دورية أكاديمية
Bacteriophage therapy and infective endocarditis - is it realistic?
العنوان: | Bacteriophage therapy and infective endocarditis - is it realistic? |
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المؤلفون: | Pedersen EC; Department of Clinical Microbiology, Copenhagen University Hospital, Copenhagen, Denmark., Lerche CJ; Department of Clinical Microbiology, Copenhagen University Hospital, Copenhagen, Denmark.; Department for Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark., Schwartz FA; Department of Clinical Microbiology, Copenhagen University Hospital, Copenhagen, Denmark., Ciofu O; Department for Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark.; European Society for Clinical Microbiology and Infectious Diseases (ESCMID) Study Group for Biofilms (ESGB), Basel, Switzerland., Azeredo J; European Society for Clinical Microbiology and Infectious Diseases (ESCMID) Study Group for Biofilms (ESGB), Basel, Switzerland.; Department of Biological Engineering, University of Minho, Braga, Portugal., Thomsen K; Department of Clinical Microbiology, Zealand University Hospital, Slagelse, Denmark., Moser C; Department of Clinical Microbiology, Copenhagen University Hospital, Copenhagen, Denmark.; Department for Immunology and Microbiology, University of Copenhagen, Copenhagen, Denmark.; European Society for Clinical Microbiology and Infectious Diseases (ESCMID) Study Group for Biofilms (ESGB), Basel, Switzerland. |
المصدر: | APMIS : acta pathologica, microbiologica, et immunologica Scandinavica [APMIS] 2024 Jul 15. Date of Electronic Publication: 2024 Jul 15. |
Publication Model: | Ahead of Print |
نوع المنشور: | Journal Article; Review |
اللغة: | English |
بيانات الدورية: | Publisher: Munksgaard Country of Publication: Denmark NLM ID: 8803400 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1600-0463 (Electronic) Linking ISSN: 09034641 NLM ISO Abbreviation: APMIS Subsets: MEDLINE |
أسماء مطبوعة: | Publication: Copenhagen : Munksgaard Original Publication: Copenhagen : Munksgaard, c1988- |
مستخلص: | Infective endocarditis (IE) is a severe infection of the inner heart. Even with current standard treatment, the mean in-hospital mortality is as high as 15-20%, and 1-year mortality is up to 40% for left-sided IE. Importantly, IE mortality rates have not changed substantially over the past 30 years, and the incidence of IE is rising. The treatment is challenging due to the bacterial biofilm mode of growth inside the heart valve vegetations, resulting in antibiotic tolerance. Achieving sufficient antibiotic anti-biofilm concentrations in the biofilms of the heart valve vegetations is problematic, even with high-dose and long-term antibiotic therapy. The increasing prevalence of IE caused by antibiotic-resistant bacteria adds to the challenge. Therefore, adjunctive antibiotic-potentiating drug candidates and strategies are increasingly being investigated. Bacteriophage therapy is a reemerging antibacterial treatment strategy for difficult-to-treat infections, mainly biofilm-associated and caused by multidrug-resistant bacteria. However, significant knowledge gaps regarding the safety and efficacy of phage therapy impede more widespread implementation in clinical practice. Hopefully, future preclinical and clinical testing will reveal whether it is a viable treatment. The objective of the present review is to assess whether bacteriophage therapy is a realistic treatment for IE. (© 2024 The Author(s). APMIS published by John Wiley & Sons Ltd on behalf of Scandinavian Societies for Pathology, Medical Microbiology and Immunology.) |
