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Antimicrobial agents and chemotherapy
03 15, 2022;66 (3): e0207121.

Considerations for the Use of Phage Therapy in Clinical Practice.

Gina A Suh, Thomas P Lodise, Pranita D Tamma, Jane M Knisely, Jose Alexander, Saima Aslam, Karen D Barton, Erica Bizzell, Katherine M C Totten, Joseph L Campbell, Benjamin K Chan, Scott A Cunningham, Katherine E Goodman, Kerryl E Greenwood-Quaintance, Anthony D Harris, Shayla Hesse, Anthony Maresso, Veronique Nussenblatt, David Pride, Michael J Rybak, Zoe Sund, David van Duin, Daria Van Tyne, Robin Patel, Antibacterial Resistance Leadership Group
Author Information
  1. Gina A Suh: Mayo Clinicgrid.66875.3a, Rochester, Minnesota, USA. ORCID
  2. Thomas P Lodise: Albany College of Pharmacy and Health Sciencesgrid.413555.3, Albany, New York, USA. ORCID
  3. Pranita D Tamma: Johns Hopkins University School of Medicinegrid.471401.7, Baltimore, Maryland, USA. ORCID
  4. Jane M Knisely: National Institutes of Health, Bethesda, Maryland, USA.
  5. Jose Alexander: Advent Health, Orlando, Florida, USA.
  6. Saima Aslam: University of California San Diego, San Diego, California, USA.
  7. Karen D Barton: Duke University, Durham, North Carolina, USA.
  8. Erica Bizzell: National Institutes of Health, Bethesda, Maryland, USA.
  9. Katherine M C Totten: Mayo Clinicgrid.66875.3a, Rochester, Minnesota, USA. ORCID
  10. Joseph L Campbell: National Institutes of Health, Bethesda, Maryland, USA.
  11. Benjamin K Chan: Yale University, New Haven, Connecticut, USA.
  12. Scott A Cunningham: Mayo Clinicgrid.66875.3a, Rochester, Minnesota, USA.
  13. Katherine E Goodman: University of Maryland School of Medicine, Baltimore, Maryland, USA.
  14. Kerryl E Greenwood-Quaintance: Mayo Clinicgrid.66875.3a, Rochester, Minnesota, USA.
  15. Anthony D Harris: University of Maryland School of Medicine, Baltimore, Maryland, USA.
  16. Shayla Hesse: National Institutes of Health, Bethesda, Maryland, USA. ORCID
  17. Anthony Maresso: Baylor College of Medicinegrid.39382.33, Houston, Texas, USA.
  18. Veronique Nussenblatt: National Institutes of Health, Bethesda, Maryland, USA.
  19. David Pride: University of California San Diego, San Diego, California, USA. ORCID
  20. Michael J Rybak: College of Pharmacy & Health Sciences and School of Medicine, Wayne State University, Detroit, Michigan, USA. ORCID
  21. Zoe Sund: Duke University, Durham, North Carolina, USA.
  22. David van Duin: University of North Carolina at Chapel Hillgrid.10698.36, Chapel Hill, North Carolina, USA. ORCID
  23. Daria Van Tyne: University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA. ORCID
  24. Robin Patel: Mayo Clinicgrid.66875.3a, Rochester, Minnesota, USA. ORCID
PMID: 35041506 DOI: 10.1128/AAC.02071-21

Abstract

Increasing antimicrobial resistance and medical device-related infections have led to a renewed interest in phage therapy as an alternative or adjunct to conventional antimicrobials. Expanded access and compassionate use cases have risen exponentially but have varied widely in approach, methodology, and clinical situations in which phage therapy might be considered. Large gaps in knowledge contribute to heterogeneity in approach and lack of consensus in many important clinical areas. The Antibacterial Resistance Leadership Group (ARLG) has convened a panel of experts in phage therapy, clinical microbiology, infectious diseases, and pharmacology, who worked with regulatory experts and a funding agency to identify questions based on a clinical framework and divided them into three themes: potential clinical situations in which phage therapy might be considered, laboratory testing, and pharmacokinetic considerations. Suggestions are provided as answers to a series of questions intended to inform clinicians considering experimental phage therapy for patients in their clinical practices.

