Bacteriophages, a New Therapeutic Solution for Inhibiting Multidrug-Resistant Bacteria Causing Wound Infection: Lesson from Animal Models and Clinical Trials

References

• SimõesD, MiguelSP, RibeiroMP, CoutinhoP, MendonçaAG, CorreiaIJ. Recent advances on antimicrobial wound dressing: a review. Eur j Pharm Biopharm. 2018;127:130–141. doi:10.1016/j.ejpb.2018.02.02229462687
   PubMed Web of Science ®Google Scholar
• ChuaAWC, KhooYC, TanBK, TanKC, FooCL, ChongSJ. Skin tissue engineering advances in severe burns: review and therapeutic applications. Burns Trauma. 2016;4(1):3. doi:10.1186/s41038-016-0027-y27574673
   PubMed Web of Science ®Google Scholar
• FijanS, FrauwallnerA, LangerholcT, et al. Efficacy of using probiotics with antagonistic activity against pathogens of wound infections: an integrative review of literature. Biomed Res Int. 2019;2019.
   Web of Science ®Google Scholar
• BowlerP, DuerdenB, ArmstrongDG. Wound microbiology and associated approaches to wound management. Clin Microbiol Rev. 2001;14(2):244–269. doi:10.1128/CMR.14.2.244-269.200111292638
   PubMed Web of Science ®Google Scholar
• WuX-D, Liu-M-M, LiangX, HuN, HuangW. Effects of perioperative supplementation with pro-/synbiotics on clinical outcomes in surgical patients: a meta-analysis with trial sequential analysis of randomized controlled trials. Clin Nutri. 2018;37(2):505–515. doi:10.1016/j.clnu.2016.10.015
   PubMed Web of Science ®Google Scholar
• BurnhamJP, KirbyJP, KollefMH. Diagnosis and management of skin and soft tissue infections in the intensive care unit: a review. Intensive Care Med. 2016;42(12):1899–1911. doi:10.1007/s00134-016-4576-027699456
   PubMed Web of Science ®Google Scholar
• CardonaAF, WilsonSE. Skin and soft-tissue infections: a critical review and the role of telavancin in their treatment. Clin Infect Dis. 2015;61(suppl_2):S69–S78. doi:10.1093/cid/civ52826316560
   PubMed Web of Science ®Google Scholar
• ShariatiA, MoradabadiA, AzimiT, Ghaznavi-RadE. Wound healing properties and antimicrobial activity of platelet-derived biomaterials. Sci Rep. 2020;10(1):1–9. doi:10.1038/s41598-020-57559-w31913322
   PubMed Web of Science ®Google Scholar
• AndonovaM, UrumovaV. Immune surveillance mechanisms of the skin against the stealth infection strategy of Pseudomonas aeruginosa. Comp Immunol Microbiol Infect Dis. 2013;36(5):433–448. doi:10.1016/j.cimid.2013.03.00323602428
   PubMed Web of Science ®Google Scholar
• ShariatiA, AsadianE, FallahF, et al. Evaluation of Nano-curcumin effects on expression levels of virulence genes and biofilm production of multidrug-resistant Pseudomonas aeruginosa isolated from burn wound infection in Tehran, Iran. Infect Drug Resist. 2019;12:2223. doi:10.2147/IDR.S21320031440064
   PubMed Web of Science ®Google Scholar
• MurrayPM, FinegoldSM. Anaerobes in burn-wound infections. Rev Infect Dis. 1984;6(Supplement_1):S184–S186. doi:10.1093/clinids/6.Supplement_1.S1846372027
   PubMedGoogle Scholar
• GlikJ, KaweckiM, GaździkT, NowakM. The impact of the types of microorganisms isolated from blood and wounds on the results of treatment in burn patients with sepsis. Polish J Surg. 2012;84(1):6–16. doi:10.2478/v10035-012-0002-7
   Google Scholar
• BahramianA, KhoshnoodS, ShariatiA, DoustdarF, ChiraniAS, HeidaryM. Molecular characterization of the pilS2 gene and its association with the frequency of Pseudomonas aeruginosa plasmid pKLC102 and PAPI-1 pathogenicity island. Infect Drug Resist. 2019;12:221. doi:10.2147/IDR.S18852730666137
   PubMed Web of Science ®Google Scholar
• ShafiqM, HuangJ, RahmanSU, et al. High incidence of multidrug-resistant Escherichia coli coharboring mcr-1 and blaCTX-M-15 recovered from pigs. Infect Drug Resist. 2019;12:2135. doi:10.2147/IDR.S20947331410033
   PubMed Web of Science ®Google Scholar
• AbatC, FournierP-E, JimenoM-T, RolainJ-M, RaoultD. Extremely and pandrug-resistant bacteria extra-deaths: myth or reality? Eur J Clin Microbiol Infect Dis. 2018;37(9):1687–1697. doi:10.1007/s10096-018-3300-029956024
   PubMed Web of Science ®Google Scholar
• KwiatekM, ParasionS, NakoniecznaA. Therapeutic bacteriophages as a rescue treatment for drug‐resistant infections–an in vivo studies overview. J Appl Microbiol. 2019.
