76
Views
0
CrossRef citations to date
0
Altmetric
REVIEW

Virulence Factors and Carbapenem-Resistance Mechanisms in Hypervirulent Klebsiella Pneumoniae

, , , , &
Pages 1551-1559 | Received 01 Feb 2024, Accepted 11 Apr 2024, Published online: 21 Apr 2024

References

  • 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
  • Liu YC, Cheng DL, Lin CL. Klebsiella pneumoniae liver abscess associated with septic endophthalmitis. Arch Intern Med. 1986;146(10):1913–1916.
  • Russo TA, Marr CM. Hypervirulent Klebsiella pneumoniae. Clin Microbiol Rev. 2019;32(3):e00001–19. doi:10.1128/CMR.00001-19
  • Tan TY, Ong M, Cheng Y, et al. Hypermucoviscosity, rmpA, and aerobactin are associated with community-acquired Klebsiella pneumoniae bacteremic isolates causing liver abscess in Singapore. J Microbiol Immunol Infect. 2019;52(1):30–34. doi:10.1016/j.jmii.2017.07.003
  • Huang Y, Cai Y, He W, et al. Clinical and molecular epidemiological characteristics of hypervirulent and carbapenem-resistant Klebsiella pneumoniae causing blood stream infection. Chin J Nosocomiol. 2023;33(22):3417–3422.
  • Qiao Y, Sun H, Li J, et al. Clinical and molecular characteristics of carbapenem-resistant hypervirulent Klebsiella pneumoniae in a teaching hospital. Chin J Infect Control. 2022;21(12):1185–1192.
  • Lee CH, Liu JW, Su LH, et al. Hypermucoviscosity associated with Klebsiella pneumoniae-mediated invasive syndrome: a prospective cross-sectional study in Taiwan. Int J Infect Dis. 2010;14(8):e688–92.
  • Yu WL, Ko WC, Cheng KC, et al. Comparison of prevalence of virulence factors for Klebsiella pneumoniae liver abscesses between isolates with capsular K1 /K2 and non-K1 /K2 serotypes. Diagn Microbiol Infect Dis. 2008;62(1):1–6.
  • Lee HC, Chuang YC, Yu WL, et al. Clinical implications of hypermucoviscosity phenotype in Klebsiella pneumoniae isolates: association with invasive syndrome in patients with community-acquired bacteraemia. J Intern Med. 2006;259(6):606–614.
  • Harada S, Doi Y. Hypervirulent Klebsiella pneumoniae: a call for consensus definition and international collaboration. J Clin Microbiol. 2018;56(9):e00959–18.
  • Yu F, Lv J, Niu S, et al. Multiplex PCR analysis for rapid detection of Klebsiella pneumoniae carbapenem-resistant (Sequence Type 258[ST258]and ST11) and hypervirulent (ST23, ST65, ST86, and ST375) strains. J Clin Microbiol. 2018;56(9):e00731–18.
  • Russo TA, Olson R, Fang CT, et al. Identification of biomarkers for differentiation of hypervirulent Klebsiella pneumoniae from classical K.Pneumoniae. J Clin Microbiol. 2018;56(9):e00776–18.
  • Fan Q, Yang X, Hu R, et al. Application of PEG-344 gene encoding metabolite transporter in virulence identification of Klebsiella pneumoniae. Chin J Infect Control. 2022;21(5):414–419.
  • 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
  • Han YL, Wen XH, Zhao W, et al. Epidemiological characteristics and molecular evolution mechanisms of carbapenem-resistant hypervirulent Klebsiella pneumoniae. Front Microbiol. 2022;13:1003783. doi:10.3389/fmicb.2022.1003783
  • Lan P, Jiang Y, Zhou J, et al. 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
  • Shon AS, Russo TA. Hypervirulent Klebsiella pneumoniae: the next superbug? Future Microbiol. 2012;7(6):669–671.
  • Lev AI, Astashkin EI, Kislichkina AA, et al. Comparative analysis of Klebsiella pneumoniae strains isolated in 2012–2016 that differ by antibiotic resistance genes and virulence genes profiles. Pathog Glob Health. 2018;112(3):142–151.
