Abstract
Upsurge in the instances of antibiotic-resistant uropathogenic Escherichia .coli (UPECs) strains has repositioned the attention of researchers towards a century old antimicrobial approach popularly known as phage therapy. Rise of extended spectrum beta lactamase (ESBL) and biofilm producing strains has added another step of hurdle in treatment of uropathogens with conventional antibiotics, thus providing a further impetus for search for exploring new therapeutic measures. In this direction, bacteriophages, commonly called phages, are recently being considered as potential alternatives for treatment of UPECs. Phages are the tiniest form of viruses which are ubiquitous in nature and highly specific for their host. This review discusses the possible ways of using natural phages, genetically engineered phages, and phage lytic enzymes (PLEs) as an alternative antimicrobial treatment for urinary tract infections. The review also sheds light on the synergistic use of conventional antibiotics with phages or PLEs for treatment of uropathogens. These methods of using phages and their derivatives, alone or in combination with antibiotics, have proved fruitful so far in in vitro studies. However, in vivo studies are required to make them accessible for human use. The present review is a concerted effort towards putting together all the information available on the subject.
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Abdelkader K, Gerstmans H, Saafan A, Dishisha T, Briers Y (2019) The preclinical and clinical progress of bacteriophages and their lytic enzymes: the parts are easier than the whole. Viruses 11:96. https://doi.org/10.3390/v11020096
Abedon ST, García P, Mullany P, Aminov R (2017) Editorial: phage therapy: past, present and future. Front Microbiol 8:981. https://doi.org/10.3389/fmicb.2017.00981
Ackermann H-W, Krisch HM (1997) A catalogue of T4-type bacteriophages. Arch Virol 142:2329–2345
Akova M (2016) Epidemiology of antimicrobial resistance in bloodstream infections. Virulence 7:252–266. https://doi.org/10.1080/21505594.1159366
Aminov RI (2010) A brief history of the antibiotic era: lessons learned and challenges for the future. Front Microbiol 1:1–7. https://doi.org/10.3389/fmicb.2010.00134
Bedi MS, Verma V, Chhibber S (2009) Amoxicillin and specific bacteriophage can be used together for eradication of biofilm of Klebsiella pneumoniae B5055. World J Microbiol Biotechnol 25:1145–1151. https://doi.org/10.1007/s11274-009-9991-8
Beloin C, Roux A, Ghigo JM (2008) Escherichia coli biofilms. Curr Top Microbiol Immunol 322:249–289
Bolocan AS, Callanan J, Forde A, Ross P, Hill C (2016) Phage therapy targeting Escherichia coli—a story with no end? FEMS Microbiol Lett 363:1–5. https://doi.org/10.1093/femsle/fnw256
Briers Y, Lavigne R (2015) Breaking barriers: expansion of the use of endolysins as novel antibacterials against gram-negative bacteria. Future Microbiol 10:377–390. https://doi.org/10.2217/fmb.15.8
Briers Y, Walmagh M, Grymonprez B, Biebl M, Pirnay JP, Defraine V, Michiels J, Cenens W, Aertsen A, Miller S, Lavigne R (2014a) Art-175 is a highly efficient antibacterial against multidrug-resistant strains and persisters of Pseudomonas aeruginosa. Antimicrob Agents Chemother 58:3774–3784. https://doi.org/10.1128/AAC.02668-14
