rico A (2016) Environmental and human health risks of antimicrobials used in Fenneropenaeus chinensis aquaculture production in China Environ Sci Pollut Res Int 23:15689–15702. doi: 10.1007/s11356-016-6733-y CrossRefPubMedGoogle Scholar
  9. 9.
    Baharoglu Z, Mazel D (2011) Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance Antimicrob Agents Chemother 55:2438–2441. doi: 10.1128/AAC.01549-10 CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Shah SQ, Cabello FC, L'Abée-Lund TM, Tomova A, Godfrey HP, Buschmann AH, Sørum H (2014) Antimicrobial resistance and antimicrobial resistance genes in marine bacteria from salmon aquaculture and non-aquaculture sites Environ Microbiol 16:1310–1320. doi: 10.1111/1462-2920.12421 CrossRefPubMedGoogle Scholar
  11. 11.
    Muziasari WI, Parnanen K, Johnson TA, Lyra C, Karkman A, Stedtfeld RD, Tamminen M, Tiedje JM, Virta M (2016) Aquaculture changes the profile of antibiotic resistance and mobile genetic element associated genes in Baltic Sea sediments FEMS Microbiol Ecol 92:fiw052. doi: 10.1093/femsec/fiw052 CrossRefPubMedGoogle Scholar
  12. 12.
    Angulo FJ, Nargund VN, Chiller TC (2004) Evidence of an association between use of anti-microbial agents in food animals and anti-microbial resistance among bacteria isolated from humans and the human health consequences of such resistance J Vet Med B Infect Dis Vet Public Health 51:374–379CrossRefPubMedGoogle Scholar
  13. 13.
    Love DC, Rodman S, Neff RA, Nachman KE (2011) Veterinary drug residues in seafood inspected by the European Union, United States, Canada, and Japan from 2000 to 2009 Environ Sci Technol 45:7232–7240. doi: 10.1021/es201608q CrossRefPubMedGoogle Scholar
  14. 14.
    Chen DQ, Yang L, Luo YT, Mao MJ, Lin YP, Wu AW (2013) Prevalence and characterization of quinolone resistance in Laribacter hongkongensis from grass carp and Chinese tiger frog J Med Microbiol 62:1559–1564. doi: 10.1099/jmm.0.059451-0 CrossRefPubMedGoogle Scholar
  15. 15.
    Roy Chowdhury P, McKinnon J, Wyrsch E, Hammond JM, Charles IG, Djordjevic SP (2014) Genomic interplay in bacterial communities: implications for growth promoting practices in animal husbandry Front Microbiol 5:394. doi: 10.3389/fmicb.2014.00394 CrossRefPubMedPubMedCentralGoogle Scholar
  16. 16.
    Deng YT, Wu YL, Tan AP, Huang YP, Jiang L, Xue HJ, Wang WL, Luo L, Zhao F (2014) Analysis of antimicrobial resistance genes in Aeromonas spp. isolated from cultured freshwater animals in China Microb Drug Resist 20:350–356. doi: 10.1089/mdr.2013.0068 CrossRefPubMedGoogle Scholar
  17. 17.
    Hooper DC, Jacoby GA (2016) Topoisomerase inhibitors: fluoroquinolone mechanisms of action and resistance. Cold Spring Harb Perspect Med 6. doi: 10.1101/cshperspect.a025320
  18. 18.
    Robicsek A, Jacoby GA, Hooper DC (2006) The worldwide emergence of plasmid-mediated quinolone resistance Lancet Infect Dis 6:629–640CrossRefPubMedGoogle Scholar
  19. 19.
    Fonseca EL, Vicente AC (2013) Epidemiology of qnrVC alleles and emergence out of the Vibrionaceae family J Med Microbiol 62:1628–1630. doi: 10.1099/jmm.0.062661-0 CrossRefPubMedGoogle Scholar
  20. 20.