References: | Que Y‐A, Moreillon P. Infective endocarditis. Nat Rev Cardiol. 2011;8:322–336. Østergaard L, Valeur N, Tuxen CD, Bundgaard H, Iversen K, Moser C, et al. Infective endocarditis. Ugeskr Laeger. 2022;184:V10210751. Mostaghim AS, Lo HYA, Khardori N. A retrospective epidemiologic study to define risk factors, microbiology, and clinical outcomes of infective endocarditis in a large tertiary‐care teaching hospital. SAGE Open Med. 2017;5:205031211774177. Park LP, Chu VH, Peterson G, Skoutelis A, Lejko‐Zupa T, Bouza E, et al. Validated risk score for predicting 6‐month mortality in infective endocarditis. J Am Heart Assoc. 2016;5:e003016. Abegaz TM, Bhagavathula AS, Gebreyohannes EA, Mekonnen AB, Abebe TB. Short‐ and long‐term outcomes in infective endocarditis patients: a systematic review and meta‐analysis. BMC Cardiovasc Disord. 2017;17:291. Corbellino M, Kieffer N, Kutateladze M, Balarjishvili N, Leshkasheli L, Askilashvili L, 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. 2020;70:1998–2001. Suh GA, Lodise TP, Tamma PD, Knisely JM, Alexander J, Aslam S, et al. Considerations for the use of phage therapy in clinical practice. Antimicrob Agents Chemother. 2022;66:e0207121. Cameron D, Valente LG, Pitton M, Prazak J, Que Y‐A. Bacteriophages for the treatment of biofilm‐associated infections. AntibBiofilm strategies. Switzerland: Springer; 2022. p. 186–199. Sulakvelidze A, Alavidze Z, Morris JG. Bacteriophage therapy. Antimicrob Agents Chemother. 2001;45:649–659. Clokie MRJ, Millard AD, Letarov AV, Heaphy S. Phages in nature. Bacteriophage. 2011;1:31–45. Pirnay J‐P, Djebara S, Steurs G, Griselain J, Cochez C, de Soir S, et al. Personalized bacteriophage therapy outcomes for 100 consecutive cases: a multicentre, multinational, retrospective observational study. Nat Microbiol. 2024;9:1434–1453. Moreillon P, Que Y‐A. Infective endocarditis. Lancet. 2004;363:139–149. Fernández‐Hidalgo N, Tornos Mas P. Epidemiology of infective endocarditis in Spain in the last 20 years. Rev Esp Cardiol. 2013;66:728–733. Delgado V, Ajmone Marsan N, de Waha S, Bonaros N, Brida M, Burri H, et al. 2023 ESC guidelines for the management of endocarditis. Eur Heart J. 2023;44:3948–4042. Wilson WR, Karchmer AW, Dajani AS, Taubert KA, Bayer A, Kaye D, et al. Antibiotic treatment of adults with infective endocarditis due to streptococci, enterococci, staphylococci, and HACEK microorganisms. JAMA. 1995;274:1706–1713. Werdan K, Dietz S, Löffler B, Niemann S, Bushnaq H, Silber RE, et al. Mechanisms of infective endocarditis: pathogen‐host interaction and risk states. Nat Rev Cardiol. 2014;11:35–50. Hoen B, Xavier D. Infective endocarditis. N Engl J Med. 2013;369:784–785. Lerche CJ, Schwartz F, Theut M, Fosbøl EL, Iversen K, Bundgaard H, et al. Anti‐biofilm approach in infective endocarditis exposes new treatment strategies for improved outcome. Front Cell Dev Biol. 2021;9:643335. Lerche CJ, Christophersen LJ, Goetze JP, Nielsen PR, Thomsen K, Enevold C, et al. Adjunctive dabigatran therapy improves outcome of experimental left‐sided Staphylococcus aureus endocarditis. PLoS One. 2019;14:e0215333. Ciofu O, Moser C, Jensen PØ, Høiby N. Tolerance and resistance of microbial biofilms. Nat Rev Microbiol. 