2023 / 04

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DOI: 10.47183/mes.2023.058

REVIEW

Combination of bacteriophages and antibiotics as the most effective therapy against Staphylococcus aureus

Abdraimova NK, Shitikov EA, Gorodnichev RB, Kornienko MA
About authors

Lopukhin Federal Research and Clinical Center of Physical-Chemical Medicine of the Federal Medical Biological Agency, Moscow, Russia

Correspondence should be addressed: Narina K. Abdraimova
Malaya Pirogovskaya, 1a, Moscow, 119435, Russia; moc.liamg@aniranavomiardba

About paper

Funding: the work was supported by the Russian Science Foundation grant No. 22-15-00443, https://rscf.ru/project/22-15-00443/

Author contribution: Abdraimova NK — analysis of literature, article authoring and editing, approval of its final version; Shitikov EA — analysis of literature, article authoring and editing, approval of its final version; Gorodnichev RB — article editing, approval of its final version; Kornienko MA — conceptualization, analysis of literature, article authoring and editing, approval of its final version.

Received: 2023-10-20 Accepted: 2023-12-05 Published online: 2023-12-31
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  1. Wagenlehner FME, Dittmar F. Re: global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Eur Urol. 2022; 82 (6): 658.
  2. Gherardi G. Staphylococcus aureus infection: pathogenesis and antimicrobial resistance. Int J Mol Sci. 2023; 24 (9): 81–82.
  3. Fishovitz J, Hermoso JA, Chang M., Mobashery S. PenicillinBinding Protein 2a of Methicillin-Resistant Staphylococcus aureus. IUBMB Life. 2014; 66: 572–7.
  4. McGuinness WA, Malachowa N, DeLeo FR. Vancomycin resistance in Staphylococcus aureus. Yale J. Biol. Med. 2017; 90: 269–81.
  5. Burdett V. Tet(M)-promoted release of tetracycline from ribosomes is GTP dependent. J Bacteriol. 1996; 178: 3246–51.
  6. Locke JB, Hilgers M, Shaw, KJ. Novel Ribosomal Mutations in Staphylococcus aureus Strains Identified through Selection with the Oxazolidinones Linezolid and Torezolid (TR-700). Antimicrob Agents Chemother. 2009; 53: 5265–74.
  7. Jensen SO, Lyon BR. Genetics of antimicrobial resistance in Staphylococcus aureus. Future Microbiol. 2009; 4: 565–82.
  8. Dashtbani-Roozbehani A, Brown MH. Efflux Pump Mediated Antimicrobial Resistance by Staphylococci in Health-Related Environments: Challenges and the Quest for Inhibition. Antibiot Basel Switz. 2021; 10: 1502.
  9. Idrees M, Sawant S, Karodia N, Rahman A. Staphylococcus aureus biofilm: morphology, genetics, pathogenesis and treatment strategies. Int J Environ Res Public Health. 2021; 18: 7602.
  10. Tikunova NV, Voroshilova NN, Polygach OA, Morozova VV, Tikunov AY, Kurilshhikov AM, et al. Genetic characteristics and range of antibacterial activity of the bacteriophages, which are a part of manufactured serie of drugs — pyobacteriophage polyvalent purified. Epidemiology and Vaccinal Prevention. 2016; 15 (2 (87)): 93–100. Russian.
  11. Nikolich MP, Filippov AA. Bacteriophage therapy: developments and directions. Antibiotics. 2020; 9: 135.
  12. Lin DM, Koskella B, Lin HC. Phage therapy: An alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol. Ther. 2017; 8: 162–73.
  13. Kebriaei R, Lev KL, Stamper KC, Lehman SM, Morales S, Rybak MJ. Bacteriophage AB-SA01 Cocktail in Combination with Antibiotics against MRSA-VISA Strain in an In Vitro Pharmacokinetic/Pharmacodynamic Model. Antimicrob Agents Chemother. 2021; 65 (1): e01863-20.
