Advertisement

Plasmid-mediated quinolone resistance in Enterobacteriaceae: a systematic review with a focus on Mediterranean countries

  • B. Yanat
  • J.-M. Rodríguez-Martínez
  • A. Touati
Review

Abstract

Quinolones are a family of synthetic broad-spectrum antimicrobial drugs. These molecules have been widely prescribed to treat various infectious diseases and have been classified into several generations based on their spectrum of activity. Quinolones inhibit bacterial DNA synthesis by interfering with the action of DNA gyrase and topoisomerase IV. Mutations in the genes encoding these targets are the most common mechanisms of high-level fluoroquinolone resistance. Moreover, three mechanisms for plasmid-mediated quinolone resistance (PMQR) have been discovered since 1998 and include Qnr proteins, the aminoglycoside acetyltransferase AAC(6′)-Ib-cr, and plasmid-mediated efflux pumps QepA and OqxAB. Plasmids with these mechanisms often encode additional antimicrobial resistance (extended spectrum beta-lactamases [ESBLs] and plasmidic AmpC [pAmpC] ß-lactamases) and can transfer multidrug resistance. The PMQR determinants are disseminated in Mediterranean countries with prevalence relatively high depending on the sources and the regions, highlighting the necessity of long-term surveillance for the future monitoring of trends in the occurrence of PMQR genes.

Keywords

Efflux Pump Nalidixic Acid Quinolone Resistance Mutant Preventive Concentration Quinolone Resistance Determine Region 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Compliance with ethical standards

Conflicts of interest

None to declare.

Funding

None to declare.

References

  1. 1.
    Lesher GY, Froelich EJ, Gruett MD, Bailey JH, Brundage RP (1962) 1,8-naphthyridine derivatives. a new class of chemotherapeutic agents. J Med Chem 5:1063–1065CrossRefGoogle Scholar
  2. 2.
    Naeem A, Badshah SL, Muska M, Ahmad N, Khan K (2016) The current case of quinolones: synthetic approaches and antibacterial activity. Molecules 21:268PubMedCrossRefGoogle Scholar
  3. 3.
    Jacoby GA (2005) Mechanisms of resistance to quinolones. Clin Infect Dis 41:120–126CrossRefGoogle Scholar
  4. 4.
    Jacoby GA, Strahilevitz J, Hooper DC (2014) Plasmid-mediated quinolone resistance. Microbiol Spectr DOI: 10.1128/microbiolspec.PLAS-0006-2013 PubMedPubMedCentralGoogle Scholar
  5. 5.
    Poirel L, Cattoir V, Nordmann P (2012) Plasmid mediated quinolone resistance; interactions between human, animal, and environmental ecologies. Front Microbiol 3(24):1–7Google Scholar
  6. 6.
    Oliphant CM, Green GM (2002) Quinolones: a comprehensive review. Am Fam Physician 65:455–464PubMedGoogle Scholar
  7. 7.
    Paton JH, Reeves DS (1988) Fluoroquinolone antibiotics. Microbiology, pharmacokinetics and clinical use. Drugs 36:193–228PubMedCrossRefGoogle Scholar
  8. 8.
    Redgrave LS, Sutton SB, Webber MA, Piddock LJV (2014) Fluoroquinolone resistance: mechanisms, impact on bacteria, and role in evolutionary success. Trends Microbiol 22(8):438–445PubMedCrossRefGoogle Scholar
  9. 9.
    Álvarez-Hernández DA, Garza-Mayén GS, Vázquez-López R (2015) Quinolonas. Perspectivas actuales y mecanismos de resistencia. Rev Chilena Infectol 32(5):499–504PubMedCrossRefGoogle Scholar
  10. 10.
    Mohammadhosseini N, Pordeli M, Safavi M, Firoozpour L, Amin F, Kabudanian Ardestani S, Edraki N, Shafiee A, Foroumadi A (2015) Novel N-2-(furyl)-2-(chlorobenzyloxyimino) ethyl piperazinyl quinolones: synthesis, cytotoxic evaluation and structure-activity relationship. Iran J Pharm Res 14(4):1095–1103PubMedPubMedCentralGoogle Scholar
  11. 11.
    Cross RM, Flanigan DL, Monastyrskyi A, LaCrue AN, Saenz FE, Maignan JR et al (2014) Orally bioavailable 6-chloro-7-methoxy-4(1H)-quinolones efficacious against multiple stages of plasmodium. J Med Chem 57:8860–8879PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Boothe D, Boeckh A, Simpson B, Dubose K (2006) Comparison of pharmacodynamics and pharmacokinetic indices of efficacy for 5 fluoroquinolones toward pathogens of dogs and cats. J Vet Inter Med 20:1297–1306CrossRefGoogle Scholar
  13. 13.
    Hawkey PM (2003) Mechanisms of quinolone action and microbial response. J Antimicrob Chemother 51(1):29–35PubMedCrossRefGoogle Scholar
  14. 14.
    Kohanski MA, Dwyer DJ, Collins JJ (2010) How antibiotics kill bacteria: from targets to networks. Nat Rev Microbiol 8(6):423–435PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Ruiz J (2003) Mechanisms of resistance to quinolones: target alterations, decreased accumulation and DNA gyrase protection. J Antimicrob Chemother 51:1109–1117PubMedCrossRefGoogle Scholar
  16. 16.
