Review

An exegesis of bacteriophage therapy: An emerging player in the fight against anti-microbial resistance

  • Received: 08 May 2020 Accepted: 19 July 2020 Published: 22 July 2020
  • Bacteriophages (simply referred to as Phages) are a class of viruses with the ability to infect and kill prokaryotic cells (bacteria), but are unable to infect mammalian cells. This unique ability to achieve specific infectiousness by bacteriophages has been harnessed in antibacterial treatments dating back almost a decade before the antibiotic era began. Bacteriophages were used as therapeutic agents in treatment of dysentery caused by Shigella dysenteriae as far back as 1919 and in the experimental treatment of a wide variety of other bacterial infections caused by Vibrio cholerae, Staphylococcus sp., Pseudomonas sp. etc, with varying degrees of success. Phage therapy and its many prospects soon fell out of favour in western medicine after the Second World War, with the discovery of penicillin. The Soviet Union and other countries in Eastern Europe however mastered the craft of bacteriophage isolation, purification and cocktail preparation, with phage-based therapeutics becoming widely available over-the-counter. With the recent rise in cases of multi-drug resistant bacterial infections, the clamour for a return to phage therapy, as a potential solution to the anti-microbial resistance (AMR) crisis has grown louder. This review provides an extensive exposé on phage therapy, addressing its historical use, evidences of its safety and efficacy, its pros and cons when compared with antibiotics, cases of compassionate use for treating life-threatening antibiotic-resistant infections, the limitations to its acceptance and how these may be circumvented.

    Citation: Oluwafolajimi Adesanya, Tolulope Oduselu, Oluwawapelumi Akin-Ajani, Olubusuyi M. Adewumi, Olusegun G. Ademowo. An exegesis of bacteriophage therapy: An emerging player in the fight against anti-microbial resistance[J]. AIMS Microbiology, 2020, 6(3): 204-230. doi: 10.3934/microbiol.2020014

    Related Papers:

  • Bacteriophages (simply referred to as Phages) are a class of viruses with the ability to infect and kill prokaryotic cells (bacteria), but are unable to infect mammalian cells. This unique ability to achieve specific infectiousness by bacteriophages has been harnessed in antibacterial treatments dating back almost a decade before the antibiotic era began. Bacteriophages were used as therapeutic agents in treatment of dysentery caused by Shigella dysenteriae as far back as 1919 and in the experimental treatment of a wide variety of other bacterial infections caused by Vibrio cholerae, Staphylococcus sp., Pseudomonas sp. etc, with varying degrees of success. Phage therapy and its many prospects soon fell out of favour in western medicine after the Second World War, with the discovery of penicillin. The Soviet Union and other countries in Eastern Europe however mastered the craft of bacteriophage isolation, purification and cocktail preparation, with phage-based therapeutics becoming widely available over-the-counter. With the recent rise in cases of multi-drug resistant bacterial infections, the clamour for a return to phage therapy, as a potential solution to the anti-microbial resistance (AMR) crisis has grown louder. This review provides an extensive exposé on phage therapy, addressing its historical use, evidences of its safety and efficacy, its pros and cons when compared with antibiotics, cases of compassionate use for treating life-threatening antibiotic-resistant infections, the limitations to its acceptance and how these may be circumvented.


    加载中

    Abbreviation IBMV: Eliava Institute of Bacteriophage Microbiology & Virology; WHO: World Health Organization; AMR: Anti-Microbial Resistance; CDC: Centre for Disease Control & Prevention; USA: United States of America; FDA: Food and Drug Administration; TNF: Tumor Necrosis Factor; IFN–Interferon; EPS: Extracellular Polymeric Substance; CF: Cystic Fibrosis; ARG: Antibiotics Resistance Gene; DNA: Deoxyribonucleic Acid; CRISPR: Clustered Regularly Interspersed Short Palindromic Repeats; PCR: Polymerase Chain Reaction; MRSA: Methicillin Resistant ; MRCNS: Methicillin Resistant Coagulase Negative ; EUR: Euro;
    Acknowledgments



    None

    Conflict of Interest



    The authors declare no conflict of interest

    Author Contributions



    OA and TO conceived and designed the study; performed the literature search and prepared the manuscript. OA-A participated in the literature search, provided the illustrations used and reviewed the manuscript for writing errors. MA and OA reviewed and edited the manuscript for intellectual content. All authors have approved the final manuscript for publication.

