Skip to main content
Top
Published in: Journal of Translational Medicine 1/2019

Open Access 01-12-2019 | Antibiotic | Review

Exploring the whole standard operating procedure for phage therapy in clinical practice

Authors: Zelin Cui, Xiaokui Guo, Tingting Feng, Li Li

Published in: Journal of Translational Medicine | Issue 1/2019

Login to get access

Abstract

We have entered the post-antibiotic era. Phage therapy has recently been given renewed attention because bacteriophages are easily available and can kill bacteria. Many reports have demonstrated successful phage treatment of bacterial infection, whereas some studies have shown that phage therapy is not as effective as expected. In general, establishment of a standard operating procedure will ensure the success of phage therapy. In this paper, the whole operating procedure for phage therapy in clinical practice is explored and analyzed to comprehensively understand the success of using phage for the treatment of bacterial infectious disease in the future. The procedure includes the following: enrollment of patients for phage therapy; establishment of phage libraries; pathogenic bacterial isolation and identification; screening for effective phages against pathogenic bacteria; phage formulation preparation; phage preparation administration strategy and route; monitoring the efficacy of phage therapy; and detection of the emergence of phage-resistant strains. Finally, we outline the whole standard operating procedure for phage therapy in clinical practice. It is believed that phage therapy will be used successfully, especially in personalized medicine for the treatment of bacterial infectious diseases. Hopefully, this procedure will provide support for the entry of phage therapy into the clinic as soon as possible.
Literature
1.
go back to reference Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J, Lessor L, Barr JJ, Reed SL, Rohwer F, Benler S, 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.PubMedPubMedCentralCrossRef Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J, Lessor L, Barr JJ, Reed SL, Rohwer F, Benler S, 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.PubMedPubMedCentralCrossRef
2.
go back to reference Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis. 2010;10(9):597–602.PubMedPubMedCentralCrossRef Kumarasamy KK, Toleman MA, Walsh TR, Bagaria J, Butt F, Balakrishnan R, Chaudhary U, Doumith M, Giske CG, Irfan S, et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis. 2010;10(9):597–602.PubMedPubMedCentralCrossRef
4.
go back to reference Wittebole X, De Roock S, Opal SM. A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence. 2013;4(8):226–35. Wittebole X, De Roock S, Opal SM. A historical overview of bacteriophage therapy as an alternative to antibiotics for the treatment of bacterial pathogens. Virulence. 2013;4(8):226–35.
5.
go back to reference Shatzkes K, Connell ND, Kadouri DE. Predatory bacteria: a new therapeutic approach for a post-antibiotic era. Future Microbiol. 2017;12:469–72.PubMedCrossRef Shatzkes K, Connell ND, Kadouri DE. Predatory bacteria: a new therapeutic approach for a post-antibiotic era. Future Microbiol. 2017;12:469–72.PubMedCrossRef
6.
go back to reference Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.PubMedCrossRef Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson-Liljequist B, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.PubMedCrossRef
7.
go back to reference Bartsch SM, McKinnell JA, Mueller LE, Miller LG, Gohil SK, Huang SS, Lee BY. Potential economic burden of carbapenem-resistant Enterobacteriaceae (CRE) in the United States. Clin Microbiol Infect. 2017;23(1):48.PubMedCrossRef Bartsch SM, McKinnell JA, Mueller LE, Miller LG, Gohil SK, Huang SS, Lee BY. Potential economic burden of carbapenem-resistant Enterobacteriaceae (CRE) in the United States. Clin Microbiol Infect. 2017;23(1):48.PubMedCrossRef
8.
go back to reference Kim YJ, Kim SI, Lee YD, Choi HJ, Choi JY, Yoon SK, You YK, Kim DG. Carbapenem-resistant Acinetobacter baumannii bacteremia in liver transplant recipients. Transplant Proc. 2018;50(4):1132–5.PubMedCrossRef Kim YJ, Kim SI, Lee YD, Choi HJ, Choi JY, Yoon SK, You YK, Kim DG. Carbapenem-resistant Acinetobacter baumannii bacteremia in liver transplant recipients. Transplant Proc. 2018;50(4):1132–5.PubMedCrossRef
10.