  • Zhang R, Dong N, Huang Y, et al. Evolution of tigecycline- and colistin-resistant CRKP (carbapenem-resistant Klebsiella pneumoniae) in vivo and its persistence in the GI tract. Emerg Microbes Infect. 2018;7(1):127. doi:10.1038/s41426-018-0129-7
  • Hu F, Guo Y, Zhu D, et al. Chinet surveillance of antimicrobial resistance among the bacterial isolates in 2021. Chin J Infect Chemother. 2022;22(5):521–530. doi:10.16718/j.1009-7708.2022.05.001
  • Cejas D, Fernández Canigia L, Rincón Cruz G, et al. First isolate of KPC-2-producing Klebsiella pneumonaie sequence type 23 from the Americas. J Clin Microbiol. 2014;52(9):3483–3485. doi:10.1128/JCM.00726-14
  • Shankar C, Nabarro LE, Devanga Ragupathi NK, et al. Draft genome sequences of three hypervirulent carbapenem-resistant Klebsiella pneumoniae isolates from bacteremia. Genome Announc. 2016;4(6):e01081–16. doi:10.1128/genomeA.01081-16
  • Arena F, Henrici De Angelis L, D’Andrea MM, et al. Infections caused by carbapenem-resistant Klebsiella pneumoniae with hypermucoviscous phenotype: a case report and literature review. Virulence. 2017;8(8):1900–1908. doi:10.1080/21505594.2017.1286439
  • Ahmed MAEE, Yang Y, Yang Y, et al. Emergence of Hypervirulent Carbapenem-Resistant Klebsiella pneumoniae Coharboring a blaNDM-1-Carrying Virulent Plasmid and a blaKPC-2-Carrying Plasmid in an Egyptian Hospital. mSphere. 2021;6(3):e00088–21. doi:10.1128/mSphere.00088-21
  • Yao B, Xiao X, Wang F, et al. Clinical and molecular characteristics of multi-clone carbapenem-resistant hypervirulent (hypermucoviscous) Klebsiella pneumoniae isolates in a tertiary hospital in Beijing, China. Int J Infect Dis. 2015;37:107–112. doi:10.1016/j.ijid.2015.06.023
  • Zhou Y, Wang X, Shen J, et al. Endogenous Endophthalmitis Caused by Carbapenem-Resistant Hypervirulent Klebsiella Pneumoniae: a Case Report and Literature Review. Ocul Immunol Inflamm. 2019;27(7):1099–1104. doi:10.1080/09273948
  • 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
  • Siu LK, Fung CP, Chang FY, et al. Molecular typing and virulence analysis of serotype K1 Klebsiella pneumoniae strains isolated from liver abscess patients and stool samples from noninfectious subjects in Hong Kong, Singapore, and Taiwan. J Clin Microbiol. 2011;49(11):3761–3765. doi:10.1128/JCM.00977-11
  • Chung DR, Lee SS, Lee HR, et al. Emerging invasive liver abscess caused by K1 serotype Klebsiella pneumoniae in Korea. J Infect. 2007;54(6):578–583. doi:10.1016/j.jinf.2006.11.008
  • Moore R, O’Shea D, Geoghegan T, et al. Community-acquired Klebsiella pneumoniae liver abscess: an emerging infection in Ireland and Europe. Infection. 2013;41(3):681–686. doi:10.1007/s15010-013-0408-0
  • Nadasy KA, Domiati-Saad R, Tribble MA. Invasive Klebsiella pneumoniae syndrome in North America. Clin Infect Dis. 2007;45(3):e25–8. doi:10.1086/519424
  • 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):6115–6120. doi:10.1128/AAC.01127-16
  • Ye M, Tu J, Jiang J, et al. Clinical and Genomic Analysis of Liver Abscess-Causing Klebsiella pneumoniae Identifies New Liver Abscess-Associated Virulence Genes. Front Cell Infect Microbiol. 2016;6:165. doi:10.3389/fcimb.2016.00165
  • Bialek-Davenet S, Nicolas-Chanoine MH, Decré D, Brisse S. Microbiological and clinical characteristics of bacteraemia caused by the hypermucoviscosity phenotype of Klebsiella pneumoniae in Korea. Epidemiol Infect. 2013;141(1):188. doi:10.1017/S0950268812002051