Keywords

Pseudomonas aeruginosa Staphylococcus aureus biofilms phages

References

  1. Viruses. 2019 Oct 16;11(10): [PMID: 31623253]
  2. Front Microbiol. 2019 Jul 23;10:1674 [PMID: 31396188]
  3. PLoS One. 2013;8(2):e56022 [PMID: 23418497]
  4. J Appl Microbiol. 2009 Nov;107(5):1651-7 [PMID: 19457041]
  5. J Heart Lung Transplant. 2019 Apr;38(4):475-476 [PMID: 30661974]
  6. Nat Rev Microbiol. 2004 Feb;2(2):166-73 [PMID: 15040264]
  7. Bioinformatics. 2012 Mar 1;28(5):614-8 [PMID: 22238260]
  8. Viruses. 2014 Oct 03;6(10):3778-86 [PMID: 25285538]
  9. Microb Biotechnol. 2011 Sep;4(5):643-50 [PMID: 21481199]
  10. Pediatr Pulmonol. 2021 Feb;56 Suppl 1:S4-S9 [PMID: 33434411]
  11. Front Med (Lausanne). 2021 May 05;8:569159 [PMID: 34026768]
  12. Trends Microbiol. 2009 Feb;17(2):66-72 [PMID: 19162482]
  13. EMBO Mol Med. 2021 Sep 7;13(9):e13936 [PMID: 34369652]
  14. Adv Colloid Interface Sci. 2017 Nov;249:100-133 [PMID: 28688779]
  15. Clin Exp Dermatol. 2005 Jan;30(1):23-6 [PMID: 15663496]
  16. Sci Rep. 2015 Nov 12;5:16532 [PMID: 26559140]
  17. Ups J Med Sci. 2019 Nov;124(4):218-227 [PMID: 31724901]
  18. J Infect Dev Ctries. 2010 Jun 30;4(6):367-77 [PMID: 20601788]
  19. Arch Immunol Ther Exp (Warsz). 1987;35(5):569-83 [PMID: 3455647]
  20. Open Forum Infect Dis. 2020 Aug 27;7(9):ofaa389 [PMID: 33005701]
  21. Sci Rep. 2018 Sep 20;8(1):14140 [PMID: 30237558]
  22. Front Microbiol. 2016 Aug 03;7:1198 [PMID: 27536286]
  23. Pharmaceuticals (Basel). 2021 Mar 08;14(3): [PMID: 33800146]
  24. PLoS One. 2014 Jul 25;9(7):e102600 [PMID: 25061757]
  25. mBio. 2021 Apr 27;12(2): [PMID: 33906920]
  26. Antimicrob Agents Chemother. 2019 Dec 20;64(1): [PMID: 31527029]
  27. Res Microbiol. 2018 Nov;169(9):540-542 [PMID: 29777836]
  28. Sci Rep. 2021 Apr 1;11(1):7387 [PMID: 33795704]
  29. Front Microbiol. 2016 Sep 08;7:1352 [PMID: 27660623]
  30. Diagnostics (Basel). 2020 Dec 22;11(1): [PMID: 33375202]
  31. mBio. 2020 Aug 4;11(4): [PMID: 32753497]
  32. Methods Mol Biol. 2009;501:141-9 [PMID: 19066818]
  33. Antimicrob Agents Chemother. 2020 Jun 23;64(7): [PMID: 32393490]
  34. J Chromatogr A. 2011 Apr 29;1218(17):2438-44 [PMID: 21238969]
  35. Evol Med Public Health. 2018 Mar 08;2018(1):60-66 [PMID: 29588855]
  36. Viruses. 2018 Dec 25;11(1): [PMID: 30585199]
  37. Open Forum Infect Dis. 2018 Oct 24;5(11):ofy269 [PMID: 30474047]
  38. J Virol. 2002 Jun;76(11):5557-64 [PMID: 11991984]
  39. Annu Rev Virol. 2021 Sep 29;8(1):415-435 [PMID: 34014761]