12.
13.
go back to reference Kutateladze M, Adamia R. Phage therapy experience at the Eliava Institute. Med Mal Infect. 2008;38(8):426–30.PubMedCrossRef Kutateladze M, Adamia R. Phage therapy experience at the Eliava Institute. Med Mal Infect. 2008;38(8):426–30.PubMedCrossRef
14.
go back to reference Chanishvili N. Phage therapy–history from Twort and d’Herelle through Soviet experience to current approaches. Adv Virus Res. 2012;83:3–40.PubMedCrossRef Chanishvili N. Phage therapy–history from Twort and d’Herelle through Soviet experience to current approaches. Adv Virus Res. 2012;83:3–40.PubMedCrossRef
16.
go back to reference Lin DM, Koskella B, Lin HC. Phage therapy: an alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol Ther. 2017;8(3):162–73.PubMedPubMedCentralCrossRef Lin DM, Koskella B, Lin HC. Phage therapy: an alternative to antibiotics in the age of multi-drug resistance. World J Gastrointest Pharmacol Ther. 2017;8(3):162–73.PubMedPubMedCentralCrossRef
17.
go back to reference El Haddad L, Harb CP, Gebara MA, Stibich MA, Chemaly RF. A systematic and critical review of bacteriophage therapy against multi-drug resistant ESKAPE organisms in humans. Clin Infect Dis. 2018;69(1):167–78.CrossRef El Haddad L, Harb CP, Gebara MA, Stibich MA, Chemaly RF. A systematic and critical review of bacteriophage therapy against multi-drug resistant ESKAPE organisms in humans. Clin Infect Dis. 2018;69(1):167–78.CrossRef
18.
go back to reference Dedrick RM, Guerrero-Bustamante CA, Garlena RA, Russell DA, Ford K, Harris K, Gilmour KC, Soothill J, Jacobs-Sera D, Schooley RT, et al. Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nat Med. 2019;25(5):730–3.PubMedPubMedCentralCrossRef Dedrick RM, Guerrero-Bustamante CA, Garlena RA, Russell DA, Ford K, Harris K, Gilmour KC, Soothill J, Jacobs-Sera D, Schooley RT, et al. Engineered bacteriophages for treatment of a patient with a disseminated drug-resistant Mycobacterium abscessus. Nat Med. 2019;25(5):730–3.PubMedPubMedCentralCrossRef
19.
go back to reference Marza JA, Soothill JS, Boydell P, Collyns TA. Multiplication of therapeutically administered bacteriophages in Pseudomonas aeruginosa infected patients. Burns. 2006;32(5):644–6.PubMedCrossRef Marza JA, Soothill JS, Boydell P, Collyns TA. Multiplication of therapeutically administered bacteriophages in Pseudomonas aeruginosa infected patients. Burns. 2006;32(5):644–6.PubMedCrossRef
20.
go back to reference Jault P, Leclerc T, Jennes S, Pirnay JP, Que YA, Resch G, Rousseau AF, Ravat F, Carsin H, Le Floch R, 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. 2018;19(1):35–45.PubMedCrossRef Jault P, Leclerc T, Jennes S, Pirnay JP, Que YA, Resch G, Rousseau AF, Ravat F, Carsin H, Le Floch R, 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. 2018;19(1):35–45.PubMedCrossRef
21.
go back to reference Sarker SA, Sultana S, Reuteler G, Moine D, Descombes P, Charton F, Bourdin G, McCallin S, Ngom-Bru C, Neville T, et al. Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. EBioMedicine. 2016;4:124–37.PubMedPubMedCentralCrossRef Sarker SA, Sultana S, Reuteler G, Moine D, Descombes P, Charton F, Bourdin G, McCallin S, Ngom-Bru C, Neville T, et al. Oral phage therapy of acute bacterial diarrhea with two coliphage preparations: a randomized trial in children from Bangladesh. EBioMedicine. 2016;4:124–37.PubMedPubMedCentralCrossRef
22.