    [1] Lin DM, Koskella B, Lin HC (2017) Phage therapy: An alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol Ther 8: 162-173. doi: 10.4292/wjgpt.v8.i3.162
    [2] Hankin ME (1896) The bactericidal action of the waters of the Jamuna and Ganges rivers on Cholera microbes. Ann Inst Pasteur 10: 511-523.
    [3] Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5: 226-235. doi: 10.4161/viru.25991
    [4] Chanishvili N (2012) Phage therapy-history from Twort and d'Herelle through Soviet experience to current approaches. Adv Virus Res 83: 3-40. doi: 10.1016/B978-0-12-394438-2.00001-3
    [5] d'Herelle F (1931) Bacteriophage as a treatment in acute medical and surgical infections. Bull N Y Acad Med 7: 329-348.
    [6] Rohde C, Wittmann J, Kutter E (2018) Bacteriophages: A therapy concept against multi-drug–resistant bacteria. Surg Infect (Larchmt) 19: 737-744. doi: 10.1089/sur.2018.184
    [7] Principi N, Silvestri E, Esposito S (2019) Advantages and limitations of bacteriophages for the treatment of bacterial infections. Front Pharmacol 10: 513. doi: 10.3389/fphar.2019.00513
    [8] Chanishvili N (2016) Bacteriophages as therapeutic and prophylactic means: summary of the Soviet and Post Soviet experiences. Curr Drug Deliv 13: 309-323. doi: 10.2174/156720181303160520193946
    [9] Abedon ST, Kuhl SJ, Blasdel BG, et al. (2011) Phage treatment of human infections. Bacteriophage 1: 66-85. doi: 10.4161/bact.1.2.15845
    [10] Carlton RM (1999) Phage therapy: past history and future prospects. Arch Immunol Ther Exp 47: 267-274.
    [11] Suttle CA (2007) Marine viruses--major players in the global ecosystem. Nat Rev Microbiol 5: 801-812. doi: 10.1038/nrmicro1750
    [12] Wittebole X, De Roock S, Opal SM (2014) A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence 5: 226-235. doi: 10.4161/viru.25991
    [13] Keen EC (2015) A century of phage research: bacteriophages and the shaping of modern biology. Bioessays 37: 6-9. doi: 10.1002/bies.201400152
    [14] Clokie MR, Millard AD, Letarov AV, et al. (2011) Phages in nature. Bacteriophage 1: 31-45. doi: 10.4161/bact.1.1.14942
    [15] Weber-Dąbrowska B, Jończyk-Matysiak E, Żaczek M, et al. (2016) Bacteriophage procurement for therapeutic purposes. Front Microbiol 7: 1177.
    [16] Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28: 127-181. doi: 10.1016/j.femsre.2003.08.001
    [17] Rakhuba DV, Kolomiets EI, Dey ES, et al. (2010) Bacteriophage receptors, mechanisms of phage adsorption and penetration into host cell. Pol J Microbiol 59: 145-155. doi: 10.33073/pjm-2010-023
    [18] Young R (2013) Phage lysis: do we have the hole story yet? Curr Opin Microbiol 16: 790-797. doi: 10.1016/j.mib.2013.08.008
    [19] Delbrück M (1940) The growth of bacteriophage and lysis of the host. J Gen Physiol 23: 643-660. doi: 10.1085/jgp.23.5.643
    [20] Salmond GP, Fineran PC (2015) A century of the phage: past, present and future. Nat Rev Microbiol 13: 777-786. doi: 10.1038/nrmicro3564
    [21] Brabban AD, Hite E, Callaway TR (2005) Evolution of foodborne pathogens via temperate bacteriophage-mediated gene transfer. Foodborne Pathog Dis 2: 287-303. doi: 10.1089/fpd.2005.2.287
    [22] Duncan CJ, Scott S (2005) What caused the Black Death? Postgrad Med J 81: 315-320. doi: 10.1136/pgmj.2004.024075
    [23] Yoshikawa TT (2002) Antimicrobial resistance and aging: beginning of the end of the antibiotic era? J Am Geriatr Soc 50: S226-S229. doi: 10.1046/j.1532-5415.50.7s.2.x
    [24] Rosenblatt-Farrell N (2009) The landscape of antibiotic resistance. Environ Health Perspect 117: A244-A250.
