179
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Assessing the Emergence of Resistance in vitro and Invivo: Linezolid Combined with Fosfomycin Against Fosfomycin-Sensitive and Resistant Enterococcus

ORCID Icon, , , , , , , ORCID Icon, , & show all
Pages 4995-5010 | Published online: 30 Aug 2022

References

  • Starling S. Bacterial evolution: the origins of pathogenic enterococci. Nat Rev Microbiol. 2017;15(7):382–383. doi:10.1038/nrmicro.2017.65
  • Ch’ng JH, Chong KKL, Lam LN, et al. Biofilm-associated infection by enterococci. Nat Rev Microbiol. 2019;17(2):82–94. doi:10.1038/s41579-018-0107-z
  • Dahl A, Iversen K, Fosbol E, et al. Reply: Enterococcus faecalis infective endocarditis. J Am Coll Cardiol. 2019;74(19):2435–2436. doi:10.1016/j.jacc.2019.09.011
  • García-Solache M, Rice LB. The Enterococcus: a model of adaptability to its environment. Clin Microbiol Rev. 2019;32(2):e00058–18. doi:10.1128/CMR.00058-18
  • Gouliouris T, Coll F, Ludden C, et al. Quantifying acquisition and transmission of Enterococcus faecium using genomic surveillance. Nat Microbiol. 2021;6(1):103–111. doi:10.1038/s41564-020-00806-7
  • Arredondo-Alonso S, Top J, McNally A, et al. Plasmids shaped the recent emergence of the major nosocomial pathogen Enterococcus faecium. mBio. 2020;11(1):e03284–19. doi:10.1128/mBio.03284-19
  • Abbott IJ, Meletiadis J, Belghanch I, et al. Fosfomycin efficacy and emergence of resistance among Enterobacteriaceae in an in vitro dynamic bladder infection model. J Antimicrob Chemother. 2018;73(3):709–719. doi:10.1093/jac/dkx441
  • Van Tyne D, Gilmore MS. Raising the alarmone: within-host evolution of antibiotic-tolerant. Enterococcus Faecium mBio. 2017;8(1):e00066–17.
  • Chuang YC, Lin HY, Chen PY, et al. Survival of patients with vancomycin-resistant Enterococcus faecium bacteremia treated with conventional or high doses of daptomycin or linezolid is associated with the rate of bacterial clearance. Crit Care Med. 2018;46(10):1634–1642. doi:10.1097/CCM.0000000000003264
  • Schwartz MD, Shive DK, Shaikh ZH. Delayed discovery of linezolid-resistant, vancomycin-resistant Enterococcus faecium: lessons learned. Clin Infect Dis. 2004;38(1):155–156. doi:10.1086/380465
  • Yan Y, Yang G, Li Y, et al. Factorial design and post-antibiotic sub-MIC effects of linezolid combined with fosfomycin against vancomycin-resistant enterococci. Ann Transl Med. 2022;10(3):148. doi:10.21037/atm-21-4595
  • Qi C, Xu S, Wu M, et al. Pharmacodynamics of linezolid-plus-fosfomycin against vancomycin-susceptible and -resistant enterococci in vitro and in vivo of A Galleria mellonella larval infection model. Infect Drug Resist. 2019;12:3497–3505. doi:10.2147/IDR.S219117
  • Tao Y, Duma L, Rossez Y. Galleria mellonella as a good model to study Acinetobacter baumannii pathogenesis. Pathogens. 2021;10(11):1483. doi:10.3390/pathogens10111483
  • Piatek M, Sheehan G, Kavanagh K. Galleria mellonella: the versatile host for drug discovery, in vivo toxicity testing and characterising host-pathogen interactions. Antibiotics. 2021;10(12):1545. doi:10.3390/antibiotics10121545
  • Ménard G, Rouillon A, Cattoir V, et al. Galleria mellonella as a suitable model of bacterial infection: past, present and future. Front Cell Infect Microbiol. 2021;11:782733. doi:10.3389/fcimb.2021.782733