go back to reference Merabishvili M, Pirnay JP, Verbeken G, Chanishvili N, Tediashvili M, Lashkhi N, Glonti T, Krylov V, Mast J, Van Parys L, et al. Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PLoS ONE. 2009;4(3):e4944.PubMedPubMedCentralCrossRef Merabishvili M, Pirnay JP, Verbeken G, Chanishvili N, Tediashvili M, Lashkhi N, Glonti T, Krylov V, Mast J, Van Parys L, et al. Quality-controlled small-scale production of a well-defined bacteriophage cocktail for use in human clinical trials. PLoS ONE. 2009;4(3):e4944.PubMedPubMedCentralCrossRef
23.
go back to reference Bruttin A, Brussow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother. 2005;49(7):2874–8.PubMedPubMedCentralCrossRef Bruttin A, Brussow H. Human volunteers receiving Escherichia coli phage T4 orally: a safety test of phage therapy. Antimicrob Agents Chemother. 2005;49(7):2874–8.PubMedPubMedCentralCrossRef
25.
go back to reference Hood IV, Berger JM. Viral hijacking of a replicative helicase loader and its implications for helicase loading control and phage replication. Elife. 2016;5:e14158.PubMedPubMedCentralCrossRef Hood IV, Berger JM. Viral hijacking of a replicative helicase loader and its implications for helicase loading control and phage replication. Elife. 2016;5:e14158.PubMedPubMedCentralCrossRef
26.
go back to reference Tunjungputri RN, Mobegi FM, Cremers AJ, van der Gaast-de Jongh CE, Ferwerda G, Meis JF, Roeleveld N, Bentley SD, Pastura AS, van Hijum SA, et al. Phage-derived protein induces increased platelet activation and is associated with mortality in patients with invasive pneumococcal disease. Bio. 2017;8(1):e01984. Tunjungputri RN, Mobegi FM, Cremers AJ, van der Gaast-de Jongh CE, Ferwerda G, Meis JF, Roeleveld N, Bentley SD, Pastura AS, van Hijum SA, et al. Phage-derived protein induces increased platelet activation and is associated with mortality in patients with invasive pneumococcal disease. Bio. 2017;8(1):e01984.
27.
go back to reference Browne AS, Midwinter AC, Withers H, Cookson AL, Biggs PJ, Marshall JC, Benschop J, Hathaway S, Haack NA, Akhter RN, et al. Molecular epidemiology of shiga toxin-producing Escherichia coli (STEC) on New Zealand Dairy farms: application of a culture-independent assay and whole-genome sequencing. Appl Environ Microbiol. 2018;84(14):1345.CrossRef Browne AS, Midwinter AC, Withers H, Cookson AL, Biggs PJ, Marshall JC, Benschop J, Hathaway S, Haack NA, Akhter RN, et al. Molecular epidemiology of shiga toxin-producing Escherichia coli (STEC) on New Zealand Dairy farms: application of a culture-independent assay and whole-genome sequencing. Appl Environ Microbiol. 2018;84(14):1345.CrossRef
28.
go back to reference Cui Z, Feng T, Gu F, Li Q, Dong K, Zhang Y, Zhu Y, Han L, Qin J, Guo X. Characterization and complete genome of the virulent Myoviridae phage JD007 active against a variety of Staphylococcus aureus isolates from different hospitals in Shanghai, China. Virol J. 2017;14(1):26.PubMedPubMedCentralCrossRef Cui Z, Feng T, Gu F, Li Q, Dong K, Zhang Y, Zhu Y, Han L, Qin J, Guo X. Characterization and complete genome of the virulent Myoviridae phage JD007 active against a variety of Staphylococcus aureus isolates from different hospitals in Shanghai, China. Virol J. 2017;14(1):26.PubMedPubMedCentralCrossRef
29.
go back to reference Moebus K, Nattkemper H. Bacteriophage sensitivity patterns among bacteria isolated from marine waters. Helgoländer Meeresuntersuchungen. 1981;34(3):375–85.CrossRef Moebus K, Nattkemper H. Bacteriophage sensitivity patterns among bacteria isolated from marine waters. Helgoländer Meeresuntersuchungen. 1981;34(3):375–85.CrossRef
30.