    [25] World Health Organization (2014)  Antimicrobial resistance global report on surveillance. Available from: URL: https://www.who.int/drugresistance/documents/surveillancereport/en/.
    [26] United Nations (2016)  High-level meeting on antimicrobial resistance 2016. Available from: http://www.un.org/pga/71/2016/09/21/press-release-hlmeeting-on-antimicrobial-resistance/.
    [27] Laxminarayan R, Duse A, Wattal C, et al. (2013) Antibiotic resistance-the need for global solutions. Lancet Infect Dis 13: 1057-1098. doi: 10.1016/S1473-3099(13)70318-9
    [28] Audi H (2016) The Review on Antimicrobial Resistance: The global challenge of drug-resistant infections. AMR Review Available from: https://www.wipo.int/edocs/mdocs/mdocs/en/wipo_who_wto_ip_ge_16/wipo_who_wto_ip_ge_16_www_356156.pdf.
    [29] (2017) World Health OrganisationPrioritization of pathogens to guide discovery, research and development of new antibiotics for drug-resistant bacterial infections, including tuberculosis. Geneva: 88.
    [30] Luepke KH, Suda KJ, Boucher H, et al. (2017) Past, present, and future of antibacterial economics: increasing bacterial resistance, limited antibiotic pipeline, and societal implications. Pharmacotherapy 37: 71-84. doi: 10.1002/phar.1868
    [31] World Health Organisation (2020)  Lack of new antibiotics threatens global efforts to contain drug-resistant infections. Available from: https://www.who.int/news-room/detail/17-01-2020-lack-of-new-antibiotics-threatens-global-efforts-to-contain-drug-resistant-infections.
    [32] Centers for Disease Control and Prevention (2013) Vital signs: carbapenem-resistant Enterobacteriaceae. MMWR Morb Mortal Wkly Rep 62: 165-170.
    [33] Nagel TE (2018) Delivering phage products to combat antibiotic resistance in developing countries: lessons learned from the HIV/AIDS Epidemic in Africa. Viruses 10: 345. doi: 10.3390/v10070345
    [34] Summers WC (2001) Bacteriophage therapy. Annu Rev Microbiol 55: 437-451. doi: 10.1146/annurev.micro.55.1.437
    [35] Hodyra-Stefaniak K, Miernikiewicz P, Drapała J, et al. (2015) Mammalian Host-Versus-Phage immune response determines phage fate in vivo. Sci Rep 5: 14802. doi: 10.1038/srep14802
    [36] Bordet J (1925) Le probleme de l'autolyse microbienne transmissible ou du bacteriophage. Ann Inst Pasteur (Paris) 39: 711-763.
    [37] Sankaran N (2010) The bacteriophage, its role in immunology: how Macfarlane Burnet's phage research shaped his scientific style. Stud Hist Philos Biol Biomed Sci 41: 367-375. doi: 10.1016/j.shpsc.2010.10.012
    [38] Ruska H (1940) Die Sichtbarmachung der bakteriophagen Lyse im Ubermikroskop. Naturwissenschaften 28: 45-46. doi: 10.1007/BF01486931
    [39] Górski A, Międzybrodzki R, Jończyk-Matysiak E, et al. (2019) The fall and rise of phage therapy in modern Medicine. Expert Opin Biol Th 11: 1115-1117. doi: 10.1080/14712598.2019.1651287
    [40] McCallin S, Sacher JC, Zheng J, et al. (2019) Current State of Compassionate Phage Therapy. Viruses 11: 343. doi: 10.3390/v11040343
    [41] Kutateladze M, Adamia R (2008) Phage therapy experience at the Eliava Institute. Med Mal Infect 38: 426-430. doi: 10.1016/j.medmal.2008.06.023
    [42] Chanishvili N, Sharp R (2008) Bacteriophage therapy: experience from the Eliava Institute, Georgia. Microbiol Australia 29: 96-101. doi: 10.1071/MA08096
    [43] Babalova EG, Katsitadze KT, Sakvarelidze LA, et al. (1968) Preventive value of dried dysentery bacteriophage. Zhurnal mikrobiologii epidemiologii iimmunobiologii 45: 143-145.
    [44] Miedzybrodzki R, Borysowski J, Weber-Dabrowska B, et al. (2012) Clinical aspects of phage therapy. Adv Virus Res 83: 73-121. doi: 10.1016/B978-0-12-394438-2.00003-7
