Loss and gain of ceftazidime-avibactam susceptibility in a non-carbapenemase-producing K1-ST23 hypervirulent Klebsiella pneumoniae

References

• Zhang Y, Zhao C, Wang Q, et al. High prevalence of hypervirulent Klebsiella pneumoniae infection in China: geographic distribution, clinical characteristics, and antimicrobial resistance. Antimicrob Agents Chemother. 2016;60(10):6115–12. doi: 10.1128/AAC.01127-16
   PubMed Web of Science ®Google Scholar
• Li J, Ren J, Wang W, et al. Risk factors and clinical outcomes of hypervirulent Klebsiella pneumoniae induced bloodstream infections. Eur J Clin Microbiol Infect Dis. 2018;37(4):679–689. doi: 10.1007/s10096-017-3160-z
   PubMed Web of Science ®Google Scholar
• Zhang Y, Jin L, Ouyang P, et al. Evolution of hypervirulence in carbapenem-resistant Klebsiella pneumoniae in China: a multicentre, molecular epidemiological analysis. J Antimicrob Chemother. 2020;75(2):327–336. doi: 10.1093/jac/dkz446
   PubMed Web of Science ®Google Scholar
• Zhao J, Liu C, Liu Y, et al. Genomic characteristics of clinically important ST11 Klebsiella pneumoniae strains worldwide. J Glob Antimicrob Resist. 2020;22:519–526. doi: 10.1016/j.jgar.2020.03.023
   PubMed Web of Science ®Google Scholar
• Tian D, Liu X, Chen W, et al. Prevalence of hypervirulent and carbapenem-resistant Klebsiella pneumoniae under divergent evolutionary patterns. Emerg Microbes Infect. 2022;11(1):1936–1949. doi: 10.1080/22221751.2022.2103454
   PubMed Web of Science ®Google Scholar
• Castanheira M, Doyle TB, Hubler C, et al. Ceftazidime-avibactam activity against a challenge set of carbapenem-resistant enterobacterales: Ompk36 L3 alterations and β-lactamases with ceftazidime hydrolytic activity lead to elevated MIC values. Int J Antimicrob Agents. 2020;56(1):106011. doi: 10.1016/j.ijantimicag.2020.106011
   PubMed Web of Science ®Google Scholar
• Yu F, Lv J, Niu S, et al. In vitro activity of ceftazidime-avibactam against carbapenem-resistant and hypervirulent Klebsiella pneumoniae isolates. Antimicrob Agents Chemother. 2018;62(8):e01031–18. doi: 10.1128/AAC.01031-18
   PubMed Web of Science ®Google Scholar
• Gaibani P, Re MC, Campoli C, et al. Bloodstream infection caused by KPC-producing Klebsiella pneumoniae resistant to ceftazidime/avibactam: epidemiology and genomic characterization. Clin Microbiol Infect. 2020;26(4):.e516.1–.e516.4. doi: 10.1016/j.cmi.2019.11.011
   Web of Science ®Google Scholar
• Wang C, Zhao J, Liu Z, et al. In vivo Selection of Imipenem Resistance Among Ceftazidime-Avibactam-Resistant, Imipenem-Susceptible Klebsiella pneumoniae Isolate With KPC-33 Carbapenemase. Front Microbiol. 2021;12:727946. doi: 10.3389/fmicb.2021.727946
   PubMed Web of Science ®Google Scholar
• Venditti C, Butera O, Meledandri M, et al. Molecular analysis of clinical isolates of ceftazidime-avibactam-resistant Klebsiella pneumoniae. Clin Microbiol Infect. 2021;27(7):.e1040.1–.e1040.6. doi: 10.1016/j.cmi.2021.03.001
   Web of Science ®Google Scholar
• Liu L, Feng Y, Long H, et al. Sequence type 273 carbapenem-resistant Klebsiella pneumoniae carrying blaNDM-1 and blaIMP-4. Antimicrob Agents Chemother. 2018;62(6). doi: 10.1128/AAC.00160-18
   Web of Science ®Google Scholar
• Li D, Liao W, Huang HH, et al. Emergence of hypervirulent Ceftazidime/Avibactam-resistant Klebsiella pneumoniae isolates in a Chinese tertiary hospital. Infect Drug Resist 13:2673–2680. 10.2147/IDR.S257477. 2020.