go back to reference Synnott AJ, Kuang Y, Kurimoto M, Yamamichi K, Iwano H, Tanji Y. Isolation from sewage influent and characterization of novel Staphylococcus aureus bacteriophages with wide host ranges and potent lytic capabilities. Appl Environ Microbiol. 2009;75(13):4483–90.PubMedPubMedCentralCrossRef Synnott AJ, Kuang Y, Kurimoto M, Yamamichi K, Iwano H, Tanji Y. Isolation from sewage influent and characterization of novel Staphylococcus aureus bacteriophages with wide host ranges and potent lytic capabilities. Appl Environ Microbiol. 2009;75(13):4483–90.PubMedPubMedCentralCrossRef
31.
go back to reference Ding B, Li Q, Guo M, Dong K, Zhang Y, Guo X, Liu Q, Li L, Cui Z. Prevention of dermal abscess formation caused by Staphylococcus aureus using phage JD007 in nude mice. Front Microbiol. 2018;9:1553.PubMedPubMedCentralCrossRef Ding B, Li Q, Guo M, Dong K, Zhang Y, Guo X, Liu Q, Li L, Cui Z. Prevention of dermal abscess formation caused by Staphylococcus aureus using phage JD007 in nude mice. Front Microbiol. 2018;9:1553.PubMedPubMedCentralCrossRef
32.
go back to reference Cui Z, Guo X, Dong K, Zhang Y, Li Q, Zhu Y, Zeng L, Tang R, Li L. Safety assessment of Staphylococcus phages of the family Myoviridae based on complete genome sequences. Sci Rep. 2017;7:41259.PubMedPubMedCentralCrossRef Cui Z, Guo X, Dong K, Zhang Y, Li Q, Zhu Y, Zeng L, Tang R, Li L. Safety assessment of Staphylococcus phages of the family Myoviridae based on complete genome sequences. Sci Rep. 2017;7:41259.PubMedPubMedCentralCrossRef
33.
go back to reference Maura D, Galtier M, Le Bouguenec C, Debarbieux L. Virulent bacteriophages can target O104:H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrob Agents Chemother. 2012;56(12):6235–42.PubMedPubMedCentralCrossRef Maura D, Galtier M, Le Bouguenec C, Debarbieux L. Virulent bacteriophages can target O104:H4 enteroaggregative Escherichia coli in the mouse intestine. Antimicrob Agents Chemother. 2012;56(12):6235–42.PubMedPubMedCentralCrossRef
34.
go back to reference Llaca-Diaz JM, Mendoza-Olazaran S, Camacho-Ortiz A, Flores S, Garza-Gonzalez E. One-year surveillance of ESKAPE pathogens in an intensive care unit of Monterrey, Mexico. Chemotherapy. 2012;58(6):475–81.PubMedCrossRef Llaca-Diaz JM, Mendoza-Olazaran S, Camacho-Ortiz A, Flores S, Garza-Gonzalez E. One-year surveillance of ESKAPE pathogens in an intensive care unit of Monterrey, Mexico. Chemotherapy. 2012;58(6):475–81.PubMedCrossRef
35.
go back to reference Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. Bad bugs, no drugs: no ESKAPE! an update from the infectious diseases society of America. Clin Infect Dis. 2009;48(1):1–12.PubMedCrossRef Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, Scheld M, Spellberg B, Bartlett J. Bad bugs, no drugs: no ESKAPE! an update from the infectious diseases society of America. Clin Infect Dis. 2009;48(1):1–12.PubMedCrossRef
36.
go back to reference Gu J, Liu X, Li Y, Han W, Lei L, Yang Y, Zhao H, Gao Y, Song J, Lu R, et al. A method for generation phage cocktail with great therapeutic potential. PLoS ONE. 2012;7(3):e31698.PubMedPubMedCentralCrossRef Gu J, Liu X, Li Y, Han W, Lei L, Yang Y, Zhao H, Gao Y, Song J, Lu R, et al. A method for generation phage cocktail with great therapeutic potential. PLoS ONE. 2012;7(3):e31698.PubMedPubMedCentralCrossRef
37.
