71
Views
0
CrossRef citations to date
0
Altmetric
Review

Expert opinion on antimicrobial therapies: is there enough scientific evidence to state that targeted therapies outperform non-targeted ones?

ORCID Icon, ORCID Icon & ORCID Icon
Pages 593-609 | Received 28 Nov 2023, Accepted 04 Apr 2024, Published online: 15 Apr 2024

References

  • Mulchandani R, Wang Y, Gilbert M, et al. Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLOS Glob Public Heal. 2023;3(2):e0001305. doi: 10.1371/journal.pgph.0001305
  • Browne AJ, Chipeta MG, Haines-Woodhouse G, et al. Global antibiotic consumption and usage in humans, 2000–18: a spatial modelling study. Lancet Planet Heal. 2021;5:e893–e904. doi: 10.1016/S2542-5196(21)00280-1
  • Klein EY, Van Boeckel TP, Martinez EM, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci USA. 2018;115:E3463–E3470. doi: 10.1073/pnas.1717295115
  • Jonas OB, Irwin A, Berthe FCJ, et al. Drug-resistant infections: a threat to our economic future (Vol. 2): final report. Hnp/agriculture Glob. Antimicrob. Resist. Initiat. (WA) D.C. World Bank Group.
  • Gonzales RD, Schreckenberger PC, Graham MB, et al. Infections due to vancomycin-resistant Enterococcus faecium resistant to linezolid. Lancet. 2001;357:1179. doi: 10.1016/S0140-6736(00)04376-2
  • PD L, HK M, HA M, et al. Extended-Spectrum β-Lactamases in Klebsiella pneumoniae Bloodstream Isolates from Seven Countries: Dominance and Widespread Prevalence of SHV- and CTX-M-Type β-Lactamases. Antimicrob Agents Chemother. 2003;47(11):3554–3560. doi: 10.1128/aac.47.11.3554-3560.2003
  • Walsh TR, Weeks J, Livermore DM, et al. Dissemination of NDM-1 positive bacteria in the New Delhi environment and its implications for human health: an environmental point prevalence study. Lancet Infect Dis. 2011;11:355–362. doi: 10.1016/S1473-3099(11)70059-7
  • Khan AU, Maryam L, Structure ZR. Structure, Genetics and Worldwide Spread of New Delhi Metallo-β-lactamase (NDM): a threat to public health. BMC Microbiol. 2017;17(1):101. doi: 10.1186/s12866-017-1012-8
  • O’Neill J. Tackling drug-resistant infections globally: Final report and recommendations. 2016.
  • Yang B, Fang D, Lv Q, et al. Targeted therapeutic strategies in the battle against pathogenic bacteria. Front Pharmacol. 2021;12:673239. doi: 10.3389/fphar.2021.673239
  • Sears P, Ichikawa Y, Ruiz N, et al. Advances in the treatment of Clostridium difficile with fidaxomicin: a narrow spectrum antibiotic. Ann NY Acad Sci. 2013;1291:33–41. doi: 10.1111/nyas.12135
  • Marchandin H, Anjou C, Poulen G, et al. In vivo emergence of a still uncommon resistance to fidaxomicin in the urgent antimicrobial resistance threat Clostridioides difficile. J Antimicrob Chemother. 2023;78:1992–1999. doi: 10.1093/jac/dkad194
  • Ma B, Fang C, Lu L, et al. The antimicrobial peptide thanatin disrupts the bacterial outer membrane and inactivates the NDM-1 metallo-β-lactamase. Nat Commun. 2019;10:3517. doi: 10.1038/s41467-019-11503-3
  • Ruoslahti E. Peptides as targeting elements and tissue penetration devices for nanoparticles. Adv Mater. 2012;24:3747–3756. doi: 10.1002/adma.201200454
  • Yang S, Han X, Yang Y, et al. Bacteria-targeting nanoparticles with microenvironment- responsive antibiotic release to eliminate intracellular staphylococcus aureus and associated infection. ACS Appl Mater Interfaces. 2018;10(17):14299–14311. doi: 10.1021/acsami.7b15678