2022;20:621–635. Lerche CJ, Christophersen LJ, Trøstrup H, Thomsen K, Jensen PØ, Hougen HP, et al. Low efficacy of tobramycin in experimental Staphylococcus aureus endocarditis. Eur J Clin Microbiol Infect Dis. 2015;34:2349–2357. Jung C‐J, Yeh CY, Shun CT, Hsu RB, Cheng HW, Lin CS, et al. Platelets enhance biofilm formation and resistance of endocarditis‐inducing streptococci on the injured heart valve. J Infect Dis. 2012;205:1066–1075. Tan JS, Kaplan S, Terhune CA, Hamburger M. Successful two‐week treatment schedule for penicillin‐susceptible streptococcus viridans endocarditis. Lancet. 1971;2:1340–1343. Christie RV. Penicillin in subacute bacterial endocarditis. Br Med J. 1946;1:381–383. Bloomfield AL, Armstrong CD, Kirby WM. The treatment of subacute bacterial endocarditis with penicillin. J Clin Invest. 1945;24:251–267. Degraff AC. The present status of the treatment of subacute bacterial endocarditis. Bull N Y Acad Med. 1941;17:423–433. Sauer K, Stoodley P, Goeres DM, Hall‐Stoodley L, Burmølle M, Stewart PS, et al. The biofilm life cycle: expanding the conceptual model of biofilm formation. Nat Rev Microbiol. 2022;20:608–620. Lerche CJ, Christophersen LJ, Kolpen M, Nielsen PR, Trøstrup H, Thomsen K, et al. Hyperbaric oxygen therapy augments tobramycin efficacy in experimental Staphylococcus aureus endocarditis. Int J Antimicrob Agents. 2017;50:406–412. Chen H, Wang Q, Yin Y, Li S, Niu DK, Wang H. Genotypic variations between wild‐type and small colony variant of Staphylococcus aureus in prosthetic valve infectious endocarditis: a comparative genomic and transcriptomic analysis. Int J Antimicrob Agents. 2018;51:655–658. Iversen K, Ihlemann N, Gill SU, Madsen T, Elming H, Jensen KT, et al. Partial oral versus intravenous antibiotic treatment of endocarditis. N Engl J Med. 2019;380:415–424. Bock M, Theut AM, van Hasselt JGC, Wang H, Fuursted K, Høiby N, et al. Attainment of target antibiotic levels by Oral treatment of left‐sided infective endocarditis: a POET substudy. Clin Infect Dis. 2023;77:242–251. Knudsen IJD, Frimodt‐Møller N. Ældre får flere bivirkninger og mere resistensudvikling af antibiotika. Ugeskr Laeger. 2013;175:2854–2857. Forde A, Hill C. Phages of life – the path to pharma. Br J Pharmacol. 2018;175:412–418. Hansen MF, Svenningsen SL, Røder HL, Middelboe M, Burmølle M. Big impact of the tiny: bacteriophage–bacteria interactions in biofilms. Trends Microbiol. 2019;27:739–752. González S, Fernández L, Gutiérrez D, Campelo AB, Rodríguez A, García P. Analysis of different parameters affecting diffusion, propagation and survival of Staphylophages in bacterial biofilms. Front Microbiol. 2018;9:2348. Briers Y, Walmagh M, Grymonprez B, Biebl M, Pirnay JP, Defraine V, et al. Art‐175 is a highly efficient antibacterial against multidrug‐resistant strains and persisters of Pseudomonas aeruginosa. Antimicrob Agents Chemother. 2014;58:3774–3784. Alves DR, Gaudion A, Bean JE, Perez Esteban P, Arnot TC, Harper DR, et al. Combined use of bacteriophage K and a novel bacteriophage to reduce Staphylococcus aureus biofilm formation. Appl Environ Microbiol. 2014;80:6694–6703. Lehman SM, Donlan RM. 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. 2015;59:1127–1137. Aslam S, Lampley E, Wooten D, Karris M, Benson C, Strathdee S, et al. Lessons learned from the first 10 consecutive cases of intravenous bacteriophage therapy to treat multidrug‐resistant bacterial infections at a single center in the United States. Open Forum Infect Dis. 2020;7:ofaa389. El Haddad L, Harb CP, Gebara MA, Stibich MA, Chemaly RF. A systematic and critical review of bacteriophage therapy against multidrug‐resistant ESKAPE organisms in humans. Clin Infect Dis. 2019;69:167–178. Petrovic Fabijan A, Lin RCY, Ho J, Maddocks S, Ben Zakour NL, Iredell JR, et al. Safety of bacteriophage therapy in severe Staphylococcus aureus infection. Nat Microbiol. 