go back to reference Habusha M, Tzipilevich E, Fiyaksel O, Ben-Yehuda S. A mutant bacteriophage evolved to infect resistant bacteria gained a broader host range. Mol Microbiol. 2019;111(6):1463–75.PubMedCrossRef Habusha M, Tzipilevich E, Fiyaksel O, Ben-Yehuda S. A mutant bacteriophage evolved to infect resistant bacteria gained a broader host range. Mol Microbiol. 2019;111(6):1463–75.PubMedCrossRef
38.
go back to reference Chen J, Quiles-Puchalt N, Chiang YN, Bacigalupe R, Fillol-Salom A, Chee MSJ, Fitzgerald JR, Penades JR. Genome hypermobility by lateral transduction. Science. 2018;362(6411):207–12.PubMedCrossRef Chen J, Quiles-Puchalt N, Chiang YN, Bacigalupe R, Fillol-Salom A, Chee MSJ, Fitzgerald JR, Penades JR. Genome hypermobility by lateral transduction. Science. 2018;362(6411):207–12.PubMedCrossRef
39.
go back to reference Malik DJ, Sokolov IJ, Vinner GK, Mancuso F, Cinquerrui S, Vladisavljevic GT, Clokie MRJ, Garton NJ, Stapley AGF, Kirpichnikova A. Formulation, stabilisation and encapsulation of bacteriophage for phage therapy. Adv Coll Interface Sci. 2017;249:100–33.CrossRef Malik DJ, Sokolov IJ, Vinner GK, Mancuso F, Cinquerrui S, Vladisavljevic GT, Clokie MRJ, Garton NJ, Stapley AGF, Kirpichnikova A. Formulation, stabilisation and encapsulation of bacteriophage for phage therapy. Adv Coll Interface Sci. 2017;249:100–33.CrossRef
40.
go back to reference Vandenheuvel D, Singh A, Vandersteegen K, Klumpp J, Lavigne R, Van den Mooter G. Feasibility of spray drying bacteriophages into respirable powders to combat pulmonary bacterial infections. Eur J Pharm Biopharm. 2013;84(3):578–82.PubMedCrossRef Vandenheuvel D, Singh A, Vandersteegen K, Klumpp J, Lavigne R, Van den Mooter G. Feasibility of spray drying bacteriophages into respirable powders to combat pulmonary bacterial infections. Eur J Pharm Biopharm. 2013;84(3):578–82.PubMedCrossRef
41.
go back to reference Hoe S, Semler DD, Goudie AD, Lynch KH, Matinkhoo S, Finlay WH, Dennis JJ, Vehring R. Respirable bacteriophages for the treatment of bacterial lung infections. J Aerosol Med Pulm Drug Del. 2013;26(6):317–35.CrossRef Hoe S, Semler DD, Goudie AD, Lynch KH, Matinkhoo S, Finlay WH, Dennis JJ, Vehring R. Respirable bacteriophages for the treatment of bacterial lung infections. J Aerosol Med Pulm Drug Del. 2013;26(6):317–35.CrossRef
42.
go back to reference Golshahi L, Lynch KH, Dennis JJ, Finlay WH. In vitro lung delivery of bacteriophages KS4-M and PhiKZ using dry powder inhalers for treatment of Burkholderia cepacia complex and Pseudomonas aeruginosa infections in cystic fibrosis. J Appl Microbiol. 2011;110(1):106–17.PubMedCrossRef Golshahi L, Lynch KH, Dennis JJ, Finlay WH. In vitro lung delivery of bacteriophages KS4-M and PhiKZ using dry powder inhalers for treatment of Burkholderia cepacia complex and Pseudomonas aeruginosa infections in cystic fibrosis. J Appl Microbiol. 2011;110(1):106–17.PubMedCrossRef
43.
go back to reference Boulanger P. Purification of bacteriophages and SDS-PAGE analysis of phage structural proteins from ghost particles. Methods Mol Biol. 2009;502:227–38.PubMedCrossRef Boulanger P. Purification of bacteriophages and SDS-PAGE analysis of phage structural proteins from ghost particles. Methods Mol Biol. 2009;502:227–38.PubMedCrossRef
44.