   PubMed Web of Science ®Google Scholar
• KutterE, KuhlS, AlavidzeZ, BlasdelB. Phage therapy: bacteriophages as natural, self-limiting antibiotics. Textbook Nat Med. 2005;112:945–956.
   Google Scholar
• SevgiM, TokluA, VecchioD. R Hamblin M. Topical antimicrobials for burn infections–an update. Recent Pat Antiinfect Drug Discov. 2013;8(3):161–197. doi:10.2174/1574891X0866613111214344724215506
   PubMedGoogle Scholar
• CooperR, Kirketerp-MøllerK. Non-antibiotic antimicrobial interventions and antimicrobial stewardship in wound care. J Wound Care. 2018;27(6):355–377. doi:10.12968/jowc.2018.27.6.35529883284
   PubMed Web of Science ®Google Scholar
• TsiourisCG, KelesiM, VasilopoulosG, KalemikerakisI, PapageorgiouEG. The efficacy of probiotics as pharmacological treatment of cutaneous wounds: meta-analysis of animal studies. Eur J Pharm Sci. 2017;104:230–239. doi:10.1016/j.ejps.2017.04.00228392493
   PubMed Web of Science ®Google Scholar
• MoghadamMT, AmirmozafariN, ShariatiA, et al. How phages overcome the challenges of drug resistant bacteria in clinical infections. Infect Drug Resist. 2020;13:45. doi:10.2147/IDR.S23435332021319
   PubMed Web of Science ®Google Scholar
• AzimiT, MosadeghM, NasiriMJ, SabourS, KarimaeiS, NasserA. Phage therapy as a renewed therapeutic approach to mycobacterial infections: a comprehensive review. Infect Drug Resist. 2019;12:2943. doi:10.2147/IDR.S21863831571947
   PubMed Web of Science ®Google Scholar
• MatsuzakiS, RashelM, UchiyamaJ, et al. Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J Infect Chemother. 2005;11(5):211–219. doi:10.1007/s10156-005-0408-916258815
   PubMedGoogle Scholar
• KumariS, HarjaiK, ChhibberS. Efficacy of bacteriophage treatment in murine burn wound infection induced by Klebsiella pneumoniae. J Microbiol Biotechnol. 2009;19(6):622–628. doi:10.4014/jmb.0808.49319597322
   PubMed Web of Science ®Google Scholar
• FalagasME, BliziotisIA, KasiakouSK, SamonisG, AthanassopoulouP, MichalopoulosA. Outcome of infections due to pandrug-resistant (PDR) Gram-negative bacteria. BMC Infect Dis. 2005;5(1):24. doi:10.1186/1471-2334-5-2415819983
   PubMed Web of Science ®Google Scholar
• KunkalekarR, PrabhuM, NaikM, SalkerA. Silver-doped manganese dioxide and trioxide nanoparticles inhibit both gram positive and gram negative pathogenic bacteria. Colloids Surf B Biointerfaces. 2014;113:429–434. doi:10.1016/j.colsurfb.2013.09.03624140741
   PubMed Web of Science ®Google Scholar
• MoreheadMS, ScarbroughC. Emergence of global antibiotic resistance. Primary Care. 2018;45(3):467–484. doi:10.1016/j.pop.2018.05.00630115335
   PubMed Web of Science ®Google Scholar
• CollF, PhelanJ, Hill-CawthorneGA, et al. Genome-wide analysis of multi-and extensively drug-resistant Mycobacterium tuberculosis. Nat Genet. 2018;50(2):307–316. doi:10.1038/s41588-017-0029-029358649
   PubMed Web of Science ®Google Scholar
• AndersonDJ, ChenLF, WeberDJ, et al. Enhanced terminal room disinfection and acquisition and infection caused by multidrug-resistant organisms and Clostridium difficile (the Benefits of Enhanced Terminal Room Disinfection study): a cluster-randomised, multicentre, crossover study. The Lancet. 2017;389(10071):805–814. doi:10.1016/S0140-6736(16)31588-4
   PubMed Web of Science ®Google Scholar
• AzimiT, ShariatiA, FallahF, et al. Mycobacterium tuberculosis genotyping using MIRU-VNTR typing. J Mazandaran Univ Med Sci. 2017;27(149):40–48.
