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Plasmid-mediated quinolone resistance (PMQR) among Enterobacteriales in Latin America: a systematic review

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The plasmid-mediated quinolone resistance (PMQR) genes have changed the resistance pattern to quinolones, especially among Enterobacteriales. The dissemination of these genes in Latin American countries, where the prescription of fluoroquinolones is high, has been described in several studies; however, no review of the impact of PMQR in this continent has been conducted. This review summarized current knowledge about the circulation of PMQR among Enterobacteriales in Latin American. After the search and selection, 61 articles were included in the study. Most of studies reported PMQR genes among Enterobacteriales from human (47/61, 77%) and animal (18/61, 29.5%) samples, recovered mainly in Brazil (23/61, 37.7%), Mexico (11/61, 18%), and Uruguay (7/61, 11.5%). Nine different PMQR genes (qnrA, qnrB, qnrS, qnrD, qnrE, aac-(6′)-Ib-cr, oqxA, oqxB, and qepA) were found in Latin America, with aac (6′)-Ib-cr (37/61, 60.6%) and qnrB (26/61, 42.6%) being the most frequently reported. Escherichia coli (40/61, 65.6%) was the species most frequently reported to carry a PMQR gene, followed by Klebsiella pneumoniae (24/61, 39.3%), Enterobacter cloacae (15/61, 24.6%), and Salmonella spp. (14/61, 22.9%). Thus, this review provides important information which might help in designing measures to control the spread of quinolone resistance determinants on this continent.

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References

  1. Lima WG, Alves MC, Cruz WS, Paiva MC (2018) Chromosomally encoded and plasmid-mediated polymyxins resistance in Acinetobacter baumannii: a huge public health threat. Eur J Clin Microbiol Infect Dis 37:1009–1019. https://doi.org/10.1007/s10096-018-3223-9

    Article  CAS  PubMed  Google Scholar 

  2. O’ Neil J (2014) Review on antibiotic resisitance. Antimicrobial resistance : tackling a crisis for the health and wealth of nations. Health Wealth Nations. https://amr-review.org/sites/default/files/160518_Finalpaper_withcover.pdf. Accessed 5 Mar 2018

  3. Loureiro RJ, Roque F, Teixeira Rodrigues A et al (2016) O uso de antibióticos e as resistências bacterianas: breves notas sobre a sua evolução. Rev Port Saúde Pública 34:77–84. https://doi.org/10.1016/J.RPSP.2015.11.003

    Article  Google Scholar 

  4. Tadesse BT, Ashley EA, Ongarello S et al (2017) Antimicrobial resistance in Africa: a systematic review. BMC Infect Dis 17:616. https://doi.org/10.1186/s12879-017-2713-1

    Article  PubMed  PubMed Central  Google Scholar 

  5. Kakkar M, Chatterjee P, Chauhan AS et al (2018) Antimicrobial resistance in South East Asia: time to ask the right questions. Glob Health Action 11:1483637. https://doi.org/10.1080/16549716.2018.1483637

    Article  PubMed  PubMed Central  Google Scholar 

  6. Valenzuela MT, de Quadros C (2009) Antibiotic resistance in Latin America: a cause for alarm. Vaccine 27:C25–C28. https://doi.org/10.1016/j.vaccine.2009.06.005

    Article  PubMed  Google Scholar 

  7. Wirtz VJ, Dreser A, Gonzales R (2010) Trends in antibiotic utilization in eight Latin American countries, 1997-2007. Rev Panam Salud Publica 27:219–225

    Article  PubMed  Google Scholar 

  8. Leski TA, Taitt CR, Bangura U et al (2016) High prevalence of multidrug resistant Enterobacteriaceae isolated from outpatient urine samples but not the hospital environment in Bo. Sierra Leone. BMC Infect Dis 16:167. https://doi.org/10.1186/s12879-016-1495-1

