Phage Therapy in Traumatology: A Review on Perspectives for Treating Acute Wounds and Post-Surgical Complications
DOI:
https://doi.org/10.15407/microbiolj86.05.117Keywords:
pathogenic microbiota, bacteriophages, phage therapy, bacterial complications, purulent wounds, gunshot and mine-explosive injuries, antibiotic resistanceAbstract
Full-scale hostilities in Ukraine led to an unprecedented number of victims with serious injuries, including gunshot wounds, broken bones, and mine-explosive injuries. Wound infections are one of the main causes of non-combat losses of personnel. A prerequisite for the development of a wound infection, among other things, is high microbial contamination of combat wounds. Major bacteria causing such infections are staphylococci (Staphylococcus aureus, S. epidermidis), streptococci (Streptococcus pyogenes, St. agalictiae), enterococci (Enterococcus faecalis), gram-negative bacteria (Pseudomonas aeruginosa, Escherichia coli, Klebsiella pneumoniae, Acinetobacter baumannii), anaerobic bacteria (Clostridium perfringens, Bacterioides spp.), etc. Modern data indicate a change in the current species composition of causative agents of wound infections, an increase both in the polyresistance of the microbiota to antibacterial drugs and in the frequency of biofilm formation protecting pathogenic microorganisms from antimicrobial therapy and the patient’s immune response. Such purulent bacterial infections require new approaches to therapy. Taking into account the large number of combat injuries in Ukraine, the use of bacteriophages as specific agents for the biological control of pathogenic microbiota is of particular importance. In view of the nature of injuries, phage preparations intended for the treatment of purulent-surgical infections of wound and burn surfaces are considered the most promising and in demand today. This review summarizes modern data on the use of phage preparations in clinics and in orthopedics and traumatology in particular. Issues of the delivery of phages to the focus of infection, their effective dose, duration of therapy, and the possibility of combining it with antibiotic therapy are discussed. Information about phage therapy programs that have already been implemented in some countries is presented. The advantages and disadvantages of the use of bacteriophages for personalized therapy of severe patients are highlighted, and the prospects for further research are indicated.
Downloads
References
Abbas, M., Holmes, A., & Price, J. (2020). Surgical site infections following elective surgery. The Lancet Infectious Diseases, 20(8), 898-899. https://doi.org/10.1016/S1473-3099(20)30524-7
Abdul-Hassan, H.S., El-Tahan, K., Massoud, B., Gomaa, R. (1990). Bacteriophage therapy of Pseudomonas burn wound sepsis. Ann Med Burn Club, 3, 262-264.
Abedon, S. T., Danis-Wlodarczyk, K. M., & Alves, D. R. (2021). Phage therapy in the 21st century: is there modern, clinical evidence of phage-mediated efficacy? Pharmaceuticals, 14(11), 1157. https://doi.org/10.3390/ph14111157
Abedon, S. T., Kuhl, S. J., Blasdel, B. G., & Kutter, E. M. (2011). Phage treatment of human infections. Bacteriophage, 1(2), 66-85. https://doi.org/10.4161/bact.1.2.15845
Albee, F.H. (1933). The Bacteriophage in Infections of Bones and Joints. The Scientific Monthly, 37(6), 535-540.