  14. Abdraimova NK, Kornienko MA, Bespiatykh DA, Kuptsov NS, Gorodnichev RB, Shitikov EA. Combined effects of bacteriophage vB_SauM-515A1 and antibiotics on the Staphylococcus aureus clinical isolates. Bulletin of RSMU. 2022; (5): 23–30. Russian.
  15. Simon K, Pier W, Krüttgen A, Horz HP. Synergy between Phage Sb-1 and Oxacillin against Methicillin-Resistant Staphylococcus aureus. Antibiotics. 2021; 10 (7): 849.
  16. Dickey J, Perrot V. Adjunct phage treatment enhances the effectiveness of low antibiotic concentration against Staphylococcus aureus biofilms in vitro. PloS One. 2019; 14 (1): e0209390.
  17. Zaytzeff-Jern H, Meleney FL. Studies in bacteriophage VI: The effect of sulfapyridine and sulfanilamide on staphylococci and E. Coli and their respective bacteriophages. J Lab Clin Med. 1941; 26: 1756–67.
  18. Macneal WJ, Spence MJ, Blevins A. Cure of experimental staphylococcal meningitis. Exp Biol Med. 1942; 50: 176–9.
  19. Himmelweit F. Combined action of penicillin and phage on staphylococci. Lancet. 1945; 246: 104–5.
  20. Diallo K, Dublanchet A. A century of clinical use of phages: a literature review. Antibiotics (Basel). 2023; 12 (4): 751.
  21. Comeau AM, Tétart F, Trojet SN, Prère MF, Krisch HM. PhageAntibiotic Synergy (PAS): beta-lactam and quinolone antibiotics stimulate virulent phage growth. PloS One. 2007; 2 (8): e799.
  22. Vashisth M, Yashveer S, Anand T, Virmani N, Bera BC, Vaid RK. Antibiotics targeting bacterial protein synthesis reduce the lytic activity of bacteriophages. Virus Res. 2022; 321: 198909.
  23. Rahman M, Kim S, Kim SM, Seol SY, Kim J. Characterization of induced Staphylococcus aureus bacteriophage SAP-26 and its anti-biofilm activity with rifampicin. Biofouling. 2011; 27 (10): 1087–93.
  24. Kumaran D, Taha M, Yi Q, et al. Does treatment order matter? Investigating the ability of bacteriophage to augment antibiotic activity against Staphylococcus aureus biofilms. Front Microbiol. 2018; 9: 127.
  25. Kirby AE. Synergistic action of gentamicin and bacteriophage in a continuous culture population of Staphylococcus aureus. PLoS One. 2012; 7 (11): e51017.
  26. Wang L, Tkhilaishvili T, Trampuz A. Adjunctive Use of Phage Sb-1 in Antibiotics Enhances Inhibitory Biofilm Growth Activity versus Rifampin-Resistant Staphylococcus aureus Strains. Antibiotics (Basel). 2020; 9 (11): 749.
  27. Chhibber S, Kaur T, Sandeep Kaur. Co-therapy using lytic bacteriophage and linezolid: effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS One. 2013; 8 (2): e56022.
  28. Prazak J, Iten M, Cameron DR, et al. Bacteriophages Improve Outcomes in Experimental Staphylococcus aureus Ventilatorassociated Pneumonia. Am J Respir Crit Care Med. 2019; 200 (9): 1126–33.
  29. Save J, Que YA, Entenza JM, Kolenda C, Laurent F, Resch G. Bacteriophages combined with subtherapeutic doses of flucloxacillin act synergistically against Staphylococcus aureus experimental infective endocarditis. J Am Heart Assoc. 2022; 11 (3): e023080.
  30. Kornienko M, Kuptsov N, Gorodnichev R, et al. Contribution of Podoviridae and Myoviridae bacteriophages to the effectiveness of anti-staphylococcal therapeutic cocktails. Sci Rep. 2020; 10 (1): 18612.
  31. Li X, Hu T, Wei J, et al. Characterization of a Novel Bacteriophage Henu2 and Evaluation of the Synergistic Antibacterial Activity of Phage-Antibiotics. Antibiotics (Basel). 2021; 10 (2): 174.
  32. Kim M, Jo Y, Hwang YJ, et al. Phage-Antibiotic Synergy via Delayed Lysis. Appl Environ Microbiol. 2018; 84 (22): e02085-18.