go back to reference Bourdin G, Schmitt B, Marvin Guy L, Germond JE, Zuber S, Michot L, Reuteler G, Brussow H. Amplification and purification of T4-like Escherichia coli phages for phage therapy: from laboratory to pilot scale. Appl Environ Microbiol. 2013;80(4):1469–76.PubMedCrossRef Bourdin G, Schmitt B, Marvin Guy L, Germond JE, Zuber S, Michot L, Reuteler G, Brussow H. Amplification and purification of T4-like Escherichia coli phages for phage therapy: from laboratory to pilot scale. Appl Environ Microbiol. 2013;80(4):1469–76.PubMedCrossRef
45.
go back to reference Boratynski J, Syper D, Weber-Dabrowska B, Lusiak-Szelachowska M, Pozniak G, Gorski A. Preparation of endotoxin-free bacteriophages. Cell Mol Biol Lett. 2004;9(2):253–9.PubMed Boratynski J, Syper D, Weber-Dabrowska B, Lusiak-Szelachowska M, Pozniak G, Gorski A. Preparation of endotoxin-free bacteriophages. Cell Mol Biol Lett. 2004;9(2):253–9.PubMed
46.
go back to reference Hashemi H, Pouyanfard S, Bandehpour M, Mahmoudi M, Bernasconi M, Kazemi B, Mokhtari-Azad T. Efficient endotoxin removal from T7 phage preparations by a mild detergent treatment followed by ultrafiltration. Acta Virol. 2013;57(3):373–4.PubMed Hashemi H, Pouyanfard S, Bandehpour M, Mahmoudi M, Bernasconi M, Kazemi B, Mokhtari-Azad T. Efficient endotoxin removal from T7 phage preparations by a mild detergent treatment followed by ultrafiltration. Acta Virol. 2013;57(3):373–4.PubMed
47.
go back to reference Bonilla N, Rojas MI, Netto Flores Cruz G, Hung SH, Rohwer F, Barr JJ. Phage on tap-a quick and efficient protocol for the preparation of bacteriophage laboratory stocks. PeerJ. 2016;4:e2261.PubMedPubMedCentralCrossRef Bonilla N, Rojas MI, Netto Flores Cruz G, Hung SH, Rohwer F, Barr JJ. Phage on tap-a quick and efficient protocol for the preparation of bacteriophage laboratory stocks. PeerJ. 2016;4:e2261.PubMedPubMedCentralCrossRef
48.
go back to reference Beaber JW, Hochhut B, Waldor MK. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature. 2004;427(6969):72–4.PubMedCrossRef Beaber JW, Hochhut B, Waldor MK. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature. 2004;427(6969):72–4.PubMedCrossRef
49.
go back to reference Kohanski MA, DePristo MA, Collins JJ. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol Cell. 2010;37(3):311–20.PubMedPubMedCentralCrossRef Kohanski MA, DePristo MA, Collins JJ. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol Cell. 2010;37(3):311–20.PubMedPubMedCentralCrossRef
50.
51.
go back to reference Ho K, Huo W, Pas S, Dao R, Palmer KL. Loss of function mutations in epaR confer resistance to phage NPV1 infection in Enterococcus faecalis OG1RF. Antimicrob Agents Chemother. 2018;62(10):e00758.PubMedPubMedCentralCrossRef Ho K, Huo W, Pas S, Dao R, Palmer KL. Loss of function mutations in epaR confer resistance to phage NPV1 infection in Enterococcus faecalis OG1RF. Antimicrob Agents Chemother. 2018;62(10):e00758.PubMedPubMedCentralCrossRef
52.
go back to reference Chhibber S, Kaur T, Sandeep K. Co-therapy using lytic bacteriophage and linezolid: effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS ONE. 2013;8(2):e56022.PubMedPubMedCentralCrossRef Chhibber S, Kaur T, Sandeep K. Co-therapy using lytic bacteriophage and linezolid: effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS ONE. 2013;8(2):e56022.PubMedPubMedCentralCrossRef
53.