Al-Mayahi, M., Betz, M., Müller, D. A., Stern, R., Tahintzi, P., Bernard, L., ... & Uçkay, I. (2013). Remission rate of implant-related infections following revision surgery after fractures. International orthopaedics, 37, 2253-2258. https://doi.org/10.1007/s00264-013-2092-1
Arthur, T. M., Kalchayanand, N., Agga, G. E., Wheeler, T. L., & Koohmaraie, M. (2017). Evaluation of bacteriophage application to cattle in lairage at beef processing plants to reduce Escherichia coli O157: H7 prevalence on hides and carcasses. Foodborne pathogens and disease, 14(1), 17-22. https://doi.org/10.1089/fpd.2016.2189
Azevedo, M. M., Pina-Vaz, C., & Rodrigues, A. G. (2022). The role of phage therapy in burn wound infections management: advantages and pitfalls. Journal of Burn Care & Research, 43(2), 336-342. https://doi.org/10.1093/jbcr/irab175
Barki, K. G., Das, A., Dixith, S., Ghatak, P. D., Mathew-Steiner, S., Schwab, E., ... & Sen, C. K. (2019). Electric field based dressing disrupts mixed-species bacterial biofilm infection and restores functional wound healing. Annals of surgery, 269(4), 756-766. https://doi.org/10.1097/SLA.0000000000002504
Barshes, N. R., Mindru, C., Ashong, C., Rodriguez-Barradas, M., & Trautner, B. W. (2016). Treatment failure and leg amputation among patients with foot osteomyelitis. The International Journal of Lower Extremity Wounds, 15(4), 303-312. https://doi.org/10.1177/1534734616661058
Bean, J. E., Alves, D. R., Laabei, M., Esteban, P. P., Thet, N. T., Enright, M. C., & Jenkins, A. T. A. (2014). Triggered release of bacteriophage K from agarose/hyaluronan hydrogel matrixes by Staphylococcus aureus virulence factors. Chemistry of Materials, 26(24), 7201-7208. https://doi.org/10.1021/cm503974g
Bruttin, A., & Brüssow, H. (2005). Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrobial agents and chemotherapy, 49(7), 2874-2878. https://doi.org/10.1128/AAC.49.7.2874-2878.2005
Cano, E. J., Caflisch, K. M., Bollyky, P. L., Van Belleghem, J. D., Patel, R., Fackler, J., ... & Suh, G. A. (2021). Phage therapy for limb-threatening prosthetic knee Klebsiella pneumoniae infection: case report and in vitro characterization of anti-biofilm activity. Clinical Infectious Diseases, 73(1), e144-e151. https://doi.org/10.1093/cid/ciaa705
Chaney, S. B., Ganesh, K., Mathew‐Steiner, S., Stromberg, P., Roy, S., Sen, C. K., & Wozniak, D. J. (2017). Histopathological comparisons of Staphylococcus aureus and Pseudomonas aeruginosa experimental infected porcine burn wounds. Wound Repair and Regeneration, 25(3), 541-549. https://doi.org/10.1111/wrr.12527
Chang, R. Y. K., Morales, S., Okamoto, Y., & Chan, H. K. (2020). Topical application of bacteriophages for treatment of wound infections. Translational Research, 220, 153-166. https://doi.org/10.1016/j.trsl.2020.03.010
Chanishvili, N. (2012). Phage therapy-history from Twort and d'Herelle through Soviet experience to current approaches. Advances in virus research, 83, 3-40. https://doi.org/10.1016/B978-0-12-394438-2.00001-3
Cornett, E., Downey, A., & Berwick, D. (Eds.). (2016). A national trauma care system: integrating military and civilian trauma systems to achieve zero preventable deaths after injury. National Academies Press.
D'Herelle, F. (1917). Sur un microbe invisible antagoniste des bacilles dysenteriques. C R Acad Sci, 65, 373-375.
Dash, A., & Mohapatra, S. (2020). Surveillance of bacterial infections and their antibiotic resistance patterns in orthopaedic trauma surgeries at a tertiary care teaching hospital. International Journal of Orthopaedics, 6(1), 545-549. https://doi.org/10.22271/ortho.2020.v6.i1j.1920