    Belenky P, Ye JD, Porter CBM, Cohen NR, Lobritz MA, Ferrantee T et al (2015) Bactericidal antibiotics induce toxic metabolic perturbations that lead to cellular damage. Cell Rep 13(5):968–980PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Kottur J, Nair DT (2016) Reactive oxygen species play an important role in the bactericidal activity of quinolone antibiotics. Angew Chem Int Ed Engl 55(7):2397–2400PubMedCrossRefGoogle Scholar
  18. 18.
    Piddock LJ, Walters RN (1992) Bactericidal activities of five quinolones for Escherichia coli strains with mutations in genes encoding the SOS response or cell division. Antimicrob Agents Chemother 36:819–825PubMedPubMedCentralCrossRefGoogle Scholar
  19. 19.
    Yoshida H, Bogaki M, Nakamura M, Nakamura S (1990) Quinolone resistance-determining region in the DNA gyrase gyrA gene of Escherichia coli. Antimicrob Agents Chemother 34:1271–1272PubMedPubMedCentralCrossRefGoogle Scholar
  20. 20.
    Barnard FM, Maxwell A (2001) Interaction between DNA gyrase and quinolones: effects of alanine mutations at gyrA subunit residues Ser83 and Asp87. Antimicrob Agents Chemother 45:1994–2000PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Wohlkonig A, Chan PF, Fosberry AP, Homes P, Huang J, Kranz M et al (2010) Structural basis of quinolone inhibition of type IIA topoisomerases and target-mediated resistance. Nat Struct Mol Biol 17:1152–1153PubMedCrossRefGoogle Scholar
  22. 22.
    Laponogov I, Veselkov DA, Crevel IM, Pan XS, Fisher LM, Sanderson MR (2013) Structure of an ‘open’ clamp type II topoisomerase-DNA complex provides a mechanism for DNA capture and transport. Nucl Acids Res 41:9911–9923PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Everett MJ, Jin YF, Ricci V, Piddock LJV (1996) Contribution of individual mechanisms to fluoroquinolone resistance in 36 Escherichia coli strains isolated from humans and animals. Antimicrob Agents Chemother 40:2380–2386PubMedPubMedCentralGoogle Scholar
  24. 24.
    Tavio MM, Vila J, Ruiz J, Martin-Sanchez AM, Jiménez de Anta MT (1999) Mechanisms involved in the development of resistance to fluoroquinolones in Escherichia coli strains. J Antimicrob Chemother 44:735–742PubMedCrossRefGoogle Scholar
  25. 25.
    Ruiz J, Gómez J, Navia MM, Ribera A, Sierra JM, Marco F et al (2002) High prevalence of nalidixic acid resistant, ciprofloxacin susceptible phenotype among clinical isolates of Escherichia coli and other Enterobacteriaceae. Diagn Microbiol Infect Dis 42(4):257–261PubMedCrossRefGoogle Scholar
  26. 26.
    Aldred KJ, Schwanz HA, Li G, Williamson BH, McPherson SA, Turnbough CL Jr et al (2015) Activity of quinolone cp-115,955 against bacterial and human type II topoisomerases is mediated by different interactions. Biochemistry 54:1278–1286PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Machuca J, Briales A, Labrador G, Díaz-de-Alba P, López-Rojas R, Docobo-Pérez F et al (2014) Interplay between plasmid-mediated and chromosomal-mediated fluoroquinolone resistance and bacterial fitness in Escherichia coli. J Antimicrob Chemother 69(12):3203–3215PubMedCrossRefGoogle Scholar
  28. 28.
    Piddock LJ (1999) Mechanisms of fluoroquinolone resistance: an update 1994-1998. Drugs 58(2):11–18PubMedCrossRefGoogle Scholar
  29. 29.
    Hirai K, Aoyama H, Suzue S, Irikura T, Iyobe S, Mitsuhashi S (1986) Isolation and characterization of norfloxacin resistant mutants of Escherichia coli K-12. Antimicrob Agents Chemother 30:248–253PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Komp Lindgren P, Marcusson LL, Sandvang D, Frimodt-Møller N, Hughes D (2005) Biological cost of single and multiple norfloxacin resistance mutations in Escherichia coli implicated in urinary tract infections. Antimicrob Agents Chemother 49:2343–2351PubMedCrossRefGoogle Scholar
  31. 31.
    Robicsek A, Strahilevitz J, Jacoby GA, Macielag M, Abbanat D, Park CH et al (2006) Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 12:83–88PubMedCrossRefGoogle Scholar
  32. 32.
    Yamane K, Wachino J, Suzuki S, Kimura K, Shibata N, Kato (2007) New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother 51(9):3354–3360PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Hansen LH, Jensen LB, Sørensen HI, Sørensen SJ (2007) Substrate specificity of the OqxAB multidrug resistance pump in Escherichia coli and selected enteric bacteria. J Antimicrob Chemother 60:145–147PubMedCrossRefGoogle Scholar
  34. 34.
    Yoshida H, Bogaki M, Nakamura M, Yamanaka LM, Nakamura S (1991) Quinolone resistance-determining region in the DNA gyrase gyrB gene of Escherichia coli. Antimicrob Agents Chemother 35:1647–1650PubMedPubMedCentralCrossRefGoogle Scholar
  35. 35.
    Breines DM, Ouabdesselam S, Ng EY, Tankovic J, Shah S, Soussy CJ, Hooper DC (1997) Quinolone resistance locus nfxD of Escherichia coli is a mutant allele of parE gene encoding a subunit of topoisomerase IV. Antimicrob Agents Chemother 41:175–179PubMedPubMedCentralGoogle Scholar
  36. 36.