  • Li L, Chen H, Liu Y, et al. Synergistic effect of linezolid with fosfomycin against Staphylococcus aureus in vitro and in an experimental Galleria mellonella model. J Microbiol Immunol Infect. 2020;53(5):731–738. doi:10.1016/j.jmii.2018.12.007
  • Ochoa S, Fernández F, Devotto L, et al. Virulence assessment of enterohepatic Helicobacter species carried by dogs using the wax moth larvae Galleria mellonella as infection model. Helicobacter. 2021;26(4):e12808. doi:10.1111/hel.12808
  • Yang HF, Pan AJ, Hu LF, et al. Galleria mellonella as an in vivo model for assessing the efficacy of antimicrobial agents against Enterobacter cloacae infection. J Microbiol Immunol Infect. 2017;50(1):55–61. doi:10.1016/j.jmii.2014.11.011
  • Mao J, Li T, Zhang N, et al. Dose optimization of combined linezolid and fosfomycin against Enterococcus by using an in vitro pharmacokinetic/pharmacodynamic model. Microbiol Spectr. 2021;9(3):e0087121. doi:10.1128/Spectrum.00871-21
  • Melnyk AH, Wong A, Kassen R. The fitness costs of antibiotic resistance mutations. Evol Appl. 2015;8(3):273–283. doi:10.1111/eva.12196
  • Alame Emane AK, Guo X, Takiff HE, et al. Drug resistance, fitness and compensatory mutations in Mycobacterium tuberculosis. Tuberculosis. 2021;129:102091. doi:10.1016/j.tube.2021.102091
  • Kempf I, Zeitouni S. Coût biologique de la résistance aux antibiotiques: analyse et conséquences [The cost of antibiotic resistance: analysis and consequences]. Pathol Biol. 2012;60(2):e9–e14. French. doi:10.1016/j.patbio.2009.10.013
  • Li W, Liu Z, Yin W, et al. MCR expression conferring varied fitness costs on host bacteria and affecting bacteria virulence. Antibiotics. 2021;10(7):872. doi:10.3390/antibiotics10070872
  • Wang S, Liu H, Mao J, et al. Pharmacodynamics of linezolid plus fosfomycin against vancomycin-resistant Enterococcus faecium in a hollow fiber infection model. Front Microbiol. 2021;12:779885. doi:10.3389/fmicb.2021.779885
  • Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing; 30th Informational supplement.CLSI M100-S30. Wayne, PA: Clinical and Laboratory Standards Institute; 2020.
  • Davis H, Brown R, Ashcraft D, et al. In vitro synergy with fosfomycin plus doxycyclin against linezolid and vancomycin-resistant Enterococcus faecium. J Glob Antimicrob Resist. 2020;22:78–83. doi:10.1016/j.jgar.2020.01.014
  • Yang W, Liu J, Blažeković B, et al. In vitro antibacterial effects of Tanreqing injection combined with vancomycin or linezolid against methicillin-resistant Staphylococcus aureus. BMC Complement Altern Med. 2018;18(1):169. doi:10.1186/s12906-018-2231-8
  • Jemel S, Guillot J, Kallel K, et al. In vivo efficacy of voriconazole in a Galleria mellonella model of invasive infection due to azole-susceptible or resistant Aspergillus fumigatus isolates. J Fungi. 2021;7(12):1012. doi:10.3390/jof7121012
  • Xie N, Jiang L, Chen M, et al. In vitro and in vivo antibacterial activity of linezolid plus fosfomycin against Staphylococcus aureus with resistance to one drug. Infect Drug Resist. 2021;14:639–649. doi:10.2147/IDR.S290332
  • Billal DS, Fedorko DP, Yan SS, et al. In vitro induction and selection of fluoroquinolone-resistant mutants of Streptococcus pyogenes strains with multiple emm types. J Antimicrob Chemother. 2007;59(1):28–34. doi:10.1093/jac/dkl428
  • Jiang L, Cai W, Tang F, et al. Characterization of fitness cost caused by tigecycline-resistance gene tet (X6) in different host bacteria. Antibiotics. 2021;10(10):1172. doi:10.3390/antibiotics10101172