  • Cubero M, Grau I, Tubau F, et al. Hypervirulent Klebsiella pneumoniae clones causing bacteraemia in adults in a teaching hospital in Barcelona, Spain (2007–2013). Clin Microbiol Infect. 2016;22(2):154–160. doi:10.1016/j.cmi.2015.09.025
  • Parrott AM, Shi J, Aaron J, et al. Detection of multiple hypervirulent Klebsiella pneumoniae strains in a New York City hospital through screening of virulence genes. Clin Microbiol Infect. 2021;27(4):583–589. doi:10.1016/j.cmi.2020.05.012
  • Yang Y, Yang Y, Ahmed MAEE, et al. Carriage of distinct blaKPC-2 and blaOXA-48 plasmids in a single ST11 hypervirulent Klebsiella pneumoniae isolate in Egypt. BMC Genomics. 2022;23(1):20. doi:10.1186/s12864-021-08214-9
  • Lam MMC, Wyres KL, Duchêne S, et al. Population genomics of hypervirulent Klebsiella pneumoniae clonal-group 23 reveals early emergence and rapid global dissemination. Nat Commun. 2018;9(1):2703. doi:10.1038/s41467-018-05114-7
  • Qu TT, Zhou JC, Jiang Y, et al. Clinical and microbiological characteristics of Klebsiella pneumoniae liver abscess in East China. BMC Infect Dis. 2015;15:161. doi:10.1186/s12879-015-0899-7
  • Sanikhani R, Moeinirad M, Shahcheraghi F, et al. Molecular epidemiology of hypervirulent Klebsiella pneumoniae: a systematic review and meta-analysis. Iran J Microbiol. 2021;13(3):257–265. doi:10.18502/ijm.v13i3.6384
  • Shi Q, Lan P, Huang D, et al. Diversity of virulence level phenotype of hypervirulent Klebsiella pneumoniae from different sequence type lineage. BMC Microbiol. 2018;18(1):94. doi:10.1186/s12866-018-1236-2
  • Guo Y, Wang S, Zhan L, et al. Microbiological and Clinical Characteristics of Hypermucoviscous Klebsiella pneumoniae Isolates Associated with Invasive Infections in China. Front Cell Infect Microbiol. 2017;7(24). doi:10.3389/fcimb.2017.00024
  • 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
  • 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
  • Zhang R, Lin D, Chan EW, et al. 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
  • Zhan L, Wang S, Guo Y, et al. Outbreak by Hypermucoviscous Klebsiella pneumoniae ST11 Isolates with Carbapenem Resistance in a Tertiary Hospital in China. Front Cell Infect Microbiol. 2017;7:182. doi:10.3389/fcimb.2017.00182
  • Paczosa MK, Mecsas J. Klebsiella pneumoniae: going on the Offense with a Strong Defense. Microbiol Mol Biol Rev. 2016;80(3):629–661. doi:10.1128/MMBR.00078-15
  • Prokesch BC, TeKippe M, Kim J, et al. Primary osteomyelitis caused by hypervirulent Klebsiella pneumoniae. Lancet Infect Dis. 2016;16(9):e190–e195. doi:10.1016/S1473-3099(16)30021-4
  • Kim YJ, Kim SI, Kim YR, et al. Virulence factors and clinical patterns of hypermucoviscous Klebsiella pneumoniae isolated from urine. Infect Dis. 2017;49(3):178–184. doi:10.1080/23744235.2016.1244611
  • Mataseje LF, Boyd DA, Mulvey MR, et al. Two Hypervirulent Klebsiella pneumoniae Isolates Producing a blaKPC-2 Carbapenemase from a Canadian Patient. Antimicrob Agents Chemother. 2019;63(7):e00517–19. doi:10.1128/AAC.00517-19
  • Turton JF, Payne Z, Coward A, et al. Virulence genes in isolates of Klebsiella pneumoniae from the UK during 2016, including among carbapenemase gene-positive hypervirulent K1-ST23 and ‘non-hypervirulent’ types ST147, ST15 and ST383. J Med Microbiol. 2018;67(1):118–128. doi:10.1099/jmm.0.000653