Dedrick, R. M., Smith, B. E., Cristinziano, M., Freeman, K. G., Jacobs-Sera, D., Belessis, Y., ... & Hatfull, G. F. (2023). Phage therapy of Mycobacterium infections: compassionate use of phages in 20 patients with drug-resistant mycobacterial disease. Clinical infectious diseases, 76(1), 103-112. https://doi.org/10.1093/cid/ciac453
Del Pozo, J. L., & Patel, R. (2007). The challenge of treating biofilm‐associated bacterial infections. Clinical Pharmacology & Therapeutics, 82(2), 204-209. https://doi.org/10.1038/sj.clpt.6100247
Duan, Y., Young, R., & Schnabl, B. (2022). Bacteriophages and their potential for treatment of gastrointestinal diseases. Nature reviews Gastroenterology & hepatology, 19(2), 135-144. https://doi.org/10.1038/s41575-021-00536-z
Eisner, R., Lippmann, N., Josten, C., Rodloff, A. C., & Behrendt, D. (2020). Development of the bacterial spectrum and antimicrobial resistance in surgical site infections of trauma patients. Surgical Infections, 21(8), 684-693. https://doi.org/10.1089/sur.2019.158
Engeman, E., Freyberger, H. R., Corey, B. W., Ward, A. M., He, Y., Nikolich, M. P., ... & Jacobs, A. C. (2021). Synergistic killing and re-sensitization of Pseudomonas aeruginosa to antibiotics by phage-antibiotic combination treatment. Pharmaceuticals, 14(3), 184. https://doi.org/10.3390/ph14030184
Ferry, T., Boucher, F., Fevre, C., Perpoint, T., Chateau, J., Petitjean, C., ... & Laurent, F. (2018b). Innovations for the treatment of a complex bone and joint infection due to XDR Pseudomonas aeruginosa including local application of a selected cocktail of bacteriophages. Journal of Antimicrobial Chemotherapy, 73(10), 2901-2903. https://doi.org/10.1093/jac/dky263
Ferry, T., Kolenda, C., Batailler, C., Gaillard, R., Gustave, C. A., Lustig, S., ... & Lyon BJI Study group. (2021). Case report: arthroscopic "debridement antibiotics and implant retention" with local injection of personalized phage therapy to salvage a relapsing Pseudomonas aeruginosa prosthetic knee infection. Frontiers in Medicine, 8, 569159. https://doi.org/10.3389/fmed.2021.569159
Ferry, T., Kolenda, C., Batailler, C., Gustave, C. A., Lustig, S., Malatray, M., ... & Laurent, F. (2020). Phage therapy as adjuvant to conservative surgery and antibiotics to salvage patients with relapsing S. aureus prosthetic knee infection. Frontiers in Medicine, 7, 570572. https://doi.org/10.3389/fmed.2020.570572
Ferry, T., Leboucher, G., Fevre, C., Herry, Y., Conrad, A., Josse, J., ... & Laurent, F. (2018a). Salvage debridement, antibiotics and implant retention ("DAIR") with local injection of a selected cocktail of bacteriophages: is it an option for an elderly patient with relapsing Staphylococcus aureus prosthetic-joint infection? Open forum infectious diseases. 5 (11), 269. https://doi.org/10.1093/ofid/ofy269
Fish, R., Kutter, E., Bryan, D., Wheat, G., & Kuhl, S. (2018). Resolving digital staphylococcal osteomyelitis using bacteriophage - A case report. Antibiotics, 7(4), 87. https://doi.org/10.3390/antibiotics7040087
Fish, R., Kutter, E., Wheat, G., Blasdel, B., Kutateladze, M., & Kuhl, S. (2016). Bacteriophage treatment of intransigent diabetic toe ulcers: a case series. Journal of wound care, 25(Sup7), S27-S33. https://doi.org/10.12968/jowc.2016.25.7.S27
Fleming, A. (1929). On the antibacterial action of cultures of a penicillium, with special reference to their use in the isolation of B. influenzae. British journal of experimental pathology, 10(3), 226.
Flowers, L., & Grice, E. A. (2020). The skin microbiota: balancing risk and reward. Cell host & microbe, 28(2), 190-200. https://doi.org/10.1016/j.chom.2020.06.017
Fujiki, J., Nakamura, K., Nakamura, T., & Iwano, H. (2023). Fitness Trade-Offs between Phage and Antibiotic Sensitivity in Phage-Resistant Variants: Molecular Action and Insights into Clinical Applications for Phage Therapy. International Journal of Molecular Sciences, 24(21), 15628. https://doi.org/10.3390/ijms242115628