  • Xia X, Yang L, Ling Y, et al. Emergence and mechanism of resistance of tulathromycin against Mycoplasma hyopneumoniae in a PK/PD model and the fitness costs of 23S rRNA mutants. Front Vet Sci. 2022;9:801800. doi:10.3389/fvets.2022.801800
  • Mališová L, Jakubů V, Pomorská K, et al. Spread of linezolid-resistant Enterococcus spp. in human clinical isolates in the Czech Republic. Antibiotics. 2021;10(2):219. doi:10.3390/antibiotics10020219
  • Dadashi M, Sharifian P, Bostanshirin N, et al. The global prevalence of daptomycin, tigecycline, and linezolid-resistant Enterococcus faecalis and Enterococcus faecium strains from human clinical samples: a systematic review and meta-analysis. Front Med. 2021;8:720647. doi:10.3389/fmed.2021.720647
  • Olearo F, Both A, Belmar Campos C, et al. Emergence of linezolid-resistance in vancomycin-resistant Enterococcus faecium ST117 associated with increased linezolid-consumption. Int J Med Microbiol. 2021;311(2):151477. doi:10.1016/j.ijmm.2021.151477
  • Smith TT, Tamma PD, Do TB, et al. Prolonged linezolid use is associated with the development of linezolid-resistant Enterococcus faecium. Diagn Microbiol Infect Dis. 2018;91(2):161–163. doi:10.1016/j.diagmicrobio.2018.01.027
  • Egan SA, Shore AC, O’Connell B, et al. Linezolid resistance in Enterococcus faecium and Enterococcus faecalis from hospitalized patients in Ireland: high prevalence of the MDR genes optrA and poxtA in isolates with diverse genetic backgrounds. J Antimicrob Chemother. 2020;75(7):1704–1711. doi:10.1093/jac/dkaa075
  • Zhang Y, Dong G, Li J, et al. A high incidence and coexistence of multiresistance genes cfr and optrA among linezolid-resistant enterococci isolated from a teaching hospital in Wenzhou, China. Eur J Clin Microbiol Infect Dis. 2018;37(8):1441–1448. doi:10.1007/s10096-018-3269-8
  • Jiang L, Xie N, Chen M, et al. Synergistic combination of Linezolid and fosfomycin closing each other’s mutant selection window to prevent enterococcal resistance. Front Microbiol. 2021;11:605962. doi:10.3389/fmicb.2020.605962
  • Chai D, Liu X, Wang R, et al. Efficacy of Linezolid and fosfomycin in catheter-related biofilm infection caused by methicillin-resistant Staphylococcus aureus. Biomed Res Int. 2016;2016:6413982. doi:10.1155/2016/6413982
  • Falagas ME, Roussos N, Gkegkes ID, et al. Fosfomycin for the treatment of infections caused by Gram-positive cocci with advanced antimicrobial drug resistance: a review of microbiological, animal and clinical studies. Expert Opin Investig Drugs. 2009;18(7):921–944. doi:10.1517/13543780902967624
  • Cai T, Tamanini I, Mattevi D, et al. Fosfomycin trometamol and N-acetyl-L-cysteine as combined oral therapy of difficult-to-treat chronic bacterial prostatitis: results of a pilot study. Int J Antimicrob Agents. 2020;56(1):105935. doi:10.1016/j.ijantimicag.2020.105935
  • Hemapanpairoa J, Changpradub D, Thunyaharn S, et al. Vancomycin-resistant enterococcal infection in a Thai university hospital: clinical characteristics, treatment outcomes, and synergistic effect. Infect Drug Resist. 2019;12:2049–2057. doi:10.2147/IDR.S208298
  • Pan AJ, Mei Q, Ye Y, et al. Validation of the mutant selection window hypothesis with fosfomycin against Escherichia coli and Pseudomonas aeruginosa: an in vitro and in vivo comparative study. J Antibiot. 2017;70(2):166–173. doi:10.1038/ja.2016.124
