170
Views
3
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Within-Host Resistance and Virulence Evolution of a Hypervirulent Carbapenem-Resistant Klebsiella pneumoniae ST11 Under Antibiotic Pressure

ORCID Icon, , , , , & show all
Pages 7255-7270 | Received 19 Aug 2023, Accepted 07 Nov 2023, Published online: 15 Nov 2023

References

  • Navon-Venezia S, Kondratyeva K, Carattoli A. Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. Fems Microbiol Rev. 2017;41(3):252–275. doi:10.1093/femsre/fux013
  • Gu D, Dong N, Zheng Z, et al. A fatal outbreak of st11 carbapenem-resistant hypervirulent Klebsiella pneumoniae in a Chinese hospital: a molecular epidemiological study. Lancet Infect Dis. 2018;18(1):37–46. doi:10.1016/S1473-3099(17)30489-9
  • Tian D, Wang M, Zhou Y, Hu D, Jiang X. Genetic diversity and evolution of the virulence plasmids encoding aerobactin and salmochelin in Klebsiella pneumoniae. Virulence. 2021;12(1):1323–1333. doi:10.1080/21505594.2021.1924019
  • Lan P, Jiang Y, Zhou J, Yu Y. A global perspective on the convergence of hypervirulence and carbapenem resistance in Klebsiella pneumoniae. J Glob Antimicrob Resist. 2021;25:26–34. doi:10.1016/j.jgar.2021.02.020
  • Yang X, Dong N, Zhang R, Chen S. Carbapenem resistance-encoding and virulence-encoding conjugative plasmids in Klebsiella pneumoniae. Trends Microbiol. 2021;29(1):65–83. doi:10.1016/j.tim.2020.04.012
  • 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
  • Xie Y, Tian L, Li G, et al. Emergence of the third-generation cephalosporin-resistant hypervirulent Klebsiella pneumoniae due to the acquisition of a self-transferable bladha-1-carrying plasmid by an st23 strain. Virulence. 2018;9(1):838–844.
  • Xie M, Yang X, Xu Q, et al. Clinical evolution of st11 carbapenem resistant and hypervirulent Klebsiella pneumoniae. Commun Biol. 2021;4(1):650. doi:10.1038/s42003-021-02148-4
  • Zhang R, Lin D, Gu D, Chen G, Chen S. Emergence of carbapenem-resistant serotype k1 hypervirulent Klebsiella pneumoniae strains in China. Antimicrob Agents Chemother. 2015;60(1):709–711. doi:10.1128/AAC.02173-15
  • Dong N, Lin D, Zhang R, Chan EW, Chen S. Carriage of blakpc-2 by a virulence plasmid in hypervirulent Klebsiella pneumoniae. J Antimicrob Chemother. 2018;73(12):3317–3321. doi:10.1093/jac/dky358
  • Huang YH, Chou SH, Liang SW, et al. Emergence of an xdr and carbapenemase-producing hypervirulent Klebsiella pneumoniae strain in Taiwan. J Antimicrob Chemother. 2018;73(8):2039–2046. doi:10.1093/jac/dky164
  • Lam MMC, Wyres KL, Wick RR, et al. Convergence of virulence and mdr in a single plasmid vector in mdr Klebsiella pneumoniae st15. J Antimicrob Chemother. 2019;74(5):1218–1222. doi:10.1093/jac/dkz028
