Risk factors for quinolone-resistant Escherichia coli infection: a systematic review and meta-analysis

Dong-Mei Zhu, Qiu-Hong Li, Yan Shen, Qin Zhang, Dong-Mei Zhu, Qiu-Hong Li, Yan Shen, Qin Zhang

Abstract

Background: Antimicrobial resistance to quinolone is rising worldwide, especially in Escherichia coli causing various infections. Although many studies have been conducted to identify the risk factors for quinolone-resistant Escherichia coli (QREC) infection, the results are inconsistent and have not been systematically reported. The aim of the present study is to conduct a systematic review and meta-analysis to evaluate the potential risk factors for QREC infection.

Methods: A systematic search was performed to collect published data in the EMBASE, PubMed, and the Cochrane Library up to April 2019. Risk factors were analyzed using the pooled odds ratio (ORs) with 95% confidence interval (CIs).

Results: Twenty-seven trials involving 67,019 participants were included in the present study. The following risk factors associated with QREC infection were identified: (1) male (OR = 1.41), (2) hepatic cirrhosis (OR = 2.05), (3) diabetes mellitus (OR = 1.62), (4) cardiovascular disease (OR = 1.76), (5) neurogenic bladder (OR = 8.66), (6) renal dysfunction (OR = 2.47), (7) transplantation (OR = 2.37), (8) urinary tract infection (OR = 2.79) and urinary tract abnormality (OR = 1.85), (9) dementia (OR = 5.83), (10) heart failure (OR = 5.63), (11) neurologic disease (OR = 2.80), (12) immunosuppressive drugs (OR = 2.02), (13) urinary catheter (OR = 4.39), (14) nursing home resident (OR = 4.63), (15) prior surgery (OR = 2.54), (16) quinolones (OR = 7.67), (17) other antibiotics (OR = 2.74), (18) hospitalization (OR = 2.06) and (19) nosocomial infection acquisition (OR = 2.35).

Conclusions: QREC infection was associated with nineteen risk factors including prior quinolones use, hospitalization, and several comorbidities. Reducing exposure to these risk factors and modification of antibiotic use are important to prevent quinolone resistance.

Keywords: Escherichia coli; Infection; Meta-analysis; Quinolone; Resistance; Risk factor.

Conflict of interest statement

Competing interestsThe authors declare that they have no competing interests.

© The Author(s). 2020.

Figures

Fig. 1
Fig. 1
PRISMA flow chart of study selection in the meta-analysis
Fig. 2
Fig. 2
Forest plots for the association between exposure to quinolone and QREC infection. QREC, quinolone-resistant Escherichia coli; M-H, Mantel-Haenszel; CI, confidence interval
Fig. 3
Fig. 3
Funnel plot of comparison for immunosuppressive drugs uses as the potential risk factor. Each small circle represents an independent study for the indicated association. The funnel plot appears asymmetric. OR, odds ratio; SE, standard error