   Google Scholar
• PetersL, OlsonL, KhuDT, et al. Multiple antibiotic resistance as a risk factor for mortality and prolonged hospital stay: a cohort study among neonatal intensive care patients with hospital-acquired infections caused by gram-negative bacteria in Vietnam. PLoS One. 2019;14:5. doi:10.1371/journal.pone.0215666
   Web of Science ®Google Scholar
• RashelM, UchiyamaJ, UjiharaT, et al. Efficient elimination of multidrug-resistant Staphylococcus aureus by cloned lysin derived from bacteriophage ϕMR11. J Infect Dis. 2007;196(8):1237–1247. doi:10.1086/52130517955443
   PubMed Web of Science ®Google Scholar
• PallavaliRR, DegatiVL, LomadaD, ReddyMC, DurbakaVRP. Isolation and in vitro evaluation of bacteriophages against MDR-bacterial isolates from septic wound infections. PLoS One. 2017;12:7. doi:10.1371/journal.pone.0179245
   Web of Science ®Google Scholar
• MapesAC, TrautnerBW, LiaoKS, RamigRF. Development of expanded host range phage active on biofilms of multi-drug resistant Pseudomonas aeruginosa. Bacteriophage. 2016;6(1):e1096995. doi:10.1080/21597081.2015.109699527144083
   PubMedGoogle Scholar
• LarchéJ, PouillotF, EssohC, et al. Rapid identification of international multidrug resistant Pseudomonas aeruginosa clones by multiple locus VNTR analysis (MLVA) and investigation of their susceptibility to lytic bacteriophages. Antimicrob Agents Chemother. 2012. doi:10.1128/AAC.01233-12
   PubMed Web of Science ®Google Scholar
• ShokriD, Soleimani-DelfanA, FatemiSM. Assessment of phage cocktails with extended host range activity against antibiotic resistant strains of Pseudomonas aeruginosa. Comp Clin Path. 2017;26(2):417–422. doi:10.1007/s00580-016-2394-y
   Google Scholar
• Nir-PazR, GelmanD, KhouriA, et al. Successful treatment of antibiotic-resistant, poly-microbial bone infection with bacteriophages and antibiotics combination. Clin Infect Dis. 2019;69(11):2015–2018. doi:10.1093/cid/ciz22230869755
   PubMed Web of Science ®Google Scholar
• ShariatiA, AzimiT, ArdebiliA, et al. Insertional inactivation of oprD in carbapenem-resistant Pseudomonas aeruginosa strains isolated from burn patients in Tehran, Iran. New Microbes New Infect. 2018;21:75–80. doi:10.1016/j.nmni.2017.10.01329234497
   PubMedGoogle Scholar
• BertoyeA, GaillardL, CourtieuA. Adapted bacteriophages in the treatment of infections caused by antibiotic-resistant microorganisms. J Med Lyon. 1959;40(945):465.13655000
   PubMedGoogle Scholar
• BertoyeA, CourtieuA. Treatment of infections caused by pyocyanic bacilli with bacteriophages adapted by selection. J Med Lyon. 1960;41:739–751.13800030
   PubMedGoogle Scholar
• McVayCS, VelásquezM, FralickJA. Phage therapy of Pseudomonas aeruginosa infection in a mouse burn wound model. Antimicrob Agents Chemother. 2007;51(6):1934–1938. doi:10.1128/AAC.01028-0617387151
   PubMed Web of Science ®Google Scholar
• BasuS, AgarwalM, Kumar BhartiyaS, NathG, Kumar ShuklaV. An in vivo wound model utilizing bacteriophage therapy of pseudomonas aeruginosa biofilms. Ostomy Wound Manage. 2015;61(8):16–23.
   PubMedGoogle Scholar
• OliveiraA, SousaJC, SilvaAC, MeloLD, SillankorvaS. Chestnut honey and bacteriophage application to control Pseudomonas aeruginosa and Escherichia coli biofilms: evaluation in an ex vivo wound model. Front Microbiol. 2018;9:1725. doi:10.3389/fmicb.2018.0172530108574
   PubMed Web of Science ®Google Scholar
• SarhanWA, AzzazyHM. Apitherapeutics and phage-loaded nanofibers as wound dressings with enhanced wound healing and antibacterial activity. Nanomedicine. 2017;12(17):2055–2067. doi:10.2217/nnm-2017-015128805554
   PubMed Web of Science ®Google Scholar
• RazA, SerranoA, HernandezA, EulerCW, FischettiVA. Isolation of phage lysins that effectively kill Pseudomonas aeruginosa in mouse models of lung and skin infection. Antimicrob Agents Chemother. 2019;63(7):e00024–00019. doi:10.1128/AAC.00024-1931010858
   PubMed Web of Science ®Google Scholar
• SoothillJ. Bacteriophage prevents destruction of skin grafts by Pseudomonas aeruginosa. Burns. 1994;20(3):209–211. doi:10.1016/0305-4179(94)90184-88054131
   PubMed Web of Science ®Google Scholar
• HolguínA, RangelG, ClavijoV, et al. Phage ΦPan70, a putative temperate phage, controls Pseudomonas aeruginosa in planktonic, biofilm and burn mouse model assays. Viruses. 2015;7(8):4602–4623. doi:10.3390/v708283526274971
   PubMed Web of Science ®Google Scholar
• VieiraA, SilvaY, CunhaA, GomesN, AckermannH-W, AlmeidaA. Phage therapy to control multidrug-resistant Pseudomonas aeruginosa skin infections: in vitro and ex vivo experiments. Eur J Clin Microbiol Infect Dis. 2012;31(11):3241–3249. doi:10.1007/s10096-012-1691-x22777594
   PubMed Web of Science ®Google Scholar
• JaultP, LeclercT, JennesS, et al. 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. Lancet Infect Dis. 2019;19(1):35–45. doi:10.1016/S1473-3099(18)30482-130292481
   PubMed Web of Science ®Google Scholar
• Sivera MarzaJ, SoothillJ, BoydellP, CollynsT. Multiplication of therapeutically administered bacteriophages in Pseudomonas aeruginosa infected patients. Burns. 2006;32(5):644–646. doi:10.1016/j.burns.2006.02.01216781080