    [45] Nilsson AS (2019) Pharmacological limitations of phage therapy. Ups J Med Sci 124: 218-227. doi: 10.1080/03009734.2019.1688433
    [46] Smith HW, Huggins MB (1982) Successful treatment of experimental Escherichia coli infections in mice using phage: its general superiority over antibiotics. J Gen Microbiol 128: 307-318.
    [47] Watanabe R, Matsumoto T, Sano G, et al. (2007) Efficacy of bacteriophage therapy against gut-derived sepsis caused by Pseudomonas aeruginosa in mice. Antimicrob Agents Chemother 51: 446-452. doi: 10.1128/AAC.00635-06
    [48] Biswas B, Adhya S, Washart P, et al. (2002) Bacteriophage therapy rescues mice bacteremic from a clinical isolate of vancomycin-resistant Enterococcus faeciumInfect Immun 70: 204-210. doi: 10.1128/IAI.70.1.204-210.2002
    [49] Wang J, Hu B, Xu M, et al. (2006) Therapeutic effectiveness of bacteriophages in the rescue of mice with extended spectrum beta lactamase- producing Escherichia coli bacteremia. Int J Mol Med 17: 347-355.
    [50] Essoh C, Blouin Y, Loukou G, et al. (2013) The susceptibility of Pseudomonas aeruginosa strains from cystic fibrosis patients to bacteriophages. PLoS One 8: e60575. doi: 10.1371/journal.pone.0060575
    [51] Kutateladze M, Adamia R (2010) Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28: 591-595. doi: 10.1016/j.tibtech.2010.08.001
    [52] Yosef I, Manor M, Kiro R, et al. (2015) Temperate and lytic bacteriophages programmed to sensitize and kill antibiotic-resistant bacteria. Proc Natl Acad Sci USA 2015 112: 7267-7272. doi: 10.1073/pnas.1500107112
    [53] Rhoads DD, Wolcott RD, Kuskowski MA, et al. (2009) Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J Wound Care 18: 237-238. doi: 10.12968/jowc.2009.18.6.42801
    [54] Wright A, Hawkins CH, Anggard EE, et al. (2009) A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin Otolaryngol 34: 349-357. doi: 10.1111/j.1749-4486.2009.01973.x
    [55] Phagoburn (2013) Available from: http://www.phagoburn.eu/.
    [56] Jault P, Leclerc T, Jennes S, et al. (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. Lancet Infect Dis 19: 35-45. doi: 10.1016/S1473-3099(18)30482-1
    [57] Phage4Cure (2017) Available from: https://phage4cure.de/en/projekt/.
    [58] Fong SA, Drilling A, Morales S, et al. (2017) Activity of bacteriophages in removing biofilms of Pseudomonas aeruginosa isolates from chronic rhinosinusitis patients. Front Cell Infect Microbiol 7: 418. doi: 10.3389/fcimb.2017.00418
    [59] Pirnay JP, De Vos D, Verbeken G (2019) Clinical application of bacteriophages in Europe. Microbiol Aust 40: 8-15. doi: 10.1071/MA19010
    [60] Koskella B, Meaden S (2013) Understanding bacteriophage specificity in natural microbial communities. Viruses 5: 806-823. doi: 10.3390/v5030806
    [61] Domingo-Calap P, Delgado-Martínez J (2018) Bacteriophages: protagonists of a post-antibiotic era. Antibiotics (Basel) 7: E66. doi: 10.3390/antibiotics7030066
    [62] Peng Z, Addisu A, Alrabaa S, et al. (2017) Antibiotic resistance and toxin production of Clostridium difficile isolates from the hospitalized patients in a large hospital in Florida. Front. Microbiol 8: 2584. doi: 10.3389/fmicb.2017.02584
    [63] Leffler DA, Lamont JT (2015) Clostridium difficile infection. N Engl J Med 372: 1539-1548. doi: 10.1056/NEJMra1403772
    [64] Peng Z, Jin D, Kim HB, et al. (2017) Update on antimicrobial resistance in Clostridium difficile: resistance mechanisms and antimicrobial susceptibility testing. J Clin Microbiol 55: 1998-2008. doi: 10.1128/JCM.02250-16
    [65] Metsälä J, Lundqvist A, Virta LJ, et al. (2015) Prenatal and post-natal exposure to antibiotics and risk of asthma in childhood. Clin Exp Allergy 45: 137-145. doi: 10.1111/cea.12356