Briers Y, Walmagh M, Van Puyenbroeck V, Cornelissen A, Cenens W, Aertsen A, Oliveira H, Azeredo J, Verween G, Pirnay JP et al (2014b) Engineered endolysin-based “artilysins” to combat multidrugresistant gram-negative pathogens. mBio 5:e01379-14. https://doi.org/10.1128/mBio.01379-14
Buonanno AP, Damweber BJ (2006) Review of urinary tract infection. US Pharm 31:HS26–HS36
Burrowes B, Harper DR, Anderson J, McConville M, Enright MC (2011) Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev Anti-Infect Ther 9:775–785. https://doi.org/10.1586/eri.11.90
Capparelli R, Ventimiglia I, Roperto S, Fenizia D, Iannelli D (2006) Selection of an Escherichia coli O157:H7 bacteriophage for persistence in the circulatory system of mice infected experimentally. Clin Microbiol Infect 12:248–253. https://doi.org/10.1111/j.1469-0691.2005.01340.x
Carlton RM (1999) Phage therapy: past history and future prospects. Arch Immunol Ther Exp 47:267–274
Chadha P, Katare OP, Chibber S (2016) In vivo efficacy of single phage versus phage cocktail in resolving burn wound infection in BALB/c mice. Microb Pathog 99:68–77
Chaudhry WN, Concepción-Acevedo J, Park T, Andleeb S, Bull JJ, Levin BR (2017) Synergy and order effects of antibiotics and phages in killing Pseudomonas aeruginosa biofilms. PLoS One 12:e0168615. https://doi.org/10.1371/journal.pone.0168615
Chibeu A, Lingohr EJ, Masson L, Manges A, Harel J, Ackermann HW, Kropinski AM, Boerlin P (2012) Bacteriophages with the ability to degrade uropathogenic Escherichia Coli biofilms. Viruses 4:471–487. https://doi.org/10.3390/v4040471
Comeau AM, Tetart F, Trojet SN, Prere MF, Krisch HM (2007) Phage-antibiotic synergy (PAS): β-lactam and quinolone antibiotics stimulate virulent phage growth. PLoS One 2:e799. https://doi.org/10.1371/journal.pone.0000799
Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745
Coulter LB, McLean RJC, Rohde RE, Aron GM (2014) Effect of bacteriophage infection in combination with tobramycin on the emergence of resistance in Escherichia coli and Pseudomonas aeruginosa biofilms. Viruses 6:3778–3786. https://doi.org/10.3390/v6103778
Davies J (2008) Resistance redux: infectious diseases, antibiotic resistance and the future of mankind. EMBO Rep 9:S18–S21. https://doi.org/10.1038/embor.2008.69
Delbruck M (1940) The growth of bacteriophage and lysis of the host. J Gen Physiol 23:643–660
Detweiler K, Mayers D, Fletcher SG (2015) Bacteruria and urinary tract infections in the elderly. Urol Clin North Am 42:561–568
D'Herelle F (1917) On an invisible microbe antagonistic toward dysenteric bacilli: brief note by Mr. F. D’Herelle, presented by Mr. Roux. Res Microbiol 158:553–554. https://doi.org/10.1016/j.resmic.2007.07.005
DooIittle MM, Cooney JJ, Caldwell DE (1995) Lytic infection of Escherichia coli biofilms by bacteriophage T4. Can J Microbiol 41:12–18
Fischetti VA (2005) Bacteriophage lytic enzymes: novel anti-infectives. Trends Microbiol 13:491–496
Flemming HC, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S (2016) Biofilms: an emergent form of bacterial life. Nat Rev Microbiol 14:563–575. https://doi.org/10.1038/nrmicro.2016.94
Flores-Mireles AL, Walker JN, Caparon M, Hultgren SJ (2015) Urinary tract infections: epidemiology, mechanisms of infection and treatment options. Nat Rev Microbiol 13:269–284. https://doi.org/10.1038/nrmicro3432
Forti F, Roach DR, Cafora M, Pasini ME, Horner DS, Fiscarelli EV, Rossitto M, Cariani L, Briani F, Debarbieux L, Ghisotti D (2018) Design of a broad-range bacteriophage cocktail that reduces Pseudomonas aeruginosa biofilms and treats acute infections in two animal models. Antimicrob Agents Chemother 62:e02573–e02517. https://doi.org/10.1128/AAC.02573-17