References

    1. Sharma PC, Jain A, Jain S, Pahwa R, Yar MS. Ciprofloxacin. Review on developments in synthetic, analytical, and medicinal aspects. J Enzyme Inhib Med Chem. 2010;25(4):577–589. doi: 10.3109/14756360903373350.
    1. Garau J, Xercavins M, Rodriguez-Carballeira M, Gomez-Vera JR, Coll I, Vidal D, Llovet T, Ruiz-Bremon A. Emergence and dissemination of quinolone-resistant Escherichia coli in the community. Antimicrob Agents Chemother. 1999;43(11):2736–2741. doi: 10.1128/AAC.43.11.2736.
    1. Huotari K, Tarkka E, Valtonen V, Kolho E. Incidence and risk factors for nosocomial infections caused by fluoroquinolone-resistant Escherichia coli. Eur J Clin Microbiol Infect Dis. 2003;22(8):492–495. doi: 10.1007/s10096-003-0975-6.
    1. Guillemot D. Antibiotic use in humans and bacterial resistance. Curr Opin Microbiol. 1999;2(5):494–498. doi: 10.1016/S1369-5274(99)00006-5.
    1. Wenzel RP. The antibiotic pipeline--challenges, costs, and values. N Engl J Med. 2004;351(6):523–526. doi: 10.1056/NEJMp048093.
    1. Lee CR, Cho IH, Jeong BC, Lee SH. Strategies to minimize antibiotic resistance. Int J Environ Res Public Health. 2013;10(9):4274–4305. doi: 10.3390/ijerph10094274.
    1. Touchon M, Hoede C, Tenaillon O, Barbe V, Baeriswyl S, Bidet P, Bingen E, Bonacorsi S, Bouchier C, Bouvet O, et al. Organised genome dynamics in the Escherichia coli species results in highly diverse adaptive paths. PLoS Genet. 2009;5(1):e1000344. doi: 10.1371/journal.pgen.1000344.
    1. Hatahet F, Blazyk JL, Martineau E, Mandela E, Zhao Y, Campbell RE, Beckwith J, Boyd D. Altered Escherichia coli membrane protein assembly machinery allows proper membrane assembly of eukaryotic protein vitamin K epoxide reductase. Proc Natl Acad Sci U S A. 2015;112(49):15184–15189. doi: 10.1073/pnas.1521260112.
    1. Huttner A, Hatz C, van den Dobbelsteen G, Abbanat D, Hornacek A, Frölich R, Dreyer AM, Martin P, Davies T, Fae K, et al. Safety, immunogenicity, and preliminary clinical efficacy of a vaccine against extraintestinal pathogenic Escherichia coli in women with a history of recurrent urinary tract infection: a randomised, single-blind, placebo-controlled phase 1b trial. Lancet Infect Dis. 2017;17(5):528–537. doi: 10.1016/S1473-3099(17)30108-1.
    1. Manges AR, Johnson JR. Food-borne origins of Escherichia coli causing extraintestinal infections. Clin Infect Dis. 2012;55(5):712–719. doi: 10.1093/cid/cis502.
    1. Recacha E, Machuca J, Díaz-Díaz S, García-Duque A, Ramos-Guelfo M, Docobo-Pérez F, Blázquez J, Pascual A, Rodríguez-Martínez JM. Suppression of the SOS response modifies spatiotemporal evolution, post-antibiotic effect, bacterial fitness and biofilm formation in quinolone-resistant Escherichia coli. J Antimicrob Chemother. 2019;74(1):66–73.
    1. Xu X, Cui S, Zhang F, Luo Y, Gu Y, Yang B, Li F, Chen Q, Zhou G, Wang Y, et al. Prevalence and characterization of cefotaxime and ciprofloxacin co-resistant escherichia coli isolates in retail chicken carcasses and ground pork, China. Microb Drug Resist. 2014;20(1):73–81. doi: 10.1089/mdr.2012.0224.
    1. Kratochwill L, Powers M, McGraw MA, King L, O'Neill JM, Venkat A. Factors associated with ciprofloxacin-resistant Escherichia coli urinary tract infections in discharged ED patients. Am J Emerg Med. 2015;33(10):1473–1476. doi: 10.1016/j.ajem.2015.07.047.