    Chapman JS, Georgopapadokou NH (1988) Routes of quinolone permeation in Escherichia coli. Antimicrob Agents Chemother 32:438–442PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Kang HW, Woo GJ (2014) Increase of multidrug efflux pump expression in fluoroquinolone-resistant Salmonella mutants induced by ciprofloxacin selective pressure. Res Vet Sci 97(2):182–186PubMedCrossRefGoogle Scholar
  38. 38.
    Grkovic S, Brown MH, Skurray RA (2002) Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66:671–701PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Poole K (2005) Efflux-mediated antimicrobial resistance. J Antimicrob Chemother 56:20–51PubMedCrossRefGoogle Scholar
  40. 40.
    Alekshun MN, Levy SB (1997) Regulation of chromosomally mediated multiple antibiotic resistance: the mar regulon. Antimicrob Agents Chemother 41:2067–2075PubMedPubMedCentralGoogle Scholar
  41. 41.
    Yamasaki E, Yamada C, Jin X, Nair GB, Kurazono H, Yamamoto S (2015) Expression of marA is remarkably increased from the early stage of development of fluoroquinolone-resistance in uropathogenic Escherichia coli. J Infect Chemother 21(2):105–109PubMedCrossRefGoogle Scholar
  42. 42.
    Chou JH, Greenberg JT, Demple B (1998) Postranscriptional repression of Escherichia coli OmpF protein in response to redox stress: positive control of the micF antisense RNA by the soxRS locus. J Bacteriol 175:1026–1031CrossRefGoogle Scholar
  43. 43.
    Aoyama H, Sato K, Kato T, Hirai K, Mitsuhashi S (1987) Norfloxacin resistance in a clinical isolate of Escherichia coli. Antimicrob Agent Chemother 31:1640–1641CrossRefGoogle Scholar
  44. 44.
    Cohen SP, McMurry LM, Hooper DC, Wolfson JS, Levy SB (1989) Cross-resistance to fluoroquinolone in multiple-antibiotic-resistance (Mar) Escherichia coli selected by tetracycline or chloramphenicol: decreased drug accumulation associated with membrane changes in addition to OmpF reduction. Antimicrob Agents Chemother 33:1318–1325PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Mitsuyama J, Itoh Y, Takahata M, Okamoto S, Yasuda T (1992) In vitro antibacterial activities of tosufloxacin against and uptake of tosufloxacin by outer membrane mutants of Escherichia coli, Proteus mirabilis and Salmonella typhimurium. Antimicrob Agents Chemother 36:2030–2036PubMedPubMedCentralCrossRefGoogle Scholar
  46. 46.
    Martínez-Martínez L, Pascual A, Jacoby GA (1998) Quinolone resistance from a transferable plasmid. Lancet 351:797–799PubMedCrossRefGoogle Scholar
  47. 47.
    Tran JH, Jacoby GA, Hooper DC (2005) Interaction of the plasmid-encoded quinolone resistance protein QnrA with Escherichia coli topoisomerase IV. Antimicrob Agents Chemother 49(7):3050–3052PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Vetting MW, Hedge SS, Fajardo JE, Fiser A, Roderick SL, Takiff HE et al (2006) Pentapeptide repeat proteins. Biochemistry 45:1–10PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Garrido MC, Herrero M, Kolter R, Moreno F (1988) The export of the DNA replication inhibitor microcin B17 provides immunity for the host cell. EMBO J 7(6):1853–1862PubMedPubMedCentralGoogle Scholar
  50. 50.
    Tran JH, Jacoby GA (2002) Mechanism of plasmid-mediated quinolone resistance. Proc Natl Acad Sci 99:5638–5642PubMedPubMedCentralCrossRefGoogle Scholar
  51. 51.
    Hata M, Suzuki M, Matsumoto M, Takahashi M, Sato K, Ibe S et al (2005) Cloning of a novel gene for quinolone resistance from a transferable plasmid in Shigella flexneri 2b. Antimicrob Agents Chemother 49:801–803PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Jacoby GA, Walsh KE, Mills DM, Walker VJ, Oh H, Robicsek A et al (2006) qnrB, another plasmid-mediated gene for quinolone resistance. Antimicrob Agents Chemother 50(4):1178–1182PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Wang M, Guo Q, Xu X, Wang X, Ye X, Wu S et al (2009) New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 53:1892–1897PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Cavaco LM, Hasman H, Xia S, Aarestrup FM (2009) qnrD, a novel gene conferring transferable quinolone resistance in Salmonella enterica serovar Kentucky and Bovismorbificans strains of human origin. Antimicrob Agents Chemother 53:603–608PubMedCrossRefGoogle Scholar
  55. 55.
    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 54:3471–3474PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Singh R, Rajpara N, Tak J, Patel A, Mohanty P, Vinothkumar K et al (2012) Clinical isolates of Vibrio fluvialis from Kolkata, India, obtained during 2006: plasmids, the qnr gene and a mutation in gyrase A as mechanisms of multidrug resistance. J Med Microbiol 61:369–374PubMedCrossRefGoogle Scholar
  57. 57.
    Fonseca EL, Dos Santos Freitas F, Vieira VV, Vicente AC (2008) New qnr gene cassettes associated with superintegron repeats in Vibrio cholerae O1. Emerg Infect Dis 14:1129–1131PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Rodriguez-Martinez JM, Cano ME, Velasco C, Martínez-Martínez L, Pascual A (2011) Plasmid-mediated quinolone resistance: an update. J Infect Chemother 17:149–182PubMedCrossRefGoogle Scholar
  59. 59.