   PubMed Web of Science ®Google Scholar
• ChangRYK, DasT, ManosJ, KutterE, MoralesS, ChanH-K. Bacteriophage PEV20 and ciprofloxacin combination treatment enhances removal of Pseudomonas aeruginosa biofilm isolated from cystic fibrosis and wound patients. AAPS J. 2019;21(3):49. doi:10.1208/s12248-019-0315-030949776
   PubMed Web of Science ®Google Scholar
• TahaOA, ConnertonPL, ConnertonIF, El-ShibinyA. Bacteriophage ZCKP1: a potential treatment for Klebsiella pneumoniae isolated from diabetic foot patients. Front Microbiol. 2018;9:2127. doi:10.3389/fmicb.2018.0212730254618
   PubMed Web of Science ®Google Scholar
• BarrosJ, MeloLD, PoetaP, et al. Lytic bacteriophages against multidrug-resistant Staphylococcus aureus, Enterococcus faecalis and Escherichia coli isolates from orthopaedic implant-associated infections. Int J Antimicrob Agents. 2019;54(3):329–337. doi:10.1016/j.ijantimicag.2019.06.00731229670
   PubMed Web of Science ®Google Scholar
• JansenM, WahidaA, LatzS, et al. Enhanced antibacterial effect of the novel T4-like bacteriophage KARL-1 in combination with antibiotics against multi-drug resistant Acinetobacter baumannii. Sci Rep. 2018;8(1):1–12. doi:10.1038/s41598-018-32344-y29311619
   PubMed Web of Science ®Google Scholar
• CapparelliR, ParlatoM, BorrielloG, SalvatoreP, IannelliD. Experimental phage therapy against Staphylococcus aureus in mice. Antimicrob Agents Chemother. 2007;51(8):2765–2773. doi:10.1128/AAC.01513-0617517843
   PubMed Web of Science ®Google Scholar
• MorrisJL, LetsonHL, ElliottL, et al. Evaluation of bacteriophage as an adjunct therapy for treatment of peri-prosthetic joint infection caused by Staphylococcus aureus. PLoS One. 2019;14:12. doi:10.1371/journal.pone.0226574
   Web of Science ®Google Scholar
• LehmanSM, MearnsG, RankinD, et al. Design and preclinical development of a phage product for the treatment of antibiotic-resistant Staphylococcus aureus infections. Viruses. 2019;11(1):88. doi:10.3390/v11010088
   PubMed Web of Science ®Google Scholar
• Takemura-UchiyamaI, UchiyamaJ, OsanaiM, et al. Experimental phage therapy against lethal lung-derived septicemia caused by Staphylococcus aureus in mice. Microbes Infect. 2014;16(6):512–517. doi:10.1016/j.micinf.2014.02.01124631574
   PubMed Web of Science ®Google Scholar
• DingB, LiQ, GuoM, et al. Prevention of dermal abscess formation caused by Staphylococcus aureus using phage JD007 in nude mice. Front Microbiol. 2018;9:1553. doi:10.3389/fmicb.2018.0155330083139
   PubMed Web of Science ®Google Scholar
• WatanabeR, MatsumotoT, SanoG, et al. Efficacy of bacteriophage therapy against gut-derived sepsis caused by Pseudomonas aeruginosa in mice. Antimicrob Agents Chemother. 2007;51(2):446–452. doi:10.1128/AAC.00635-0617116686
   PubMed Web of Science ®Google Scholar
• FukudaK, IshidaW, UchiyamaJ, et al. Pseudomonas aeruginosa keratitis in mice: effects of topical bacteriophage KPP12 administration. PLoS One. 2012;7:10. doi:10.1371/journal.pone.0047742
   Web of Science ®Google Scholar
• WrightA, HawkinsC, ÄnggårdE, HarperD. 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. 2009;34(4):349–357. doi:10.1111/j.1749-4486.2009.01973.x19673983
   PubMed Web of Science ®Google Scholar
• WangJ, HuB, XuM, et al. Use of bacteriophage in the treatment of experimental animal bacteremia from imipenem-resistant Pseudomonas aeruginosa. Int J Mol Med. 2006;17(2):309–317.16391831
   PubMed Web of Science ®Google Scholar
• DuplessisC, BiswasB, HanischB, et al. Refractory Pseudomonas Bacteremia in a 2-year-old sterilized by bacteriophage therapy. J Pediatric Infect Dis Soc. 2018;7(3):253–256. doi:10.1093/jpids/pix05628992111
   PubMed Web of Science ®Google Scholar
• HuaY, LuoT, YangY, et al. Phage therapy as a promising new treatment for lung infection caused by carbapenem-resistant Acinetobacter baumannii in mice. Front Microbiol. 2018;8:2659. doi:10.3389/fmicb.2017.0265929375524
   PubMed Web of Science ®Google Scholar
• SchooleyRT, BiswasB, GillJJ, et al. Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother. 2017;61(10):e00954–00917. doi:10.1128/AAC.00954-1728807909
   PubMed Web of Science ®Google Scholar
• WangJ-L, KuoC-F, YehC-M, ChenJ-R, ChengM-F, HungC-H. Efficacy of φkm18p phage therapy in a murine model of extensively drug-resistant Acinetobacter baumannii infection. Infect Drug Resist. 2018;11:2301. doi:10.2147/IDR.S17970130532563
   PubMed Web of Science ®Google Scholar
• WangY, MiZ, NiuW, et al. Intranasal treatment with bacteriophage rescues mice from Acinetobacter baumannii-mediated pneumonia. Future Microbiol. 2016;11(5):631–641. doi:10.2217/fmb.16.1126925593
   PubMed Web of Science ®Google Scholar
• HungC-H, KuoC-F, WangC-H, WuC-M, TsaoN. Experimental phage therapy in treating Klebsiella pneumoniae-mediated liver abscesses and bacteremia in mice. Antimicrob Agents Chemother. 2011;55(4):1358–1365. doi:10.1128/AAC.01123-1021245450
   PubMed Web of Science ®Google Scholar
• CaoF, WangX, WangL, et al. Evaluation of the efficacy of a bacteriophage in the treatment of pneumonia induced by multidrug resistance Klebsiella pneumoniae in mice. Biomed Res Int. 2015;2015.