    Kim HB, Wang M, Park CH, Kim EC, Jacoby GA, Hooper DC (2009) oqxAB encoding a multidrug efflux pump in human clinical isolates of Enterobacteriaceae Antimicrob Agents Chemother 53:3582–3584. doi: 10.1128/AAC.01574-08 CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Ma J, Zeng Z, Chen Z, Xu X, Wang X, Deng Y, Lü D, Huang L, Zhang Y, Liu J, Wang M (2009) High prevalence of plasmid-mediated quinolone resistance determinants qnr, aac(6′)-Ib-cr, and qepA among ceftiofur-resistant Enterobacteriaceae isolates from companion and food-producing animals Antimicrob Agents Chemother 53:519–524. doi: 10.1128/AAC.00886-08 CrossRefPubMedGoogle Scholar
  22. 22.
    Nakaminami H, Noguchi N, Sasatsu M (2010) Fluoroquinolone efflux by the plasmid-mediated multidrug efflux pump QacB variant QacBIII in Staphylococcus aureus Antimicrob Agents Chemother 54:4107–4111. doi: 10.1128/AAC.01065-09 CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Rodríguez-Martínez JM, Diaz de Alba P, Briales A, Machuca J, Lossa M, Fernández-Cuenca F, Rodríguez Baño J, Martínez-Martínez L, Pascual Á (2013) Contribution of OqxAB efflux pumps to quinolone resistance in extended-spectrum-beta-lactamase-producing Klebsiella pneumoniae J Antimicrob Chemother 68:68–73. doi: 10.1093/jac/dks377 CrossRefPubMedGoogle Scholar
  24. 24.
    Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH, Bush K, Hooper DC (2006) Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase Nat Med 12:83–88CrossRefPubMedGoogle Scholar
  25. 25.
    Zhao JY, Dang H (2012) Coastal seawater bacteria harbor a large reservoir of plasmid-mediated quinolone resistance determinants in Jiaozhou Bay, China Microb Ecol 64:187–199. doi: 10.1007/s00248-012-0008-z CrossRefPubMedGoogle Scholar
  26. 26.
    Cesaro A, Bettoni RR, Lascols C, Merens A, Soussy CJ, Cambau E (2008) Low selection of topoisomerase mutants from strains of Escherichia coli harbouring plasmid-borne qnr genes J Antimicrob Chemother 61:1007–1015. doi: 10.1093/jac/dkn077 CrossRefPubMedGoogle Scholar
  27. 27.
    Martínez-Martínez L, Cano ME, Rodríguez-Martìnez JM, Calvo J, Pascual A (2008) Plasmid-mediated quinolone resistance Expert Rev Anti-Infect Ther 6:685–711CrossRefPubMedGoogle Scholar
  28. 28.
    Jakobsen L, Cattoir V, Jensen KS, Hammerum AM, Nordmann P, Frimodt-Møller N (2012) Impact of low-level fluoroquinolone resistance genes qnrA1, qnrB19 and qnrS1 on ciprofloxacin treatment of isogenic Escherichia coli strains in a murine urinary tract infection model J Antimicrob Chemother 67:2438–2444. doi: 10.1093/jac/dks224 CrossRefPubMedGoogle Scholar
  29. 29.
    Domínguez-Herrera J, Velasco C, Docobo-Pérez F, Rodríguez-Martínez JM, López-Rojas R, Briales A, Pichardo C, Díaz-de-Alba P, Rodríguez-Baño J, Pascual A, Pachón J (2013) Impact of qnrA1, qnrB1 and qnrS1 on the efficacy of ciprofloxacin and levofloxacin in an experimental pneumonia model caused by Escherichia coli with or without the GyrA mutation Ser83Leu J Antimicrob Chemother 68:1609–1615. doi: 10.1093/jac/dkt063 CrossRefPubMedGoogle Scholar
  30. 30.
    Michon A, Allou N, Chau F, Podglajen I, Fantin B, Cambau E (2011) Plasmidic qnrA3 enhances Escherichia coli fitness in absence of antibiotic exposure PLoS One 6:e24552. doi: 10.1371/journal.pone.0024552 CrossRefPubMedPubMedCentralGoogle Scholar
  31. 31.