    Poirel L, Rodriguez-Martinez JM, Mammeri H, Liard A, Nordmann P (2005) Origin of plasmid-mediated quinolone resistance determinant QnrA. Antimicrob Agents Chemother 49:3523–3525PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    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 51:2650–2651PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Jacoby GA, Griffin CM, Hooper DC (2011) Citrobacter spp.as a source of qnrB alleles. Antimicrob Agents Chemother 55:4979–4984PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Guillard T, Grillon A, De Champs C, Cartier C, Bercot B, Lebreil AL (2014) Mobile insertion cassette elements found in small nontransmissible plasmids in Proteeae may explain qnrD mobilization. PLoS One 9(2):1–8CrossRefGoogle Scholar
  63. 63.
    Malik M, Zhao X, Drlica K (2006) Lethal fragmentation of bacterial chromosomes mediated by DNA gyrase and quinolones. Mol Microbiol 61:810–825PubMedCrossRefGoogle Scholar
  64. 64.
    Baharoglu Z, Mazel D (2014) SOS, the formidable strategy of bacteria against aggressions. FEMS Microbiol Rev 38(6):1126–1145PubMedCrossRefGoogle Scholar
  65. 65.
    Wang M, Jacoby GA, Mills DM, Hoope DC (2009) SOS regulation of qnrB expression. Antimicrob Agents Chemother 53(2):821–823PubMedCrossRefGoogle Scholar
  66. 66.
    Briales A, Rodriguez-Martinez JM, Velasco C, Machuca J, Dìaz de Alba P, Blazquez J et al (2012) Exposure to diverse antimicrobials induces the expression of qnrB1, qnrD and smaqnr genes by SOS-dependent regulation. Antimicrob Chemother 67:2854–2859CrossRefGoogle Scholar
  67. 67.
    Da Re S, Garnier F, Guérin E, Campoy S, Denis F, Ploy MC (2009) The SOS response promotes qnrB quinolone-resistance expression. EMBO Rep 10(8):929–933PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Little JW, Edmiston SH, Pacelli LZ, Mount DW (1980) Cleavage of the Escherichia coli lexA protein by the recA protease. Proc Natl Acad Sci U S A 77:3225–3229PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Strahilevitz J, Jacoby GA, Hooper DC, Robicsek A (2009) Plasmid-mediated quinolone resistance: a multifaceted threat. Clin Microbiol Rev 22:664–689PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Robicsek A, Jacoby GA, Hooper DC (2006) The worldwide emergence of plasmid-mediated quinolone resistance. Lancet Infect Dis 6:629–640PubMedCrossRefGoogle Scholar
  71. 71.
    Perichon B, Courvalin P, Galimand M (2007) Transferable resistance to aminoglycosides by methylation of G1405 in 16S rRNA and to hydrophilic fluoroquinolones by QepA-mediated efflux in Escherichia coli. Antimicrob Agents Chemother 51:2464–2469PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Cattoir V, Poirel L, Nordmann P (2008) Plasmid-mediated quinolone resistance pump QepA2 in an Escherichia coli isolate from France. Antimicrob Agents Chemother 52:3801–3804PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Wang D, Huang X, Chen J, Mou Y, Li H, Yang L (2015) Characterization of genetic structures of the qepA3 gene in clinical isolates of Enterobacteriaceae. Front Microbiol 6:1147PubMedPubMedCentralGoogle Scholar
  74. 74.
    Hansen LH, Johannesen E, Burmølle M, Sørensen AH, Sørensen SJ (2004) Plasmid-encoded multidrug efflux pump conferring resistance to olaquindox in Escherichia coli. Antimicrob Agents Chemother 48:3332–3337PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Norman A, Hansen LH, She Q, Sørensen SJ (2008) Nucleotide sequence of pOLA52: a conjugative IncX1 plasmid from Escherichia coli which enables biofilm formation and multidrug efflux. Plasmid 60:59–74PubMedCrossRefGoogle Scholar
  76. 76.
    Rodriguez-Martinez JM, Diaz de Alba P, Briales A, Machuca J, Lossa M, Fernandez-Cuenca F et al (2013) Contribution of OqxAB efflux pumps to quinolone resistance in extended-spectrum-ß-lactamase-producing Klebsiella pneumoniae. Antimicrob Chemother 68:68–73CrossRefGoogle Scholar
  77. 77.
    Wong MH, Chan EW, Chen S (2015) Evolution and dissemination of OqxAB-like efflux pumps, an emerging quinolone resistance determinant among members of Enterobacteriaceae. Antimicrob Agents Chemother 59(6):3290–3297PubMedPubMedCentralCrossRefGoogle Scholar
  78. 78.
    Veleba M, Higgins PG, Gonzalez G, Seifert H, Schneidersa T (2012) Characterization of RarA, a novel AraC family multidrug resistance regulator in Klebsiella pneumoniae. Antimicrob Agents Chemother 56(8):4450–4458PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Bialek-Davenet S, Lavigne JP, Guyot K, Mayer N, Tournebize R, Brisse S et al (2015) Differential contribution of AcrAB and OqxAB efflux pumps to multidrug resistance and virulence in Klebsiella pneumoniae. J Antimicrob Chemother 70(1):81–88PubMedCrossRefGoogle Scholar
  80. 80.
    Drlica K (2003) The mutant selection window and antimicrobial resistance. J Antimicrob Chemother 52:11–17PubMedCrossRefGoogle Scholar
  81. 81.