Gordillo Altamirano, F. L., & Barr, J. J. (2019). Phage therapy in the postantibiotic era. Clinical microbiology reviews, 32(2), 10-1128. https://doi.org/10.1128/CMR.00066-18
Gu Liu, C., Green, S. I., Min, L., Clark, J. R., Salazar, K. C., Terwilliger, A. L., ... & Maresso, A. W. (2020). Phage-antibiotic synergy is driven by a unique combination of antibacterial mechanism of action and stoichiometry. MBio, 11(4), 10-1128. https://doi.org/10.1128/mBio.01462-20
Guest, J. F., Fuller, G. W., & Vowden, P. (2020). Cohort study evaluating the burden of wounds to the UK's National Health Service in 2017/2018: update from 2012/2013. BMJ open, 10(12), e045253. https://doi.org/10.1136/bmjopen-2020-045253
Haddad Kashani, H., Schmelcher, M., Sabzalipoor, H., Seyed Hosseini, E., & Moniri, R. (2018). Recombinant endolysins as potential therapeutics against antibiotic-resistant Staphylococcus aureus: current status of research and novel delivery strategies. Clinical microbiology reviews, 31(1), 10-1128. https://doi.org/10.1128/CMR.00071-17
Hathaway, H., Alves, D. R., Bean, J., Esteban, P. P., Ouadi, K., Sutton, J. M., & Jenkins, A. T. A. (2015). Poly (N-isopropylacrylamide-co-allylamine)(PNIPAM-co-ALA) nanospheres for the thermally triggered release of Bacteriophage K. European Journal of Pharmaceutics and Biopharmaceutics, 96, 437-441. https://doi.org/10.1016/j.ejpb.2015.09.013
Infectious Disease Clinical Research Program. (2020). Wound infections. Uniformed Services University of the Health Sciences Infectious Disease Clinical Research Program. https://idcrp.usuhs.edu/research-areas/wound-infections
Jain, R. K., Shukla, R., Singh, P., & Kumar, R. (2015). Epidemiology and risk factors for surgical site infections in patients requiring orthopedic surgery. European Journal of Orthopaedic Surgery & Traumatology, 25, 251-254. https://doi.org/10.1007/s00590-014-1475-3
Jault, P., Leclerc, T., Jennes, S., Pirnay, J. P., Que, Y. A., Resch, G., ... & Gabard, J. (2019). Efficacy and tolerability of a cocktail of bacteriophages to treat burn wounds infected by Pseudomonas aeruginosa (PhagoBurn): a randomised, controlled, double-blind phase 1/2 trial. The Lancet Infectious Diseases, 19(1), 35-45. https://doi.org/10.1016/S1473-3099(18)30482-1
Jeong, T. H., Hong, H. W., Kim, M. S., Song, M., & Myung, H. (2023). Characterization of three different endolysins effective against Gram-negative bacteria. Viruses, 15(3), 679. https://doi.org/10.3390/v15030679
Jikia, D., Chkhaidze, N., Imedashvili, E., Mgaloblishvili, I., Tsitlanadze, G., Katsarava, R., ... & Sulakvelidze, A. (2005). The use of a novel biodegradable preparation capable of the sustained release of bacteriophages and ciprofloxacin, in the complex treatment of multidrug‐resistant Staphylococcus aureus‐infected local radiation injuries caused by exposure to Sr90. Clinical and experimental dermatology, 30(1), 23-26. https://doi.org/10.1111/j.1365-2230.2004.01600.x
Kharina, A., Snihur, H., Andriichuk, O., Pozhylov, I., Budzanivska, I., Korniienko, N., Liutko, O., Linenko, O., Moysa, I., Poniatovskyi, V., & Shevchenko, O. Pathogenic microbiota correlating with the purulent-inflammatory processes after gunshot wounds, bone fractures and mine-explosive injuries during the war activities in Ukraine. Proceedings of the 10th International Conference 'Bioresources and Viruses', 11-13 September 2023, Kyiv, Ukraine, p.42.
