COMBINATION OF ANTIBIOTICS AND BACTERIOPHAGES TO COMBAT ANTIBIOTIC-RESISTANT MICROORGANISMS

Authors

DOI:

https://doi.org/10.11603/1681-2727.2024.3.14669

Keywords:

bacteriophages, phage-antibiotic synergy

Abstract

Despite antibiotics being the main method of combating bacterial infections today, the rapid emergence and prevalence of antibiotic resistance generate interest in alternative and supplementary antimicrobial strategies, particularly concerning infections caused by MDR, PDR, and XDR microorganisms. In recent decades, research has been conducted on the use of bacteriophages (phages) and antibiotics either separately or in combination, both in vitro and in vivo. The materials presented in the review indicate the synergistic action of phages and antibiotics when used in combination, although some experiments have shown indifferent effects and even antagonism between phages and antibiotics. Strategies involving the combination of phages and antibiotics are promising, especially concerning biofilms, including their mature forms.

Author Biographies

V. P. Shyrobokov, О. О. Bogomolets National Medical University

Academician of the NAS and NAMS of Ukraine, Professor, MD, Honored Scientist and Technician, Head of the Department of Microbiology and Parasitology with Basics of Immunology

 

V. A. Poniatovskyi , О. О. Bogomolets National Medical University

PhD, Doctoral Candidate at the Department of Microbiology and Parasitology

 

References

Sait World Health Organization. Retrieved from https://www.who.int/news/item/22-06-2022-22-06-2022-lack-of-innovation-set-to-undermine-antibiotic-performance-and-health-gains.

Murray, C. J., Ikuta, K. S., Sharara, F., Swetschinski, L., Aguilar, G. R., Gray, A., et al. (2022). Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. The Lancet, 399(10325), 629-655.

Antimicrobial resistance surveillance in Europe 2023-2021 data (2023). Stockholm: European Centre for Disease Prevention and Control and World Health Organization.

Kuzin, I., Matskov, O., Bondar, R., Lapin, R., Vovk, T., Howard, A., et al. (2023). Notes from the Field: Responding to the Wartime Spread of Antimicrobial-Resistant Organisms — Ukraine, 2022. MMWR Morb Mortal Wkly Rep, 72, 1333-1334.

Chanishvili, N. (2012). Phage therapy – history from twort and d’Herelle through Soviet experience to current approaches. Advances in Virus Research, 83, 3-40.

Waller, A. S., Yamada, T., Kristensen, D. M., Kultima, J. R., Sunagawa, S., Koonin, E. V., et al. (2014). Classification and quantification of bacteriophage taxa in human gut metagenomes. The ISME Journal, 8(7), 1391-1402.

US Food and Drug Administration (2006). Food additives permitted for direct addition to food for human consumption; bacteriophage preparation. US Food and Drug Administration, Silver Spring, MD.

Chung, K. M., Nang, S. C., & Tang, S. S. (2023). The safety of bacteriophages in treatment of diseases caused by multidrug-resistant bacteria. Pharmaceuticals, 16(10), 1347.

Kaur, G., Agarwal, R. & Sharma, R. K. (2021). Bacteriophage therapy for critical and high-priority antibiotic-resistant bacteria and phage cocktail-antibiotic formulation perspective. Food and Environmental Virology, 13(4), 433-446.

Zurabov, F., Glazunov, E., Kochetova, T., Uskevich, V., & Popova, V. (2023). Bacteriophages with depolymerase activity in the control of antibiotic resistant Klebsiella pneumoniae biofilms. Scientific Reports, 13, 15188.

Maimaiti, Z., Li, Z., Xu, C., Chen, J., Chai, W. (2023). Global trends and hotspots of phage therapy for bacterial infection: A bibliometric visualized analysis from 2001 to 2021. Frontiers in Microbiology, 13, 1067803.

Arias, C. F., Acosta, F. J., Bertocchini, F., Herrero, M. A., & Fernández-Arias, C. (2022). The coordination of anti-phage immunity mechanisms in bacterial cells. Nature Communications, 13(1), 7412.

Himmelweit, F. (1945). Combined Action of Penicillin and Bacteriophage on Staphylococci. The Lancet, 246(6361), 104-105.