    Zhao X, Drlica K (2001) Restricting the selection of antibiotic-resistant mutants: a general strategy derived from fluoroquinolone studies. Clin Infect Dis 33(3):S147–S156PubMedCrossRefGoogle Scholar
  82. 82.
    Rodríguez-Martínez JM, Velasco C, García I, Cano ME, Martínez-Martínez L, Pascual A (2007) Mutant prevention concentrations of fluoroquinolones for Enterobacteriaceae expressing the plasmid-carried quinolone resistance determinant qnrA1. Antimicrob Agents Chemother 51(6):2236–2239PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Machuca J, Briales A, Díaz-de-Alba P, Martínez-Martínez L, Pascual Á, Rodríguez-Martínez JM (2015) Effect of the efflux pump QepA2 combined with chromosomally mediated mechanisms on quinolone resistance and bacterial fitness in Escherichia coli. J Antimicrob Chemother 70(9):2524–2527PubMedCrossRefGoogle Scholar
  84. 84.
    Guillard T, Cambau E, Chau F, Massias L, de Champs C, Fantin B (2013) Ciprofloxacin treatment failure in a murine model of pyelonephritis due to an AAC(6′)-Ib-cr-producing Escherichia coli strain susceptible to ciprofloxacin in vitro. Antimicrob Agent Chemother 57(12):5830–5835CrossRefGoogle Scholar
  85. 85.
    Machuca J, Ortiz M, Recacha E, Díaz-De-Alba P, Docobo-Perez F, Rodríguez-Martínez JM et al (2016) Impact of AAC(6′)-Ib-cr in combination with chromosomal-mediated mechanisms on clinical quinolone resistance in Escherichia coli. J Antimicrob Chemother 71(11):3066–3071PubMedCrossRefGoogle Scholar
  86. 86.
    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(9):e24552PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Vinué L, Corcoran MA, Hooper DC, Jacoby GA (2016) Mutations that enhance the ciprofloxacin resistance of Escherichia coli with qnrA1. Antimicrob Agents Chemother 60(3):1537–1545PubMedCentralCrossRefGoogle Scholar
  88. 88.
    Iabadene H, Messai Y, Ammari H, Ramdani-Bouguessa N, Lounes S, Bakour R et al (2008) Dissemination of ESBL and Qnr determinants in Enterobacter cloacae in Algeria. J Antimicrob Chemother 62:133–136PubMedCrossRefGoogle Scholar
  89. 89.
    Meradi L, Djahoudi A, Abdi A, Bouchakour M, Perrier Gros Claude JD, Timinouni M (2011) Qnr and aac(6′)-Ib-cr types quinolone resistance among Enterobacteriaceae isolated in Annaba, Algeria. Pathol Biol 59(4):e73–e78PubMedCrossRefGoogle Scholar
  90. 90.
    Agabou A, Lezzar N, Ouchenane Z, Khemissi S, Satta D, Sotto A et al (2015) Clonal relationship between human and avian ciprofloxacin-resistant Escherichia coli isolates in North-Eastern Algeria. Eur J Clin Microbiol Infect Dis 35(2):227–234PubMedCrossRefGoogle Scholar
  91. 91.
    Yanat B, Machuca J, Díaz-De-Alba P, Mezhoud H, Touati A, Pascual Á et al (2016) Characterization of plasmid-mediated quinolone resistance determinants in high-level quinolone-resistant Enterobacteriaceae isolates from the community: First report of qnrD gene in Algeria. Microb Drug Resist DOI:  10.1089/mdr.2016.0031 Google Scholar
  92. 92.
    Anssour L, Messai Y, Estepa V, Torres C, Bakour R (2016) Characteristics of ciprofloxacin-resistant Enterobacteriaceae isolates recovered from wastewater of an Algerian hospital. J Infect Dev Ctries 10(7):728–734PubMedCrossRefGoogle Scholar
  93. 93.
    Literacka E, Bedenic B, Baraniak A, Fiett J, Tonkic M, Jajic-Bencic I et al (2009) bla CTX-M genes in Escherichia coli strains from Croatian hospitals are Located in new (bla CTX-M-3a) and widely spread (bla CTX-M-3a and bla CTX-M-15) genetic structures. Antimicrob Agents Chemother 4(53):1630–1635CrossRefGoogle Scholar
  94. 94.
    Ishida Y, Ahmed AM, Mahfouz NB, Kimura T, El-Khodery SA, Moawad AA et al (2010) Molecular analysis of antimicrobial resistance in Gram-negative bacteria isolated from fish farms in Egypt. J Vet Med Sci 72(6):727–734PubMedCrossRefGoogle Scholar
  95. 95.
    Hassan WM, Hashim A, Domany RAA (2012) Plasmid mediated quinolone resistance determinants qnr, aac(6′)-Ib-cr, and qepA in ESBL producing Escherichia coli clinical isolates from Egypt. Indian J Med Microbiol 30(4):442–447PubMedCrossRefGoogle Scholar
  96. 96.
    Abd El-Aziz NK, Gharib AA (2015) Coexistence of plasmid-mediated quinolone resistance determinants and AmpC-Beta-Lactamases in Escherichia coli strains in Egypt. Cell Mol Biol 61(5):29–35PubMedGoogle Scholar
  97. 97.
    Poirel L, Leviandier C, Nordmann P (2006) Prevalence and genetic analysis of plasmid-mediated quinolone resistance determinants QnrA and QnrS in Enterobacteriaceae isolates from a French University Hospital. Antimicrob Agent Chemother 50(12):3992–3997CrossRefGoogle Scholar
  98. 98.