Foxman B (2010) The epidemiology of urinary tract infection. Nat Rev Urol 7:653–660
Foxman B (2013) Urinary tract infection. In: Goldman MB, Troisi R and Rexrode KM (ed) Women and Health, 2nd edn. Academic Press, Cambridge, pp 553–564
Frieri M, Kumar K, Boutin A (2017) Antibiotic resistance. J Infect Public Health 10:369–378
Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM (2010) Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother 54:397–404. https://doi.org/10.1128/AAC.00669-09
Furfaro LL, Payne MS, Chang BJ (2018) Bacteriophage therapy: clinical trials and regulatory hurdles. Front Cell Infect Microbiol 8:376. https://doi.org/10.3389/fcimb.2018.00376
Gill JJ, Hyman P (2010) Phage choice, isolation and preparation for phage therapy. Curr Pharm Biotechnol 11:2–14
Goodridge LD (2010) Designing phage therapeutics. Curr Pharm Biotechnol 11:15–27. https://doi.org/10.2174/138920110790725348
Górski A, Międzybrodzki R, Węgrzyn G, Jończyk Matysiak E, Borysowski J, Weber Dąbrowska B (2019) Phage therapy: current status and perspectives. Med Res Rev:1–5. https://doi.org/10.1002/med.21593
Griebling TL (2004) Urinary tract infection in women. In: Litwin MS, Saigal CS (eds) Urologic diseases in America. US Government Publishing Office, Washington DC, pp 153–183
Gu J, Liu X, Li Y, Han W, Lei L, Yang Y, Zhao H, Gao Y, Song J, Lu R, Sun C, Feng X (2012) A method for generation phage cocktail with great therapeutic potential. PLoS One 7:1–8. https://doi.org/10.1371/journal.pone.0031698
Guo M, Feng C, Ren J, Zhuang X, Zhang Y, Zhu Y, Dong K, He P, Guo X, Qin J (2017) A novel antimicrobial Endolysin, LysPA26, against Pseudomonas aeruginosa. Front Microbiol 8:293. https://doi.org/10.3389/fmicb.2017.0029
Gupta K, Hooton TM, Naber KG, Wullt B, Colgan R, Miller LG, Moran GJ, Nicolle LE, Raz R, Schaeffer AJ, Soper DE (2011) International clinical practice guidelines for the treatment of acute uncomplicated cystitis and pyelonephritis in women: a 2010 update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious Diseases. Clin Infect Dis 52:e103–e120
Gutiérrez D, Fernández L, Rodríguez A, García P (2018) Are phage lytic proteins the secret weapon to kill Staphylococcus aureus? mBio 9:e01923-17. https://doi.org/10.1128/mBio.01923-17
Hankin ME (2011) The bactericidal action of the waters of the Jamuna and Ganges rivers on cholera microbes Ann. Inst. Pasteur 10:511–523 (1896). Bacteriophage 1:117–126. https://doi.org/10.4161/bact.1.3.16736
Henning U, Jann K (1979) Two-component nature of bacteriophage T4 receptor activity in Escherichia coli K-12. J Bacteriol 137:664–666
Hotchandani R, Aggarwal KK (2012) Urinary tract infections in women. Indian J Clin Pract 23:187–192
Hyman P, Abedon ST (2010) Bacteriophage host range and bacterial resistance. Adv Appl Microbiol 70:217–248. https://doi.org/10.1016/S0065-2164(10)70007-1
Jacobsen SM, Stickler DJ, Mobley HLT, Shirtliff ME (2008) Complicated catheter-associated urinary tract infections due to Escherichia coli and Proteus mirabilis. Clin Microbiol Rev 21:26–59. https://doi.org/10.1128/CMR.00019-07
Kamal F, Dennis JJ (2015) Burkholderia cepacia complex phage-antibiotic synergy (PAS): antibiotics stimulate lytic phage activity. Appl Environ Microbiol 81:1132–1138. https://doi.org/10.1128/AEM.02850-14