Bulssico, J., PapukashvilI, I., Espinosa, L., Gandon, S., & Ansaldi, M. (2023). Phage-antibiotic synergy: Cell filamentation is a key driver of successful phage predation. PLOS Pathogens, 19(9), e1011602.

Chhibber, S., Kaur, T. & Kaur, S. (2013). Co-therapy using lytic bacteriophage and linezolid: Effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS ONE, 8(2), e56022.

Torres-Barceló, C., & Hochberg, M. E. (2016). Evolutionary Rationale for Phages as Complements of Antibiotics. Trends in Microbiology, 24(4), 249-256.

Zaytzeff-Jern, H., Meleney, F. L. (1941). Studies on phage VI. the effect of sulfapyridine and sulfanilamides on staphylococci and B. coli and their respective phages. J. Lab. Clin. Med., 26, 1756-1767.

Krueger, A. P., Cohn, T., Noble, N. (1947). Effect of Penicillin on the Reaction Between Phage and Staphylococci. Experimental Biology and Medicine, 66(1), 204-205.

Hagens, S., Habel, A., & Bläsi, U. (2006). Augmentation of the Antimicrobial Efficacy of Antibiotics by Filamentous Phage. Microbial Drug Resistance, 12(3), 164-168.

Comeau, A. M., Tétart, F., Trojet, S. N., Prère, M.-F., & Krisch, H. M. (2007). Phage-Antibiotic Synergy (PAS): β-Lactam and Quinolone Antibiotics Stimulate Virulent Phage Growth. PLoS ONE, 2(8), e799.

De Soir, S., Parée, H., Kamarudin, N. H. N., Wagemans, J., Lavigne, R., Braem, A., et al. (2024). Exploiting phage-antibiotic synergies to disrupt Pseudomonas aeruginosa PAO1 biofilms in the context of orthopedic infections. Microbiology Spectrum, 12(1), e03219-23.

Liu, Y., Zhao, Y., Qian, C., Huang, Z., Feng, L., Chen, L. et al. (2023). Study of Combined Effect of Bacteriophage vB3530 and Chlorhexidine on the Inactivation of Pseudomonas aeruginosa. BMC Microbiology, 23(1), 256.

Abdraimova, N., Shitikov, E., Gorodnichev, R., & Kornienko, M. (2023). Combination of bacteriophages and antibiotics as the most effective therapy against Staphylococcus aureus. Medicine of Extreme Situations, 25(2023(4)), 37-44.

Necel, A., Bloch, S., Topka-Bielecka, G., Janiszewska, A., Łukasiak, A., Nejman-Faleńczyk, B. et al. (2022). Synergistic Effects of Bacteriophage vB_Eco4-M7 and Selected Antibiotics on the Biofilm Formed by Shiga Toxin-Producing Escherichia coli. Antibiotics, 11(6), 712.

Gordillo Altamirano, F. L., Kostoulias, X., Subedi, D., Korneev, D., Peleg, A. Y., & Barr, J. J. (2022). Phage-antibiotic combination is a superior treatment against Acinetobacter baumannii in a preclinical study. EBioMedicine, 80, 104045.

Eskenazi, A., Lood, C., Wubbolts, J., Hites, M., Balarjishvili, N., Leshkasheli, L., et al. (2022). Combination of pre-adapted bacteriophage therapy and antibiotics for treatment of fracture-related infection due to pandrug-resistant Klebsiella pneumoniae. Nature Communications, 13(1), 302.

Bulssico, J., PapukashvilI, I., Espinosa, L., Gandon, S., & Ansaldi, M. (2023). Phage-antibiotic synergy: Cell filamentation is a key driver of successful phage predation. PLOS Pathogens, 19(9), e1011602.

Chhibber, S., Kaur, T. & Kaur, S. (2013). Co-therapy using lytic bacteriophage and linezolid: Effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS ONE, 8(2), e56022.

Kaur, S., Harjai, K., & Chhibber, S. (2016). In Vivo Assessment of Phage and Linezolid Based Implant Coatings for Treatment of Methicillin Resistant S. aureus (MRSA) Mediated Orthopaedic Device Related Infections. PLOS ONE, 11(6), e0157626.