2020;5:465–472. Speck P, Smithyman A. Safety and efficacy of phage therapy via the intravenous route. FEMS Microbiol Lett. 2016;363:fnv242. Roach DR, Debarbieux L. Phage therapy: awakening a sleeping giant. Emerg Top Life Sci. 2017;1:93–103. Dufour N, Delattre R, Debarbieux L. In vivo bacteriophage biodistribution. Methods Mol Biol. 2018;1693:123–137. Strathdee SA, Hatfull GF, Mutalik VK, Schooley RT. Phage therapy: from biological mechanisms to future directions. Cell. 2023;186:17–31. Oechslin F, Piccardi P, Mancini S, Gabard J, Moreillon P, Entenza JM, et al. Synergistic interaction between phage therapy and antibiotics clears Pseudomonas aeruginosa infection in endocarditis and reduces virulence. J Infect Dis. 2016;215:703–712. Nang SC, Lin YW, Petrovic Fabijan A, Chang RYK, Rao GG, Iredell J, et al. Pharmacokinetics/pharmacodynamics of phage therapy: a major hurdle to clinical translation. Clin Microbiol Infect. 2023;29:702–709. Bertozzi Silva J, Storms Z, Sauvageau D. Host receptors for bacteriophage adsorption. FEMS Microbiol Lett. 2016;363:fnw002. Mistretta N, Brossaud M, Telles F, Sanchez V, Talaga P, Rokbi B. Glycosylation of Staphylococcus aureus cell wall teichoic acid is influenced by environmental conditions. Sci Rep. 2019;9:3212. Doub JB, Urish K, Lee M, Fackler J. Impact of bacterial phenotypic variation with bacteriophage therapy: a pilot study with prosthetic joint infection isolates. Int J Infect Dis. 2022;119:44–46. Azam AH, Tanji Y. Peculiarities of Staphylococcus aureus phages and their possible application in phage therapy. Appl Microbiol Biotechnol. 2019;103:4279–4289. Schooley RT, Biswas B, Gill JJ, Hernandez‐Morales A, Lancaster J, Lessor L, 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:e00954‐17. Khalifa L, Brosh Y, Gelman D, Coppenhagen‐Glazer S, Beyth S, Poradosu‐Cohen R, et al. Targeting Enterococcus faecalis biofilms with phage therapy. Appl Environ Microbiol. 2015;81:2696–2705. Khalifa L, Gelman D, Shlezinger M, Dessal AL, Coppenhagen‐Glazer S, Beyth N, et al. Defeating antibiotic‐ and phage‐resistant Enterococcus faecalis using a phage cocktail in vitro and in a clot model. Front Microbiol. 2018;9:326. Kelly D, McAuliffe O, O'Mahony J, Coffey A. Development of a broad‐host‐range phage cocktail for biocontrol. Bioeng Bugs. 2011;2:31–37. Dan JM, Lehman SM, al‐kolla R, Penziner S, Afshar K, Yung G, et al. Development of host immune response to bacteriophage in a lung transplant recipient on adjunctive phage therapy for a multidrug‐resistant pneumonia. J Infect Dis. 2023;227:311–316. Zhvania P, Hoyle NS, Nadareishvili L, Nizharadze D, Kutateladze M. Phage therapy in a 16‐year‐old boy with Netherton syndrome. Front Med (Lausanne). 2017;4:94. El Ghali A, Stamper K, Kunz Coyne AJ, Holger D, Kebriaei R, Alexander J, et al. Ciprofloxacin in combination with bacteriophage cocktails against multi‐drug resistant Pseudomonas aeruginosa in ex vivo simulated endocardial vegetation models. Antimicrob Agents Chemother. 2023;67:e0072823. Kunz Coyne AJ, Stamper K, el Ghali A, Kebriaei R, Biswas B, Wilson M, et al. Phage‐antibiotic cocktail rescues daptomycin and phage susceptibility against daptomycin‐nonsusceptible Enterococcus faecium in a simulated endocardial vegetation ex vivo model. Microbiol Spectr. 2023;11:e0034023. Save J, Que YA, Entenza JM, Kolenda C, Laurent F, Resch G. Bacteriophages combined with subtherapeutic doses of flucloxacillin act synergistically against Staphylococcus aureus experimental infective endocarditis. J Am Heart Assoc. 