  40. Antimicrob Agents Chemother. 2019 Dec 20;64(1): [PMID: 31611357]
  41. J Mater Chem B. 2017 Jul 21;5(27):5403-5411 [PMID: 32264080]
  42. Antibiotics (Basel). 2020 May 09;9(5): [PMID: 32397354]
  43. Front Microbiol. 2017 Nov 06;8:2170 [PMID: 29163448]
  44. J Pediatric Infect Dis Soc. 2018 Aug 17;7(3):253-256 [PMID: 28992111]
  45. PLoS One. 2012;7(10):e47742 [PMID: 23082205]
  46. mBio. 2021 Feb 9;12(1): [PMID: 33563833]
  47. mBio. 2017 Nov 21;8(6): [PMID: 29162715]
  48. Infection. 2019 Aug;47(4):665-668 [PMID: 31102236]
  49. J Med Microbiol. 2011 Nov;60(Pt 11):1697-1700 [PMID: 21737541]
  50. Vet Microbiol. 2010 Dec 15;146(3-4):309-13 [PMID: 20627620]
  51. Nature. 1973 Nov 23;246(5430):221-3 [PMID: 4586796]
  52. Front Microbiol. 2020 Oct 23;11:594868 [PMID: 33193274]
  53. Crit Care. 2017 Jun 4;21(1):129 [PMID: 28583189]
  54. Anal Chem. 1990 Apr 1;62(7):708-12 [PMID: 2327587]
  55. Viruses. 2021 Jun 29;13(7): [PMID: 34209836]
  56. J Med Microbiol. 2011 Feb;60(Pt 2):205-210 [PMID: 20965914]
  57. J Infect Dis. 2017 Mar 1;215(5):703-712 [PMID: 28007922]
  58. J Antimicrob Chemother. 2016 Aug;71(8):2071-4 [PMID: 27068400]
  59. AAPS J. 2019 Apr 4;21(3):49 [PMID: 30949776]
  60. J Microbiol Immunol Infect. 2009 Apr;42(2):134-40 [PMID: 19597645]
  61. Med J Aust. 2019 Aug;211(3):142-143.e1 [PMID: 31281964]
  62. Clin Ther. 2020 Sep;42(9):1659-1680 [PMID: 32883528]
  63. J Aerosol Med Pulm Drug Deliv. 2008 Dec;21(4):351-60 [PMID: 18800880]
  64. Microb Drug Resist. 2021 Jan;27(1):25-35 [PMID: 32543337]
  65. Am J Respir Crit Care Med. 2019 Nov 1;200(9):1179-1181 [PMID: 31437402]
  66. Antibiotics (Basel). 2020 Oct 29;9(11): [PMID: 33138034]
  67. Indian J Med Res. 2016 Jan;143(1):87-94 [PMID: 26997019]
  68. Methods Mol Biol. 2018;1693:159-170 [PMID: 29119440]
  69. J Orthop Res. 2020 Oct;38(10):2091-2103 [PMID: 32285973]
  70. Nat Microbiol. 2018 Jan;3(1):26-31 [PMID: 29085075]
  71. PLoS One. 2015 Mar 26;10(3):e0122672 [PMID: 25811193]
  72. Viruses. 2019 Apr 17;11(4): [PMID: 30999559]
  73. Viruses. 2018 Nov 08;10(11): [PMID: 30413044]
  74. J Infect. 2021 Sep;83(3):e1-e3 [PMID: 34058260]
  75. Front Microbiol. 2020 Mar 17;11:414 [PMID: 32256472]
  76. Front Microbiol. 2019 Jan 09;9:3306 [PMID: 30687285]
  77. Cell Mol Biol Lett. 2004;9(2):253-9 [PMID: 15213806]
  78. Sci Rep. 2015 Oct 06;5:14802 [PMID: 26440922]
  79. Viruses. 2018 Apr 10;10(4): [PMID: 29642590]
  80. Bacteriophage. 2011 Mar;1(2):86-93 [PMID: 22334864]