    Article  CAS  PubMed  Google Scholar 

  9. Vega S, Dowzicky MJ (2017) Antimicrobial susceptibility among Gram-positive and Gram-negative organisms collected from the Latin American region between 2004 and 2015 as part of the Tigecycline Evaluation and Surveillance Trial. Ann Clin Microbiol Antimicrob 16:50. https://doi.org/10.1186/s12941-017-0222-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Saavedra SY, Diaz L, Wiesner M et al (2017) Genomic and molecular characterization of clinical isolates of Enterobacteriaceae harboring mcr-1 in Colombia, 2002 to 2016. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.00841-17

    Article  PubMed  PubMed Central  Google Scholar 

  11. Delgado-Valverde M, Sojo-Dorado J, Pascual A, Rodríguez-Baño J (2013) Clinical management of infections caused by multidrug-resistant Enterobacteriaceae. Ther Adv Infect Dis 1:49–69. https://doi.org/10.1177/2049936113476284

    Article  PubMed  PubMed Central  Google Scholar 

  12. Paterson DL (2006) Resistance in gram-negative bacteria: Enterobacteriaceae. Am J Infect Control 34:S20–S28. https://doi.org/10.1016/j.ajic.2006.05.238(discussion S64–S73)

    Article  PubMed  Google Scholar 

  13. Foxman B (2014) Urinary tract infection syndromes: occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect Dis Clin N Am 28:1–13. https://doi.org/10.1016/j.idc.2013.09.003

    Article  Google Scholar 

  14. Foxman B (2014) Urinary Tract Infection Syndromes. Infect Dis Clin North Am 28:1–13. https://doi.org/10.1016/j.idc.2013.09.003

    Article  PubMed  Google Scholar 

  15. Cortes-Penfield NW, Trautner BW, Jump RLP (2017) Urinary tract infection and asymptomatic bacteriuria in older adults. Infect Dis Clin North Am 31:673–688. https://doi.org/10.1016/j.idc.2017.07.002

    Article  PubMed  PubMed Central  Google Scholar 

  16. Hooper DC, Jacoby GA (2015) Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci 1354:12–31. https://doi.org/10.1111/nyas.12830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wannmacher L (2004) Uso indiscriminado de antibióticos e resistência microbiana: Uma guerra perdida? Uso Racion Medicam temas selecionados 1:1–5

    Google Scholar 

  18. Falcão JM, Pisco AM, Simões JA et al (2003) Prescrição de antibacterianos em clínica geral: um estudo na rede médicos-sentinela. Rev Port Med Geral e Fam 19:315–329. https://doi.org/10.32385/RPMGF.V19I4.9954

    Article  Google Scholar 

  19. Hernández A, Sánchez MB, Martínez JL (2011) Quinolone resistance: much more than predicted. Front Microbiol 2:22. https://doi.org/10.3389/fmicb.2011.00022

    Article  PubMed  PubMed Central  Google Scholar 

  20. Martínez-Martínez L, Pascual A, Jacoby GA (1998) Quinolone resistance from a transferable plasmid. Lancet 351:797–799. https://doi.org/10.1016/S0140-6736(97)07322-4

    Article  PubMed  Google Scholar 

  21. Ruiz J, Pons MJ, Gomes C (2012) Transferable mechanisms of quinolone resistance. Int J Antimicrob Agents 40:196–203. https://doi.org/10.1016/j.ijantimicag.2012.02.011

    Article  CAS  PubMed  Google Scholar 

  22. Rodríguez-Martínez JM, Machuca J, Cano ME et al (2016) Plasmid-mediated quinolone resistance: two decades on. Drug Resist Updat 29:13–29. https://doi.org/10.1016/j.drup.2016.09.001

    Article  PubMed  Google Scholar 

  23. Vos T, Allen C, Arora M et al (2016) Global, regional, and national incidence, prevalence, and years lived with disability for 310 diseases and injuries, 1990–2015: a systematic analysis for the Global Burden of Disease Study 2015. Lancet 388:1545–1602. https://doi.org/10.1016/S0140-6736(16)31678-6