   PubMed Web of Science ®Google Scholar
• Both A, Buttner H, Huang J, et al. Emergence of ceftazidime/avibactam non-susceptibility in an MDR Klebsiella pneumoniae isolate. J Antimicrob Chemother. 2017;72(9):2483–2488. doi: 10.1093/jac/dkx179
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang S, Chen W, et al. CRISPR-Cas9 and CRISPR-Assisted cytidine deaminase enable precise and efficient genome editing in Klebsiella pneumoniae. Appl Environ Microbiol. 2018;84(23):e01834–18. doi: 10.1128/AEM.01834-18
   PubMed Web of Science ®Google Scholar
• Li Z, Liu X, Lei Z, et al. Genetic diversity of polymyxin-resistance mechanisms in clinical isolates of carbapenem-resistant Klebsiella pneumoniae: a multicenter study in China. Microbiol Spectr. 2023;11(2):e0523122. doi: 10.1128/spectrum.05231-22
   PubMed Web of Science ®Google Scholar
• Shon AS, Bajwa RP, Russo TA. Hypervirulent (hypermucoviscous) Klebsiella pneumoniae: a new and dangerous breed. Virulence. 2013;4(2):107–118. doi: 10.4161/viru.22718
   PubMed Web of Science ®Google Scholar
• Jiang H, Lei R, Ding SW, et al. Skewer: a fast and accurate adapter trimmer for next-generation sequencing paired-end reads. BMC Bioinf. 2014;15(1):182. doi: 10.1186/1471-2105-15-182
   PubMed Web of Science ®Google Scholar
• Prjibelski A, Antipov D, Meleshko D, et al. Using SPAdes De Novo Assembler. Curr Protoc Bioinform. 2020;70(1):e102. doi: 10.1002/cpbi.102
   PubMedGoogle Scholar
• Wick RR, Judd LM, Gorrie CL, et al. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol. 2017;13(6):e1005595. doi: 10.1371/journal.pcbi.1005595
   PubMed Web of Science ®Google Scholar
• Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069. doi: 10.1093/bioinformatics/btu153
   PubMed Web of Science ®Google Scholar
• Choi Y, Sims GE, Murphy S, et al. Predicting the functional effect of amino acid substitutions and indels. PLOS ONE. 2012;7(10):e46688. doi: 10.1371/journal.pone.0046688
   PubMed Web of Science ®Google Scholar
• Darling AC, Mau B, Blattner FR, et al. Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 2004;14(7):1394–1403. doi: 10.1101/gr.2289704
   PubMed Web of Science ®Google Scholar
• Siguier P, Perochon J, Lestrade L, et al. Isfinder: the reference centre for bacterial insertion sequences. Nucleic Acids Res. 2006;34(90001):D32–6. doi: 10.1093/nar/gkj014
   PubMed Web of Science ®Google Scholar
• Solovyev V, Salamov A. Automatic Annotation of Microbial Genomes and Metagenomic Sequences. Metagenomics And Its Applications In Agriculture. Hauppauge (NY): Nova Science Publishers; 2011. p. 61–78.