  81. Microbiol Immunol. 2009 May;53(5):301-4 [PMID: 19457172]
  82. Front Microbiol. 2020 Jun 04;11:1161 [PMID: 32582101]
  83. Front Microbiol. 2018 Aug 07;9:1832 [PMID: 30131795]
  84. FEMS Microbiol Ecol. 2017 Jan;93(1): [PMID: 27737900]
  85. Eur J Clin Microbiol Infect Dis. 2012 Nov;31(11):3241-9 [PMID: 22777594]
  86. Med Mycol. 2019 Apr 1;57(Supplement_2):S179-S188 [PMID: 30816971]
  87. Emerg Microbes Infect. 2021 Dec;10(1):612-618 [PMID: 33703996]
  88. J Chromatogr B Analyt Technol Biomed Life Sci. 2008 Jan 15;861(2):177-80 [PMID: 17588505]
  89. Viral Immunol. 2014 Aug;27(6):295-304 [PMID: 24893003]
  90. Nat Microbiol. 2020 Mar;5(3):465-472 [PMID: 32066959]
  91. Antimicrob Agents Chemother. 2005 Jul;49(7):2874-8 [PMID: 15980363]
  92. Front Microbiol. 2020 Sep 18;11:538060 [PMID: 33072008]
  93. Med Mal Infect. 2008 Aug;38(8):426-30 [PMID: 18687542]
  94. Sci Rep. 2016 May 26;6:26717 [PMID: 27225966]
  95. Antimicrob Agents Chemother. 2020 Feb 21;64(3): [PMID: 31871084]
  96. Viruses. 2021 Jun 21;13(6): [PMID: 34205687]
  97. Eur J Pharm Sci. 2017 Sep 30;107:168-182 [PMID: 28711712]
  98. Open Ophthalmol J. 2015 Nov 04;9:167-8 [PMID: 26862360]
  99. Front Microbiol. 2016 Oct 24;7:1681 [PMID: 27822205]
  100. PeerJ. 2014 Sep 25;2:e590 [PMID: 25279269]
  101. Bull Exp Biol Med. 2020 Apr;168(6):748-752 [PMID: 32328936]
  102. Antimicrob Agents Chemother. 2011 Jan;55(1):426-8 [PMID: 20974862]
  103. Curr Opin Infect Dis. 2020 Aug;33(4):298-303 [PMID: 32657966]
  104. Int J Pharm. 2011 Sep 15;416(1):280-7 [PMID: 21771648]
  105. Front Microbiol. 2018 Aug 02;9:1696 [PMID: 30116226]
  106. Clin Pharmacol Ther. 2000 Sep;68(3):225-30 [PMID: 11014403]
  107. Bacteriophage. 2011 Jan;1(1):46-49 [PMID: 21687534]
  108. Europace. 2020 Apr 1;22(4):597 [PMID: 31740948]
  109. Open Forum Infect Dis. 2018 Mar 23;5(4):ofy064 [PMID: 29687015]
  110. J Theor Biol. 2008 Mar 7;251(1):121-36 [PMID: 18160076]
  111. Lancet Infect Dis. 2021 Mar;21(3):427-436 [PMID: 32949500]
  112. Eur J Pharm Sci. 2012 Sep 29;47(2):297-304 [PMID: 22750416]
  113. Sci Rep. 2017 Aug 15;7(1):8292 [PMID: 28811656]
  114. Appl Environ Microbiol. 1985 Jan;49(1):19-23 [PMID: 3156556]
  115. J Glob Antimicrob Resist. 2017 Mar;8:179-185 [PMID: 28232228]
  116. Antibiotics (Basel). 2019 Jul 25;8(3): [PMID: 31349628]
  117. J Nanobiotechnology. 2017 Apr 24;15(1):32 [PMID: 28438164]
  118. Front Pharmacol. 2021 Jun 10;12:692614 [PMID: 34177601]