    Article  Google Scholar 

  24. Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6:e1000100. https://doi.org/10.1371/journal.pmed.1000100

    Article  PubMed  PubMed Central  Google Scholar 

  25. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174

    Article  CAS  PubMed  Google Scholar 

  26. Minarini LAR, Poirel L, Cattoir V et al (2008) Plasmid-mediated quinolone resistance determinants among enterobacterial isolates from outpatients in Brazil. J Antimicrob Chemother 62:474–478. https://doi.org/10.1093/jac/dkn237

    Article  CAS  PubMed  Google Scholar 

  27. González F, Pallecchi L, Rossolini GM, Araque M (2012) Plasmid-mediated quinolone resistance determinant qnrB19 in non-typhoidal Salmonella enterica strains isolated in Venezuela. J Infect Dev Ctries 6:462–464

    Article  PubMed  Google Scholar 

  28. González F, Araque M (2013) Association of transferable quinolone resistance determinant qnrB19 with extended-spectrum β -lactamases in Salmonella Give and Salmonella Heidelberg in Venezuela. Int J Microbiol 2013:628185. https://doi.org/10.1155/2013/628185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. González A, Nieves B (2016) Aminoglycoside and quinolone resistance in strains of Klebsiella pneumonia isolated from two units of intensive care unit of the University of the Andes Hospital, Merida, Venezuela between 2007 and 2009. Medicas UIS 29:21–30. https://doi.org/10.18273/revmed.v29n2-2016002

    Article  Google Scholar 

  30. Poirel L, Cattoir V, Nordmann P (2012) Plasmid-mediated quinolone resistance; interactions between human, animal, and environmental ecologies. Front Microbiol 3:24. https://doi.org/10.3389/fmicb.2012.00024

    Article  PubMed  PubMed Central  Google Scholar 

  31. Carattoli A (2009) Resistance plasmid families in Enterobacteriaceae. Antimicrob Agents Chemother 53:2227–2238. https://doi.org/10.1128/AAC.01707-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Ruiz E, Sáenz Y, Zarazaga M 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 67:886–897. https://doi.org/10.1093/jac/dkr548

    Article  CAS  PubMed  Google Scholar 

  33. Deng Y-T, Zeng Z-L, Tian W et al (2013) Prevalence and characteristics of rmtB and qepA in Escherichia coli isolated from diseased animals in China. Front Microbiol 4:198. https://doi.org/10.3389/fmicb.2013.00198

    Article  PubMed  PubMed Central  Google Scholar 

  34. Cunha MPV, Davies YM, Cerdeira L et al (2017) Complete DNA sequence of an IncM1 plasmid bearing the novel qnrE1 plasmid-mediated quinolone resistance variant and blaCTX-M-8 from Klebsiella pneumoniae sequence type 147. Antimicrob Agents Chemother. https://doi.org/10.1128/AAC.00592-17

    Article  PubMed  PubMed Central  Google Scholar 

  35. Jacoby G, Cattoir V, Hooper D et al (2008) qnr Gene nomenclature. Antimicrob Agents Chemother 52:2297–2299. https://doi.org/10.1128/AAC.00147-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Wang M, Guo Q, Xu X et al (2009) New plasmid-mediated quinolone resistance gene, qnrC, found in a clinical isolate of Proteus mirabilis. Antimicrob Agents Chemother 53:1892–1897. https://doi.org/10.1128/AAC.01400-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Pons MJ, Gomes C, Ruiz J (2013) QnrVC, a new transferable Qnr-like family. Enferm Infecc Microbiol Clin 31:191–192. https://doi.org/10.1016/j.eimc.2012.09.008

    Article  PubMed  Google Scholar 

  38. Stephenson S, Brown P, Wilks M (2009) P75 Emergence of qnr-mediated quinolone resistance among Enterobacteriaceae in Jamaica. Int J Antimicrob Agents 34:S51. https://doi.org/10.1016/S0924-8579(09)70294-8