    [66] Cox LM, Blaser MJ (2015) Antibiotics in early life and obesity. Nat Rev Endocrinol 11: 182-190. doi: 10.1038/nrendo.2014.210
    [67] Mikkelsen KH, Allin KH, Knop FK (2016) Effect of antibiotics on gut microbiota, glucose metabolism and body weight regulation: a review of the literature. Diabetes Obes Metab 18: 444-453. doi: 10.1111/dom.12637
    [68] Chibani-Chennoufi S, Sidoti J, Bruttin A, et al. (2004) In vitro and in vivo bacteriolytic activities of Escherichia coli phages: implications for phage therapy. Antimicrob Agents Chemother 48: 2558-2569. doi: 10.1128/AAC.48.7.2558-2569.2004
    [69] Mai V, Ukhanova M, Reinhard MK, et al. (2015) Bacteriophage administration significantly reduces Shigella colonization and shedding by Shigella-challenged mice without deleterious side effects and distortions in the gut microbiota. Bacteriophage 5: e1088124. doi: 10.1080/21597081.2015.1088124
    [70] Galtier M, De Sordi L, Maura D, et al. (2016) Bacteriophages to reduce gut carriage of antibiotic resistant uropathogens with low impact on microbiota composition. Environ Microbiol 18: 2237-2245. doi: 10.1111/1462-2920.13284
    [71] Servick K (2016) Drug development. Beleaguered phage therapy trial presses on. Science 352: 1506. doi: 10.1126/science.352.6293.1506
    [72] Bourdin G, Navarro A, Sarker SA, et al. (2014) Coverage of diarrhoea-associated Escherichia coli isolates from different origins with two types of phage cocktails. Microb Biotechnol 7: 165-176. doi: 10.1111/1751-7915.12113
    [73] Sarker SA, Sultana S, Reuteler G, et al. (2016) Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. EBio Medicine 4: 124-137.
    [74] Latz S, Wahida A, Arif A, et al. (2016) Preliminary survey of local bacteriophages with lytic activity against multi-drug resistant bacteria. J Basic Microbiol 56: 1117-1123. doi: 10.1002/jobm.201600108
    [75] Granowitz EV, Brown RB (2008) Antibiotic adverse reactions and drug interactions. Crit Care Clin 24: 421-422. doi: 10.1016/j.ccc.2007.12.011
    [76] Novotný J, Novotný M (1999) Adverse drug reactions to antibiotics and major antibiotic drug interactions. Gen Physiol Biophys 18: 126-139.
    [77] Vallejos A (2007) Adverse reactions by antibiotics in a pediatric and neonatal intensive care unit in Bogotá. Biomedica 27: 66-75. doi: 10.7705/biomedica.v27i1.234
    [78] Bhattacharya S (2010) The facts about penicillin allergy: a review. J Adv Pharm Technol Res 1: 11-17.
    [79] Bruttin A, Brüssow H (2005) Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother 49: 2874-2878. doi: 10.1128/AAC.49.7.2874-2878.2005
    [80] McCallin S, Alam Sarker S, Barretto C, et al. (2013) Safety analysis of a Russian phage cocktail: from metagenomic analysis to oral application in healthy human subjects. Virology 443: 187-196. doi: 10.1016/j.virol.2013.05.022
    [81] Górski A, Wazna E, Dabrowska BW, et al. (2006) Bacteriophage translocation. FEMS Immunol Med Microbiol 46: 313-319. doi: 10.1111/j.1574-695X.2006.00044.x
    [82] Kniotek M, Weber-Dabrowska B, Dabrowska K, et al. (2004b) Phages as immunomodulators of antibody production. Genomic Issues, Immune System Activation and Allergy, Immunology 33-36.
    [83] Tetz G, Tetz V (2016) Bacteriophage infections of microbiota can lead to leaky gut in an experimental rodent model. Gut Pathog 8: 33. doi: 10.1186/s13099-016-0109-1
    [84] Meddings JB, Swain MG (2000) Environmental stress-induced gastrointestinal permeability is mediated by endogenous glucocorticoids in the Rat. Gastroenterology 119: 1019-1028. doi: 10.1053/gast.2000.18152
    [85] Borysowski J, Górski A (2008) Is phage therapy acceptable in the immunocompromised host? Int J Infect Dis 12: 466-471. doi: 10.1016/j.ijid.2008.01.006