  • Saeed S, Zafar J, Khan B, et al. Utility of 99mTc-labelled antimicrobial peptide ubiquicidin (29-41) in the diagnosis of diabetic foot infection. Eur J Nucl Med Mol Imaging. 2013;40:737–743. doi: 10.1007/s00259-012-2327-1
  • Zasloff M. Antimicrobial peptides of multicellular organisms. Nature. 2002;415:389–395. doi: 10.1038/415389a
  • Hussain S, Joo J, Kang J, et al. Antibiotic-loaded nanoparticles targeted to the site of infection enhance antibacterial efficacy. Nat Biomed Eng. 2018;2:95–103. doi: 10.1038/s41551-017-0187-5
  • Ma B, Chen Y, Hu G, et al. Ovotransferrin antibacterial peptide coupling mesoporous silica nanoparticle as an effective antibiotic delivery system for treating bacterial infection in vivo. ACS Biomater Sci Eng. 2022;8(1):109–118. doi: 10.1021/acsbiomaterials.1c01267
  • Ma B, Guo Y, Fu X, et al. Identification and antimicrobial mechanisms of a novel peptide derived from egg white ovotransferrin hydrolysates. LWT - Food Sci Technol. 2020;131:109720. doi: 10.1016/j.lwt.2020.109720
  • Pan L, Jiang D, Pan L, et al. ICAM-1-targeted and antibacterial peptide modified polymeric nanoparticles for specific combating sepsis. Mater Des. 2022;222:111007. doi: 10.1016/j.matdes.2022.111007
  • Al Musaimi O, Lombardi L, Williams DR, et al. Strategies for improving peptide stability and delivery. Pharmaceuticals. 2022;15(10):1283. doi: 10.3390/ph15101283
  • Chen H, Liu C, Chen D, et al. Bacteria-targeting conjugates based on antimicrobial peptide for bacteria diagnosis and therapy. Mol Pharm. 2015;12(7):2505–2516. doi: 10.1021/acs.molpharmaceut.5b00053
  • Brezden A, Mohamed MF, John S, et al. Dual targeting of intracellular pathogenic bacteria with a cleavable conjugate of kanamycin and an antibacterial, cell penetrating peptide dual targeting of intracellular pathogenic bacteria with a cleavable conjugate of kanamycin and an Antibacterial. J Am Chem Soc. 2016;138(34):10945–10949. doi: 10.1021/jacs.6b04831
  • Jiang Y, Han M, Bo Y, et al. “Metaphilic” cell-penetrating polypeptide-vancomycin conjugate e ffi ciently eradicates intracellular bacteria via a dual mechanism. ACS Cent Sci. 2020;6(12):2267–2276. doi: 10.1021/acscentsci.0c00893
  • Zurawski DV, McLendon MK. Monoclonal Antibodies as an Antibacterial Approach Against Bacterial Pathogens. Antibiotics. 2020;9(4):155. doi: 10.3390/antibiotics9040155
  • Lu LL, Suscovich TJ, Fortune SM, et al. Beyond binding: antibody effector functions in infectious diseases. Nat Rev Immunol. 2018;18:46–61. doi: 10.1038/nri.2017.106
  • Le H, Arnoult C, Dé E, et al. Antibody-conjugated nanocarriers for targeted antibiotic delivery: application in the treatment of bacterial biofilms. Biomacromolecules. 2021;22:1639–1653. doi: 10.1021/acs.biomac.1c00082
  • Becker S, Frankel MB, Schneewind O, et al. Release of protein a from the cell wall of Staphylococcus aureus. PNAS. 2014;111:1574–1579. doi: 10.1073/pnas.1317181111
  • Deng R, Zhou C, Li D, et al. Preclinical and translational pharmacokinetics of a novel THIOMAB™ antibody-antibiotic conjugate against Staphylococcus aureus. MAbs. 2019;11(6):1162–1174. doi: 10.1080/19420862.2019.1627152
  • Melicent P, RM E, Rong D, et al. A phase 1, randomized, single-ascending-dose study to investigate the safety, tolerability, and pharmacokinetics of DSTA4637S, an anti-staphylococcus aureus thiomab antibody-antibiotic conjugate, in healthy volunteers. Antimicrob Agents Chemother. 2019;63(6):doi: 10.1128/aac.02588-18