  33. Kebriaei R, Lev K, Morrisette T, Stamper KC, Abdul-Mutakabbir JC, Lehman SM, et al. Bacteriophage-Antibiotic Combination Strategy: an Alternative against Methicillin-Resistant Phenotypes of Staphylococcus aureus. Antimicrob Agents Chemother. 2020; 64 (7): e00461-20.
  34. Berryhill BA, Huseby DL, McCall IC, Hughes D, Levin BR. Evaluating the potential efficacy and limitations of a phage for joint antibiotic and phage therapy of Staphylococcus aureus infections. Proc Natl Acad Sci USA. 2021; 118 (10): e2008007118.
  35. Loganathan A, Manohar P, Nachimuthu R. Phage-antibiotic combination: an effective method for eradication of Staphylococcus aureus. bioRxiv. Available from: https://www.biorxiv.org/content/1 0.1101/2023.03.27.534482v2.
  36. Gilbert P, Maira-Litran T, McBain AJ, Rickard AH, Whyte FW. The physiology and collective recalcitrance of microbial biofilm communities. Adv Microb Physiol. 2002; 46: 202–56.
  37. Archer NK, Mazaitis MJ, Costerton JW, Leid JG, Powers ME, Shirtliff ME. Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence. 2011; 2 (5): 445–59.
  38. Costerton JW, Montanaro L, Arciola CR. Biofilm in implant infections: its production and regulation. Int J Artif Organs. 2005; 28 (11): 1062–8.
  39. Oliveira WF, Silva PMS, Silva RCS, et al. Staphylococcus aureus and Staphylococcus epidermidis infections on implants. J Hosp Infect. 2018; 98 (2): 111–7.
  40. Cho OH, Bae IG, Moon SM, Park SY, Kwak YG, Kim BN, et al. Therapeutic outcome of spinal implant infections caused by Staphylococcus aureus: A retrospective observational study. Medicine (Baltimore). 2018; 97 (40): e12629.
  41. Kaur S, Harjai K, Chhibber S. Bacteriophage mediated killing of Staphylococcus aureus in vitro on orthopaedic K wires in presence of linezolid prevents implant colonization. PLoS One. 2014; 9 (3): e90411.
  42. Joo H, Wu SM, Soni I, Wang-Crocker C, Matern T, Beck JP, et al. Phage and Antibiotic Combinations Reduce Staphylococcus aureus in Static and Dynamic Biofilms Grown on an Implant Material. Viruses. 2023; 15 (2): 460.
  43. Taha M, Arnaud T, Lightly TJ, Peters D, Wang L, Chen W, et al. Combining bacteriophage and vancomycin is efficacious against MRSA biofilm-like aggregates formed in synovial fluid. Front Med (Lausanne). 2023; 10: 1134912.
  44. Akturk E, Oliveira H, Santos SB, Costa S, Kuyumcu S, Melo LDR, et al. Synergistic Action of Phage and Antibiotics: Parameters to Enhance the Killing Efficacy Against Mono and Dual-Species Biofilms. Antibiotics (Basel). 2019; 8 (3): 103.
  45. Doub JB, Ng VY, Lee M, Chi A, Lee A, Würstle S, et al. Salphage: Salvage Bacteriophage Therapy for Recalcitrant MRSA Prosthetic Joint Infection. Antibiotics (Basel). 2022; 11 (5): 616.
  46. Yilmaz C, Colak M, Yilmaz BC, Ersoz G, Kutateladze M, Gozlugol M. Bacteriophage therapy in implant-related infections: an experimental study. J Bone Joint Surg Am. 2013; 95 (2): 117–25.
  47. Gilbey T, Ho J, Cooley LA, Petrovic Fabijan A, Iredell JR. Adjunctive bacteriophage therapy for prosthetic valve endocarditis due to Staphylococcus aureus. Med J Aust. 2019; 211 (3): 142-143.e1.
  48. Aslam S, Pretorius V, Lehman SM, Morales S, Schooley RT. Novel bacteriophage therapy for treatment of left ventricular assist device infection. J Heart Lung Transplant. 2019; 38 (4): 475–6.
  49. Ramirez-Sanchez C, Gonzales F, Buckley M, Biswas B, Henry M, Deschenes MV, et al. Successful treatment of Staphylococcus aureus prosthetic joint infection with bacteriophage therapy. Viruses. 2021; 13 (6): 1182.