    [86] Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8: 881-890. doi: 10.3201/eid0809.020063
    [87] Rutherford ST, Bassler BL (2012) Bacterial Quorum Sensing: Its Role in Virulence and Possibilities for Its Control. Cold Spring Harb Perspect Med 2: a012427. doi: 10.1101/cshperspect.a012427
    [88] Donlan RM (2009) Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 17: 66-72. doi: 10.1016/j.tim.2008.11.002
    [89] Motlagh AM, Bhattacharjee AS, Goel R (2016) Biofilm control with natural and genetically-modified phages. World J Microbiol Biotechnol 32: 67. doi: 10.1007/s11274-016-2009-4
    [90] Harper DR, Parracho HM, Walker J, et al. (2014) Bacteriophages biofilms. Antibiotics 3: 270-284. doi: 10.3390/antibiotics3030270
    [91] Curtin JJ, Donlan RM (2006) Using bacteriophages to reduce formation of catheter-associated biofilms by Staphylococcus epidermidisAntimicrob Agents Chemother 50: 1268-1275. doi: 10.1128/AAC.50.4.1268-1275.2006
    [92] Yan J, Mao J, Xie J (2014) Bacteriophage polysaccharide depolymerases and biomedical applications. Bio Drugs 28: 265-274.
    [93] Lu TK, Collins JJ (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci 104: 11197-11202. doi: 10.1073/pnas.0704624104
    [94] Zaky A, Escobar I, Motlagh AM, et al. (2012) Determining the influence of active cells and conditioning layer on early stage biofilm formation using cellulose acetate ultrafiltration membranes. Desalination 286: 296-303. doi: 10.1016/j.desal.2011.11.040
    [95] Gabisoniya TG, Loladze MZ, Nadiradze MM, et al. (2016) Effects of bacteriophages on biofilm formation by strains of Pseudomonas aeruginosaAppl Biochem Microbiol 52: 293-297. doi: 10.1134/S0003683816030042
    [96] Corbin BD, McLean RJ, Aron GM (2001) Bacteriophage T4 multiplication in a glucose limited Escherichia coli biofilm. Can J Microbiol 47: 680-684. doi: 10.1139/w01-059
    [97] Ceri H, Olson ME, Stremick C, et al. (1999) The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37: 1771-1776. doi: 10.1128/JCM.37.6.1771-1776.1999
    [98] Amorena B, Gracia E, Monzón M, et al. (1999) Antibiotic susceptibility assay for Staphylococcus aureus in biofilms developed in vitro. J Antimicrob Chemother 44: 43-55. doi: 10.1093/jac/44.1.43
    [99] Hanlon GW, Denyer SP, Olliff CJ, et al. (2001) Reduction of exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 67: 2746-2753. doi: 10.1128/AEM.67.6.2746-2753.2001
    [100] Kittler S, Wittmann J, Mengden R, et al. (2016) The use of bacteriophages as One-Health approach to reduce multi drug resistant bacteria. Sustain Chem Pharm 5: 80-83. doi: 10.1016/j.scp.2016.06.001
    [101] Piffaretti JC (2016) Antibiotic resistance: The emergence of plasmid-mediated colistin resistance enhances the need of a proactive one-health approach. FEMS Microbiol Lett 363: fnw034. doi: 10.1093/femsle/fnw034
    [102] Seed KD (2015) Battling phages: how bacteria defend against viral attack. PLoS Pathog 11: e1004847. doi: 10.1371/journal.ppat.1004847
    [103] Riede I, Eschbach ML (1986) Evidence that TraT interacts with OmpA of Escherichia coliFEBS Lett 205: 241-245. doi: 10.1016/0014-5793(86)80905-X
    [104] Nordström K, Forsgren A (1974) Effect of protein A on adsorption of bacteriophages to Staphylococcus aureusJ Virol 14: 198-202. doi: 10.1128/JVI.14.2.198-202.1974
    [105] Liu M, Deora R, Doulatov SR, A, et al. (2002) Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295: 2091-2094. doi: 10.1126/science.1067467
    [106] Seed KD, Faruque SM, Mekalanos JJ, et al. (2012) Phase variable O antigen biosynthetic genes control expression of the major protective antigen and bacteriophage receptor in Vibrio cholerae O1. PLoS Pathog 8: e1002917. doi: 10.1371/journal.ppat.1002917
