248
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

In vitro Activity of Cefepime/Avibactam Against Carbapenem Resistant Klebsiella pneumoniae and Integrative Metabolomics-Proteomics Approach for Resistance Mechanism: A Single-Center Study

, , , , & ORCID Icon
Pages 6061-6077 | Received 11 May 2023, Accepted 02 Aug 2023, Published online: 11 Sep 2023

References

  • Patel G, Huprikar S, Factor SH, Jenkins SG, Calfee DP. Outcomes of carbapenem-resistant Klebsiella pneumoniae infection and the impact of antimicrobial and adjunctive therapies. Infect Control Hosp Epidemiol. 2008;29(12):1099–1106. doi:10.1086/592412
  • Huang W, Qiao F, Zhang Y, et al. In-hospital medical costs of infections caused by carbapenem-resistant Klebsiella pneumoniae. Clin Infect Dis. 2018;67(suppl_2):S225–S230. doi:10.1093/cid/ciy642
  • World Health Organization. Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics. Geneva, Switzerland: World Health Organization; 2017.
  • Yahav D, Giske CG, Grāmatniece A, Abodakpi H, Tam VH, Leibovici L. New β-Lactam-β-Lactamase Inhibitor Combinations. Clin Microbiol Rev. 2020;34(1). doi:10.1128/CMR.00115-20
  • Katip W, Rayanakorn A, Oberdorfer P, Taruangsri P, Nampuan T. Short versus long course of colistin treatment for carbapenem-resistant A. baumannii in critically ill patients: a propensity score matching study. J Infect Public Health. 2023;16(8):1249–1255. doi:10.1016/j.jiph.2023.05.024
  • Roach EJ, Uehara T, Daigle DM, Six DA, Khursigara CM, Lainhart W. The next-generation β-lactamase inhibitor taniborbactam restores the morphological effects of cefepime in KPC-producing Escherichia coli. Microbiol Spectr. 2021;9(2):e0091821. doi:10.1128/Spectrum.00918-21
  • Everaert A, Coenye T. Effect of β-Lactamase inhibitors on in vitro activity of β-Lactam antibiotics against Burkholderia cepacia complex species. Antimicrob Resist Infect Control. 2016;5(1):44. doi:10.1186/s13756-016-0142-3
  • Ehmann DE, Jahić H, Ross PL, et al. Avibactam is a covalent, reversible, non-β-lactam β-lactamase inhibitor. Proc Natl Acad Sci U S A. 2012;109(29):11663–11668. doi:10.1073/pnas.1205073109
  • van Haren MJ, Tehrani K, Kotsogianni I, et al. Cephalosporin prodrug inhibitors overcome metallo-β-lactamase driven antibiotic resistance. Chemistry. 2021;27(11):3806–3811. doi:10.1002/chem.202004694
  • Katip W, Yoodee J, Uitrakul S, Oberdorfer P. Efficacy of loading dose colistin versus carbapenems for treatment of extended spectrum beta lactamase producing Enterobacteriaceae. Sci Rep. 2021;11(1):18. doi:10.1038/s41598-020-78098-4
  • Ehmann DE, Jahic H, Ross PL, et al. Kinetics of avibactam inhibition against Class A, C, and D β-lactamases. J Biol Chem. 2013;288(39):27960–27971. doi:10.1074/jbc.M113.485979
  • Li H, Estabrook M, Jacoby GA, Nichols WW, Testa RT, Bush K. In vitro susceptibility of characterized β-lactamase-producing strains tested with avibactam combinations. Antimicrob Agents Chemother. 2015;59(3):1789–1793. doi:10.1128/aac.04191-14
  • 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):124.e1–124.e4. doi:10.1016/j.cmi.2019.08.020
  • Tumbarello M, Raffaelli F, Giannella M, et al. Ceftazidime-avibactam use for Klebsiella pneumoniae carbapenemase-producing K. pneumoniae infections: a retrospective observational multicenter study. Clin Infect Dis. 2021;73(9):1664–1676. doi:10.1093/cid/ciab176
  • Kloezen W, Melchers RJ, Georgiou PC, Mouton JW, Meletiadis J. Activity of cefepime in combination with the Novel β-Lactamase Inhibitor Taniborbactam (VNRX-5133) against extended-spectrum-β-lactamase-producing isolates in in vitro checkerboard assays. Antimicrob Agents Chemother. 2021;65(4). doi:10.1128/AAC.02338-20
  • Lima O, Sousa A, Longueira-Suárez R, et al. Ceftazidime-avibactam treatment in bacteremia caused by OXA-48 carbapenemase-producing Klebsiella pneumoniae. Eur J Clin Microbiol Infect Dis. 2022;41(9):1173–1182. doi:10.1007/s10096-022-04482-9
  • Göttig S, Frank D, Mungo E, et al. Emergence of ceftazidime/avibactam resistance in KPC-3-producing Klebsiella pneumoniae in vivo. J Antimicrob Chemother. 2019;74(11):3211–3216. doi:10.1093/jac/dkz330
  • Han X, Shi Q, Mao Y, et al. Emergence of ceftazidime/avibactam and tigecycline resistance in carbapenem-resistant Klebsiella pneumoniae due to in-host microevolution. Front Cell Infect Microbiol. 2021;11:757470. doi:10.3389/fcimb.2021.757470