  • Shen F, Tang X, Cheng W, et al. Fosfomycin enhances phagocyte-mediated killing of Staphylococcus aureus by extracellular traps and reactive oxygen species. Sci Rep. 2016;6:19262. doi:10.1038/srep19262
  • Thieme L, Hartung A, Makarewicz O, et al. In vivo synergism of ampicillin, gentamicin, ceftaroline and ceftriaxone against Enterococcus faecalis assessed in the Galleria mellonella infection model. J Antimicrob Chemother. 2020;75(8):2173–2181. doi:10.1093/jac/dkaa129
  • Killiny N. Generous hosts: why the larvae of greater wax moth, Galleria mellonella is a perfect infectious host model? Virulence. 2018;9(1):860–865. doi:10.1080/21505594.2018.1454172
  • Stanojević S, Blagojević V, Ćuruvija I, et al. Lactobacillus rhamnosus affects rat peritoneal cavity cell response to stimulation with gut microbiota: focus on the host innate immunity. Inflammation. 2021;44(6):2429–2447. doi:10.1007/s10753-021-01513-z
  • Trinh TD, Smith JR, Rybak MJ. Parenteral Fosfomycin for the treatment of multidrug resistant bacterial infections: the rise of the epoxide. Pharmacotherapy. 2019;39(11):1077–1094. doi:10.1002/phar.2326
  • Tsegka KG, Voulgaris GL, Kyriakidou M, et al. Intravenous fosfomycin for the treatment of patients with bone and joint infections: a review. Expert Rev Anti Infect Ther. 2022;20(1):33–43. doi:10.1080/14787210.2021.1932463
  • Guo Y, Tomich AD, McElheny CL, et al. High-level Fosfomycin resistance in vancomycin-resistant Enterococcus faecium. Emerg Infect Dis. 2017;23(11):1902–1904. doi:10.3201/eid2311.171130
  • Theophel K, Schacht VJ, Schlüter M, et al. The importance of growth kinetic analysis in determining bacterial susceptibility against antibiotics and silver nanoparticles. Front Microbiol. 2014;5:544. doi:10.3389/fmicb.2014.00544
  • Scortti M, Lacharme-Lora L, Wagner M, et al. Coexpression of virulence and fosfomycin susceptibility in Listeria: molecular basis of an antimicrobial in vitro-in vivo paradox. Nat Med. 2006;12(5):515–517. doi:10.1038/nm1396
  • Scortti M, Han L, Alvarez S, et al. Epistatic control of intrinsic resistance by virulence genes in Listeria. PLoS Genet. 2018;14(9):e1007525. doi:10.1371/journal.pgen.1007525
  • Deng Y, Xu H, Su Y, et al. Horizontal gene transfer contributes to virulence and antibiotic resistance of Vibrio harveyi 345 based on complete genome sequence analysis. BMC Genomics. 2019;20(1):761. doi:10.1186/s12864-019-6137-8
  • Pourbaix A, Guérin F, Lastours V, et al. Biological cost of fosfomycin resistance in Escherichia coli in a murine model of urinary tract infection. Int J Med Microbiol. 2017;307(8):452–459. doi:10.1016/j.ijmm.2017.09.019
  • Taglialegna A, Varela MC, Rosato RR, et al. VraSR and virulence trait modulation during daptomycin resistance in methicillin-resistant Staphylococcus aureus infection. mSphere. 2019;4(1):e00557–18. doi:10.1128/mSphere.00557-18
  • Parrett A, Reed JM, Gardner SG, et al. Metabolic changes associated with adaptive resistance to daptomycin in Streptococcus mitis-oralis. BMC Microbiol. 2020;20(1):162. doi:10.1186/s12866-020-01849-w
  • Marchi AP, Perdigão Neto LV, Martins RCR, et al. Vancomycin-resistant enterococci isolates colonizing and infecting haematology patients: clonality, and virulence and resistance profile. J Hosp Infect. 2018;99(3):346–355. doi:10.1016/j.jhin.2017.10.010