  • Turton J, Davies F, Turton J, Perry C, Payne Z, Pike R. Hybrid resistance and virulence plasmids in “high-risk” clones of Klebsiella pneumoniae, including those carrying blandm-5. Microorganisms. 2019;7(9):1–11. doi:10.3390/microorganisms7090326
  • Zhao Y, Zhang X, Torres VVL, et al. An outbreak of carbapenem-resistant and hypervirulent Klebsiella pneumoniae in an intensive care unit of a major teaching hospital in Wenzhou, China. Front Public Health. 2019;7:229. doi:10.3389/fpubh.2019.00229
  • Serio AW, Keepers T, Andrews L, Krause KM. Aminoglycoside revival: review of a historically important class of antimicrobials undergoing rejuvenation. Ecosal Plus. 2018;8(1):1–20. doi:10.1128/ecosalplus.ESP-0002-2018
  • Raut A, Sharma D, Suvarna V. A status update on pharmaceutical analytical methods of aminoglycoside antibiotic: amikacin. Crit Rev Anal Chem. 2022;52(2):375–391. doi:10.1080/10408347.2020.1803042
  • Yang W, Hu F. Research updates of plasmid-mediated aminoglycoside resistance 16s rRNA methyltransferase. Antibiotics. 2022;11(7). doi:10.3390/antibiotics11070906
  • Wachino JI, Doi Y, Arakawa Y. Aminoglycoside resistance: updates with a focus on acquired 16s ribosomal RNA methyltransferases. Infect Dis Clin North Am. 2020;34(4):887–902. doi:10.1016/j.idc.2020.06.002
  • Kawai A, Suzuki M, Tsukamoto K, Minato Y, Doi Y. Functional and structural characterization of acquired 16s rRNA methyltransferase npmb1 conferring pan-aminoglycoside resistance. Antimicrob Agents Chemother. 2021;65(10):e100921. doi:10.1128/AAC.01009-21
  • Camelena F, Morel F, Merimeche M, et al. Genomic characterization of 16s rRNA methyltransferase-producing Escherichia coli isolates from the Parisian area, France. J Antimicrob Chemother. 2020;75(7):1726–1735. doi:10.1093/jac/dkaa105
  • Uchida H, Tada T, Tohya M, et al. Emergence in Japan of an isolate of Klebsiella pneumoniae co-harbouring bla(kpc-2) and rmtb. J Glob Antimicrob Resist. 2019;17:157–159. doi:10.1016/j.jgar.2018.11.026
  • Amin M, Mehdipour G, Navidifar T. High distribution of 16s rRNA methylase genes rmtb and arma among Enterobacter cloacae strains isolated from an ahvaz teaching hospital, Iran. Acta Microbiol Immunol Hung. 2019;66(3):337–348. doi:10.1556/030.66.2019.009
  • Nagasawa M, Kaku M, Kamachi K, et al. Loop-mediated isothermal amplification assay for 16s rRNA methylase genes in gram-negative bacteria. J Infect Chemother. 2014;20(10):635–638. doi:10.1016/j.jiac.2014.08.013
  • CLSI. Performance Standards for Antimicrobial Susceptibility Testing. 31st ed. Wayne, PA: Clinical and Laboratory Standards Institute; 2021.