  • Teo JQ, Fauzi N, Ho JJ, et al. In vitro bactericidal activities of combination antibiotic therapies against carbapenem-resistant Klebsiella pneumoniae with different carbapenemases and sequence types. Front Microbiol. 2021;12:779988. doi:10.3389/fmicb.2021.779988
  • Aktaş Z, Kayacan C, Oncul O. In vitro activity of avibactam (NXL104) in combination with β-lactams against Gram-negative bacteria, including OXA-48 β-lactamase-producing Klebsiella pneumoniae. Int J Antimicrob Agents. 2012;39(1):86–89. doi:10.1016/j.ijantimicag.2011.09.012
  • Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing, 30th ed.M100-Ed30. Wayne, PA: Clinical and Laboratory Standards Institute; 2020.
  • Khalid A, Lubián AF, Ma L, Lin RCY, Iredell JR. Characterizing the role of porin mutations in susceptibility of beta lactamase producing Klebsiella pneumoniae isolates to ceftaroline and ceftaroline-avibactam. Int J Infect Dis. 2020;93:252–257. doi:10.1016/j.ijid.2020.02.005
  • Chen X, Tian J, Luo C, Wang X, Li X, Wang M. Cell Membrane Remodeling Mediates Polymyxin B Resistance in Klebsiella pneumoniae: an Integrated Proteomics and Metabolomics Study. Front Microbiol. 2022;13:810403. doi:10.3389/fmicb.2022.810403
  • Fan LP, Yu Y, Huang S, et al. Genetic characterization and passage instability of a novel hybrid virulence plasmid in a ST23 hypervirulent Klebsiella pneumoniae. Front Cell Infect Microbiol. 2022;12:870779. doi:10.3389/fcimb.2022.870779
  • Hong SH, Wang X, Wood TK. Controlling biofilm formation, prophage excision and cell death by rewiring global regulator H-NS of Escherichia coli. Microb Biotechnol. 2010;3(3):344–356. doi:10.1111/j.1751-7915.2010.00164.x
  • Huang F, Fitchett N, Razo-Gutierrez C, et al. The H-NS regulator plays a role in the stress induced by carbapenemase expression in Acinetobacter baumannii. mSphere. 2020;5(4). doi:10.1128/mSphere.00793-20
  • Rodgers D, Le C, Pimentel C, et al. Histone-like nucleoid-structuring protein (H-NS) regulatory role in antibiotic resistance in Acinetobacter baumannii. Sci Rep. 2021;11(1):18414. doi:10.1038/s41598-021-98101-w
  • Behringer MG, Choi BI, Miller SF, et al. Escherichia coli cultures maintain stable subpopulation structure during long-term evolution. Proc Natl Acad Sci U S A. 2018;115(20):E4642–e4650. doi:10.1073/pnas.1708371115
  • Tang M, Wei X, Wan X, Ding Z, Ding Y, Liu J. The role and relationship with efflux pump of biofilm formation in Klebsiella pneumoniae. Microb Pathog. 2020;147:104244. doi:10.1016/j.micpath.2020.104244
  • Varadarajan AR, Allan RN, Valentin JDP, et al. An integrated model system to gain mechanistic insights into biofilm-associated antimicrobial resistance in Pseudomonas aeruginosa MPAO1. NPJ Biofilms Microbiomes. 2020;6(1):46. doi:10.1038/s41522-020-00154-8
  • Ares MA, Fernández-Vázquez JL, Rosales-Reyes R, et al. H-NS nucleoid protein controls virulence features of Klebsiella pneumoniae by regulating the expression of type 3 pili and the capsule polysaccharide. Front Cell Infect Microbiol. 2016;6:13. doi:10.3389/fcimb.2016.00013
  • Yu Z, Zhang J, Ding M, et al. SspA positively controls exopolysaccharides production and biofilm formation by up-regulating the algU expression in Pseudoalteromonas sp. R3. Biochem Biophys Res Commun. 2020;533(4):988–994. doi:10.1016/j.bbrc.2020.09.118
  • Kim S, Li XH, Hwang HJ, Lee JH, Ercolini D. Thermoregulation of pseudomonas aeruginosa biofilm formation. Appl Environ Microbiol. 2020;86(22). doi:10.1128/AEM.01584-20
  • Bossé JT, Sinha S, Li MS, et al. Regulation of pga operon expression and biofilm formation in Actinobacillus pleuropneumoniae by sigmaE and H-NS. J Bacteriol. 2010;192(9):2414–2423. doi:10.1128/jb.01513-09
  • Wang H, Ayala JC, Silva AJ, Benitez JA. The histone-like nucleoid structuring protein (H-NS) is a repressor of Vibrio cholerae exopolysaccharide biosynthesis (vps) genes. Appl Environ Microbiol. 2012;78(7):2482–2488. doi:10.1128/aem.07629-11
  • Belik AS, Tarasova NN, Khmel IA. Регулирование образования биопленок в Escherichia coli K12: влияние мутаций в генах овв, StpA, lon и rpoN [Regulation of biofilm formation in Escherichia coli K12: effect of mutations in HNS, StpA, lon, and rpoN genes]. Mol Gen Mikrobiol Virusol. 2008;4:3–5. Russian.