   Google Scholar
• Liao Y, Smyth GK, Shi W. The subread aligner: fast, accurate and scalable read mapping by seed-and-vote. Nucleic Acids Res. 2013;41(10):e108. doi: 10.1093/nar/gkt214
   PubMed Web of Science ®Google Scholar
• Liao Y, Smyth GK, Shi W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30(7):923–930. doi: 10.1093/bioinformatics/btt656
   PubMed Web of Science ®Google Scholar
• Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15(12):550. doi: 10.1186/s13059-014-0550-8
   PubMed Web of Science ®Google Scholar
• Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol. 2011;12(6):R60. doi: 10.1186/gb-2011-12-6-r60
   PubMed Web of Science ®Google Scholar
• Yang X, Wai-Chi Chan E, Zhang R, et al. A conjugative plasmid that augments virulence in Klebsiella pneumoniae. Nat Microbiol. 2019;4(12):2039–2043. doi: 10.1038/s41564-019-0566-7
   PubMed Web of Science ®Google Scholar
• Carlone GM, Thomas ML, Rumschlag HS, et al. Rapid microprocedure for isolating detergent-insoluble outer membrane proteins from Haemophilus species. J Clin Microbiol. 1986;24(3):330–332. doi: 10.1128/jcm.24.3.330-332.1986
   PubMed Web of Science ®Google Scholar
• Dupont H, Gaillot O, Goetgheluck A-S, et al. Molecular characterization of carbapenem-nonsusceptible enterobacterial isolates collected during a prospective interregional survey in France and susceptibility to the novel ceftazidime-avibactam and aztreonam-avibactam combinations. Antimicrob Agents Chemother. 2016;60(1):215–221. doi: 10.1128/AAC.01559-15
   PubMed Web of Science ®Google Scholar
• Giner G, Smyth GK. Statmod: probability calculations for the inverse gaussian distribution. R J. 2016;8(1):339–351. doi: 10.32614/RJ-2016-024
   Google Scholar
• Yin D, Wu S, Yang Y, et al. Results from the China Antimicrobial Surveillance Network (CHINET) in 2017 of the in vitro activities of ceftazidime-avibactam and ceftolozane-tazobactam against clinical isolates of Enterobacteriaceae and Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2019;63(4):e02431–18. doi: 10.1128/AAC.02431-18
   PubMed Web of Science ®Google Scholar
• Zhang P, Shi Q, Hu H, et al. Emergence of ceftazidime/avibactam resistance in carbapenem-resistant Klebsiella pneumoniae in China. Clin Microbiol Infect. 2020;26(1):.e124.1–.e124.4. doi: 10.1016/j.cmi.2019.08.020
   Web of Science ®Google Scholar
• Humphries RM, Hemarajata P. Resistance to ceftazidime-avibactam in Klebsiella pneumoniae due to porin mutations and the increased expression of KPC-3. Antimicrob Agents Chemother. 2017;61(6):00537–17. doi: 10.1128/AAC.00537-17
   PubMed Web of Science ®Google Scholar
• Xu M, Zhao J, Xu L, et al. Emergence of transferable ceftazidime–avibactam resistance in KPC-producing Klebsiella pneumoniae due to a novel CMY AmpC β-lactamase in China. Clin Microbiol Infect. 2022;28(1):.e136.1–.e136.6. doi: 10.1016/j.cmi.2021.05.026
   Web of Science ®Google Scholar
• Salverda ML, De Visser JA, Barlow M. Natural evolution of TEM-1 β-lactamase: experimental reconstruction and clinical relevance. FEMS Microbiol Rev. 2010;34(6):1015–1036. doi: 10.1111/j.1574-6976.2010.00222.x
   PubMed Web of Science ®Google Scholar
• Rice LB, Carias LL, Hujer AM, et al. High-level expression of chromosomally encoded SHV-1 β-lactamase and an outer membrane protein change confer resistance to ceftazidime and piperacillin- tazobactam in a clinical isolate of Klebsiella pneumoniae. Antimicrob Agents Chemother. 2000;44(2):362–367. doi: 10.1128/AAC.44.2.362-367.2000
   PubMed Web of Science ®Google Scholar
• Nuesch-Inderbinen MT, Kayser FH, Hachler H. Survey and molecular genetics of SHV beta-lactamases in Enterobacteriaceae in Switzerland: two novel enzymes, SHV-11 and SHV-12. Antimicrob Agents Chemother. 1997;41(5):943–949. doi: 10.1128/AAC.41.5.943
   PubMed Web of Science ®Google Scholar
