Detection and characterization of tigecycline heteroresistance in E. cloacae: clinical and microbiological findings

References

• Lockhart SR, Abramson MA, Beekmann SE, et al. Antimicrobial resistance among Gram-negative bacilli causing infections in intensive care unit patients in the United States between 1993 and 2004. J Clin Microbiol. 2007;45(10):3352–3359. doi: 10.1128/JCM.01284-07
   PubMed Web of Science ®Google Scholar
• Marimuthu K, Venkatachalam I, Khong WX, et al. Clinical and molecular epidemiology of carbapenem-resistant Enterobacteriaceae among adult inpatients in Singapore. Clin Infect Dis. 2017;64(Suppl_2):S68–S75. doi: 10.1093/cid/cix113
   PubMed Web of Science ®Google Scholar
• Jia X, Dai W, Ma W, et al. Carbapenem-resistant E. cloacae in Southwest China: molecular analysis of resistance and risk factors for infections caused by NDM-1-producers. Front Microbiol. 2018;9:658. doi: 10.3389/fmicb.2018.00658
   PubMed Web of Science ®Google Scholar
• Kadri SS, Adjemian J, Lai YL, et al. Difficult-to-treat resistance in gram-negative Bacteremia at 173 US hospitals: retrospective cohort analysis of prevalence, predictors, and outcome of resistance to all first-line agents. Clin Infect Dis. 2018;67(12):1803–1814.
   PubMed Web of Science ®Google Scholar
• Sader HS, Castanheira M, Flamm RK, et al. Tigecycline activity tested against carbapenem-resistant Enterobacteriaceae from 18 European nations: results from the SENTRY surveillance program (2010–2013). Diagn Microbiol Infect Dis. 2015;83(2):183–186. doi: 10.1016/j.diagmicrobio.2015.06.011
   PubMed Web of Science ®Google Scholar
• Poirel L, Jayol A, Nordmann P. Polymyxins: antibacterial activity, susceptibility testing, and resistance mechanisms encoded by plasmids or chromosomes. Clin Microbiol Rev. 2017;30(2):557–596. doi: 10.1128/CMR.00064-16
   PubMed Web of Science ®Google Scholar
• Livermore DM. Tigecycline: what is it, and where should it be used? J Antimicrob Chemother. 2005;56(4):611–614. doi: 10.1093/jac/dki291
   PubMed Web of Science ®Google Scholar
• Keeney D, Ruzin A, McAleese F, et al. MarA-mediated overexpression of the AcrAB efflux pump results in decreased susceptibility to tigecycline in Escherichia coli. J Antimicrob Chemother. 2008;61(1):46–53. doi: 10.1093/jac/dkm397
   PubMed Web of Science ®Google Scholar
• Zhong X, Xu H, Chen D, et al. First emergence of acrAB and oqxAB mediated tigecycline resistance in clinical isolates of Klebsiella pneumoniae pre-dating the use of tigecycline in a Chinese hospital. PLoS One. 2014;9(12):e115185. doi: 10.1371/journal.pone.0115185
   PubMed Web of Science ®Google Scholar
• Ruzin A, Keeney D, Bradford PA. AdeABC multidrug efflux pump is associated with decreased susceptibility to tigecycline in Acinetobacter calcoaceticus-Acinetobacter baumannii complex. J Antimicrob Chemother. 2007;59(5):1001–1004. doi: 10.1093/jac/dkm058
   PubMed Web of Science ®Google Scholar
• Perez A, Poza M, Aranda J, et al. Effect of transcriptional activators SoxS, RobA, and RamA on expression of multidrug efflux pump AcrAB-TolC in Enterobacter cloacae. Antimicrob Agents Chemother. 2012;56(12):6256–6266. doi: 10.1128/AAC.01085-12
   PubMed Web of Science ®Google Scholar
• Veleba M, De Majumdar S, Hornsey M, et al. Genetic characterization of tigecycline resistance in clinical isolates of Enterobacter cloacae and Enterobacter aerogenes. J Antimicrob Chemother. 2013;68(5):1011–1018. doi: 10.1093/jac/dks530
   PubMed Web of Science ®Google Scholar
• Tumbarello M, Losito AR, Giamarellou H. Optimizing therapy in carbapenem-resistant Enterobacteriaceae infections. Curr Opin Infect Dis. 2018;31(6):566–577. doi: 10.1097/QCO.0000000000000493
   PubMed Web of Science ®Google Scholar
• Sun JD, Huang SF, Yang SS, et al. Impact of carbapenem heteroresistance among clinical isolates of invasive Escherichia coli in Chongqing, southwestern China. Clin Microbiol Infect. 2015;21(5):469e461–410. doi: 10.1016/j.cmi.2014.12.013
   Web of Science ®Google Scholar
• Hung KH, Wang MC, Huang AH, et al. Heteroresistance to cephalosporins and penicillins in Acinetobacter baumannii. J Clin Microbiol. 2012;50(3):721–726. doi: 10.1128/JCM.05085-11
   PubMed Web of Science ®Google Scholar
• He J, Jia X, Yang S, et al. Heteroresistance to carbapenems in invasive Pseudomonas aeruginosa infections. Int J Antimicrob Agents. 2018;51(3):413–421. doi: 10.1016/j.ijantimicag.2017.10.014
   PubMed Web of Science ®Google Scholar
• Zhang C, Xu X, Pu S, et al. Characterization of carbapenemases, extended spectrum beta-lactamases, quinolone resistance and aminoglycoside resistance determinants in carbapenem-non-susceptible Escherichia coli from a teaching hospital in Chongqing, Southwest China. Infect Genet Evol. 2014;27:271–276. doi: 10.1016/j.meegid.2014.07.031
   PubMed Web of Science ®Google Scholar
• Perez A, Canle D, Latasa C, et al. Cloning, nucleotide sequencing, and analysis of the AcrAB-TolC efflux pump of Enterobacter cloacae and determination of its involvement in antibiotic resistance in a clinical isolate. Antimicrob Agents Chemother. 2007;51(9):3247–3253. doi: 10.1128/AAC.00072-07
   PubMed Web of Science ®Google Scholar
• Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 2001;25(4):402–408. doi: 10.1006/meth.2001.1262
   PubMed Web of Science ®Google Scholar
• Tenover FC, Arbeit RD, Goering RV, et al. Interpreting chromosomal DNA restriction patterns produced by pulsed-field gel electrophoresis: criteria for bacterial strain typing. J Clin Microbiol. 1995;33(9):2233–2239.