    [107] Drulis-Kawa Z, Majkowska-Skrobek G, Maciejewska B, et al. (2012) Learning from Bacteriophages–advantages and limitations of phage and phage-encoded protein applications. Curr Protein Pept Sci 13: 699-722. doi: 10.2174/138920312804871193
    [108] Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Future Microbiol 8: 769-783. doi: 10.2217/fmb.13.47
    [109] Koskella B, Brockhurst MA (2014) Bacteria-phage coevolution as a driver of ecological and evolutionary processes in microbial communities. FEMS Microbiol Rev 38: 916-931. doi: 10.1111/1574-6976.12072
    [110] Torres-Barceló C (2018) Phage therapy faces evolutionary challenges. Viruses 10: E323. doi: 10.3390/v10060323
    [111] Chan BK, Sistrom M, Wertz JE, et al. (2016) Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosaSci Rep 6: 26717. doi: 10.1038/srep26717
    [112] Penadés JR, Chen J, Quiles-Puchalt N, et al. (2015) Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol 23: 171-178. doi: 10.1016/j.mib.2014.11.019
    [113] Marti E, Variatza E, Balcázar JL (2014) Bacteriophages as a reservoir of extended-spectrum ß-lactamase and fluoroquinolone resistance genes in the environment. Clin Microbiol Infect 20: O456-O459. doi: 10.1111/1469-0691.12446
    [114] Rodriguez-Mozaz S, Chamorro S, Marti E, et al. (2015) Occurrence of antibiotics and antibiotic resistance genes in hospital and urban wastewaters and their impact on the receiving river. Water Res 69: 234-242. doi: 10.1016/j.watres.2014.11.021
    [115] Subirats J, Sànchez-Melsió A, Borrego CM, et al. (2016) Metagenomic analysis reveals that bacteriophages are reservoirs of antibiotic resistance genes. Int J Antimicrob Agents 48: 163-167. doi: 10.1016/j.ijantimicag.2016.04.028
    [116] Quirós P, Colomer-Lluch M, Martínez-Castillo A, et al. (2014) Antibiotic resistance genes in the bacteriophage DNA fraction of human fecal samples. AntimicrobAgents Chemother 58: 606-609. doi: 10.1128/AAC.01684-13
    [117] Griffiths AJF, Miller JH, Suzuki DT, et al. (2000) Transduction. An Introduction to Genetic Analysis New York.
    [118] Fancello L, Desnues C, Raoult D, et al. (2011) Bacteriophages and diffusion of genes encoding antimicrobial resistance in cystic fibrosis sputum microbiota. J Antimicrob Chemother 66: 2448-2454. doi: 10.1093/jac/dkr315
    [119] Edgar R, Friedman N, Molshanski-Mor S, et al. (2012) Reversing bacterial resistance to antibiotics by phage-mediated delivery of dominant sensitive genes. Appl Environ Microbiol 78: 744-751. doi: 10.1128/AEM.05741-11
    [120] Bogovazova GG, Voroshilova NN, Bondarenko VM (1991) The efficacy of Klebsiella pneumoniae bacteriophage in the therapy of experimental Klebsiella infection. Zh Mikrobiol Epidemiol Immunobiol 4: 5-8.
    [121] Miedzybrodzki R, Fortuna W, Weber-Dabrowska B, et al. (2007) Phage therapy of staphylococcal infections (including MRSA) may be less expensive than antibiotic treatment. Postepy Hig Med Dosw 61: 461-465.
    [122] Founou RC, Founou LL, Essack SY (2017) Clincal and economic impact of antibiotic resistance in developing countries: A systematic review and meta-analysis. PLoS One 12: e0189621. doi: 10.1371/journal.pone.0189621
    [123] Tadesse BT, Ashley EA, Ongarello S, et al. (2017) Antimicrobial resistance in Africa: a systematic review. BMC Infect Dis 17: 616. doi: 10.1186/s12879-017-2713-1
    [124] Koko AS, Ackermann HW, Taiwo MA, et al. (2011) Nigerian phages: The first bacteriophages from Tropical Africa. Afr J Microbiol Res 5: 2207-2210.