   Web of Science ®Google Scholar
• ChhibberS, KaurS, KumariS. Therapeutic potential of bacteriophage in treating Klebsiella pneumoniae B5055-mediated lobar pneumonia in mice. J Med Microbiol. 2008;57(12):1508–1513. doi:10.1099/jmm.0.2008/002873-019018021
   PubMed Web of Science ®Google Scholar
• AnandT, VirmaniN, KumarS, et al. Phage therapy for treatment of virulent Klebsiella pneumoniae infection in mouse model. J Global Antimicrob Resist. 2019.
   PubMedGoogle Scholar
• CorbellinoM, KiefferN, KutateladzeM, et al. Eradication of a multidrug-resistant, carbapenemase-producing klebsiella pneumoniae isolate following oral and intra-rectal therapy with a custom made, lytic bacteriophage preparation. Clin Infect Dis. 2019.
   Web of Science ®Google Scholar
• KhanA, XuM, WangT, et al. Catechol cross-linked antimicrobial peptide hydrogels prevent multidrug-resistant Acinetobacter baumannii infection in burn wounds. Biosci Rep. 2019;39:6. doi:10.1042/BSR20190504
   Web of Science ®Google Scholar
• GholamiM, HaghshenasM, MoshiriM, et al. Frequency of 16S rRNA methylase and aminoglycoside-modifying enzyme genes among clinical isolates of Acinetobacter baumannii in Iran. Iran J Pathol. 2017;12(4):329–338.29563928
   PubMedGoogle Scholar
• AminM, NavidifarT, ShooshtariFS, et al. Association between biofilm formation, structure, and the expression levels of genes related to biofilm formation and biofilm-specific resistance of acinetobacter baumannii strains isolated from burn infection in Ahvaz, Iran. Infect Drug Resist. 2019;12:3867. doi:10.2147/IDR.S22898131853190
   PubMed Web of Science ®Google Scholar
• RegeimbalJM, JacobsAC, CoreyBW, et al. Personalized therapeutic cocktail of wild environmental phages rescues mice from Acinetobacter baumannii wound infections. Antimicrob Agents Chemother. 2016;60(10):5806–5816. doi:10.1128/AAC.02877-1527431214
   PubMed Web of Science ®Google Scholar
• LeshkasheliL, KutateladzeM, BalarjishviliN, et al. Efficacy of newly isolated and highly potent bacteriophages in a mouse model of XDRAB bacteremia. J Global Antimicrob Resist. 2019;19:255–261. doi:10.1016/j.jgar.2019.05.005
   PubMed Web of Science ®Google Scholar
• YinS, HuangG, ZhangY, et al. Phage Abp1 rescues human cells and mice from infection by pan-drug resistant Acinetobacter baumannii. Cell Physiol Biochem. 2017;44(6):2337–2345. doi:10.1159/00048611729258062
   PubMedGoogle Scholar
• WuM, HuK, XieY, et al. A novel phage PD-6A3, and its endolysin Ply6A3, with extended lytic activity against Acinetobacter baumannii. Front Microbiol. 2019;9:3302. doi:10.3389/fmicb.2018.0330230687281
   PubMed Web of Science ®Google Scholar
• ShivaswamyVC, KalasuramathSB, SadanandCK, et al. Ability of bacteriophage in resolving wound infection caused by multidrug-resistant Acinetobacter baumannii in uncontrolled diabetic rats. Microbial Drug Resist. 2015;21(2):171–177. doi:10.1089/mdr.2014.0120
   PubMed Web of Science ®Google Scholar
• KusradzeI, KarumidzeN, RigvavaS, et al. Characterization and testing the efficiency of Acinetobacter baumannii phage vB-GEC_Ab-M-G7 as an antibacterial agent. Front Microbiol. 2016;7:1590. doi:10.3389/fmicb.2016.0159027757110
   PubMed Web of Science ®Google Scholar
• NorburyW, HerndonDN, TanksleyJ, JeschkeMG, FinnertyCC, Society SSCotSI. Infection in burns. Surg Infect (Larchmt). 2016;17(2):250–255. doi:10.1089/sur.2013.13426978531
   PubMed Web of Science ®Google Scholar
• ShahsavanS, EmaneiniM, KhoshgnabBN, et al. A high prevalence of mupirocin and macrolide resistance determinant among Staphylococcus aureus strains isolated from burnt patients. Burns. 2012;38(3):378–382. doi:10.1016/j.burns.2011.09.00422040930
   PubMed Web of Science ®Google Scholar
• KhosraviAD, HoveizaviH, FarshadzadehZ. The prevalence of genes encoding leukocidins in Staphylococcus aureus strains resistant and sensitive to methicillin isolated from burn patients in Taleghani Hospital, Ahvaz, Iran. Burns. 2012;38(2):247–251. doi:10.1016/j.burns.2011.08.00221924558
   PubMed Web of Science ®Google Scholar
• HashemiA, JaberiS, ShariatiA, et al. Identification of inducible clindamycin resistance in staphylococcus aureus strains isolated from hospitalized patients in hospitals of Tehran City (Iran). Qom Univ Med Sci J. 2018;11(12):52–60.