Kaper JB, Nataro JP, Mobley HL (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140. https://doi.org/10.1038/nrmicro818
Kelly D, McAuliffe O, Ross RP, Coffey A (2012) Prevention of Staphylococcus aureus biofilm formation and reduction in established biofilm density using a combination of phage K and modified derivatives. Lett Appl Microbiol 54:286–291. https://doi.org/10.1111/j.1472-765X.2012.03205
Kim M, Jo Y, Hwang YJ, Hong HW, Hong SS, Park K, Myung H (2018) Phage antibiotic synergy via delayed lysis. Appl Environ Microbiol 84:e02085–e02018. https://doi.org/10.1128/AEM.02085-18
Kline KA, Bowdish DM (2016) Infection in an aging population. Curr Opin Microbiol 29:63–67. https://doi.org/10.1016/j.mib.2015.11.003
Knezevic P, Curcin S, Aleksic V, Petrusic M, Vlaski L (2013) Phage-antibiotic synergism: a possible approach to combating Pseudomonas aeruginosa. Res Microbiol 164:55–60. https://doi.org/10.1016/j.resmic.2012.08.008
Kutter E, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S et al (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11:69–86. https://doi.org/10.2174/138920110790725401
Lane MC, Lockatell V, Monterosso G, Lamphier D, Weinert J, Hebel JR, Johnson DE, Mobley HL (2005) Role of motility in the colonization of uropathogenic Escherichia coli in the urinary tract. Infect Immun 73:7644–7656
Lehman SM, Donlan RM (2015) Bacteriophage-mediated control of a two-species biofilm formed by microorganisms causing catheter-associated urinary tract infections in an in vitro urinary catheter model. Antimicrob Agents Chemother 59:1127–1137. https://doi.org/10.1128/AAC.03786-14
Lenski RE (1984) Two-step resistance by Escherichia coli B to bactreriophage T2. Genetics 107:1–7
Letrado P, Corsini B, Díez-Martínez R, Bustamante N, Yuste JE, García P (2018) Bactericidal synergism between antibiotics and phage endolysin Cpl-711 to kill multidrug-resistant pneumococcus. Future Microbiol 13:1215–1223. https://doi.org/10.2217/fmb-2018-0077
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. https://doi.org/10.4292/wjgpt.v8.i3.162
Lindberg AA (1973) Bacteriophage receptors. Annu Rev Microbiol 27:205–241. https://doi.org/10.1146/annurev.mi.27.100173.001225
Loc-Carrillo C, Abedon ST (2011) Pros and cons of phage therapy. Bacteriophage 1:111–114. https://doi.org/10.4161/bact.1.2.14590
Lu TK, Collins JJ (2007) Dispersing biofilms with engineered enzymatic bacteriophage. Proc Natl Acad Sci U S A 104:11197–11202. https://doi.org/10.1073/pnas.0704624104
Lu TK, Koeris MS (2011) The next generation of bacteriophage therapy. Curr Opin Microbiol 14:524–531. https://doi.org/10.1016/j.mib.2011.07.028
Lukacik P, Barnard T, Keller PW et al (2012a) Structural engineering of a phage lysin that target gram-negative pathogens. Proc Natl Acad Sci U S A 109:9857–9862. https://doi.org/10.1073/pnas.1203472109
Lukacik P, Barnard TJ, Buchanan SK (2012b) Using a bacteriocin structure to engineer a phage lysin that targets Yersinia pestis. Biochem Soc Trans 40:1503–1506. https://doi.org/10.1042/BST20120209
Ma Q, Guo Z, Gao C, Zhu R, Wang S, Yu L, Qin W, Xia X, Gu J, Yan G, Lei L (2017) Enhancement of the direct antimicrobial activity of Lysep3 against Escherichia coli by inserting cationic peptides into its C-terminus. Antonie Leeuwenhoek 110:347–355. https://doi.org/10.1007/s10482-016-0806-2