  • Li G, Shi J, Zhao Y, et al. Identification of hypervirulent Klebsiella pneumoniae isolates using the string test in combination with Galleria mellonella infectivity. Eur J Clin Microbiol Infect Dis. 2020;39(9):1673–1679. doi:10.1007/s10096-020-03890-z
  • Russo TA, Olson R, MacDonald U, et al. Aerobactin, but not yersiniabactin, salmochelin, or enterobactin, enables the growth/survival of hypervirulent (hypermucoviscous) Klebsiella pneumoniae ex vivo and in vivo. Infect Immun. 2015;83(8):3325–3333. doi:10.1128/IAI.00430-15
  • Russo TA, Olson R, Macdonald U, et al. Aerobactin mediates virulence and accounts for increased siderophore production under iron-limiting conditions by hypervirulent (hypermucoviscous) Klebsiella pneumoniae. Infect Immun. 2014;82(6):2356–2367. doi:10.1128/IAI.01667-13
  • Walker KA, Miner TA, Palacios M, et al. A Klebsiella pneumoniae Regulatory Mutant Has Reduced Capsule Expression but Retains Hypermucoviscosity. mBio. 2019;10(2):e00089–19. doi:10.1128/mBio.00089-19
  • Walker KA, Treat LP, Sepúlveda VE, et al. The Small Protein RmpD Drives Hypermucoviscosity in Klebsiella pneumoniae. mBio. 2020;11(5):e01750–20. doi:10.1128/mBio.01750-20
  • Nassif X, Fournier JM, Arondel J, et al. Mucoid phenotype of Klebsiella pneumoniae is a plasmid-encoded virulence factor. Infect Immun. 1989;57(2):546–552. doi:10.1128/iai.57.2.546-552.1989
  • Shankar C, Veeraraghavan B, Nabarro LEB, et al. Whole genome analysis of hypervirulent Klebsiella pneumoniae isolates from community and hospital acquired bloodstream infection. BMC Microbiol. 2018;18(1):6. doi:10.1186/s12866-017-1148-6
  • Wang W, Tian D, Hu D, et al. Different regulatory mechanisms of the capsule in hypervirulent Klebsiella pneumonia: ”direct” wcaJ variation vs. ”indirect” rmpA regulation. Front Cell Infect Microbiol. 2023;13(1108818). doi:10.3389/fcimb.2023.1108818
  • Song S, Zhao S, Wang W, et al. Characterization of ST11 and ST15 Carbapenem-Resistant Hypervirulent Klebsiella pneumoniae from Patients with Ventilator-Associated Pneumonia. Infect Drug Resist. 2023;16:6017–6028. doi:10.2147/IDR.S426901
  • Altayb HN, Elbadawi HS, Baothman O, et al. Genomic Analysis of Multidrug-Resistant Hypervirulent (Hypermucoviscous) Klebsiella pneumoniae Strain Lacking the Hypermucoviscous Regulators (rmpA/rmpA2). Antibiotics. 2022;11(5):596. doi:10.3390/antibiotics11050596
  • Yang X, Sun Q, Li J, et al. Molecular epidemiology of carbapenem-resistant hypervirulent Klebsiella pneumoniae in China. Emerg Microbes Infect. 2022;11(1):841–849. doi:10.1080/22221751.2022.2049458
  • Fang CT, Chuang YP, Shun CT, Chang SC, Wang JT. A novel virulence gene in Klebsiella pneumoniae strains causing primary liver abscess and septic metastatic complications. J Exp Med. 2004;199(5):697–705. doi:10.1084/jem.20030857
  • Fang CT, Lai SY, Yi WC, et al. The function of wzy_K1 (magA), the serotype K1 polymerase gene in Klebsiella pneumoniae cps gene cluster. J Infect Dis. 2010;201(8):1268–1269. doi:10.1086/652183
  • Struve C, Roe CC, Stegger M, et al. Mapping the Evolution of Hypervirulent Klebsiella pneumoniae. mBio. 2015;6(4):e00630. doi:10.1128/mBio.00630-15
  • Guo L, Wang L, Zhao Q, et al. Genomic analysis of KPC-2-producing Klebsiella pneumoniae ST11 isolates at the respiratory department of a tertiary care hospital in Beijing. China Front Microbiol. 2022;13:929826.