    1. Pena C, Albareda JM, Pallares R, Pujol M, Tubau F, Ariza J. Relationship between quinolone use and emergence of ciprofloxacin- resistant Escherichia coli in bloodstream infections. Antimicrob Agents Chemother. 1995;39(2):520–524. doi: 10.1128/AAC.39.2.520.
    1. Stang A. Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol. 2010;25(9):603–605. doi: 10.1007/s10654-010-9491-z.
    1. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. BMJ (Clinical research ed) 2003;327(7414):557–560. doi: 10.1136/bmj.327.7414.557.
    1. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med. 2002;21(11):1539–1558. doi: 10.1002/sim.1186.
    1. Cheong HJ, Yoo CW, Sohn JW, Kim WJ, Kim MJ, Park SC. Bacteremia due to quinolone-resistant Escherichia coli in a teaching hospital in South Korea. Clin Infect Dis. 2001;33(1):48–53. doi: 10.1086/320873.
    1. Sotto A, De Boever CM, Fabbro-Peray P, Gouby A, Sirot D, Jourdan J. Risk factors for antibiotic-resistant Escherichia coli isolated from hospitalized patients with urinary tract infections: a prospective study. J Clin Microbiol. 2001;39(2):438–444. doi: 10.1128/JCM.39.2.438-444.2001.
    1. Eom JS, Hwang BY, Sohn JW, Kim WJ, Kim MJ, Park SC, Cheong HJ. Clinical and molecular epidemiology of quinolone-resistant Escherichia coli isolated from urinary tract infection. Microb Drug Resist. 2002;8(3):227–234. doi: 10.1089/107662902760326959.
    1. Lautenbach E, Fishman NO, Bilker WB, Castiglioni A, Metlay JP, Edelstein PH, Strom BL. Risk factors for fluoroquinolone resistance in nosocomial Escherichia coli and Klebsiella pneumoniae infections. Arch Intern Med. 2002;162(21):2469–2477. doi: 10.1001/archinte.162.21.2469.
    1. Killgore KM, March KL, Guglielmo BJ. Risk factors for community-acquired ciprofloxacin-resistant Escherichia coli urinary tract infection. Ann Pharmacother. 2004;38(7–8):1148–1152. doi: 10.1345/aph.1D622.
    1. Maslow JN, Lee B, Lautenbach E. Fluoroquinolone-resistant Escherichia coli carriage in long-term care facility. Emerg Infect Dis. 2005;11(6):889–894. doi: 10.3201/eid1106.041335.
    1. Colodner R, Kometiani I, Chazan B, Raz R. Risk factors for community-acquired urinary tract infection due to quinolone-resistant E. coli. Infection. 2008;36(1):41–45. doi: 10.1007/s15010-007-7083-y.
    1. Johnson L, Sabel A, Burman WJ, Everhart RM, Rome M, MacKenzie TD, Rozwadowski J, Mehler PS, Price CS. Emergence of Fluoroquinolone resistance in outpatient urinary Escherichia coli isolates. Am J Med. 2008;121(10):876–884. doi: 10.1016/j.amjmed.2008.04.039.
    1. Lin CY, Huang SH, Chen TC, Lu PL, Lin WR, Chen YH. Risk factors of ciprofloxacin resistance in urinary Escherichia coli isolates. J Microbiol Immunol Infect. 2008;41(4):325–331.
    1. Lautenbach E, Metlay JP, Weiner MG, Bilker WB, Tolomeo P, Mao X, Nachamkin I, Fishman NO. Gastrointestinal tract colonization with fluoroquinolone-resistant Escherichia coli in hospitalized patients: changes over time in risk factors for resistance. Infect Control Hosp Epidemiol. 2009;30(1):18–24. doi: 10.1086/592703.
    1. Rooney PJ, O'Leary MC, Loughrey AC, McCalmont M, Smyth B, Donaghy P, Badri M, Woodford N, Karisik E, Livermore DM. Nursing homes as a reservoir of extended-spectrum beta-lactamase (ESBL)-producing ciprofloxacin-resistant Escherichia coli. J Antimicrob Chemother. 2009;64(3):635–641. doi: 10.1093/jac/dkp220.