  • Bao K, Bostanci N, Thurnheer T, et al. Aggregatibacter actinomycetemcomitans H-NS promotes biofilm formation and alters protein dynamics of other species within a polymicrobial oral biofilm. NPJ Biofilms Microbiomes. 2018;4(1):12. doi:10.1038/s41522-018-0055-4
  • Lin GH, Hsieh MC, Shu HY. Role of iron-containing alcohol dehydrogenases in Acinetobacter baumannii ATCC 19606 stress resistance and virulence. Int J Mol Sci. 2021;22(18):9921.
  • Pony P, Rapisarda C, Terradot L, Marza E, Fronzes R. Filamentation of the bacterial bi-functional alcohol/aldehyde dehydrogenase AdhE is essential for substrate channeling and enzymatic regulation. Nat Commun. 2020;11(1):1426. doi:10.1038/s41467-020-15214-y
  • Zhou H, Luo C, Fang X, et al. Loss of GltB inhibits biofilm formation and biocontrol efficiency of bacillus subtilis Bs916 by altering the production of γ-polyglutamate and three lipopeptides. PLoS One. 2016;11(5):e0156247. doi:10.1371/journal.pone.0156247
  • Nishino K, Hayashi-Nishino M, Yamaguchi A. H-NS modulates multidrug resistance of Salmonella enterica serovar Typhimurium by repressing multidrug efflux genes acrEF. Antimicrob Agents Chemother. 2009;53(8):3541–3543. doi:10.1128/aac.00371-09
  • Duan Y, Liu S, Gao Y, Zhang P, Mao D, Luo Y. Macrolides mediate transcriptional activation of the msr(E)-mph(E) operon through histone-like nucleoid-structuring protein (HNS) and cAMP receptor protein (CRP). J Antimicrob Chemother. 2022;77(2):391–399. doi:10.1093/jac/dkab395
  • Li H, Wang Y, Chen Q, et al. Identification of functional interactome of colistin resistance protein MCR-1 in Escherichia coli. Front Microbiol. 2020;11:583185. doi:10.3389/fmicb.2020.583185
  • Adilakshmi T, Bellur DL, Woodson SA. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature. 2008;455(7217):1268–1272. doi:10.1038/nature07298
  • Kim H, Abeysirigunawarden SC, Chen K, et al. Protein-guided RNA dynamics during early ribosome assembly. Nature. 2014;506(7488):334–338. doi:10.1038/nature13039
  • Nowotny V, Nierhaus KH. Assembly of the 30S subunit from Escherichia coli ribosomes occurs via two assembly domains which are initiated by S4 and S7. Biochemistry. 1988;27(18):7051–7055. doi:10.1021/bi00418a057
  • Nishi K, Morel-Deville F, Hershey JW, Leighton T, Schnier J. An eIF-4A-like protein is a suppressor of an Escherichia coli mutant defective in 50S ribosomal subunit assembly. Nature. 1988;336(6198):496–498. doi:10.1038/336496a0
  • Müller AL, Gu W, Patsalo V, Deutzmann JS, Williamson JR, Spormann AM. An alternative resource allocation strategy in the chemolithoautotrophic archaeon Methanococcus maripaludis. Proc Natl Acad Sci U S A. 2021;118(16):e2025854118.