Khomenko, I. P., Korol, S. O., Khalik, S. V., Shapovalov, V. Y., Yenin, R. V., Нerasimenko, O. S., & Tertyshnyі S. V. (2021). Clinical and Epidemiological analysis of the structure of combat surgical injury during Antiterrorist operation / Joint Forces Operation. Ukrainian Journal of Military Medicine, 2(2), 5-13. https://doi.org/10.46847/ujmm.2021.2(2)-005
Kim, H. Y., Chang, R. Y. K., Morales, S., & Chan, H. K. (2021). Bacteriophage-delivering hydrogels: Current progress in combating antibiotic resistant bacterial infection. Antibiotics, 10(2), 130. https://doi.org/10.3390/antibiotics10020130
Klyackiy, Y. P., Tribyshnoy, O. V., Tryfanov, I. I., & Kosilo, V. V. (2022). Treatment of purulous-inflammatory complications of bullet and mine explosive injuries of extremities. Modern medical technology, 3, 60-65. https://doi.org/10.34287/MMT.3(54).2022.11
Kumari, S., Harjai, K., & Chhibber, S. (2010). Topical treatment of Klebsiella pneumoniae B5055 induced burn wound infection in mice using natural products. The Journal of Infection in Developing Countries, 4(06), 367-377. https://doi.org/10.3855/jidc.312
Kyrylenko T. (2023). During the war: how many Ukrainians die and are injured at work. Mirror of the Week. URL: https://zn.ua/ukr/UKRAINE/pid-chas-vijni-skilki-ukrajintsiv-hinut-i-travmujutsja-na-roboti.html
Labrie, S. J., Samson, J. E., & Moineau, S. (2010). Bacteriophage resistance mechanisms. Nature Reviews Microbiology, 8(5), 317-327. https://doi.org/10.1038/nrmicro2315
Lauman, P., & Dennis, J. J. (2021). Advances in phage therapy: targeting the Burkholderia cepacia complex. Viruses, 13(7), 1331. https://doi.org/10.3390/v13071331
LaVergne, S., Hamilton, T., Biswas, B., Kumaraswamy, M., Schooley, R. T., & Wooten, D. (2018). Phage therapy for a multidrug-resistant Acinetobacter baumannii craniectomy site infection. Open forum infectious diseases. 5(4), ofy064. https://doi.org/10.1093/ofid/ofy064
Lecion, D., Fortuna, W., Dąbrowska, K., Międzybrodzki, R., Weber-Dąbrowska, B., & Górski, A. (2013). Application of microbiological quantitative methods for evaluation of changes in the amount of bacteria in patients with wounds and purulent fistulas subjected to phage therapy and for assessment of phage preparation effectiveness (in vitro studies). Advances in Medical Sciences, 58(2), 257-264. https://doi.org/10.2478/ams-2013-0004
Leverentz, B., Conway, W. S., Janisiewicz, W., & Camp, M. J. (2004). Optimizing concentration and timing of a phage spray application to reduce Listeria monocytogenes on honeydew melon tissue. Journal of food protection, 67(8), 1682-1686. https://doi.org/10.4315/0362-028X-67.8.1682
Lienard, A., Hosny, M., Jneid, J., Schuldiner, S., Cellier, N., Sotto, A., ... & Pantel, A. (2021). Escherichia coli isolated from diabetic foot osteomyelitis: clonal diversity, resistance profile, virulence potential, and genome adaptation. Microorganisms, 9(2), 380. https://doi.org/10.3390/microorganisms9020380
Lu, Y., Cai, W. J., Ren, Z., & Han, P. (2022). The role of Staphylococcal biofilm on the surface of implants in orthopedic infection. Microorganisms, 10(10), 1909. https://doi.org/10.3390/microorganisms10101909
Luo, J., Xie, L., Yang, M., Liu, M., Li, Q., Wang, P., ... & Luo, C. (2023). Synergistic antibacterial effect of phage pB3074 in combination with antibiotics targeting cell wall against multidrug-resistant Acinetobacter baumannii in vitro and ex vivo. Microbiology Spectrum, 11(4), e00341-23. https://doi.org/10.1128/spectrum.00341-23
Mäntynen, S., Laanto, E., Oksanen, H. M., Poranen, M. M., & Díaz-Muñoz, S. L. (2021). Black box of phage-bacterium interactions: Exploring alternative phage infection strategies. Open biology, 11(9), 210188. https://doi.org/10.1098/rsob.210188
Mavrich, T. N., & Hatfull, G. F. (2019). Evolution of superinfection immunity in cluster A mycobacteriophages. MBio, 10(3), 10-1128. https://doi.org/10.1128/mBio.00971-19