Kamal, F., & Dennis, J. J. (2015). Burkholderia cepacia Complex Phage-Antibiotic Synergy (PAS): Antibiotics Stimulate Lytic Phage Activity. Applied and Environmental Microbiology, 81(3), 1132-1138.

Li, Y., Xiao, P., Wang, Y., Hao, Y. (2020). Mechanisms and Control Measures of Mature Biofilm Resistance to Antimicrobial Agents in the Clinical Context. ACS Omega, 5(36), 22684-22690.

Kumaran, D., Taha, M., Yi, Q., Ramirez-Arcos, S., Diallo, J., Carli, A. et al. (2018). Does Treatment Order Matter? Investigating the Ability of Bacteriophage to Augment Antibiotic Activity against Sta­phylococcus aureus Biofilms. Frontiers in Microbiology, 9(127), 1-11.

Nakamura, S., Nii, F., Shimizu, M., & Watanabe, I. (1971). Inhibition of Phage Growth by an Antibiotic Rugulosin Isolated from Myrothecium verucaria. Japanese Journal of Microbiology, 15(2), 113-120.

Kever, L., Hardy, A., Luthe, T., Hünnefeld, M., Gätgens, C., Milke, L. et al. (2022). Aminoglycoside antibiotics inhibit phage infection by blocking an early step of the infection cycle. mBio, 13(3), e00783-22.

Akturk, E., Melo, L. D. R., Oliveira, H., Crabbé, A., Coenye, T., & Azeredo, J. (2023). Combining phages and antibiotic to enhance antibiofilm efficacy against an in vitro dual species wound biofilm. Biofilm, 6, 100147.

Meier, D., & Hofschneider, P. H. (1972). Effect of rifampicin on the growth of RNA bacteriophage M12. FEBS Letters, 25(1), 179-183.

Geiduschek, E., Sklar, J. (1969). Role of Host RNA Polymerase in Phage Development: Continual Requirement for a Host RNA Polymerase Component in a Bacteriophage Development. Nature, 221, 833-836.

Rahman, M., Kim, S., Kim, S. M., Seol, S. Y., & Kim, J. (2011). Characterization of induced Staphylococcus aureus bacteriophage SAP-26 and its anti-biofilm activity with rifampicin. Biofouling, 27(10), 1087-1093.

Pons, B. J., van Houte, S., Westra, E. R., Chevallereau, A. (2023). Ecology and evolution of phages encoding anti-CRISPR proteins. Journal of Molecular Biology, 435(7), 167974.

Dimitriu, T., Kurilovich, E., Łapińska, U., Severinov, K., Pagliara, S., Szczelkun, M. D., et al. (2022). Bacteriostatic antibiotics promote CRISPR-cas adaptive immunity by enabling increased spacer acquisition. Cell Host Microbe, 30(1), 31-40.

Segall, A. M., Roach, D. R., & Strathdee, S. A. (2019). Stronger together? Perspectives on phage-antibiotic synergy in clinical applications of phage therapy. Current Opinion in Microbiology, 51, 46-50.

Gordillo Altamirano, F. L., Kostoulias, X., Subedi, D., Korneev, D., Peleg, A. Y., & Barr, J. J. (2022). Phage-antibiotic combination is a superior treatment against Acinetobacter baumannii in a preclinical study. EBioMedicine, 80, 104045.

Stachurska, X., Roszak, M., Jabłońska, J., Mizielińska, M., & Nawrotek, P. (2021). Double-Layer Agar (DLA) Modifications for the First Step of the Phage-Antibiotic Synergy (PAS) Identification. Antibiotics, 10(11), 1306.

Published

2024-10-11

How to Cite

Shyrobokov, V. P., & Poniatovskyi , V. A. (2024). COMBINATION OF ANTIBIOTICS AND BACTERIOPHAGES TO COMBAT ANTIBIOTIC-RESISTANT MICROORGANISMS. Infectious Diseases – Infektsiyni Khvoroby, (3), 4–10. https://doi.org/10.11603/1681-2727.2024.3.14669

Issue

Section

Editorial