   Google Scholar
• MurrayCK, HolmesRL, EllisMW, et al. Twenty-five year epidemiology of invasive methicillin-resistant Staphylococcus aureus (MRSA) isolates recovered at a burn center. Burns. 2009;35(8):1112–1117. doi:10.1016/j.burns.2009.02.01319477601
   PubMed Web of Science ®Google Scholar
• PengC, HanawaT, AzamAH, et al. Silviavirus phage ɸMR003 displays a broad host range against methicillin-resistant Staphylococcus aureus of human origin. Appl Microbiol Biotechnol. 2019;103(18):7751–7765. doi:10.1007/s00253-019-10039-231388727
   PubMed Web of Science ®Google Scholar
• SethAK, GeringerMR, NguyenKT, et al. Bacteriophage therapy for Staphylococcus aureus biofilm–infected wounds: a new approach to chronic wound care. Plast Reconstr Surg. 2013;131(2):225–234. doi:10.1097/PRS.0b013e31827e47cd23357984
   PubMed Web of Science ®Google Scholar
• ChopraS, HarjaiK, ChhibberS. Potential of combination therapy of endolysin MR-10 and minocycline in treating MRSA induced systemic and localized burn wound infections in mice. Int J Med Microbiol. 2016;306(8):707–716. doi:10.1016/j.ijmm.2016.08.00327616281
   PubMed Web of Science ®Google Scholar
• ChhibberS, KaurJ, KaurS. Liposome entrapment of bacteriophages improves wound healing in a diabetic mouse MRSA infection. Front Microbiol. 2018;9:561. doi:10.3389/fmicb.2018.0056129651276
   PubMed Web of Science ®Google Scholar
• ChhibberS, KaurT, KaurS. 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. doi:10.1371/journal.pone.0056022
   Web of Science ®Google Scholar
• ChengM, ZhangL, ZhangH, et al. An ointment consisting of the phage lysin LysGH15 and apigenin for decolonization of methicillin-resistant Staphylococcus aureus from skin wounds. Viruses. 2018;10(5):244. doi:10.3390/v10050244
   PubMed Web of Science ®Google Scholar
• FishR, KutterE, WheatG, BlasdelB, KutateladzeM, KuhlS. Compassionate use of bacteriophage therapy for foot ulcer treatment as an effective step for moving toward clinical trials. Bacteriophage Ther Springer. 2018;159–170.
   Google Scholar
• FishR, KutterE, WheatG, BlasdelB, KutateladzeM, KuhlS. Bacteriophage treatment of intransigent diabetic toe ulcers: a case series. J Wound Care. 2016;25(Sup7):S27–S33. doi:10.12968/jowc.2016.25.Sup7.S2726949862
   PubMed Web of Science ®Google Scholar
• KiaeiS, MoradiM, NaveHH, HashemizadehZ, Taati-MoghadamM, Kalantar-NeyestanakiD. Emergence of co-existence of bla NDM with rmtC and qnrB genes in clinical carbapenem-resistant Klebsiella pneumoniae isolates in burning center from southeast of Iran. Folia Microbiol (Praha). 2019;64(1):55–62. doi:10.1007/s12223-018-0630-330003527
   PubMed Web of Science ®Google Scholar
• MoradiM, NorouziA, TaatimoghadamM. Prevalence of bla-CTX-M, bla-SHV, and bla-TEM Genes and comparison of antibiotic resistance pattern in extended-spectrum β-lactamase producing and non-producing groups of Klebsiella pneumoniae Isolated from Clinical Samples in Kerman Hospitals. J Fasa Univ Med Sci. 2016;6(1):120–128.