    Cattoir V, Nordmann P (2009) Plasmid-mediated quinolone resistance in gram-negative bacterial species: an update Curr Med Chem 16:1028–1046CrossRefPubMedGoogle Scholar
  32. 32.
    Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A (2009) Plasmid-mediated quinolone resistance: a multifaceted threat Clin Microbiol Rev 22:664–689. doi: 10.1128/microbiolspec.PLAS-0006-2013 CrossRefPubMedPubMedCentralGoogle Scholar
  33. 33.
    Nordmann P, Poirel L (2005) Emergence of plasmid-mediated resistance to quinolones in Enterobacteriaceae J Antimicrob Chemother 56:463–469CrossRefPubMedGoogle Scholar
  34. 34.
    Rosewarne CP, Pettigrove V, Stokes HW, Parsons YM (2010) Class 1 integrons in benthic bacterial communities: abundance, association with Tn402-like transposition modules and evidence for coselection with heavy-metal resistance FEMS Microbiol Ecol 72:35–46. doi: 10.1111/j.1574-6941.2009.00823.x CrossRefPubMedGoogle Scholar
  35. 35.
    Stokes HW, Gillings MR (2011) Gene flow, mobile genetic elements and the recruitment of antibiotic resistance genes into gram-negative pathogens FEMS Microbiol Rev 35:790–819. doi: 10.1111/j.1574-6976.2011.00273.x CrossRefPubMedGoogle Scholar
  36. 36.
    Cattoir V, Poirel L, Mazel D, Soussy CJ, Nordmann P (2007) Vibrio splendidus as the source of plasmid-mediated QnrS-like quinolone resistance determinants Antimicrob Agents Chemother 51:2650–2651CrossRefPubMedPubMedCentralGoogle Scholar
  37. 37.
    Cattoir V, Poirel L, Aubert C, Soussy CJ, Nordmann P (2008) Unexpected occurrence of plasmid-mediated quinolone resistance determinants in environmental Aeromonas spp Emerg Infect Dis 14:231–237. doi: 10.3201/eid1402.070677 CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Xia R, Guo X, Zhang Y, Xu H (2010) qnrVC-like gene located in a novel complex class 1 integron harboring the ISCR1 element in an Aeromonas punctata strain from an aquatic environment in Shandong Province, China Antimicrob Agents Chemother 54:3471–3474. doi: 10.1128/AAC.01668-09 CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Han JE, Kim JH, Choresca Jr CH, Shin SP, Jun JW, Chai JY, Park SC (2012) First description of ColE-type plasmid in Aeromonas spp. carrying quinolone resistance (qnrS2) gene Lett Appl Microbiol 55:290–294. doi: 10.1111/j.1472-765X.2012.03293.x CrossRefPubMedGoogle Scholar
  40. 40.
    Del Castillo CS, Hikima J, Jang HB, Nho SW, Jung TS, Wongtavatchai J, Kondo H, Hirono I, Takeyama H, Aoki T (2013) Comparative sequence analysis of a multidrug-resistant plasmid from Aeromonas hydrophila Antimicrob Agents Chemother 57:120–129. doi: 10.1128/AAC.01239-12 CrossRefPubMedPubMedCentralGoogle Scholar
  41. 41.
    Quiroga MP, Andres P, Petroni A, Soler Bistué AJ, Guerriero L, Vargas LJ, Zorreguieta A, Tokumoto M, Quiroga C, Tolmasky ME, Galas M, Centrón D (2007) Complex class 1 integrons with diverse variable regions, including aac(6′)-Ib-cr, and a novel allele, qnrB10, associated with ISCR1 in clinical enterobacterial isolates from Argentina Antimicrob Agents Chemother 51:4466–4470CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Chen YT, Liao TL, Liu YM, Lauderdale TL, Yan JJ, Tsai SF (2009) Mobilization of qnrB2 and ISCR1 in plasmids Antimicrob Agents Chemother 53:1235–1237. doi: 10.1128/AAC.00970-08 CrossRefPubMedGoogle Scholar
  43. 43.