  • Liu BT, Su WQ. Whole genome sequencing of NDM-1-producing serotype K1 ST23 hypervirulent Klebsiella pneumoniae in China. J Med Microbiol. 2019;68(6):866–873. doi:10.1099/jmm.0.000996
  • Karlsson M, Stanton RA, Ansari U, et al. Identification of a Carbapenemase-Producing Hypervirulent Klebsiella pneumoniae Isolate in the United States. Antimicrob Agents Chemother. 2019;63(7):e00519. doi:10.1128/AAC.00519-19
  • Dong N, Yang X, Zhang R, et al. 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
  • Siu LK, Huang DB, Chiang T. Plasmid transferability of KPC into a virulent K2 serotype Klebsiella pneumoniae. BMC Infect Dis. 2014;14:176. doi:10.1186/1471-2334-14-176
  • Liu Y, Long D, Xiang TX, et al. Whole genome assembly and functional portrait of hypervirulent extensively drug-resistant NDM-1 and KPC-2 co-producing Klebsiella pneumoniae of capsular serotype K2 and ST86. J Antimicrob Chemother. 2019;74(5):1233–1240. doi:10.1093/jac/dkz023
  • Roulston KJ, Bharucha T, Turton JF, et al. A case of NDM-carbapenemase-producing hypervirulent Klebsiella pneumoniae sequence type 23 from the UK. JMM Case Rep. 2018;5(9):e005130. doi:10.1099/jmmcr.0.005130
  • Li G, Jia L, Wan L, et al. Acquisition of a novel conjugative multidrug-resistant hypervirulent plasmid leads to hypervirulence in clinical carbapenem-resistant Klebsiella pneumoniae strains. mLife. 2023;2(3):217–338.
  • Liu Y, Liu PP, Wang LH, et al. Capsular Polysaccharide Types and Virulence-Related Traits of Epidemic KPC-Producing Klebsiella pneumoniae Isolates in a Chinese University Hospital. Microb Drug Resist. 2017;23(7):901–907. doi:10.1089/mdr.2016.0222
  • Dong N, Liu L, Zhang R, et al. An IncR Plasmid Harbored by a Hypervirulent Carbapenem-Resistant Klebsiella pneumoniae Strain Possesses Five Tandem Repeats of the blaKPC-2:NTEKPC-Id Fragment. Antimicrob Agents Chemother. 2019;63(3):e01775–18. doi:10.1128/AAC.01775-18
  • Shu L, Dong N, Lu J, et al. Emergence of OXA-232 Carbapenemase-Producing Klebsiella pneumoniae That Carries a pLVPK-Like Virulence Plasmid among Elderly Patients in China. Antimicrob Agents Chemother. 2019;63(3):e02246–18. doi:10.1128/AAC.02246-18
  • Liu X, Li D, Hu Y, et al. Molecular epidemiological characterization of hypervirulent carbapenem-resistant Klebsiella pneumoniae in a hospital in Henan Province from 2020 to 2022. Chin J Prev Med. 2023;57(8):1222–1230. doi:10.3760/cma.j.cn112150-20230320-00204
  • Xu Y, Zhang J, Wang M, et al. Mobilization of the nonconjugative virulence plasmid from hypervirulent Klebsiella pneumoniae. Genome Med. 2021;13(1):119. doi:10.1186/s13073-021-00936-5
  • 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
  • Yang X, Xie M, Xu Q, et al. Transmission of pLVPK-like virulence plasmid in Klebsiella pneumoniae mediated by an Incl1 conjugative helper plasmid. iScience. 2022;25(6):104428. doi:10.1016/j.isci.2022.104428
  • Ramirez MS, Traglia GM, Lin DL, et al. Plasmid-Mediated Antibiotic Resistance and Virulence in Gram-negatives: the Klebsiella pneumoniae Paradigm. Microbiol Spectr. 2014;2(5):1–15. doi:10.1128/microbiolspec
  • Dong N, Lin D, Zhang R, et al. 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