Manning SD (2010) Escherichia coli infections. Deadly Disease and Epidemics. Chelsea House Publishers, NewYork
Martens E, Demain AL (2017) The antibiotic resistance crisis, with a focus on the United States. J Antibiot 70:520–526. https://doi.org/10.1038/ja.2017.30
Matsuzaki S, Rashel M, Uchiyama J, Sakurai S, Ujihara T, Kuroda M, Imai S, Ikeuchi M, Tani T, Fujieda M, Wakiguchi H (2005) Bacteriophage therapy: a revitalized therapy against bacterial infectious diseases. J Infect Chemother 11:211–219. https://doi.org/10.1007/s10156-005-0408-9
McCallin S, Sacher JC, Zheng J, Chan BK (2019) Current state of compassionate phage therapy. Viruses 11:343. https://doi.org/10.3390/v11040343
Møller-Olsen C, Ho SFS, Shukla RD, Feher T, Sagona AP (2018) Engineered K1F bacteriophages kill intracellular Escherichia coli K1 in human epithelial cells. Sci Rep 8:17559. https://doi.org/10.1038/s41598-018-35859-6
Montag D, Hashemolhosseini S, Henning U (1990) Receptor recognizing proteins of T-even type bacteriophages. The receptor recognizing area of proteins 37 of phages T4 Tula and Tulb. J Mol Biol 216:327–334. https://doi.org/10.1016/S0022-2836(05)80324-9
Mulvey MA (2002) Adhesion and entry of uropathogenic Escherichia coli. Cell Microbiol 4:257–271
Nishikawa H, Yasuda M, Uchiyama J, Rashel M, Maeda Y, Takemura I, Sugihara S, Ujihara T, Shimizu Y, Shuin T, Matsuzaki S (2008) T-even-related bacteriophages as candidates for treatment of Escherichia coli urinary tract infections. Arch Virol 153:507–515. https://doi.org/10.1007/s00705-007-0031-4
Oechslin F, Piccardi P, Mancini S, Gabard J, Moreillon P, Entenza JM, Resch G, Que Y-A (2017) Synergistic interaction between phage therapy and antibiotics clears Pseudomonas aeruginosa infection in endocarditis and reduces virulence. J Infect Dis 215:703–712. https://doi.org/10.1093/infdis/jiw632
Oliveira H, Sao-Jose C, Azeredo J (2018) Phage-derived peptidoglycan degrading enzymes: challenges and future prospects for in vivo therapy. Viruses 10:292. https://doi.org/10.3390/v10060292
Paul VD, Rajagopalan SS, Sundarrajan S, George SE, Asrani JY, Pillai R, Chikkamadaiah R, Durgaiah M, Sriram B, Padmanabhan S (2011a) A novel bacteriophage tail-associated muralytic enzyme (TAME) from phage K and its development into a potent antistaphylococcal protein. BMC Microbiol 11:226. https://doi.org/10.1186/1471-2180-11-226
Paul VD, Sundarrajan S, Rajagopalan SS, Hariharan S, Kempashanaiah N, Padmanabhan S, Sriram B, Ramachandran J (2011b) Lysis-deficient phages as novel therapeutic agents for controlling bacterial infection. BMC Microbiol 11:195. https://doi.org/10.1186/1471-2180-11-195
Pei R, Lamas-Samanamud GR (2014) Inhibition of biofilm formation by T7 bacteriophages producing quorum-quenching enzymes. Appl Environ Microbiol 80:5340–5348. https://doi.org/10.1128/AEM.01434-14
Pena C, Gudiol C, Tubau F, Saballs M, Pujol M, Dominguez MA, Calatayud L, Ariza J, Gudiol F (2006) Risk-factors for acquisition of extended-spectrum β-lactamase-producing Escherichia coli among hospitalised patients. Clin Microbiol Infect 12:279–284. https://doi.org/10.1111/j.1469-0691.2005.01358.x
Pires DP, Cleto S, Sillankorva S, Azeredo J, Lu TK (2016) Genetically engineered phages: a review of advances over the last decade. Microbiol Mol Biol Rev 80:523–543. https://doi.org/10.1128/MMBR.00069-15