  • Soliman C, Pier GB, Ramsland PA. ScienceDirect Antibody recognition of bacterial surfaces and extracellular polysaccharides. Curr Opin Struct Biol. 2020;62:48–55. doi: 10.1016/j.sbi.2019.12.001
  • Zhou C, Lehar S, Gutierrez J, et al. Pharmacokinetics and pharmacodynamics of DSTA4637A: A novel THIOMAB™ antibody antibiotic conjugate against Staphylococcus aureus in mice. MAbs. 2016;8(8):1612–1619. doi: 10.1080/19420862.2016.1229722
  • Zhou C, Cai H, Baruch A, et al. Sustained activity of novel THIOMAB antibody-antibiotic conjugate against Staphylococcus aureus in a mouse model: Longitudinal pharmacodynamic assessment by bioluminescence imaging. PLOS ONE. 2019;14(10):e0224096. doi: 10.1371/journal.pone.0224096
  • Ma Z, Kang M, Meng S, et al. Selective Killing of Shiga Toxin-Producing Escherichia coli with Antibody-Conjugated Chitosan Nanoparticles in the Gastrointestinal Tract. ACS Appl Mater Interfaces. 2020;12(16):18332–18341. doi: 10.1021/acsami.0c02177
  • Johnson K, Delaney JC, Guillard T, et al. Development of an antibody fused with an antimicrobial peptide targeting Pseudomonas aeruginosa: A new approach to prevent and treat bacterial infections. PLOS Pathog Pathog. 2023;19(9):e1011612. doi: 10.1371/journal.ppat.1011612
  • Takahashi M. Aptamers targeting cell surface proteins. Biochimie. 2018;145:63–72. doi: 10.1016/J.BIOCHI.2017.11.019
  • Thiviyanathan V, Gorenstein DG. Aptamers and the next generation of diagnostic reagents. Proteomics Clinical Apps. 2012;6(11–12):563–573. doi: 10.1002/prca.201200042
  • Soundy J, Day D. Delivery of antibacterial silver nanoclusters to Pseudomonas aeruginosa using species-specific DNA aptamers. J Med Microbiol. 2020;69:640–652. doi: 10.1099/jmm.0.001174
  • Soundy J, Day D, Omri A. Selection of DNA aptamers specific for live Pseudomonas aeruginosa. PLOS ONE. 2017;12(9):e0185385. doi: 10.1371/journal.pone.0185385
  • Sengupta B, Corley C, Cobb K, et al. DNA Scaffolded Silver Clusters: A Critical Study. Molecules. 2016;21:216. doi: 10.3390/molecules21020216
  • Javani S, Lorca R, Latorre A, et al. Antibacterial Activity of DNA-Stabilized Silver Nanoclusters Tuned by Oligonucleotide Sequence. ACS Appl Mater Interfaces. 2016;8:10147–10154. doi: 10.1021/acsami.6b00670
  • Gomez GF, Huang R, Eckert G, et al. Effect of phototherapy on the metabolism of Streptococcus mutans biofilm based on a colorimetric tetrazolium assay. J Oral Sci. 2018;60:242–246. doi: 10.2334/josnusd.17-0203
  • Suresh MK, Biswas R, Biswas L. An update on recent developments in the prevention and treatment of Staphylococcus aureus biofilms. Int J Med Microbiol. 2019;309:1–12. doi: 10.1016/J.IJMM.2018.11.002
  • Chen Y, Gao Y, Chen Y, et al. Nanomaterials-based photothermal therapy and its potentials in antibacterial treatment. J Control Release. 2020;328:251–262. doi: 10.1016/J.JCONREL.2020.08.055
  • Zhou W, Jiang X, Zhen X. Development of organic photosensitizers for antimicrobial photodynamic therapy. Biomater Sci. 2023;11:5108–5128. doi: 10.1039/D3BM00730H
  • Wang F, Tan J, Zhang S, et al. Efficient Eradication of Bacterial Biofilms with Highly Specific Graphene-Based Nanocomposite Sheets. ACS Biomater Sci Eng. 2021;7:5118–5128. doi: 10.1021/acsbiomaterials.1c00575
  • Zhang Y, Wen C, Liu Y, et al. NIR responsive composite nanomaterials with in-situ deposition of cascaded nanozymes for multiple synergistic therapy of bacterial infection in diabetic mice. Chem Eng J. 2023;470:144345. doi: 10.1016/J.CEJ.2023.144345