    Cambau E, Lascols C, Sougakoff W, Bebear C, Bonnet R, Cavallo JD et al (2006) Occurrence of qnrA-positive clinical isolates in French teaching hospitals during 2002–2005. Clin Microbiol Infect 12:1013–1020PubMedCrossRefGoogle Scholar
  99. 99.
    Guillard T, Cholley P, Limelette A, Hocquet D, Matton L, Guyeux C et al (2015) Fluoroquinolone resistance mechanisms and population structure of Enterobacter cloacae non-susceptible to ertapenem in North-Eastern France. Front Microbiol 6:1186PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Mavroidi A, Miriagou V, Liakopoulos A, Tzelepi E, Stefos A, Dalekos GN et al (2012) Ciprofloxacin-resistant Escherichia coli in Central Greece: mechanisms of resistance and molecular identification. BMC Infect Dis 12:371–376PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Chmelnitsky I, Hermesh O, Navon-Venezia S, Strahilevitz J, Carmeli Y (2009) Detection of aac(6′)-Ib-cr in KPC-producing Klebsiella pneumoniae isolates from Tel Aviv, Israel. J Antimicrob Chemother 64:718–722PubMedCrossRefGoogle Scholar
  102. 102.
    Musumeci R, Rausa M, Giovannoni R, Cialdella A, Bramati S, Sibra B et al (2012) Prevalence of plasmid-mediated quinolone resistance genes in uropathogenic Escherichia coli isolated in a teaching hospital of northern Italy. Microb Drug Resist 18(1):33–41PubMedCrossRefGoogle Scholar
  103. 103.
    Donati V, Feltrin F, Hendriksen RS, Aaby Svendsen C, Cordaro G, Garcia-Fernandez A (2014) Extended-spectrum-beta-lactamases, AmpC beta-lactamases and plasmid mediated quinolone resistance in Klebsiella spp. from companion animals in Italy. PloS One 9(3):e90564PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Bouchakour M, Zerouali K, Perrier Gros Claude JD, Amarouch H, El Mdaghri N, Courvalin P et al (2010) Plasmid-mediated quinolone resistance in expanded spectrum beta-lactamase producing Enterobacteriaceae in Morocco. J Infect Dev Ctries 4(12):799–803Google Scholar
  105. 105.
    Barguigua A, Ouair H, El Otmani F, Saile R, El Mdaghri N, El Azhari M et al (2015) Fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae in community setting in Casablanca. Infect Dis 47(1):27–32CrossRefGoogle Scholar
  106. 106.
    Barguigua A, Zerouali K, Katfy K, El Otmani F, Timinouni M, Elmdaghri N (2015) Occurrence of OXA-48 and NDM-1 carbapenemase-producing Klebsiella pneumoniae in a Moroccan university hospital in Casablanca. Morocco Infect Genet Evol 31:142–148PubMedCrossRefGoogle Scholar
  107. 107.
    Tayh G, Ben Sallem R, Ben Yahia H, Gharsa H, Klib N, Boudabous A et al (2016) First report of extended-spectrum β-lactamases among clinical isolates of Klebsiella pneumoniae in Gaza strip, Palestine. Microb Drug Resist DOI:  10.1089/mdr.2016.0089 PubMedGoogle Scholar
  108. 108.
    Cano ME, Rodrìguez-Martìnez JM, Aguero J, Pascual A, Calvo J, Garcìa-Lobo JM et al (2009) Detection of plasmid-mediated quinolone resistance genes in clinical isolates of Enterobacter spp. in Spain. J Clin Microbiol 47(7):2033–2039PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Briales A, Rodríguez-Martínez JM, Velasco C, de Alba PD, Rodríguez-Baño J, Martínez-Martínez L et al (2012) Prevalence of plasmid-mediated quinolone resistance determinants qnr and aac(6′)-Ib-cr in Escherichia coli and Klebsiella pneumoniae producing extended-spectrum β-lactamases in Spain. Int J Antimicrob Agents 39(5):431–434PubMedCrossRefGoogle Scholar
  110. 110.
    Pérez-Moreno MO, Picó-Plana E, De Toro M, Grande-Armas J, Quiles-Fortuny V, Pons MJ et al (2013) β-Lactamases, transferable quinolone resistance determinants, and class 1 integron-mediated antimicrobial resistance in human clinical Salmonella enterica isolates of non-Typhimurium serotypes. Int J Med Microbiol 303(1):25–31PubMedCrossRefGoogle Scholar
  111. 111.
    Machuca J, Agüero J, Miró E, Conejo MD, Oteo J, Bou G et al (2016) Prevalence of quinolone resistance mechanisms in Enterobacteriaceae producing acquired AmpC β-lactamases and/or carbapenemases in Spain. Enferm Infecc Microbiol Clin DOI:  10.1016/j.eimc.2016.05.006 Google Scholar
  112. 112.
    Dahmen S, Poirel L, Mansour W, Bouallegue O, Nordmann P (2010) Prevalence of plasmid-mediated quinolone resistance determinants in Enterobacteriaceae from Tunisia. Clin Microbiol Infect 16(7):1019–1021PubMedCrossRefGoogle Scholar
  113. 113.
    Arpin C, Thabet L, Yassine H, Messadi AA, Boukadida J, Dubois V et al (2012) Evolution of an incompatibility group IncA/C plasmid harboring blaCMY-16 and qnrA6 genes and its transfer through three clones of Providencia stuartii during a two-year outbreak in a Tunisian burn unit. Antimicrob Agent Chemother 56(3):1342–1349CrossRefGoogle Scholar
  114. 114.