  • Nielsen KL, Pedersen TM, Udekwu KI, et al. Fitness cost: a bacteriological explanation for the demise of the first international methicillin-resistant Staphylococcus aureus epidemic. J Antimicrob Chemother. 2012;67(6):1325–1332. doi:10.1093/jac/dks051
  • Yokoyama M, Stevens E, Laabei M, et al. Epistasis analysis uncovers hidden antibiotic resistance-associated fitness costs hampering the evolution of MRSA. Genome Biol. 2018;19(1):94. doi:10.1186/s13059-018-1469-2
  • Knight GM, Colijn C, Shrestha S, et al. The distribution of fitness costs of resistance-conferring mutations is a key determinant for the future burden of drug-resistant tuberculosis: a model-based analysis. Clin Infect Dis. 2015;61(Suppl 3):S147–S154. doi:10.1093/cid/civ579
  • Hubbard ATM, Jafari NV, Feasey N, et al. Effect of environment on the evolutionary trajectories and growth characteristics of antibiotic-resistant Escherichia coli mutants. Front Microbiol. 2019;10:2001. doi:10.3389/fmicb.2019.02001
  • Rasouly A, Shamovsky Y, Epshtein V, et al. Analysing the fitness cost of antibiotic resistance to identify targets for combination antimicrobials. Nat Microbiol. 2021;6(11):1410–1423. doi:10.1038/s41564-021-00973-1
  • El-Gaml RM, El-Khodary NM, Abozahra RR, et al. Applying pharmacokinetic/pharmacodynamic measurements for linezolid in critically ill patients: optimizing efficacy and reducing resistance occurrence. Eur J Clin Pharmacol. 2022;78(8):1301–1310. doi:10.1007/s00228-022-03340-z
  • La H, Bodolea C, Vlase L, et al. Linezolid administration to critically Ill patients: intermittent or continuous infusion? A systematic literature search and review. Antibiotics. 2022;11(4):436. doi:10.3390/antibiotics11040436
  • Zhu LL, Zhou Q. Optimal infusion rate in antimicrobial therapy explosion of evidence in the last five years. Infect Drug Resist. 2018;11:1105–1117. doi:10.2147/IDR.S167616
  • Boak LM, Li J, Rayner CR, et al. Pharmacokinetic/pharmacodynamic factors influencing emergence of resistance to linezolid in an in vitro model. Antimicrob Agents Chemother. 2007;51(4):1287–1292. doi:10.1128/AAC.01194-06
  • Lagatolla C, Milic J, Imperi F, et al. Synergistic activity of fosfomycin and chloramphenicol against vancomycin-resistant Enterococcus faecium (VREfm) isolates from bloodstream infections. Diagn Microbiol Infect Dis. 2021;99(2):115241. doi:10.1016/j.diagmicrobio.2020.115241
  • Liu BG, Yuan XL, He DD, et al. Research progress on the oxazolidinone drug linezolid resistance. Eur Rev Med Pharmacol Sci. 2020;24(18):9274–9281. doi:10.26355/eurrev_202009_23009
  • Katip W, Okonogi S, Oberdorfer P. The thirty-day mortality rate and nephrotoxicity associated with trough serum vancomycin concentrations during treatment of enterococcal infections: a propensity score matching analysis. Front Pharmacol. 2022;12:773994. doi:10.3389/fphar.2021.773994
  • Katip W, Oberdorfer P, Monocentric Retrospective A. Study of AUC/MIC ratio of vancomycin associated with clinical outcomes and nephrotoxicity in patients with enterococcal infections. Pharmaceutics. 2021;13(9):1378. doi:10.3390/pharmaceutics13091378
  • Falagas ME, Athanasaki F, Voulgaris GL, et al. Resistance to fosfomycin: mechanisms, frequency and clinical consequences. Int J Antimicrob Agents. 2019;53(1):22–28. doi:10.1016/j.ijantimicag.2018.09.013