   PubMed Web of Science ®Google Scholar
• Brauner A, Fridman O, Gefen O, et al. Distinguishing between resistance, tolerance and persistence to antibiotic treatment. Nat Rev Microbiol. 2016;14(5):320–330. doi: 10.1038/nrmicro.2016.34
   PubMed Web of Science ®Google Scholar
• El-Halfawy OM, Valvano MA. Antimicrobial heteroresistance: an emerging field in need of clarity. Clin Microbiol Rev. 2015;28(1):191–207. doi: 10.1128/CMR.00058-14
   PubMed Web of Science ®Google Scholar
• Greer ND. Tigecycline (Tygacil): the first in the glycylcycline class of antibiotics. Proc (Bayl Univ Med Cent. 2006;19(2):155–161. doi: 10.1080/08998280.2006.11928154
   PubMedGoogle Scholar
• Chen Y, Hu D, Zhang Q, et al. Efflux pump overexpression contributes to tigecycline heteroresistance in Salmonella enterica serovar typhimurium. Front Cell Infect Microbiol. 2017;7:37.
   Google Scholar
• Hornsey M, Ellington MJ, Doumith M, et al. Emergence of AcrAB-mediated tigecycline resistance in a clinical isolate of Enterobacter cloacae during ciprofloxacin treatment. Int J Antimicrob Agents. 2010;35(5):478–481. doi: 10.1016/j.ijantimicag.2010.01.011
   PubMed Web of Science ®Google Scholar
• Guerin F, Lallement C, Isnard C, et al. Landscape of resistance-nodulation-cell division (RND)-type efflux pumps in Enterobacter cloacae complex. Antimicrob Agents Chemother. 2016;60(4):2373–2382. doi: 10.1128/AAC.02840-15
   PubMed Web of Science ®Google Scholar
• Li X, Mu X, Yang Y, et al. Rapid emergence of high-level tigecycline resistance in Escherichia coli strains harbouring blaNDM-5 in vivo. Int J Antimicrob Agents. 2016;47(4):324–327. doi: 10.1016/j.ijantimicag.2016.01.005
   PubMed Web of Science ®Google Scholar
• Perez A, Poza M, Fernandez A, et al. Involvement of the AcrAB-TolC efflux pump in the resistance, fitness, and virulence of Enterobacter cloacae. Antimicrob Agents Chemother. 2012;56(4):2084–2090. doi: 10.1128/AAC.05509-11
   PubMed Web of Science ®Google Scholar
• Tsai MH, Chu SM, Hsu JF, et al. Risk factors and outcomes for multidrug-resistant gram-negative bacteremia in the NICU. Pediatrics. 2014;133(2):e322–e329. doi: 10.1542/peds.2013-1248
   PubMed Web of Science ®Google Scholar
• Li XZ, Plesiat P, Nikaido H. The challenge of efflux-mediated antibiotic resistance in gram-negative bacteria. Clin Microbiol Rev. 2015;28(2):337–418. doi: 10.1128/CMR.00117-14
   PubMed Web of Science ®Google Scholar
• Subhadra B, Kim J, Kim DH, et al. Local repressor AcrR Regulates AcrAB efflux pump required for biofilm formation and virulence in Acinetobacter nosocomialis. Front Cell Infect Microbiol. 2018;8:270. doi: 10.3389/fcimb.2018.00270
   PubMed Web of Science ®Google Scholar
• Bialek-Davenet S, Lavigne JP, Guyot K, et al. Differential contribution of AcrAB and OqxAB efflux pumps to multidrug resistance and virulence in Klebsiella pneumoniae. J Antimicrob Chemother. 2015;70(1):81–88. doi: 10.1093/jac/dku340
   PubMed Web of Science ®Google Scholar
• Gazel D, Tatman Otkun M. Investigation of colistin heteroresistance and some factors affecting heteroresistance in carbapenem-resistant A. baumannii strains. Mediterranean Journal of Infection Microbes and Antimicrobials. 2018;6:1.
   Web of Science ®Google Scholar
• Tumbarello M, Viale P, Viscoli C, et al. Predictors of mortality in bloodstream infections caused by Klebsiella pneumoniae carbapenemase-producing K. pneumoniae: importance of combination therapy. Clin Infect Dis. 2012;55(7):943–950. doi: 10.1093/cid/cis588
   PubMed Web of Science ®Google Scholar