  • Chen L, Xing S, Lei Y, et al. A Glucose-Powered Activatable Nanozyme Breaking pH and H2O2 Limitations for Treating Diabetic Infections. Angew Chemie Int Ed. 2021;60:23534–23539. doi: 10.1002/anie.202107712
  • Dai J, Su Y, Zhong S, et al. Exosomes: key players in cancer and potential therapeutic strategy. Signal Transduct Target Ther. 2020;5:145. doi: 10.1038/s41392-020-00261-0
  • Toyofuku M, Nomura N, Eberl L. Types and origins of bacterial membrane vesicles. Nat Rev Microbiol. 2019;17:13–24. doi: 10.1038/s41579-018-0112-2
  • Wu S, Huang Y, Yan J, et al. Bacterial Outer Membrane-Coated Mesoporous Silica Nanoparticles for Targeted Delivery of Antibiotic Rifampicin against Gram-Negative Bacterial Infection in vivo. Adv Funct Mater. 2021;31:2103442. doi: 10.1002/adfm.202103442
  • Gao F, Xu L, Yang B, et al. Kill the Real with the Fake: Eliminate Intracellular Staphylococcus aureus Using Nanoparticle Coated with Its Extracellular Vesicle Membrane as Active-Targeting Drug Carrier. ACS Infect Dis. 2019;5(2):218–227. doi: 10.1021/acsinfecdis.8b00212
  • Huang W, Zhang Q, Li W, et al. Development of novel nanoantibiotics using an outer membrane vesicle- based drug efflux mechanism. J Control Release. 2020;317:1–22. doi: 10.1016/j.jconrel.2019.11.017
  • Huang W, Meng L, Chen Y, et al. Bacterial outer membrane vesicles as potential biological nanomaterials for antibacterial therapy. Acta Biomater. 2022;140:102–115. doi: 10.1016/j.actbio.2021.12.005
  • Gao J, Su Y, Wang Z. Engineering bacterial membrane nanovesicles for improved therapies in infectious diseases and cancer. Adv Drug Deliv Rev. 2022;186:114340. doi: 10.1016/j.addr.2022.114340
  • Sahli C, Moya SE, Lomas JS, et al. Recent advances in nanotechnology for eradicating bacterial biofilm. Theranostics. 2022;12:2383–2405. doi: 10.7150/thno.67296
  • Nobrega FL, Vlot M, de Jonge PA, et al. Targeting mechanisms of tailed bacteriophages. Nat Rev Microbiol. 2018;16:760–773. doi: 10.1038/s41579-018-0070-8
  • Moineau SB. Brenner’s Encycl Genet. 2nd ed. 2013p. 280–283. doi: 10.1016/B978-0-12-374984-0.00131-5.
  • He X, Yang Y, Guo Y, et al. Phage-Guided Targeting, Discriminative Imaging, and Synergistic Killing of Bacteria by AIE Bioconjugates. J Am Chem Soc. 2020;142:3959–3969. doi: 10.1021/jacs.9b12936
  • Huang Y, Ren J, Qu X. Nanozymes: Classification, Catalytic Mechanisms, Activity Regulation, and Applications. Chem Rev. 2019;119(6):4357–4412. doi: 10.1021/acs.chemrev.8b00672
  • Jin L, Cao F, Gao Y, et al. Microenvironment-Activated Nanozyme-Armed Bacteriophages Efficiently Combat Bacterial Infection. Adv Mater. 2023;35:2301349. doi: 10.1002/adma.202301349
  • Xu D, Chen WJ, Tobin-Miyaji Y, et al. Fabrication and Microscopic and Spectroscopic Characterization of Cytocompatible Self-Assembling Antimicrobial Nanofibers. ACS Infect Dis. 2018;4(9):1327–1335. doi: 10.1021/acsinfecdis.8b00069
  • Lan M, Zhao S, Liu W, et al. Photosensitizers for Photodynamic Therapy. Adv Healthc Mater. 2019;8:1900132. doi: 10.1002/adhm.201900132
  • He X, Xiong L-H, Zhao Z, et al. AIE-based theranostic systems for detection and killing of pathogens. Theranostics. 2019;9:3223–3248. doi: 10.7150/thno.31844
  • Spiresc VA, Chircov C, Mihai Grumezescu A, et al. Polymeric Nanoparticles for Antimicrobial Therapies: An up-to-date Overview. Polymers. 2021;13:724. doi: 10.3390/polym13050724
  • Nazli A, He DL, Liao D, et al. Strategies and progresses for enhancing targeted antibiotic delivery. Adv Drug Deliv Rev. 2022;189:114502. doi: 10.1016/j.addr.2022.114502