    Rodríguez-Martínez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A (2011) Plasmid-mediated quinolone resistance: an update J Infect Chemother 17:149–182. doi: 10.1007/s10156-010-0120-2 CrossRefPubMedGoogle Scholar
  44. 44.
    Buschmann AH, Tomova A, López A, Maldonado MA, Henríquez LA, Ivanova L, Moy F, Godfrey HP, Cabello FC (2012) Salmon aquaculture and antimicrobial resistance in the marine environment PLoS One 7:e42724. doi: 10.1371/journal.pone CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Tomova A, Ivanova L, Buschmann AH, Rioseco ML, Kalsi RK, Godfrey HP, Cabello FC (2015) Antimicrobial resistance genes in marine bacteria and human uropathogenic Escherichia coli from a region of intensive aquaculture Environ Microbiol Rep 7:803–809. doi: 10.1111/1758-2229.12327 CrossRefPubMedGoogle Scholar
  46. 46.
    Barton BM, Harding GP, Zuccarelli AJ (1995) A general method for detecting and sizing large plasmids Anal Biochem 226:235–240CrossRefPubMedGoogle Scholar
  47. 47.
    Liu SL, Hessel A, Sanderson KE (1993) Genomic mapping with I-Ceu I, an intron-encoded endonuclease specific for genes for ribosomal RNA, in Salmonella spp., Escherichia coli, and other bacteria Proc Natl Acad Sci U S A 90:6874–6878CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Xu H, Davies J, Miao V (2007) Molecular characterization of class 3 integrons from Delftia spp J Bacteriol 189:6276–6283CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Song JS, Jang SJ, Lee JJ, Lee JH, Bae IK, Jeong BC, Cha SS, Lee JH, Hong SK, Lee SH (2010) Association of the bla CMY-10 gene with a novel complex class 1 integron carrying an ISCR1 element in clinical isolates from Korea Clin Microbiol Infect 16:1013–1017. doi: 10.1111/j.1469-0691.2009.03002.x CrossRefPubMedGoogle Scholar
  50. 50.
    Lévesque C, Piché L, Larose C, Roy PH (1995) PCR mapping of integrons reveals several bnovel combinations of resistance genes Antimicrob Agents Chemother 39:185–191CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Sunde M, Sørum H (1999) Characterization of integrons in Escherichia coli of the normal intestinal flora of swine Microb Drug Resist 5:279–287CrossRefPubMedGoogle Scholar
  52. 52.
    Gaze WH, Abdouslam N, Hawkey PM, Wellington EM (2005) Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment Antimicrob Agents Chemother 49:1802–1807CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Stalder T, Barraud O, Casellas M, Dagot C, Ploy MC (2012) Integron involvement in environmental spread of antibiotic resistance Front Microbiol 3:119. doi: 10.3389/fmicb.2012.00119 CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Poirel L, Liard A, Rodriguez-Martinez JM, Nordmann P (2005) Vibrionaceae as a possible source of Qnr-like quinolone resistance determinants J Antimicrob Chemother 56:1118–1121CrossRefPubMedGoogle Scholar
  55. 55.
    Saga T, Kaku M, Onodera Y, Yamachika S, Sato K, Takase H (2005) Vibrio parahaemolyticus chromosomal qnr homologue VPA0095: demonstration by transformation with a mutated gene of its potential to reduce quinolone susceptibility in Escherichia coli Antimicrob Agents Chemother 49:2144–2145CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Gillings MR (2014) Integrons: past, present, and future Microbiol Mol Biol Rev 78:257–277. doi: 10.1128/MMBR.00056-13 CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Kehrenberg C, Friederichs S, de Jong A, Michael GB, Schwarz S (2006) Identification of the plasmid-borne quinolone resistance gene qnrS in Salmonella enterica serovar Infantis J Antimicrob Chemother 58:18–22CrossRefPubMedGoogle Scholar
  58. 58.