    Mnif B, Ktari S, Chaari A, Medhioub F, Rhimi F, Bouaziz M et al (2013) Nosocomial dissemination of Providencia stuartii isolates carrying bla OXA-48, bla PER-1, bla CMY-4 and qnrA6 in a Tunisian hospital. J Antimicrob Chemother 68:329–332PubMedCrossRefGoogle Scholar
  115. 115.
    Mahrouki S, Perilli M, Bourouis A, Chihi H, Ferjani M, Ben Moussa M et al (2013) Prevalence of quinolone resistance determinant qnrA6 among broad- and extended-spectrum beta-lactam-resistant Proteus mirabilis and Morganella morganii clinical isolates with sul1-type class 1 integron association in a Tunisian Hospital. Scand J Infect Dis 45(8):600–605PubMedCrossRefGoogle Scholar
  116. 116.
    Avsaroglu MD, Helmuth R, Junker E, Hertwig S, Schroeter A, Akcelik M et al (2007) Plasmid-mediated quinolone resistance conferred by qnrS1 in Salmonella enterica serovar Virchow isolated from Turkish food of avian origin. J Antimicrob Chemother 60:1146–1150PubMedCrossRefGoogle Scholar
  117. 117.
    Nazik H, Öngen B, Mete B, Aydin S, Yemisen M, Kelesoglu FM et al (2011) Coexistence of bla OXA-48 and aac(6′)-Ib-cr genes in Klebsiella pneumoniae isolates from Istanbul, Turkey. J Int Med Res 39:1932–1940PubMedCrossRefGoogle Scholar
  118. 118.
    Nazik H, Ongen B, Kuvat N (2008) Investigation of plasmid-mediated quinolone resistance among isolates obtained in a Turkish intensive care unit. Jpn J Infect Dis 61:310–312PubMedGoogle Scholar
  119. 119.
    Pelrano G, Van der Bi AK, Freeman JL, Poirel L, Nordmann P, Costello M et al (2014) Characteristics of Escherichia coli sequence type 131 isolates that produce extended-spectrum-lactamases: global distribution of the H30-Rx sublineage. Antimicrob Agent Chemother 58(73):3762–3767CrossRefGoogle Scholar
  120. 120.
    Loncaric I, Beiglböck C, Febler AT, Posautz A, Rosengarten R, Walzer C et al (2016) Characterization of ESBL- and AmpC-producing and fluoroquinolone-resistant Enterobacteriaceae isolated from Mouflons (Ovis orientalis musimon) in Austria and Germany. PLoS One 11(5):e0155786PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Cattoir V, Nordmann P, Silva-Sanchez J, Espinal P, Poirel L (2008) ISEcp1-mediated transposition of qnrB-Like gene in Escherichia coli. Antimicrob Agents Chemother 52(8):2929–2932PubMedPubMedCentralCrossRefGoogle Scholar
  122. 122.
    Kehrenberg C, Hopkins KL, Threlfall EJ, Schwarz S (2007) Complete nucleotide sequence of a small qnrS1-carrying plasmid from Salmonella enterica subsp. enterica Typhimurium DT193. J Antimicrob Chemother 60:903–905PubMedCrossRefGoogle Scholar
  123. 123.
    Ruiz E, Saénz Y, Zarazaga M, Rocha-Gracia R, Martìnez-Martìnez L, Arlet G et al (2012) qnr, aac(6′)-Ib-cr and qepA genes in Escherichia coli and Klebsiella spp.: genetic environments and plasmid and chromosomal location. J Antimicrob Chemother 67:886–897PubMedCrossRefGoogle Scholar
  124. 124.
    Deng YT, Zeng ZL, Tian W, Yang T, Liu JH (2013) Prevalence and characteristics of rmtB and qepA in Escherichia coli isolated from diseased animals in China. Front Microbiol 4:198PubMedPubMedCentralGoogle Scholar
  125. 125.
    Onuk EE, Tanrıverdi Çaycı Y, Çoban AY, Çiftci A, Balta F, Didinen BI et al (2015) Detection of the first qnrS gene positivity in aquatic Aeromonas spp. isolates in Turkey. Mikrobiyol Bul 49(1):114–123PubMedCrossRefGoogle Scholar
  126. 126.
    Yang H, Hu L, Liu Y, Ye Y, Li J (2016) Detection of the plasmid-mediated quinolone resistance determinants in clinical isolates of Acinetobacter baumannii in China. J Chemother 22:1–3CrossRefGoogle Scholar
  127. 127.
    Yang X, Xing B, Liang C, Ye Z, Zhang Y (2015) Prevalence and fluoroquinolone resistance of Pseudomonas aeruginosa in a hospital of South China. Int J Clin Exp Med 8(1):1386–1390PubMedPubMedCentralGoogle Scholar
  128. 128.
    Filippa N, Carricajo A, Grattard F, Fascia P, El Sayed F, Defilippis JP et al (2013) Outbreak of multidrug-resistant Klebsiella pneumoniae carrying qnrB1 and bla CTX-M15 in a French intensive care unit. Ann Intensive Care 3(1):18PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Ferjani S, Saidani M, Quentin C, Slim Amine F, Boutiba Ben Boubaker I, Dubois V (2014) Prevalence and characterization of uropathogenic Escherichia coli harboring plasmid-mediated quinolone resistance in a Tunisian university hospital. Diagn Microbiol Infect Dis 79(2):247CrossRefGoogle Scholar
  130. 130.