Mosselhy, D. A., Assad, M., Sironen, T., & Elbahri, M. (2021). Nanotheranostics: a possible solution for drug-resistant Staphylococcus aureus and their biofilms? Nanomaterials, 11(1), 82. https://doi.org/10.3390/nano11010082
Motififard, M., Teimouri, M., Shirani, K., Hatami, S., & Yadegari, M. (2021). Prevalence of Bacterial surgical site infection in traumatic patients undergoing orthopedic surgeries: a cross-sectional study. International Journal of Burns and Trauma, 11(3), 191. https://doi.org/10.4103/abr.abr_235_21
Mukhopadhyay, S., To, K. K., Liu, Y., Bai, C., & Leung, S. S. (2024). A thermosensitive hydrogel formulation of phage and colistin combination for the management of multidrug-resistant Acinetobacter baumannii wound infections. Biomaterials Science, 12(1), 151-163. https://doi.org/10.1039/D3BM01383A
Murray, E., Draper, L. A., Ross, R. P., & Hill, C. (2021). The advantages and challenges of using endolysins in a clinical setting. Viruses, 13(4), 680. https://doi.org/10.3390/v13040680
Nadareishvili, L., Hoyle, N., Nakaidze, N., Nizharadze, D., Kutateladze, M., Balarjishvili, N., ... & Pruidze, N. (2020). Bacteriophage therapy as a potential management option for surgical wound infections. Phage, 1(3), 158-165. https://doi.org/10.1089/phage.2020.0010
Nir-Paz, R., Gelman, D., Khouri, A., Sisson, B. M., Fackler, J., Alkalay-Oren, S., ... & Hazan, R. (2019). Successful treatment of antibiotic-resistant, poly-microbial bone infection with bacteriophages and antibiotics combination. Clinical infectious diseases, 69(11), 2015-2018. https://doi.org/10.1093/cid/ciz222
O'Flaherty, S., Ross, R. P., Meaney, W., Fitzgerald, G. F., Elbreki, M. F., & Coffey, A. (2005). Potential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals. Applied and environmental microbiology, 71(4), 1836-1842. https://doi.org/10.1128/AEM.71.4.1836-1842.2005
Onsea, J., Soentjens, P., Djebara, S., Merabishvili, M., Depypere, M., Spriet, I., ... & Metsemakers, W. J. (2019). Bacteriophage application for difficult-to-treat musculoskeletal infections: development of a standardized multidisciplinary treatment protocol. Viruses, 11(10), 891. https://doi.org/10.3390/v11100891
Pancevski, B. (2023). In Ukraine, Amputations Already Evoke Scale of World War I. The Wall Street Journal. URL: https://www.wsj.com/articles/in-ukraine-a-surge-in-amputations-reveals-the-human-cost-of-russias-war-d0bca320
Peel, T. N., & de Steiger, R. (2020). How to manage treatment failure in prosthetic joint infection. Clinical Microbiology and Infection, 26(11), 1473-1480. https://doi.org/10.1016/j.cmi.2020.06.022
Peterson, C. (2021). Economic cost of injury-United States, 2019. MMWR. Morbidity and Mortality Weekly Report, 70. https://doi.org/10.15585/mmwr.mm7048a1
Petrovic Fabijan, A., Lin, R. C., Ho, J., Maddocks, S., Ben Zakour, N. L., Iredell, J. R., & Westmead. (2020). Bacteriophage Therapy Team Khalid Ali 1 3 Venturini Carola 1 3 Chard Richard 3 7 Morales Sandra 8 Sandaradura Indy 2 3 Gilbey Tim 2. Safety of bacteriophage therapy in severe Staphylococcus aureus infection. Nature microbiology, 5(3), 465-472. https://doi.org/10.1038/s41564-019-0634-z
Pirnay, J. P., Ferry, T., & Resch, G. (2022). Recent progress toward the implementation of phage therapy in Western medicine. FEMS microbiology reviews, 46(1), fuab040. https://doi.org/10.1093/femsre/fuab040
Pirnay, J. P., Verbeken, G., Ceyssens, P. J., Huys, I., De Vos, D., Ameloot, C., & Fauconnier, A. (2018). The magistral phage. Viruses, 10(2), 64. https://doi.org/10.3390/v10020064
Pliska, N. N. (2020). Pseudomonas aeruginosa as the main causative agent of osteomyelitis and its susceptibility to antibiotics. Drug Research, 70(06), 280-285. https://doi.org/10.1055/a-1150-2372