    1. Yagci D, Yoruk F, Azap A, Memikoglu O. Prevalence and risk factors for selection of quinolone-resistant escherichia coli strains in fecal flora of patients receiving quinolone therapy. Antimicrob Agents Chemother. 2009;53(3):1287–1289. doi: 10.1128/AAC.01228-08.
    1. Jang WH, Yoo DH, Park SW. Prevalence of and risk factors for levofloxacin-Resistant E. coli isolated from outpatients with urinary tract infection. Korean J Urol. 2011;52(8):554–559. doi: 10.4111/kju.2011.52.8.554.
    1. van der Starre WE, van Nieuwkoop C, Paltansing S, van't Wout JW, Groeneveld GH, Becker MJ, Koster T, Wattel-Louis GH, Delfos NM, Ablij HC, et al. Risk factors for fluoroquinolone-resistant Escherichia coli in adults with community-onset febrile urinary tract infection. J Antimicrob Chemother. 2011;66(3):650–656. doi: 10.1093/jac/dkq465.
    1. Smithson A, Chico C, Ramos J, Netto C, Sanchez M, Ruiz J, Porron R, Bastida MT. Prevalence and risk factors for quinolone resistance among Escherichia coli strains isolated from males with community febrile urinary tract infection. Eur J Clin Microbiol Infect Dis. 2012;31(4):423–430. doi: 10.1007/s10096-011-1322-y.
    1. Bailey AM, Weant KA, Baker SN. Prevalence and risk factor analysis of resistant Escherichia coli urinary tract infections in the emergency department. Pharm Pract. 2013;11(2):96–101. doi: 10.4321/S1886-36552013000200006.
    1. Han JH, Bilker WB, Nachamkin I, Tolomeo P, Mao X, Fishman NO, Lautenbach E. Impact of antibiotic use during hospitalization on the development of gastrointestinal colonization with Escherichia coli with reduced fluoroquinolone susceptibility. Infect Control Hosp Epidemiol. 2013;34(10):1070–1076. doi: 10.1086/673155.
    1. Bedoin M, Cazorla C, Lucht F, Berthelot P, Boyer M, Carricajo A, Guérin T, Viallon A. Risk factors for quinolone-resistance in women presenting with Escherichia coli acute pyelonephritis. Med Mal Infect. 2014;44(5):206–216. doi: 10.1016/j.medmal.2014.02.003.
    1. Kim J, Kang CI, Joo EJ, Ha YE, Cho SY, Gwak GY, Chung DR, Peck KR, Song JH. Risk factor of community-onset spontaneous bacterial peritonitis caused by fluoroquinolone-resistant Escherichia coli in patients with cirrhosis. Liver Int. 2014;34(5):695–699. doi: 10.1111/liv.12374.
    1. Park KH, Oh WS, Kim ES, Park SW, Hur JA, Kim YK, Moon C, Lee JH, Lee CS, Kim BN. Factors associated with ciprofloxacin- and cefotaxime-resistant Escherichia coli in women with acute pyelonephritis in the emergency department. Int J Infect Dis. 2014;23:8–13. doi: 10.1016/j.ijid.2013.12.021.
    1. Jadoon RJ, Jalal-ud-din M, Khan SA. E. coli resistance to ciprofloxacin and common associated factors. J Coll Physicians Surg Pak. 2015;25(11):824–827.
    1. Saade EA, Suwantarat N, Zabarsky TF, Wilson B, Donskey CJ. Fluoroquinolone-resistant Escherichia coli infections after Transrectal biopsy of the prostate in the veterans affairs healthcare system. Pathog Immun. 2016;1(2):243–257. doi: 10.20411/pai.v1i2.123.
    1. Mulder M, Kiefte-de Jong JC, Goessens WHF, Visser H, Hofman A, Stricker BH, Verbon A. Risk factors for resistance to ciprofloxacin in community-acquired urinary tract infections due to Escherichia coli in an elderly population. J Antimicrob Chemother. 2017;72(1):281–289. doi: 10.1093/jac/dkw399.
    1. Yoshida H, Kojima T, Yamagishi J, Nakamura S. Quinolone-resistant mutations of the gyrA gene of Escherichia coli. Mol Gen Genet. 1988;211(1):1–7. doi: 10.1007/BF00338386.

Source: PubMed

3
購読する