    Article  Google Scholar 

  39. Robicsek A, Strahilevitz J, Jacoby GA et al (2006) Fluoroquinolone-modifying enzyme: a new adaptation of a common aminoglycoside acetyltransferase. Nat Med 12:83–88. https://doi.org/10.1038/nm1347

    Article  CAS  PubMed  Google Scholar 

  40. Machuca J, Ortiz M, Recacha E 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 71:3066–3071. https://doi.org/10.1093/jac/dkw258

    Article  CAS  PubMed  Google Scholar 

  41. Hansen LH, Johannesen E, Burmolle M et al (2004) Plasmid-encoded multidrug efflux pump conferring resistance to olaquindox in Escherichia coli. Antimicrob Agents Chemother 48:3332–3337. https://doi.org/10.1128/AAC.48.9.3332-3337.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Wong MHY, Chan EWC, Chen S (2015) Evolution and dissemination of OqxAB-Like efflux pumps, an emerging quinolone resistance determinant among members of Enterobacteriaceae. Antimicrob Agents Chemother 59:3290–3297. https://doi.org/10.1128/AAC.00310-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Casas MRT, Camargo CH, Soares FB et al (2016) Presence of plasmid-mediated quinolone resistance determinants and mutations in gyrase and topoisomerase in Salmonella enterica isolates with resistance and reduced susceptibility to ciprofloxacin. Diagn Microbiol Infect Dis 85:85–89. https://doi.org/10.1016/j.diagmicrobio.2016.01.016

    Article  CAS  PubMed  Google Scholar 

  44. Cortés-Cortés G, Lozano-Zarain P, Torres C et al (2016) Detection and molecular characterization of Escherichia coli strains producers of extended-spectrum and CMY-2 type beta-lactamases, isolated from turtles in Mexico. Vector-Borne Zoonotic Dis 16:595–603. https://doi.org/10.1089/vbz.2014.1725

    Article  PubMed  Google Scholar 

  45. Davies YM, Cunha MPV, Oliveira MGX et al (2016) Virulence and antimicrobial resistance of Klebsiella pneumoniae isolated from passerine and psittacine birds. Avian Pathol 45:194–201. https://doi.org/10.1080/03079457.2016.1142066

    Article  CAS  PubMed  Google Scholar 

  46. Albornoz E, Lucero C, Romero G et al (2017) Prevalence of plasmid-mediated quinolone resistance genes in clinical enterobacteria from Argentina. Microb Drug Resist 23:177–187. https://doi.org/10.1089/mdr.2016.0033

    Article  CAS  PubMed  Google Scholar 

  47. Nascimento T, Cantamessa R, Melo L et al (2017) International high-risk clones of Klebsiella pneumoniae KPC-2/CC258 and Escherichia coli CTX-M-15/CC10 in urban lake waters. Sci Total Environ 598:910–915. https://doi.org/10.1016/j.scitotenv.2017.03.207

    Article  CAS  PubMed  Google Scholar 

  48. Saba Villarroel PM, Gutkind GO, Di Conza JA, Radice MA (2017) First survey on antibiotic resistance markers in Enterobacteriaceae in Cochabamba, Bolivia. Rev Argent Microbiol 49:50–54. https://doi.org/10.1016/j.ram.2016.10.002

    Article  PubMed  Google Scholar 

  49. Silva-Sanchez J, Barrios H, Reyna-Flores F et al (2011) Prevalence and characterization of plasmid-mediated quinolone resistance genes in extended-spectrum β-lactamase–producing enterobacteriaceae isolates in Mexico. Microb Drug Resist 17:497–505. https://doi.org/10.1089/mdr.2011.0086

    Article  CAS  PubMed  Google Scholar 

  50. Bartoloni A, Pallecchi L, Riccobono E et al (2013) Relentless increase of resistance to fluoroquinolones and expanded-spectrum cephalosporins in Escherichia coli: 20 years of surveillance in resource-limited settings from Latin America. Clin Microbiol Infect 19:356–361. https://doi.org/10.1111/j.1469-0691.2012.03807.x