    Longhi C, Conte MP, Marazzato M, Iebba V, Totino V, Santangelo FC et al (2012) Plasmid-mediated fluoroquinolone resistance determinants in Escherichia coli from community uncomplicated urinary tract infection in an area of high prevalence of quinolone resistance. Eur J Clin Microbiol Infect Dis 31(8):1917–1921PubMedCrossRefGoogle Scholar
  131. 131.
    Dotto G, Giacomelli M, Grilli G, Ferrazzi V, Carattoli A, Fortini D et al (2014) High prevalence of oqxAB in Escherichia coli isolates from domestic and wild lagomorphs in Italy. Microb Drug Resist 20(2):118–123PubMedCrossRefGoogle Scholar
  132. 132.
    Guillard T, de Jong A, Limelette A, Lebreil AL, Madoux J, de Champs C et al (2016) Characterization of quinolone resistance mechanisms in Enterobacteriaceae recovered from diseased companion animals in Europe. Vet Microbiol 194:23–29PubMedCrossRefGoogle Scholar
  133. 133.
    Yousfi M, Mairi A, Touati A, Hassissene L, Brasme L, Guillard T et al (2016) Extended spectrum β-lactamase and plasmid mediated quinolone resistance in Escherichia coli fecal isolates from healthy companion animals in Algeria. J Infect Chemother 22(7):431–435PubMedCrossRefGoogle Scholar
  134. 134.
    Ghodousi A, Bonura C, Di Noto AM, Mammina C (2015) Extended-spectrum ß-Lactamase, AmpC-producing, and fluoroquinolone-resistant Escherichia coli in retail broiler chicken meat, Italy. Foodborne Pathog Dis 12(7):619–625PubMedCrossRefGoogle Scholar
  135. 135.
    Alouache S, Estepa V, Messai Y, Ruiz E, Torres C, Bakour R (2014) Characterization of ESBLs and associated quinolone resistance in Escherichia coli and Klebsiella pneumoniae isolates from an urban wastewater treatment plant in Algeria. Microb Drug Resist 20:30–38PubMedCrossRefGoogle Scholar
  136. 136.
    Anssour L, Messai Y, Derkaoui M, Alouache S, Estepa V, Somalo S et al (2014) ESBL, plasmidic AmpC, and associated quinolone resistance determinants in coliforms isolated from hospital effluent: first report of qnrB2, qnrB9, qnrB19, and bla CMY-4 in Algeria. J Chemother 26(2):74–79PubMedCrossRefGoogle Scholar
  137. 137.
    Ahmed AM, Shimamoto T (2011) Molecular characterization of antimicrobial resistance in Gram-negative bacteria isolated from bovine mastitis in Egypt. Microbiol Immunol 55(5):318–327PubMedCrossRefGoogle Scholar
  138. 138.
    Cubero M, Calatayud L, Tubau F, Ayats J, Peña C, Martín R et al (2013) Clonal spread of Klebsiella pneumoniae producing OXA-1 betalactamase in a Spanish hospital. Int Microbiol 16:227–233PubMedGoogle Scholar
  139. 139.
    Rogers BA, Sidjabat HE, Paterson DL (2011) Escherichia coli O25b-ST131: a pandemic, multiresistant, community-associated strain. J Antimicrob Chemother 66:1–14PubMedCrossRefGoogle Scholar
  140. 140.
    Brahmi S, Dunyach-Rémy C, Touati A, Lavigne JP (2015) CTX-M-15-producing Escherichia coli and the pandemic clone O25b-ST131 isolated from wild fish in Mediterranean Sea. Clin Microbiol Infect 21:e18–e20PubMedCrossRefGoogle Scholar
  141. 141.
    Lunn AD, Fàbrega A, Sánchez-Céspedes J, Vila J (2010) Prevalence of mechanisms decreasing quinolone-susceptibility among Salmonella spp. clinical isolates. Int Microbiol 13:15–20PubMedGoogle Scholar
  142. 142.
    Al-Gallas N, Abbassi MS, Gharbi B, Manai M, Ben Fayala MN, Bichihi R et al (2013) Occurrence of plasmid-mediated quinolone resistance determinants and rmtB gene in Salmonella enterica serovar enteritidis and Typhimurium isolated from food- animal products in Tunisia. Foodborne Pathog Dis 10(9):813–819PubMedCrossRefGoogle Scholar
  143. 143.
    Zhao J, Chen Z, Chen S, Deng Y, Liu Y, Tian W et al (2010) Prevalence and dissemination of oqxAB in Escherichia coli isolates from animals, farmworkers, and the environment. Antimicrob Agents Chemother 54(10):4219–4224PubMedPubMedCentralCrossRefGoogle Scholar
  144. 144.
    Buruk CK, Öztel Ocak H, Bayramoğlu G, Aydın F (2016) Investigation of plasmid-mediated quinolone resistance genes in quinolone-resistant Escherichia coli and Klebsiella spp. isolates from bloodstream infections. Mikrobiyol Bul 50(2):186–195PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Laboratoire d’Ecologie Microbienne, FSNVUniversité de BejaiaBejaiaAlgeria
  2. 2.Department of MicrobiologyUniversity of SevilleSevilleSpain
  3. 3.Spanish Network for the Research in Infectious Diseases (REIPI RD12/0015)Instituto de Salud Carlos IIIMadridSpain

Personalised recommendations