    Karczmarczyk M, Stephan R, Hachler H, Fanning S (2012) Complete nucleotide sequence of pVQS1 containing a quinolone resistance determinant from Salmonella enterica serovar Virchow associated with foreign travel J Antimicrob Chemother 67:1861–1864. doi: 10.1093/jac/dks158 CrossRefPubMedGoogle Scholar
  59. 59.
    Jensen RV, Depasquale SM, Harbolick EA, Hong T, Kernell AL, Kruchko DH, Modise T, Smith CE, McCarter LL, Stevens AM (2013) Complete genome sequence of prepandemic Vibrio parahaemolyticus BB22OP Genome Announc 1:e00002–e00012. doi: 10.1128/genomeA.00002-12 CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Aedo S, Ivanova L, Tomova A, Cabello FC (2014) Plasmid-related quinolone resistance determinants in epidemic Vibrio parahaemolyticus, uropathogenic Escherichia coli, and marine bacteria from an aquaculture area in Chile Microb Ecol 68:324–328. doi: 10.1007/s00248-014-0409-2 CrossRefPubMedGoogle Scholar
  61. 61.
    Ramirez MS, Nikolaidis N, Tolmasky ME (2013) Rise and dissemination of aminoglycoside resistance: the aac(6′)-Ib paradigm Front Microbiol 4:121. doi: 10.3389/fmicb.2013.00121 CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Robicsek A, Strahilevitz J, Sahm DF, Jacoby GA, Hooper DC (2006) qnr prevalence in ceftazidime-resistant Enterobacteriaceae isolates from the United States Antimicrob Agents Chemother 50:2872–2874CrossRefPubMedPubMedCentralGoogle Scholar
  63. 63.
    Jacoby GA, Griffin CM, Hooper DC (2011) Citrobacter spp. as a source of qnrB alleles Antimicrob Agents Chemother 55:4979–4984. doi: 10.1128/AAC.05187-11 CrossRefPubMedPubMedCentralGoogle Scholar
  64. 64.
    Hatosy SM, Martiny AC (2015) The ocean as a global reservoir of antibiotic resistance genes Appl Environ Microbiol 81:7593–7599. doi: 10.1128/AEM.00736-15 CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Ribeiro TG, Novais Â, Branquinho R, Machado E, Peixe L (2015) Phylogeny and comparative genomics unveil independent diversification trajectories of qnrB and genetic platforms within particular Citrobacter species Antimicrob Agents Chemother 59:5951–5958. doi: 10.1128/AAC.00027-15 CrossRefPubMedPubMedCentralGoogle Scholar
  66. 66.
    Lin M, Wu X, Yan Q, Ma Y, Huang L, Qin Y, Xu X (2016) Incidence of antimicrobial-resistance genes and integrons in antibiotic-resistant bacteria isolated from eels and aquaculture ponds Dis Aquat Org 120:115–123. doi: 10.3354/dao03013 CrossRefPubMedGoogle Scholar
  67. 67.
    Guglielmini J, Quintais L, Garcillán-Barcia MP, de la Cruz F, Rocha EPC (2011) The repertoire of ICE in prokaryotes underscores the unity, diversity, and ubiquity of conjugation PLoS Genet 7:e1002222. doi: 10.1371/journal.pgen.1002222 CrossRefPubMedPubMedCentralGoogle Scholar
  68. 68.
    Silva J, Zemelman R, Mandoca MA, Henríquez M, Merino C, González C (1987) Antibiotic-resistant gram negative bacilli isolated from sea water and shellfish. Possible epidemiological implications Rev Latinoam Microbiol 29:165–169PubMedGoogle Scholar
  69. 69.
    Miranda CD, Zemelman R (2001) Antibiotic resistant bacteria in fish from the Concepcion Bay, Chile Mar Pollut Bull 42:1096–1102CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Microbiology and ImmunologyNew York Medical CollegeValhallaUSA
  2. 2.Institute of Physiology, Faculty of MedicineComenius University in BratislavaBratislavaSlovakia
  3. 3.Centro i~mar and CeBiBUniversidad de Los LagosPuerto MonttChile
  4. 4.Department of PathologyNew York Medical CollegeValhallaUSA

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