• Schneider I, Queenan AM, Markovska R, et al. New variant of CTX-M-Type extended-spectrum β-lactamases, CTX-M-71, with a Gly238Cys substitution in a K lebsiella pneumoniae isolate from Bulgaria. Antimicrob Agents Chemother. 2009;53(10):4518–4521. doi: 10.1128/AAC.00461-09
   PubMed Web of Science ®Google Scholar
• Sabatini A, Brisdelli F, Celenza G, et al. Interaction of carbapenems and β-lactamase inhibitors towards CTX-M-15 and CTX-M-15 G238C mutant. J Glob Antimicrob Resist. 2017;10:95–100. doi: 10.1016/j.jgar.2017.04.004
   PubMed Web of Science ®Google Scholar
• Pages JM, Peslier S, Keating TA, et al. Role of the outer membrane and Porins in susceptibility of β-lactamase-producing Enterobacteriaceae to ceftazidime-avibactam. Antimicrob Agents Chemother. 2015;60(3):1349–1359. doi: 10.1128/AAC.01585-15
   PubMed Web of Science ®Google Scholar
• Fajardo-Lubian A, Ben Zakour NL, Agyekum A, et al. Host adaptation and convergent evolution increases antibiotic resistance without loss of virulence in a major human pathogen. PLOS Pathog. 2019;15(3):e1007218. doi: 10.1371/journal.ppat.1007218
   PubMed Web of Science ®Google Scholar
• Shen Z, Ding B, Ye M, et al. High ceftazidime hydrolysis activity and porin OmpK35 deficiency contribute to the decreased susceptibility to ceftazidime/avibactam in KPC-producing Klebsiella pneumoniae. J Antimicrob Chemother. 2017;72(7):1930–1936. doi: 10.1093/jac/dkx066
   PubMed Web of Science ®Google Scholar
• Nelson K, Hemarajata P, Sun D, et al. Resistance tO ceftazidime-avibactam is due to transposition of KPC in a porin-deficient strain of Klebsiella pneumoniae with increased efflux activity. Antimicrob Agents Chemother. 2017;61(10):e00989–17. doi: 10.1128/AAC.00989-17
   PubMed Web of Science ®Google Scholar
• Hamzaoui Z, Ocampo-Sosa A, Fernandez Martinez M, et al. Role of association of OmpK35 and OmpK36 alteration and blaESBL and/or blaAmpC genes in conferring carbapenem resistance among non-carbapenemase-producing Klebsiella pneumoniae. Int J Antimicrob Agents. 2018;52(6):898–905. doi: 10.1016/j.ijantimicag.2018.03.020
   PubMed Web of Science ®Google Scholar
• Kaczmarek FM, Dib-Hajj F, Shang W, et al. High-level carbapenem resistance in a Klebsiella pneumoniae clinical isolate is due to the combination of bla ACT-1 β-lactamase production, porin OmpK35/36 insertional inactivation, and down-regulation of the phosphate transport porin PhoE. Antimicrob Agents Chemother. 2006;50(10):3396–3406. doi: 10.1128/AAC.00285-06
   PubMed Web of Science ®Google Scholar
• Foudraine DE, Strepis N, Stingl C, et al. Exploring antimicrobial resistance to beta-lactams, aminoglycosides and fluoroquinolones in E. coli and K. pneumoniae using proteogenomics. Sci Rep. 2021;11(1):12472. doi: 10.1038/s41598-021-91905-w
   PubMed Web of Science ®Google Scholar
• Findlay J, Hamouda A, Dancer SJ, et al. Rapid acquisition of decreased carbapenem susceptibility in a strain of Klebsiella pneumoniae arising during meropenem therapy. Clin Microbiol Infect. 2012;18(2):140–146. doi: 10.1111/j.1469-0691.2011.03515.x
   PubMed Web of Science ®Google Scholar
• Shields RK, Clancy CJ, Hao B, et al. Effects of Klebsiella pneumoniae carbapenemase subtypes, extended-spectrum β-lactamases, and porin mutations on the in vitro activity of ceftazidime-avibactam against carbapenem-resistant K. pneumoniae. Antimicrob Agents Chemother. 2015;59(9):5793–5797. doi: 10.1128/AAC.00548-15
   PubMed Web of Science ®Google Scholar
• Grobner S, Linke D, Schutz W, et al. Emergence of carbapenem-non-susceptible extended-spectrum β-lactamase-producing Klebsiella pneumoniae isolates at the university hospital of Tübingen, Germany. J Med Microbiol. 2009;58(7):912–922. doi: 10.1099/jmm.0.005850-0
   PubMed Web of Science ®Google Scholar
• Rocker A, Lacey JA, Belousoff MJ, et al. Global Trends in Proteome Remodeling of the Outer Membrane Modulate Antimicrobial Permeability in Klebsiella pneumoniae. MBio. 2020;11(2):e00603–20. doi: 10.1128/mBio.00603-20
   PubMed Web of Science ®Google Scholar