    Article  CAS  PubMed  Google Scholar 

  51. Silva-Sánchez J, Cruz-Trujillo E, Barrios H et al (2013) Characterization of plasmid-mediated quinolone resistance (PMQR) genes in extended-spectrum β-lactamase-producing enterobacteriaceae pediatric clinical isolates in Mexico. PLoS ONE 8:e77968. https://doi.org/10.1371/journal.pone.0077968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Rincón G, Radice M, Giovanakis M et al (2014) First report of plasmid-mediated fluoroquinolone efflux pump QepA in Escherichia coli clinical isolate ST68, in South America. Diagn Microbiol Infect Dis 79:70–72. https://doi.org/10.1016/j.diagmicrobio.2014.01.007

    Article  CAS  PubMed  Google Scholar 

  53. Yamane K, Wachino J-I, Suzuki S et al (2007) New plasmid-mediated fluoroquinolone efflux pump, QepA, found in an Escherichia coli clinical isolate. Antimicrob Agents Chemother 51:3354–3360. https://doi.org/10.1128/AAC.00339-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Fu Y, Zhang W, Wang H et al (2013) Specific patterns of gyr A mutations determine the resistance difference to ciprofloxacin and levofloxacin in Klebsiella pneumoniae and Escherichia coli. BMC Infect Dis 13:8. https://doi.org/10.1186/1471-2334-13-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Terlizzi ME, Gribaudo G, Maffei ME (2017) UroPathogenic Escherichia coli (UPEC) infections: virulence factors, bladder responses, antibiotic, and non-antibiotic antimicrobial strategies. Front Microbiol 8:1566. https://doi.org/10.3389/fmicb.2017.01566

    Article  PubMed  PubMed Central  Google Scholar 

  56. Wang X, Wang Y, Zhou Y et al (2018) Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumoniae. Emerg Microbes Infect 7:122. https://doi.org/10.1038/s41426-018-0124-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Benaicha H, Barrijal S, Ezzakkioui F, Elmalki F (2017) Prevalence of PMQR genes in E. coli and Klebsiella spp. isolated from North-West of Morocco. J Glob Antimicrob Resist 10:321–325. https://doi.org/10.1016/j.jgar.2017.05.024

    Article  PubMed  Google Scholar 

  58. Regitano JB, Leal RMP (2010) Comportamento e impacto ambiental de antibióticos usados na produção animal brasileira. Rev Bras Ciência do Solo 34:601–616. https://doi.org/10.1590/S0100-06832010000300002

    Article  CAS  Google Scholar 

  59. Boxall ABA, Johnson P, Smith EJ et al (2006) Uptake of veterinary medicines from soils into plants. J Agric Food Chem 54:2288–2297. https://doi.org/10.1021/jf053041t

    Article  CAS  PubMed  Google Scholar 

  60. Food and Agriculture Organization of the United Nations (2016) Food and agriculture data. http://www.fao.org/faostat/en/#home. Accessed 7 Mar 2019

  61. Liberati A, Altman DG, Tetzlaff J et al (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate healthcare interventions: explanation and elaboration. BMJ 339:b2700. https://doi.org/10.1136/bmj.b2700

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

The authors would like to thank the UFSJ/PPGCF and UFMG/Departamento de Produtos Farmacêuticos for the availability of bibliographic support. V.R.M.O is grateful to Pró Reitoria de Pesquisa e Pós Graduação (PROPE/UFSJ) for the opportunity to undertake scientific initiation. W.G.L. is grateful to Coordenação de Aperfeiçoamento de Pessoal do Nível Superior (CAPES) for a Ph.D. fellowship.

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Vieira, D.C., Lima, W.G. & de Paiva, M.C. Plasmid-mediated quinolone resistance (PMQR) among Enterobacteriales in Latin America: a systematic review. Mol Biol Rep 47, 1471–1483 (2020). https://doi.org/10.1007/s11033-019-05220-9

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