2022;11:e023080. Save J, Que Y‐A, Entenza J, Resch G. Subtherapeutic doses of vancomycin synergize with bacteriophages for treatment of experimental methicillin‐resistant Staphylococcus aureus infective endocarditis. Viruses. 2022;14:1792. Gilbey T, Ho J, Cooley LA, Petrovic Fabijan A, Iredell JR. Adjunctive bacteriophage therapy for prosthetic valve endocarditis due to Staphylococcus aureus. Med J Aust. 2019;211:142–143.e1. Prazak J, Valente LG, Iten M, Federer L, Grandgirard D, Soto S, et al. Benefits of aerosolized phages for the treatment of pneumonia due to methicillin‐resistant Staphylococcus aureus: an experimental study in rats. J Infect Dis. 2022;225:1452–1459. Chan BK, Sistrom M, Wertz JE, Kortright KE, Narayan D, Turner PE. Phage selection restores antibiotic sensitivity in MDR Pseudomonas aeruginosa. Sci Rep. 2016;6:26717. Burmeister AR, Fortier A, Roush C, Lessing AJ, Bender RG, Barahman R, et al. Pleiotropy complicates a trade‐off between phage resistance and antibiotic resistance. Proc Natl Acad Sci USA. 2020;117:11207–11216. Dickey J, Perrot V. Adjunct phage treatment enhances the effectiveness of low antibiotic concentration against Staphylococcus aureus biofilms in vitro. PLoS One. 2019;14:e0209390. Lood R, Winer BY, Pelzek AJ, Diez‐Martinez R, Thandar M, Euler CW, et al. Novel phage lysin capable of killing the multidrug‐resistant gram‐negative bacterium Acinetobacter baumannii in a mouse bacteremia model. Antimicrob Agents Chemother. 2015;59:1983–1991. Gilmer DB, Schmitz JE, Euler CW, Fischetti VA. Novel bacteriophage lysin with broad lytic activity protects against mixed infection by Streptococcus pyogenes and methicillin‐resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2013;57:2743–2750. Jun SY, Jung GM, Yoon SJ, Youm SY, Han HY, Lee JH, et al. Pharmacokinetics of the phage endolysin‐based candidate drug SAL 200 in monkeys and its appropriate intravenous dosing period. Clin Exp Pharmacol Physiol. 2016;43:1013–1016. Jun SY, Jang IJ, Yoon S, Jang K, Yu KS, Cho JY, et al. Pharmacokinetics and tolerance of the phage endolysin‐based candidate drug SAL200 after a single intravenous administration among healthy volunteers. Antimicrob Agents Chemother. 2017;61:e02629‐16. Meng X, Shi Y, Ji W, Meng X, Zhang J, Wang H, et al. Application of a bacteriophage lysin to disrupt biofilms formed by the animal pathogen Streptococcus suis. Appl Environ Microbiol. 2011;77:8272–8279. Doub JB. Bacteriophage therapy: are we running before we have learned to walk? Eur J Clin Microbiol Infect Dis. 2023;42:1281–1283. Lægemiddelstyrrelsen. Faser i kliniske forsøg. Copenhagen: Danish Medicines Agency; 2019. EUPATI. Sådan fremstilles et lægemiddel. Trin 6: Fase I – bevis for virkningsmekanisme. Cooper CJ, Khan Mirzaei M, Nilsson AS. Adapting drug approval pathways for bacteriophage‐based therapeutics. Front Microbiol. 2016;7:1209. Nexa Biome. AI Revolutionises bacteriophage research for human, animal, and harvest health. Glasgow: Nesa Biome; 2023. Chiang YN, Penadés JR, Chen J. Genetic transduction by phages and chromosomal islands: the new and noncanonical. PLoS Pathog. 2019;15:e1007878. |
فهرسة مساهمة: | Keywords: Phage therapy; biofilm; infective endocarditis; treatment |
تواريخ الأحداث: | Date Created: 20240715 Latest Revision: 20240715 |
رمز التحديث: | 20240715 |
DOI: | 10.1111/apm.13455 |
PMID: | 39007242 |
قاعدة البيانات: | MEDLINE |
تدمد: | 1600-0463 |
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DOI: | 10.1111/apm.13455 |