  119. J Pharm Pharmacol. 2017 Mar;69(3):244-253 [PMID: 28033675]
  120. Res Microbiol. 2013 Jan;164(1):55-60 [PMID: 23000091]
  121. Arch Immunol Ther Exp (Warsz). 2000;48(6):547-51 [PMID: 11197610]
  122. Front Med (Lausanne). 2020 Jul 31;7:342 [PMID: 32850878]
  123. Front Microbiol. 2018 Feb 05;9:127 [PMID: 29459853]
  124. Mol Biotechnol. 2004 Feb;26(2):133-46 [PMID: 14764939]
  125. Adv Virus Res. 2012;82:1-32 [PMID: 22420849]
  126. Virology. 2009 May 25;388(1):21-30 [PMID: 19339031]
  127. Nat Med. 2021 Aug;27(8):1357-1361 [PMID: 34239133]
  128. Antimicrob Agents Chemother. 2020 Aug 20;64(9): [PMID: 32571816]
  129. Nat Rev Microbiol. 2015 Oct;13(10):641-50 [PMID: 26373372]
  130. Int Microbiol. 2017 Sep;20(3):116-120 [PMID: 29446802]
  131. Emerg Microbes Infect. 2020 Dec;9(1):771-774 [PMID: 32212918]
  132. Clin Infect Dis. 2019 Jun 18;69(1):167-178 [PMID: 30395179]
  133. Med Res Rev. 2019 Sep;39(5):2000-2025 [PMID: 30887551]
  134. Clin Exp Med. 2009 Dec;9(4):303-12 [PMID: 19350363]
  135. Antibiotics (Basel). 2020 Jul 04;9(7): [PMID: 32635429]
  136. Front Microbiol. 2017 Jul 10;8:1283 [PMID: 28740489]
  137. PLoS One. 2019 May 9;14(5):e0216292 [PMID: 31071103]
  138. Viruses. 2019 Sep 23;11(10): [PMID: 31548497]
  139. Front Microbiol. 2016 Aug 03;7:1209 [PMID: 27536293]
  140. Clin Otolaryngol. 2009 Aug;34(4):349-57 [PMID: 19673983]
  141. Curr Issues Mol Biol. 2021;40:81-164 [PMID: 32503951]
  142. Microbiol Mol Biol Rev. 2019 Oct 30;83(4): [PMID: 31666296]
  143. Sci Rep. 2017 Jul 24;7(1):6319 [PMID: 28740225]
  144. Transplant Proc. 2003 Jun;35(4):1385-6 [PMID: 12826166]
  145. J Pharm Sci. 2003 May;92(5):1066-76 [PMID: 12712427]
  146. Curr Pharm Biotechnol. 2010 Jan;11(1):28-47 [PMID: 20214606]
  147. Antimicrob Agents Chemother. 2017 Sep 22;61(10): [PMID: 28807909]
  148. Anal Biochem. 2019 Oct 1;582:113354 [PMID: 31276652]
  149. PLoS One. 2017 Jan 11;12(1):e0168615 [PMID: 28076361]
  150. J Biol Chem. 2000 Nov 24;275(47):36949-56 [PMID: 10938278]
  151. Eur J Cardiothorac Surg. 2020 May 1;57(5):1003-1004 [PMID: 31651936]
  152. J Antimicrob Chemother. 2018 Oct 1;73(10):2901-2903 [PMID: 30060002]
  153. Front Med (Lausanne). 2020 Nov 16;7:570572 [PMID: 33304911]
  154. Lett Appl Microbiol. 2007 Sep;45(3):313-7 [PMID: 17718845]
  155. Front Microbiol. 2019 Nov 12;10:2537 [PMID: 31781060]
  156. Bacteriophage. 2016 Aug 11;6(3):e1220348 [PMID: 27738558]
  157. Virology. 2012 Dec 20;434(2):265-70 [PMID: 23079104]