    [125] Montso PK, Mlambo V, Ateba CN (2019) Characterization of lytic bacteriophages infecting multidrug-resistant shiga toxigenic atypical Escherichia coli O177 strains isolated from Cattle feces. Front Public Health 7: 355. doi: 10.3389/fpubh.2019.00355
    [126] Ochieng JM, Oduor O, Onkoba N, et al. (2016) Experimental phage therapy against haematogenous multi-drug resistant Staphylococcus aereus pneumoniae in mice. Afr J Lab Med 5: a435.
    [127] Kim S, Rahman M, Seol S, et al. (2012) Pseudomonas aeruginosa bacteriophage PA1O requires type IV pili for infection and shows broad bactericidal and biofilm removal activities. Appl Environ Microbiol 78: 6380-6385. doi: 10.1128/AEM.00648-12
    [128] Gutierrez D, Vandenheuvel D, Martinez B, et al. (2015) Two phages, phiIPLARODI and phiIPLA-C1C, lyse mono- and dual-species staphylococcal biofilms. Appl Environ Microbiol 81: 3336-3348. doi: 10.1128/AEM.03560-14
    [129] Chhibber S, Bansal S, Kaur S (2015) Disrupting the mixed-species biofilm of Klebsiella pneumoniae B5055 and Pseudomonas aeruginosa PAO using bacteriophages alone or in combination with xylitol. Microbiology 161: 1369-1377. doi: 10.1099/mic.0.000104
    [130] Junka AF, Rakoczy R, Szymczyk P, et al. (2018) Application of rotating magnetic fields increase the activity of antimicrobials against wound biofilm pathogens. Sci Rep 8: 167. doi: 10.1038/s41598-017-18557-7
    [131] Li L-L, Yu P, Wang X, et al. (2017) Enhanced biofilm penetration for microbial control by polyvalent phages conjugated with magnetic colloidal nanoparticle clusters (CNCs). Environ Sci Nano 4: 1817-1826. doi: 10.1039/C7EN00414A
    [132] Gallego del Sol F, Penades JR, Marina A (2019) Deciphering the molecular mechanisms underpinning phage arbitrium communication systems. Molecular Cell 74: 59-72. doi: 10.1016/j.molcel.2019.01.025
    [133] Yoichi M, Abe M, Miyanaga K, et al. (2015) Alteration of tail fiber protein gp38 enables T2 phage to infect Escherichia coli O157: H7. J Biotechnol 115: 101-107. doi: 10.1016/j.jbiotec.2004.08.003
    [134] Maichi F, Synnott AJ, Yamamichi K, et al. (2009) Site specific recombination of T2 phage using IP008 long tail fiber genes provides a targeted method for expanding host range while retaining lytic activity. FEMS Microbiol Lett 295: 211-217. doi: 10.1111/j.1574-6968.2009.01588.x
    [135] Kiro R, Shitrit D, Qimron U (2014) Efficient engineering of a bacteriophage genome using the type I-E CRISPR-Cas system. RNA Biol 11: 42-44. doi: 10.4161/rna.27766
    [136]  Directive 2001/83/EC of the European Parliament and the Council on the Community code relating to medicinal products for human use. Available from: https://ec.europa.eu/health/sites/health/files/files/eudralex/vol-1/dir_2001_83_consol_2012/dir_2001_83_cons_2012_en.pdf.
    [137] Pirnay JP, Verbeken G, Ceyssens PJ, et al. (2018) The magistral phage. Viruses 10: e64. doi: 10.3390/v10020064
    [138]  Agence nationale de sécurité du médicament et des produits de santé. Comité scientifique specialise temporaire: Phagothérapie. Available from: http://ansm.sante.fr/content/download/91159/1144681/version/1/file/CR_CSST_Phagotherapie_CSST201611013_24-03-2016.pdf.
    [139] Schooley RT, Biswas B, Gill JJ, et al. (2017) Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother 61: e00954-17. doi: 10.1128/AAC.00954-17
  • Reader Comments
  • © 2020 the Author(s), licensee AIMS Press. This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
通讯作者: 陈斌, bchen63@163.com
  • 1. 

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索

Metrics

Article views(9763) PDF downloads(635) Cited by(13)

Article outline

Figures and Tables

Figures(2)  /  Tables(2)

/

DownLoad:  Full-Size Img  PowerPoint
Return
Return

Catalog