  • Hua Y, Wang J, Huang M, et al. Outer membrane vesicles-transmitted virulence genes mediate the emergence of new antimicrobial-resistant hypervirulent Klebsiella pneumoniae. Emerg Microbes Infect. 2022;11(1):1281–1292. doi:10.1080/22221751.2022.2065935
  • Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol. 2017;13(6):e1005595. doi:10.1371/journal.pcbi.1005595
  • Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinformatics. 2014;30(14):2068–2069. doi:10.1093/bioinformatics/btu153
  • Wang M, Goh YX, Tai C, Wang H, Deng Z, Ou HY. Vrprofile2: detection of antibiotic resistance-associated mobilome in bacterial pathogens. Nucleic Acids Res. 2022;50(W1):W768–773. doi:10.1093/nar/gkac321
  • Jin X, Chen Q, Shen F, et al. Resistance evolution of hypervirulent carbapenem-resistant Klebsiella pneumoniae st11 during treatment with tigecycline and polymyxin. Emerg Microbes Infect. 2021;10(1):1129–1136. doi:10.1080/22221751.2021.1937327
  • Alikhan NF, Petty NK, Ben ZN, Beatson SA. Blast ring image generator (brig): simple prokaryote genome comparisons. BMC Genomics. 2011;12:402. doi:10.1186/1471-2164-12-402
  • Sullivan MJ, Petty NK, Beatson SA. Easyfig: a genome comparison visualizer. Bioinformatics. 2011;27(7):1009–1010. doi:10.1093/bioinformatics/btr039
  • Wang X, Chen G, Wu X, et al. Increased prevalence of carbapenem resistant Enterobacteriaceae in hospital setting due to cross-species transmission of the bla ndm-1 element and clonal spread of progenitor resistant strains. Front Microbiol. 2015;6:595. doi:10.3389/fmicb.2015.00595
  • 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. doi:10.1128/jcm.33.9.2233-2239.1995
  • Mukherjee S, Bhadury P, Mitra S, et al. Hypervirulent Klebsiella pneumoniae causing neonatal bloodstream infections: emergence of ndm-1-producing hypervirulent st11-k2 and st15-k54 strains possessing plvpk-associated markers. Microbiol Spectr. 2023;11(2):e412122. doi:10.1128/spectrum.04121-22
  • Semenec L, Cain AK, Dawson CJ, et al. Cross-protection and cross-feeding between Klebsiella pneumoniae and Acinetobacter baumannii promotes their co-existence. Nat Commun. 2023;14(1):702. doi:10.1038/s41467-023-36252-2
  • Tian D, Wang W, Li M, et al. Acquisition of the conjugative virulence plasmid from a cg23 hypervirulent Klebsiella pneumoniae strain enhances bacterial virulence. Front Cell Infect Microbiol. 2021;11:752011. doi:10.3389/fcimb.2021.752011
  • Wang L, Zhang Y, Liu Y, et al. Effects of chlorogenic acid on antimicrobial, antivirulence, and anti-quorum sensing of carbapenem-resistant Klebsiella pneumoniae. Front Microbiol. 2022;13:997310. doi:10.3389/fmicb.2022.997310
  • Loyola IH, Brito IL. Characterizing conjugative plasmids from an antibiotic-resistant dataset for use as broad-host delivery vectors. Front Microbiol. 2023;14:1199640. doi:10.3389/fmicb.2023.1199640
  • Lai YC, Peng HL, Chang HY. Rmpa2, an activator of capsule biosynthesis in Klebsiella pneumoniae cg43, regulates k2 cps gene expression at the transcriptional level. J Bacteriol. 2003;185(3):788–800. doi:10.1128/JB.185.3.788-800.2003
  • Zhou K, Xiao T, David S, et al. Novel subclone of carbapenem-resistant Klebsiella pneumoniae sequence type 11 with enhanced virulence and transmissibility, China. Emerg Infect Dis. 2020;26(2):289–297. doi:10.3201/eid2602.190594
  • Zhou C, Wu Q, He L, et al. Clinical and molecular characteristics of carbapenem-resistant hypervirulent Klebsiella pneumoniae isolates in a tertiary hospital in shanghai, China. Infect Drug Resist. 2021;14:2697–2706. doi:10.2147/IDR.S321704