Pires DP, Melo LDR, Vilas Boas D, Sillankorva S, Azeredo J (2017) Phage therapy as an alternative or complementary strategy to prevent and control biofilm-related infections. Curr Opin Microbiol 39:48–56. https://doi.org/10.1016/j.mib.2017.09.004
Pirnay JP, De Vos D, Verbeken G et al (2010) The phage therapy paradigm: Prêt-à-porter or Sur-mesure? Pharm Res 28:934–937. https://doi.org/10.1007/s11095-010-0313-5
Pushpalatha KS (2008) Urinary tract infection and management. J Nighting Nursing Times 4:28–32
Rodriguez L, Martinez B, Zhou Y, Rodriguez A, Donovan DM, Garcia P (2011) Lytic activity of the virion-associated peptidoglycan hydrolase HydH5 of Staphylococcus aureus bacteriophage vb_SauS-phiiPLA88. BMC Microbiol 11:138. https://doi.org/10.1186/1471-2180-11-138
Rodríguez-Rubio L, Gutiérrez D, Donovan DM, Martínez B, Rodríguez A, García P (2016) Phage lytic proteins: biotechnological applications beyond clinical antimicrobials. Crit Rev Biotechnol 36:542–552. https://doi.org/10.3109/07388551.2014.993587
Ronald A (2003) The etiology of urinary tract infection: traditional and emerging pathogens. Dis Mon 49:71–82. https://doi.org/10.1067/mda.2003.8
Ryan EM, Mahmoud Y, Alkawareek RF, Donnelly GBF (2012) Synergistic phage-antibiotic combinations for the control of Escherichia coli biofilms in vitro. FEMS Immunol Med Microbiol 65:395–398. https://doi.org/10.1111/j.1574-695X.2012.00977.x
Salazar O, Asenjo JA (2007) Enzymatic lysis of microbial cells. Biotechnol Lett 29:985–994. https://doi.org/10.1007/s10529-007-9345-2
Salman AE, Abdulamir AS (2014) Assessment of bacteriophage cocktails used in treating multiple-drug resistant Pseudomonas aeruginosa. Int J Curr Microbiol App Sci 3:711–723
Samsygina GA, Boni EG (1984) Bacteriophages and phage therapy in pediatric practice. Pediatriia 4:67–70
Sao-José C (2018) Engineering of phage-derived lytic enzymes: improving their potential as antimicrobials. Antibiotics 7:29. https://doi.org/10.3390/antibiotics7020029
Schirmeier E, Zimmermann P, Hofmann V, Biebl M, Gerstmans H, Maervoet VE, Briers Y (2017) Inhibitory and bactericidal effect of Artilysin® Art-175 against colistin-resistant mcr-1-positive Escherichia coli isolates. Int J Antimicrob Agents 51:528–529. https://doi.org/10.1016/j.ijantimicag.2017.08.027
Schmelcher M, Donovan DM, Loessner MJ (2012) Bacteriophage endolysins as novel antimicrobials. Future Microbiol 7:1147–1171. https://doi.org/10.2217/fmb.12.97
Scholl D, Rogers S, Adhya S, Merril CR (2001) Bacteriophage K1–5 encodes two different tail fiber proteins, allowing it to infect and replicate on both K1 and K5 strains of Escherichia coli. J Virol 75:2509–2515
Sharma G, Sharma S, Sharma P, Chandola D, Dang S, Gupta S, Gabrani R (2016) Escherichia coli biofilm: development and therapeutic strategies. J Appl Microbiol 121:309–319. https://doi.org/10.1111/jam.13078
Sillankorva S, Oliveira D, Moura A, Henriques M, Faustino A, Nicolau A, Azeredo J (2010) Efficacy of a broad host range lytic bacteriophage against E. coli adhered to urothelium. Curr Microbiol 62:1128–1132. https://doi.org/10.1007/s00284-010-9834-8
Singh SB, Barrett JF (2006) Empirical antibacterial drug discovery - foundation in natural products. Biochem Pharmacol 71:1006–1015. https://doi.org/10.1016/j.bcp.2005.12.016
Sulakvelidze A, Alavidze Z, Morris JG Jr (2001) Bacteriophage therapy. Antimicrob Agents Chemother 45:649–659. https://doi.org/10.1128/AAC.45.3.649-659.2001