  • Yang X, Xie B, Peng H, et al. Eradicating intracellular MRSA via targeted delivery of lysostaphin and vancomycin with mannose-modified exosomes. J Control Release. 2021;329:454–467. doi: 10.1016/j.jconrel.2020.11.045
  • Chen M, Xie S, Wei J, et al. Antibacterial Micelles with Vancomycin-Mediated Targeting and pH/Lipase-Triggered Release of Antibiotics. ACS Appl Mater Interfaces. 2018;10(43):36814–36823. doi: 10.1021/acsami.8b16092
  • Angsantikul P, Thamphiwatana S, Zhang Q, et al. Coating Nanoparticles with Gastric Epithelial Cell Membrane for Targeted Antibiotic Delivery against Helicobacter pylori Infection. Adv Ther. 2018;1(2):1800016. doi: 10.1002/adtp.201800016
  • Hu F, Qi G, Kenry, et al. Visualization and in situ Ablation of Intracellular Bacterial Pathogens through Metabolic Labeling. Angew Chemie Int Ed. 2020;59(24):9288–9292. doi: 10.1002/anie.201910187
  • Feng W, Li G, Kang X, et al. Cascade-Targeting Poly (amino acid) Nanoparticles Eliminate Intracellular Bacteria via On-Site Antibiotic Delivery. Adv Mater. 2022;34:2109789. doi: 10.1002/adma.202109789
  • Kell AJ, Stewart G, Ryan S, et al. Vancomycin-Modified Nanoparticles for Efficient Targeting and Preconcentration of Gram-Positive and Gram-Negative Bacteria. ACS Nano. 2008;2:1777–1788. doi: 10.1021/nn700183g
  • Hubbard BK, Walsh CT. Biosynthesis of Antibiotics Vancomycin Assembly: Nature ’ s Way. Angew Chemie Int Ed. 2003;42(7):730–765. doi: 10.1002/anie.200390202
  • Cao Y, Wei X, Cai P, et al. Colloids and Surfaces B: Biointerfaces Preferential adsorption of extracellular polymeric substances from bacteria on clay minerals and iron oxide. Colloids Surf B Biointerfaces. 2011;83:122–127. doi: 10.1016/j.colsurfb.2010.11.018
  • Ping Y, Hu X, Yao Q, et al. Engineering bioinspired bacteria-adhesive clay nanoparticles with a membrane-disruptive property for the treatment of Helicobacter pylori infection. Nanoscale. 2016;8:16486–16498. doi: 10.1039/C6NR05551F
  • Ma J, Jiang L, Liu G. Cell membrane-coated nanoparticles for the treatment of bacterial infection. WIREs Nanomed Nanobiotechnol. 2022;14(5):e1825. doi: 10.1002/wnan.1825
  • Meng Z, Pan L, Qian S, et al. Materials & Design Antimicrobial peptide nanoparticles coated with macrophage cell membrane for targeted antimicrobial therapy of sepsis. Mater Des. 2023;229:111883. doi: 10.1016/j.matdes.2023.111883
  • Ghosh M, Miller PA, Möllmann U, et al. Targeted Antibiotic Delivery: Selective Siderophore Conjugation with Daptomycin Confers Potent Activity against Multidrug Resistant Acinetobacter baumannii Both in vitro and in vivo. J Med Chem. 2017;60:4577–4583. doi: 10.1021/acs.jmedchem.7b00102
  • Oh S-H, Park H-S, Kim H-S, et al. Antimicrobial activities of LCB10-0200, a novel siderophore cephalosporin, against the clinical isolates of Pseudomonas aeruginosa and other pathogens. Int J Antimicrob Agents. 2017;50:700–706. doi: 10.1016/j.ijantimicag.2017.06.001
  • Tang L, Chen X, Tong Q, et al. Biocompatible, bacteria-targeting resveratrol nanoparticles fabricated by Mannich molecular condensation for accelerating infected wound healing. J Mater Chem B. 2022;10:9280–9294. doi: 10.1039/D2TB01697D
  • Hu C-M, Fang RH, Wang K-C, et al. Nanoparticle biointerfacing by platelet membrane cloaking. Nature. 2015;526(7571):118–121. doi: 10.1038/nature15373

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.