Rahman, M. U., Wang, W., Sun, Q., Shah, J. A., Li, C., Sun, Y., ... & Wang, S. (2021). Endolysin, a promising solution against antimicrobial resistance. Antibiotics, 10(11), 1277. https://doi.org/10.3390/antibiotics10111277
Ramirez-Sanchez, C., Gonzales, F., Buckley, M., Biswas, B., Henry, M., Deschenes, M. V., ... & Aslam, S. (2021). Successful treatment of Staphylococcus aureus prosthetic joint infection with bacteriophage therapy. Viruses, 13(6), 1182. https://doi.org/10.3390/v13061182
Roach, D. R., Leung, C. Y., Henry, M., Morello, E., Singh, D., Di Santo, J. P., ... & Debarbieux, L. (2017). Synergy between the host immune system and bacteriophage is essential for successful phage therapy against an acute respiratory pathogen. Cell host & microbe, 22(1), 38-47. https://doi.org/10.1016/j.chom.2017.06.018
Ronayne, E. A., Wan, Y. S., Boudreau, B. A., Landick, R., & Cox, M. M. (2016). P1 Ref endonuclease: a molecular mechanism for phage-enhanced antibiotic lethality. PLoS genetics, 12(1), e1005797. https://doi.org/10.1371/journal.pgen.1005797
Roy, S., Elgharably, H., Sinha, M., Ganesh, K., Chaney, S., Mann, E., ... & Sen, C. K. (2014). Mixed‐species biofilm compromises wound healing by disrupting epidermal barrier function. The Journal of pathology, 233(4), 331-343. https://doi.org/10.1002/path.4360
Roy, S., Santra, S., Das, A., Dixith, S., Sinha, M., Ghatak, S., ... & Sen, C. K. (2020). Staphylococcus aureus biofilm infection compromises wound healing by causing deficiencies in granulation tissue collagen. Annals of surgery, 271(6), 1174-1185. https://doi.org/10.1097/SLA.0000000000003053
Sandar, W. P., Saw, S., Kumar, A. M., Camara, B. S., & Sein, M. M. (2021). Wounds, antimicrobial resistance and challenges of implementing a surveillance system in Myanmar: a mixed-methods study. Tropical medicine and infectious disease, 6(2), 80. https://doi.org/10.3390/tropicalmed6020080
Schmitt, D. S., Siegel, S. D., & Selle, K. (2023). Applications of designer phage encoding recombinant gene payloads. Trends in Biotechnology. https://doi.org/10.1016/j.tibtech.2023.09.008
Sebeny, P. J., Riddle, M. S., & Petersen, K. (2008). Acinetobacter baumannii skin and soft-tissue infection associated with war trauma. Clinical Infectious Diseases, 47(4), 444-449. https://doi.org/10.1086/590568
Secor, P. R., Burgener, E. B., Kinnersley, M., Jennings, L. K., Roman-Cruz, V., Popescu, M., ... & Bollyky, P. L. (2020). Pf bacteriophage and their impact on Pseudomonas virulence, mammalian immunity, and chronic infections. Frontiers in immunology, 11, 244. https://doi.org/10.3389/fimmu.2020.00244
Sen, C. K. (2021). Human wound and its burden: updated 2020 compendium of estimates. Advances in wound care, 10(5), 281-292. https://doi.org/10.1089/wound.2021.0026
Senneville, E., Joulie, D., Legout, L., Valette, M., Dezeque, H., Beltrand, E., ... & Migaud, H. (2011). Outcome and predictors of treatment failure in total hip/knee prosthetic joint infections due to Staphylococcus aureus. Clinical infectious diseases, 53(4), 334-340. https://doi.org/10.1093/cid/cir402
Shelton, W. L., Krause, P. C., Fox, R., Lowe, M., de Latin, L., Leonardi, C., ... & Wichern, E. (2023). Risk of infection following gunshot wound fractures to the foot and ankle: a multicenter retrospective study. The Journal of Foot and Ankle Surgery, 62(1), 50-54. https://doi.org/10.1053/j.jfas.2022.03.011
Slopek, S., Weber-Dabrowska, B., Dabrowski, M., & Kucharewicz-Krukowska, A. (1987). Results of bacteriophage treatment of suppurative bacterial infections in the years 1981-1986. Archivum immunologiae et therapiae experimentalis, 35(5), 569-583.