   Google Scholar
• SánchezM, HerruzoR, MarbánA, et al. Risk factors for outbreaks of multidrug-resistant Klebsiella pneumoniae in critical burn patients. J Burn Care Res. 2012;33(3):386–392. doi:10.1097/BCR.0b013e318231df9521979841
   PubMed Web of Science ®Google Scholar
• BahramianA, ShariatiA, AzimiT, et al. First report of New Delhi metallo-β-lactamase-6 (NDM-6) among Klebsiella pneumoniae ST147 strains isolated from dialysis patients in Iran. Infect Genet Evol. 2019;69:142–145. doi:10.1016/j.meegid.2019.01.03030684646
   PubMed Web of Science ®Google Scholar
• NasserS, MabroukA, MaherA. Colonization of burn wounds in Ain Shams University burn unit. Burns. 2003;29(3):229–233. doi:10.1016/S0305-4179(02)00285-112706615
   PubMed Web of Science ®Google Scholar
• BogovazovaG, VoroshilovaN, BondarenkoV. The efficacy of Klebsiella pneumoniae bacteriophage in the therapy of experimental Klebsiella infection. Zh Mikrobiol Epidemiol Immunobiol. 1991;(4):5–8.
   PubMed Web of Science ®Google Scholar
• MalikR, ChhibberS. Protection with bacteriophage KØ1 against fatal Klebsiella pneumoniae-induced burn wound infection in mice. J Microbiol Immunol Infect. 2009;42(2):134–140.19597645
   PubMedGoogle Scholar
• ChadhaP, KatareOP, ChhibberS. Liposome loaded phage cocktail: enhanced therapeutic potential in resolving Klebsiella pneumoniae mediated burn wound infections. Burns. 2017;43(7):1532–1543. doi:10.1016/j.burns.2017.03.02928502784
   PubMed Web of Science ®Google Scholar
• ChadhaP, KatareOP, ChhibberS. In vivo efficacy of single phage versus phage cocktail in resolving burn wound infection in BALB/c mice. Microb Pathog. 2016;99:68–77. doi:10.1016/j.micpath.2016.08.00127498362
   PubMed Web of Science ®Google Scholar
• KumariS, HarjaiK, ChhibberS. Bacteriophage versus antimicrobial agents for the treatment of murine burn wound infection caused by Klebsiella pneumoniae B5055. J Med Microbiol. 2011;60(2):205–210. doi:10.1099/jmm.0.018580-020965914
   PubMed Web of Science ®Google Scholar
• KumariS, HarjaiK, ChhibberS. Evidence to support the therapeutic potential of bacteriophage Kpn5 in burn wound infection caused by Klebsiella pneumoniae in BALB/c mice. J Microbiol Biotechnol. 2010;20(5):935–941. doi:10.4014/jmb.0909.0901020519918
   PubMed Web of Science ®Google Scholar
• PatelDR, BhartiyaSK, KumarR, ShuklaVK, NathG. Use of customized bacteriophages in the treatment of chronic nonhealing wounds: a prospective study. Int J Low Extrem Wounds. 2019;1534734619881076.31752578
   PubMed Web of Science ®Google Scholar
• ÖrmäläA-M, JalasvuoriM. Phage therapy: should bacterial resistance to phages be a concern, even in the long run? Bacteriophage. 2013;3(1):e24219. doi:10.4161/bact.2421923819105
   PubMedGoogle Scholar
• KrylovV, ShaburovaO, KrylovS, PletenevaE. A genetic approach to the development of new therapeutic phages to fight Pseudomonas aeruginosa in wound infections. Viruses. 2013;5(1):15–53. doi:10.3390/v5010015
   Web of Science ®Google Scholar
• KutateladzeM, AdamiaR. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol. 2010;28(12):591–595. doi:10.1016/j.tibtech.2010.08.00120810181
   PubMed Web of Science ®Google Scholar
• DearbornAD, DoklandT. Mobilization of pathogenicity islands by Staphylococcus aureus strain Newman bacteriophages. Bacteriophage. 2012;2(2):70–78. doi:10.4161/bact.2063223050217
   PubMedGoogle Scholar
• ChenJ, NovickRP. Phage-mediated intergeneric transfer of toxin genes. Science. 2009;323(5910):139–141. doi:10.1126/science.116478319119236
   PubMed Web of Science ®Google Scholar
• DossJ, CulbertsonK, HahnD, CamachoJ, BarekziN. A review of phage therapy against bacterial pathogens of aquatic and terrestrial organisms. Viruses. 2017;9(3):50. doi:10.3390/v9030050
   PubMed Web of Science ®Google Scholar
• Mohammed-AliMN, JamalludeenNM. Isolation and characterization of bacteriophage against methicillin resistant Staphylococcus aureus. J Med Microb Diagn. 2015;5(213):2161–0703.1000213.