  158. Viruses. 2015 Aug 20;7(8):4783-99 [PMID: 26308042]
  159. Evol Appl. 2012 Sep;5(6):583-92 [PMID: 23028399]
  160. Appl Environ Microbiol. 2015 Feb;81(3):1132-8 [PMID: 25452284]
  161. Nat Protoc. 2020 Sep;15(9):2867-2890 [PMID: 32709990]
  162. Nat Biotechnol. 2006 Apr;24(4):455-60 [PMID: 16565728]
  163. Pediatr Pulmonol. 2020 Nov;55(11):2990-2994 [PMID: 32662948]
  164. JAMA Otolaryngol Head Neck Surg. 2019 Aug 1;145(8):723-729 [PMID: 31219531]
  165. Viruses. 2018 Feb 06;10(2): [PMID: 29415431]
  166. Emerg Microbes Infect. 2018 Oct 10;7(1):168 [PMID: 30302018]
  167. Nat Med. 2019 May;25(5):730-733 [PMID: 31068712]
  168. J Bone Joint Surg Am. 2013 Jan 16;95(2):117-25 [PMID: 23324958]
  169. Antibiotics (Basel). 2020 May 05;9(5): [PMID: 32380707]
  170. FEMS Microbiol Lett. 2016 Feb;363(3): [PMID: 26738755]
  171. Cell Host Microbe. 2017 Jul 12;22(1):38-47.e4 [PMID: 28704651]
  172. Pharm Res. 2017 Oct;34(10):2084-2096 [PMID: 28646325]
  173. J Virol Methods. 2014 Feb;196:86-92 [PMID: 24211298]
  174. Evol Appl. 2016 Feb 18;9(4):583-95 [PMID: 27099623]
  175. F1000Res. 2016 Nov 29;5:2782 [PMID: 27990274]
  176. Lancet Infect Dis. 2019 Jan;19(1):35-45 [PMID: 30292481]
  177. Adv Appl Microbiol. 2011;77:1-40 [PMID: 22050820]
  178. Clin Infect Dis. 2020 Apr 15;70(9):1998-2001 [PMID: 31414123]
  179. Nucleic Acids Res. 2002 Mar 15;30(6):1292-305 [PMID: 11884626]
  180. Clin Infect Dis. 2019 Nov 13;69(11):2015-2018 [PMID: 30869755]
  181. PLoS One. 2012;7(11):e51017 [PMID: 23226451]
  182. J Appl Microbiol. 2012 Dec;113(6):1530-9 [PMID: 22985454]
  183. J Infect Dis. 2019 Apr 16;219(9):1439-1447 [PMID: 30476337]
  184. Burns. 2006 Aug;32(5):644-6 [PMID: 16781080]
  185. J Clin Microbiol. 2019 Jul 26;57(8): [PMID: 31092596]
  186. Am J Transplant. 2019 Sep;19(9):2631-2639 [PMID: 31207123]
  187. Clin Infect Dis. 2021 Jul 1;73(1):e144-e151 [PMID: 32699879]
  188. Front Immunol. 2019 Nov 14;10:2607 [PMID: 31803179]
  189. PLoS One. 2019 Nov 22;14(11):e0220421 [PMID: 31756187]
  190. Res Microbiol. 2018 Nov;169(9):531-539 [PMID: 29777835]

Grants

  1. T32 AR056950/NIAMS NIH HHS
  2. U19 AI157981/NIAID NIH HHS
  3. UL1 TR001863/NCATS NIH HHS
  4. UM1 AI104681/NIAID NIH HHS

MeSH Term

Bacteriophages
Compassionate Use Trials
Drug Resistance, Bacterial
Humans
Phage Therapy
Journal Article Research Support, N.I.H., Extramural Review
Article has an altmetric score of 143

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