  • Dong N, Yang X, Zhang R, Chan EW, Chen S. Tracking microevolution events among st11 carbapenemase-producing hypervirulent Klebsiella pneumoniae outbreak strains. Emerg Microbes Infect. 2018;7(1):146. doi:10.1038/s41426-018-0146-6
  • Chen Y, Marimuthu K, Teo J, et al. Acquisition of plasmid with carbapenem-resistance gene blakpc2 in hypervirulent Klebsiella pneumoniae, Singapore. Emerg Infect Dis. 2020;26(3):549–559. doi:10.3201/eid2603.191230
  • Yu FY, Yao D, Pan JY, et al. High prevalence of plasmid-mediated 16s rRNA methylase gene rmtb among Escherichia coli clinical isolates from a Chinese teaching hospital. BMC Infect Dis. 2010;10:184. doi:10.1186/1471-2334-10-184
  • Chen Y, Chang H, Lai Y, Pan C, Tsai S, Peng H. Sequencing and analysis of the large virulence plasmid plvpk of Klebsiella pneumoniae cg43. Gene. 2004;337:189–198. doi:10.1016/j.gene.2004.05.008
  • Zhou Y, Ai W, Guo Y, et al. Co-occurrence of rare arma-, rmtb-, and kpc-2-encoding multidrug-resistant plasmids and hypervirulence iuc operon in st11-kl47 Klebsiella pneumoniae. Microbiol Spectr. 2022;10(2):e237121. doi:10.1128/spectrum.02371-21
  • Xia P, Yi M, Yuan Y, et al. Coexistence of multidrug resistance and virulence in a single conjugative plasmid from a hypervirulent Klebsiella pneumoniae isolate of sequence type 25. Msphere. 2022;7(6):e47722. doi:10.1128/msphere.00477-22
  • Jia X, Zhu Y, Jia P, et al. Emergence of a superplasmid coharboring hypervirulence and multidrug resistance genes in Klebsiella pneumoniae poses new challenges to public health. Microbiol Spectr. 2022;10(6):e263422. doi:10.1128/spectrum.02634-22
  • Yang X, Wai-Chi CE, Zhang R, Chen S. A conjugative plasmid that augments virulence in Klebsiella pneumoniae. Nat Microbiol. 2019;4(12):2039–2043. doi:10.1038/s41564-019-0566-7
  • 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
  • Choby JE, Howard-Anderson J, Weiss DS. Hypervirulent Klebsiella pneumoniae - clinical and molecular perspectives. J Intern Med. 2020;287(3):283–300. doi:10.1111/joim.13007
  • Long D, Zhu L, Du F, et al. Phenotypical profile and global transcriptomic profile of hypervirulent Klebsiella pneumoniae due to carbapenemase-encoding plasmid acquisition. BMC Genomics. 2019;20(1):480. doi:10.1186/s12864-019-5705-2
  • Choi MJ, Ko KS. Loss of hypermucoviscosity and increased fitness cost in colistin-resistant Klebsiella pneumoniae sequence type 23 strains. Antimicrob Agents Chemother. 2015;59(11):6763–6773. doi:10.1128/AAC.00952-15
  • Zhang Y, Wang X, Wang S, et al. Emergence of colistin resistance in carbapenem-resistant hypervirulent Klebsiella pneumoniae under the pressure of tigecycline. Front Microbiol. 2021;12:756580. doi:10.3389/fmicb.2021.756580
  • Fursova AD, Fursov MV, Astashkin EI, et al. Early response of antimicrobial resistance and virulence genes expression in classical, hypervirulent, and hybrid hvkp-mdr Klebsiella pneumoniae on antimicrobial stress. Antibiotics. 2022;11(1):7. doi:10.3390/antibiotics11010007
  • Pu D, Zhao J, Lu B, et al. Within-host resistance evolution of a fatal st11 hypervirulent carbapenem-resistant Klebsiella pneumoniae. Int J Antimicrob Agents. 2023;61(4):106747. doi:10.1016/j.ijantimicag.2023.106747
  • Zhang R, Liu L, Zhou H, et al. Nationwide surveillance of clinical carbapenem-resistant Enterobacteriaceae (cre) strains in China. Ebiomedicine. 2017;19:98–106. doi:10.1016/j.ebiom.2017.04.032
  • Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev. 2019;32(3):e00001–19. doi:10.1128/CMR.00001-19
  • Wyres KL, Wick RR, Judd LM, et al. Distinct evolutionary dynamics of horizontal gene transfer in drug resistant and virulent clones of Klebsiella pneumoniae. PLoS Genet. 2019;15(4):e1008114. doi:10.1371/journal.pgen.1008114