  • Liu J, Wei Q, Wang Z, Sun X, He QY. Proteomic Study of the adaptive mechanism of ciprofloxacin-resistant Staphylococcus aureus to the host environment. J Proteome Res. 2022;21(6):1537–1547. doi:10.1021/acs.jproteome.2c00140
  • Tomlinson BR, Malof ME, Shaw LN. A global transcriptomic analysis of Staphylococcus aureus biofilm formation across diverse clonal lineages. Microb Genom. 2021;7(7):e000598.
  • Das B, Bhadra RK. (p)ppGpp metabolism and antimicrobial resistance in bacterial pathogens. Front Microbiol. 2020;11:563944. doi:10.3389/fmicb.2020.563944
  • De Boer HA, Bakker AJ, Gruber M. Breakdown of ppGpp in spoT and spoT-cells of Escherichia coli. manganese and energy requirement and tetracycline inhibition. FEBS Lett. 1977;79(1):19–24. doi:10.1016/0014-5793(77)80341-4
  • Fitzsimmons LF, Liu L, Kant S, et al. SpoT induces intracellular salmonella virulence programs in the phagosome. mBio. 2020;11(1):10–128.
  • Kim HY, Go J, Lee KM, Oh YT, Yoon SS. Guanosine tetra- and pentaphosphate increase antibiotic tolerance by reducing reactive oxygen species production in Vibrio cholerae. J Biol Chem. 2018;293(15):5679–5694. doi:10.1074/jbc.RA117.000383
  • Spira B, Ospino K. Diversity in E. coli (p)ppGpp Levels and Its Consequences. Front Microbiol. 2020;11:1759. doi:10.3389/fmicb.2020.01759
  • Wu J, Long Q, Xie J. (p)ppGpp and drug resistance. J Cell Physiol. 2010;224(2):300–304. doi:10.1002/jcp.22158
  • Ishiguro EE, Ramey WD. Inhibition of in vitro peptidoglycan biosynthesis in Escherichia coli by guanosine 5’-diphosphate 3’-diphosphate. Can J Microbiol. 1980;26(12):1514–1518. doi:10.1139/m80-253
  • Hugonnet JE, Mengin-Lecreulx D, Monton A, et al. Factors essential for L,D-transpeptidase-mediated peptidoglycan cross-linking and β-lactam resistance in Escherichia coli. Elife. 2016;5. doi:10.7554/eLife.19469
  • Jung HW, Kim K, Islam MM, Lee JC, Shin M. Role of ppGpp-regulated efflux genes in Acinetobacter baumannii. J Antimicrob Chemother. 2020;75(5):1130–1134. doi:10.1093/jac/dkaa014
  • Zhang Y, Zborníková E, Rejman D, Gerdes K, Swanson MS. Novel (p)ppGpp binding and metabolizing proteins of Escherichia coli. mBio. 2018;9(2). doi:10.1128/mBio.02188-17
  • Wang JD, Sanders GM, Grossman AD. Nutritional control of elongation of DNA replication by (p)ppGpp. Cell. 2007;128(5):865–875. doi:10.1016/j.cell.2006.12.043
  • Stayton MM, Fromm HJ. Guanosine 5’-diphosphate-3’-diphosphate inhibition of adenylosuccinate synthetase. J Biol Chem. 1979;254(8):2579–2581. doi:10.1016/S0021-9258(17)30108-4
  • Guo Y, Liu N, Lin Z, et al. Mutations in porin LamB contribute to ceftazidime-avibactam resistance in KPC-producing Klebsiella pneumoniae. Emerg Microbes Infect. 2021;10(1):2042–2051. doi:10.1080/22221751.2021.1984182
  • Klebba PE, Hofnung M, Charbit A. A model of maltodextrin transport through the sugar-specific porin, LamB, based on deletion analysis. EMBO j. 1994;13(19):4670–4675. doi:10.1002/j.1460-2075.1994.tb06790.x
  • García-Sureda L, Juan C, Doménech-Sánchez A, Albertí S. Role of Klebsiella pneumoniae LamB Porin in antimicrobial resistance. Antimicrob Agents Chemother. 2011;55(4):1803–1805. doi:10.1128/aac.01441-10
  • Zgurskaya HI, Rybenkov VV. Permeability barriers of Gram-negative pathogens. Ann N Y Acad Sci. 2020;1459(1):5–18. doi:10.1111/nyas.14134
  • Jia FF, Pang XH, Zhu DQ, Zhu ZT, Sun SR, Meng XC. Role of the luxS gene in bacteriocin biosynthesis by Lactobacillus plantarum KLDS1.0391: a proteomic analysis. Sci Rep. 2017;7(1):13871. doi:10.1038/s41598-017-13231-4