go back to reference Lusiak-Szelachowska M, Zaczek M, Weber-Dabrowska B, Miedzybrodzki R, Klak M, Fortuna W, Letkiewicz S, Rogoz P, Szufnarowski K, Jonczyk-Matysiak E, et al. Phage neutralization by sera of patients receiving phage therapy. Viral Immunol. 2014;27(6):295–304.PubMedPubMedCentralCrossRef Lusiak-Szelachowska M, Zaczek M, Weber-Dabrowska B, Miedzybrodzki R, Klak M, Fortuna W, Letkiewicz S, Rogoz P, Szufnarowski K, Jonczyk-Matysiak E, et al. Phage neutralization by sera of patients receiving phage therapy. Viral Immunol. 2014;27(6):295–304.PubMedPubMedCentralCrossRef
54.
go back to reference Colom J, Cano-Sarabia M, Otero J, Arinez-Soriano J, Cortes P, Maspoch D, Llagostera M. Microencapsulation with alginate/CaCO3: a strategy for improved phage therapy. Sci Rep. 2017;7:41441.PubMedPubMedCentralCrossRef Colom J, Cano-Sarabia M, Otero J, Arinez-Soriano J, Cortes P, Maspoch D, Llagostera M. Microencapsulation with alginate/CaCO3: a strategy for improved phage therapy. Sci Rep. 2017;7:41441.PubMedPubMedCentralCrossRef
55.
go back to reference Woolwine JD, Gerberding JL. Effect of testing method on apparent activities of antiviral disinfectants and antiseptics. Antimicrob Agents Chemother. 1995;39(4):921–3.PubMedPubMedCentralCrossRef Woolwine JD, Gerberding JL. Effect of testing method on apparent activities of antiviral disinfectants and antiseptics. Antimicrob Agents Chemother. 1995;39(4):921–3.PubMedPubMedCentralCrossRef
57.
go back to reference Hosseinidoust Z, Tufenkji N, van de Ven TG. Predation in homogeneous and heterogeneous phage environments affects virulence determinants of Pseudomonas aeruginosa. Appl Environ Microbiol. 2013;79(9):2862–71.PubMedPubMedCentralCrossRef Hosseinidoust Z, Tufenkji N, van de Ven TG. Predation in homogeneous and heterogeneous phage environments affects virulence determinants of Pseudomonas aeruginosa. Appl Environ Microbiol. 2013;79(9):2862–71.PubMedPubMedCentralCrossRef
58.
go back to reference Cai R, Wu M, Zhang H, Zhang Y, Cheng M, Guo Z, Ji Y, Xi H, Wang X, Xue Y, et al. A smooth-type, phage-resistant Klebsiella pneumoniae mutant strain reveals OmpC is indispensable for GH-K3 infection. Appl Environ Microbiol. 2018;84(21):e01585.PubMedPubMedCentralCrossRef Cai R, Wu M, Zhang H, Zhang Y, Cheng M, Guo Z, Ji Y, Xi H, Wang X, Xue Y, et al. A smooth-type, phage-resistant Klebsiella pneumoniae mutant strain reveals OmpC is indispensable for GH-K3 infection. Appl Environ Microbiol. 2018;84(21):e01585.PubMedPubMedCentralCrossRef
59.
60.
go back to reference Sarker SA, McCallin S, Barretto C, Berger B, Pittet AC, Sultana S, Krause L, Huq S, Bibiloni R, Bruttin A, et al. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology. 2012;434(2):222–32.PubMedCrossRef Sarker SA, McCallin S, Barretto C, Berger B, Pittet AC, Sultana S, Krause L, Huq S, Bibiloni R, Bruttin A, et al. Oral T4-like phage cocktail application to healthy adult volunteers from Bangladesh. Virology. 2012;434(2):222–32.PubMedCrossRef
Metadata
Title
Exploring the whole standard operating procedure for phage therapy in clinical practice
Authors
Zelin Cui
Xiaokui Guo
Tingting Feng
Li Li
Publication date
01-12-2019
Publisher
BioMed Central
Keyword
Antibiotic
Published in
Journal of Translational Medicine / Issue 1/2019
Electronic ISSN: 1479-5876
DOI
https://doi.org/10.1186/s12967-019-2120-z

Other articles of this Issue 1/2019

Journal of Translational Medicine 1/2019 Go to the issue