   Google Scholar
• RossA, WardS, HymanP. More is better: selecting for broad host range bacteriophages. Front Microbiol. 2016;7:1352. doi:10.3389/fmicb.2016.0135227660623
   PubMed Web of Science ®Google Scholar
• WitteboleX, De RoockS, OpalSM. A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence. 2014;5(1):226–235. doi:10.4161/viru.2599123973944
   PubMed Web of Science ®Google Scholar
• SulakvelidzeA, AlavidzeZ, MorrisJG. Bacteriophage therapy. Antimicrob Agents Chemother. 2001;45(3):649–659. doi:10.1128/AAC.45.3.649-659.200111181338
   PubMed Web of Science ®Google Scholar
• WernickiA, NowaczekA, Urban-ChmielR. Bacteriophage therapy to combat bacterial infections in poultry. Virol J. 2017;14(1):179. doi:10.1186/s12985-017-0849-728915819
   PubMed Web of Science ®Google Scholar
• ŻaczekM, GórskiA, SkaradzińskaA, Łusiak-SzelachowskaM, Weber-DąbrowskaB. Phage penetration of eukaryotic cells: practical implications. Future Virol. 2019.
   Web of Science ®Google Scholar
• Jończyk-MatysiakE, Weber-DąbrowskaB, OwczarekB, et al. Phage-phagocyte interactions and their implications for phage application as therapeutics. Viruses. 2017;9(6):150. doi:10.3390/v9060150
   PubMed Web of Science ®Google Scholar
• MeadenS, KoskellaB. Exploring the risks of phage application in the environment. Front Microbiol. 2013;4:358. doi:10.3389/fmicb.2013.0035824348468
   PubMed Web of Science ®Google Scholar
• NobregaFL, CostaAR, KluskensLD, AzeredoJ. Revisiting phage therapy: new applications for old resources. Trends Microbiol. 2015;23(4):185–191. doi:10.1016/j.tim.2015.01.00625708933
   PubMed Web of Science ®Google Scholar
• PaulVD, SundarrajanS, RajagopalanSS, et al. Lysis-deficient phages as novel therapeutic agents for controlling bacterial infection. BMC Microbiol. 2011;11(1):195. doi:10.1186/1471-2180-11-19521880144
   PubMed Web of Science ®Google Scholar
• AckermannH-W, TremblayD, MoineauS. Long-term bacteriophage preservation. WFCC Newsletter. 2004;38(1):35–40.
   Google Scholar
• JończykE, KłakM, MiędzybrodzkiR, GórskiA. The influence of external factors on bacteriophages. Folia Microbiol (Praha). 2011;56(3):191–200. doi:10.1007/s12223-011-0039-821625877
   PubMed Web of Science ®Google Scholar
• HarrisonE, BrockhurstMA. Ecological and evolutionary benefits of temperate phage: what does or doesn’t kill you makes you stronger. BioEssays. 2017;39(12):1700112. doi:10.1002/bies.201700112
   Web of Science ®Google Scholar
• MonteiroR, PiresDP, CostaAR, AzeredoJ. Phage therapy: going temperate? Trends Microbiol. 2019;27(4):368–378. doi:10.1016/j.tim.2018.10.00830466900
   PubMed Web of Science ®Google Scholar
• GorskiA, MiedzybrodzkiR, BorysowskiJ, et al. Bacteriophage therapy for the treatment of infections. Curr Opinion Invest Drugs. 2009;10(8):766–774.
   PubMedGoogle Scholar
• DaviesEV, WinstanleyC, FothergillJL, JamesCE. The role of temperate bacteriophages in bacterial infection. FEMS Microbiol Lett. 2016;363:5. doi:10.1093/femsle/fnw015
   Web of Science ®Google Scholar
• ShaikhN, TarrPI. Escherichia coli O157: H7 Shiga toxin-encoding bacteriophages: integrations, excisions, truncations, and evolutionary implications. J Bacteriol. 2003;185(12):3596–3605. doi:10.1128/JB.185.12.3596-3605.200312775697
   PubMed Web of Science ®Google Scholar
• WaldorMK, MekalanosJJ. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science. 1996;272(5270):1910–1914. doi:10.1126/science.272.5270.19108658163
   PubMed Web of Science ®Google Scholar
• PirnayJ-P, De VosD, VerbekenG, et al. The phage therapy paradigm: pret-a-porter or sur-mesure? Pharm Res. 2011;28(4):934–937. doi:10.1007/s11095-010-0313-521063753
   PubMed Web of Science ®Google Scholar
• ChanishviliN, SharpR. Eliava Institute of bacteriophage, microbiology and virology, Tbilisi, Georgia In: A Literature Review of the Practical Application of Bacteriophage Research Tbilisi. Eliava Foundation; 2009.
   Google Scholar
• KutterE, De VosD, GvasaliaG, et al. Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol. 2010;11(1):69–86. doi:10.2174/13892011079072540120214609
   PubMed Web of Science ®Google Scholar
• MiędzybrodzkiR, BorysowskiJ, Weber-DąbrowskaB. et al., Clinical aspects of phage therapy In: Advances in Virus Research. Vol. 83 Elsevier; 2012:73–121.22748809
   PubMedGoogle Scholar
• StaffordN. Switzerland Is to Fund Complementary Therapies for Six Years While Effectiveness Is Evaluated. British Medical Journal Publishing Group; 2011.
   Google Scholar
• WeldRJ, ButtsC, HeinemannJA. Models of phage growth and their applicability to phage therapy. J Theor Biol. 2004;227(1):1–11. doi:10.1016/S0022-5193(03)00262-514969703
   PubMed Web of Science ®Google Scholar