Tacconelli; Magrini (2017) Global priority list of antiobiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. World Health Organization. www.who.int/medicines/publications/WHO-PPL-Short_Summary_25Feb-ET_NM_WHO.pdf. Accessed 27 February 2017
Tanji Y, Shimada T, Yoichi M, Miyanaga K, Hori K, Unno H (2004) Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl Microbiol Biotechnol 64:270–274
Tetart F, Desplats C, Kutateladze M, Monod C, Ackermann H-W, Krisch HM (2001) Phylogeny of the major head and tail genes of the wide-ranging T4-type bacteriophages. J Bacteriol 183:358–366. https://doi.org/10.1128/JB.183.1.358-366.2001
Torres-Barceló C, Arias-Sánchez FI, Vasse M, Ramsayer J, Kaltz O, Hochberg ME (2014) A Window of Opportunity to Control the Bacterial Pathogen Pseudomonas aeruginosa Combining Antibiotics and Phages. PLoS ONE 9:e106628. https://doi.org/10.1371/journal.pone.0106628
Twort FW (1915) An investigation on the nature of the ultramicroscopic viruses. Lancet 186:1241–1243. https://doi.org/10.1016/S0140-6736(01)20383-3
Ujmajuridze A, Chanishvili N, Goderdzishvili M, Leitner L, Mehnert U, Chkhotua A, Kessler TM, Sybesma W (2018) Adapted bacteriophages for treating urinary tract infections. Front Microbiol 9:1832. https://doi.org/10.3389/fmicb.2018.01832
Vaara M (1992) Agents that increase the permeability of the outer membrane. Microbiol Rev 56:395–411
Vogeleer P, Tremblay YDN, Mafu AA, Jacques M, Harel J (2014) Life on the outside: role of biofilms in environmental persistence of Shiga-toxin producing Escherichia coli. Front Microbiol 5:317. https://doi.org/10.3389/fmicb.2014.00317
Vouillamoz J, Entenza JM, Giddey M, Fischetti VA, Moreillon P, Resch G (2013) Bactericidal synergism between daptomycin and the phage lysin Cpl-1 in a mouse model of pneumococcal bacteraemia. Int J Antimicrob Agents 42:416–421. https://doi.org/10.1016/j.ijantimicag.2013.06.020
Wang S, Gu J, Lv M, Guo Z, Yan G, Yu L, du C, Feng X, Han W, Sun C, Lei L (2017) The antibacterial activity of E. coli bacteriophage lysin lysep3 is enhanced by fusing the Bacillus amyloliquefaciens bacteriophage endolysin binding domain D8 to the C-terminal region. J Microbiol 55:403–408. https://doi.org/10.1007/s12275-017-6431-6
Warren JW, Abrutyn E, Hebel JR, Johnson JR, Schaeffer AJ, Stamm WE (1999) Guidelines for antimicrobial treatment of uncomplicated acute bacterial cystitis and acute pyelonephritis in women. Infectious Diseases Society of America (IDSA). Clin Infect Dis 29:745–758
Watanabe R, Matsumoto T, Sano G, Ishii Y, Tateda K, Sumiyama Y, Uchiyama J, Sakurai S, Matsuzaki S, Imai S, Yamaguchi K (2007) Efficacy of bacteriophage therapy against gut-derived sepsis caused by Pseudomonas aeruginosa in mice. Antimicrob Agents Chemother 51:446–452. https://doi.org/10.1128/AAC.00635-06
Wright KJ, Seed PC, Hultgren SJ (2005) Uropathogenic Escherichia coli flagella aid in efficient urinary tract colonization. Infect Immun 73:7657–7668. https://doi.org/10.1128/IAI.73.11.7657-7668.2005
Yen M, Cairns LS, Camilli A (2017) A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. Nat Commun 8:1–7. https://doi.org/10.1038/ncomms14187
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Malik, S., Sidhu, P.K., Rana, J. et al. Managing urinary tract infections through phage therapy: a novel approach. Folia Microbiol 65, 217–231 (2020). https://doi.org/10.1007/s12223-019-00750-y
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DOI: https://doi.org/10.1007/s12223-019-00750-y