Solomenny A.N. (2021). Determination of qualitative composition of modern wound-healing drugs for the needs of the medical service of the Armed Forces of the Ukraine for the peace time and the special period. UJMM. 2(3), 93-102. https://doi.org/10.46847/ujmm.2021.3(2)-093
Soothill, J. S. (1994). Bacteriophage prevents destruction of skin grafts by Pseudomonas aeruginosa. Burns, 20(3), 209-211. https://doi.org/10.1016/0305-4179(94)90184-8
Stewart, L., Li, P., Blyth, M. D. M., Campbell, W. R., Petfield, J. L., Krauss, M., ... & Tribble, D. R. (2020). Antibiotic practice patterns for extremity wound infections among blast-injured subjects. Military medicine, 185(Supplement 1), 628-636. https://doi.org/10.1093/milmed/usz211
Strathdee, S. A., Hatfull, G. F., Mutalik, V. K., & Schooley, R. T. (2023). Phage therapy: From biological mechanisms to future directions. Cell, 186(1), 17-31. https://doi.org/10.1016/j.cell.2022.11.017
Summers, W. C. (2012). The strange history of phage therapy. Bacteriophage, 2(2), 130-133. https://doi.org/10.4161/bact.20757
Taati Moghadam, M., Khoshbayan, A., Chegini, Z., Farahani, I., & Shariati, A. (2020). Bacteriophages, a new therapeutic solution for inhibiting multidrug-resistant bacteria causing wound infection: lesson from animal models and clinical trials. Drug design, development and therapy, 1867-1883. https://doi.org/10.2147/DDDT.S251171
Tagliaferri, T. L., Jansen, M., & Horz, H. P. (2019). Fighting pathogenic bacteria on two fronts: phages and antibiotics as combined strategy. Frontiers in cellular and infection microbiology, 9, 22. https://doi.org/10.3389/fcimb.2019.00022
Tkhilaishvili, T., Winkler, T., Müller, M., Perka, C., & Trampuz, A. (2019). Bacteriophages as adjuvant to antibiotics for the treatment of periprosthetic joint infection caused by multidrug-resistant Pseudomonas aeruginosa. Antimicrobial agents and chemotherapy, 64(1), 10-1128. https://doi.org/10.1128/AAC.00924-19
Urish, K. L., & Cassat, J. E. (2020). Staphylococcus aureus osteomyelitis: bone, bugs, and surgery. Infection and immunity, 88(7), 10-1128. https://doi.org/10.1128/IAI.00932-19
Van Belleghem, J. D., Dąbrowska, K., Vaneechoutte, M., Barr, J. J., & Bollyky, P. L. (2018). Interactions between bacteriophage, bacteria, and the mammalian immune system. Viruses, 11(1), 10. https://doi.org/10.3390/v11010010
van der Vlugt, R. A., & Verbeek, M. (2008). Bacteriophages: therapeuticals and alternative applications: Onderzoeksrapport commissie genetische modificatie (No. 2008-03). Cogem. https://edepot.wur.nl/139007
Verbeken, G., & Pirnay, J. P. (2022). European regulatory aspects of phage therapy: Magistral phage preparations. Current Opinion in Virology, 52, 24-29. https://doi.org/10.1016/j.coviro.2021.11.005
Wright, A., Hawkins, C. H., Änggård, E. E., & Harper, D. R. (2009). A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic‐resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clinical otolaryngology, 34(4), 349-357. https://doi.org/10.1111/j.1749-4486.2009.01973.x
Wu, Y. K., Cheng, N. C., & Cheng, C. M. (2019). Biofilms in chronic wounds: pathogenesis and diagnosis. Trends in biotechnology, 37(5), 505-517. https://doi.org/10.1016/j.tibtech.2018.10.011
Yan, W., Banerjee, P., Liu, Y., Mi, Z., Bai, C., Hu, H., ... & Leung, S. S. (2021). Development of thermosensitive hydrogel wound dressing containing Acinetobacter baumannii phage against wound infections. International journal of pharmaceutics, 602, 120508. https://doi.org/10.1016/j.ijpharm.2021.120508
Zarutskyi, Y. L., & Shudrak, A. A. (Eds). (2014). Instructions for military field surgery. Kyiv: SPD Chaplynska NV.
Zavhorodnii, S. M., Kotenko, O. I., Danyliuk, M. B., & Kubrak, M. A. (2023). Surgical treatment of isolated soft tissue gunshot shrapnel injuries by combining primary delayed sutures with platelet-rich autoplasma injections into mine-explosive wounds. Zaporozhye мedical journal, 25(4), 339-345. https://doi.org/10.14739/2310-1210.2023.4.269875
Zheliba, M. D., Verba, A. V., Bohush, H. L., Martsynkovskyy, I. P., Kondratyuk, V. M., Kovalchuk, V. P., ... & Fomina, N. S. (2019). Microbiological aspects of limbs wound infection and its complex treatment with the use of vacuum-therapy in persons injured in war actions. Modern medical technology, (3), 50-55. https://doi.org/10.34287/MMT.3(42).2019.4
Downloads
Published
Issue
Section
License
Copyright (c) 2024 Mikrobiolohichnyi Zhurnal

This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.