The applications of animal models in phage therapy: An update.

Fazal Mehmood Khan, Prasanth Manohar, Vijay Singh Gondil, Nancy Mehra, Greater Kayode Oyejobi, Nelson Odiwuor, Tauseef Ahmad, Guangtao Huang
Author Information
  1. Fazal Mehmood Khan: College of Civil and Transportation Engineering, Shenzhen University, Shenzhen, China. ORCID
  2. Prasanth Manohar: School of Biosciences and Technology, Vellore Institute of Technology, Vellore, India. ORCID
  3. Vijay Singh Gondil: Key Laboratory of Special Pathogens and Biosafety, Center for Biosafety Mega-Science, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, Hubei, China. ORCID
  4. Nancy Mehra: Department of Pediatrics, Advanced Pediatrics Centre, Postgraduate Institute of Medical Education and Research, Chandigarh, India.
  5. Greater Kayode Oyejobi: Key Laboratory of Special Pathogens and Biosafety, Center for Biosafety Mega-Science, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, Hubei, China. ORCID
  6. Nelson Odiwuor: Key Laboratory of Special Pathogens and Biosafety, Center for Biosafety Mega-Science, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, Hubei, China. ORCID
  7. Tauseef Ahmad: Department of Epidemiology and Health Statistics, School of Public Health, Southeast University, Nanjing, China. ORCID
  8. Guangtao Huang: Department of Burn and Plastic Surgery, Shenzhen Institute of Translational Medicine, The First Affiliated Hospital of Shenzhen University, Shenzhen, China.

Abstract

The rapid increase in antibiotic resistance presents a dire situation necessitating the need for alternative therapeutic agents. Among the current alternative therapies, phage therapy (PT) is promising. This review extensively summarizes preclinical PT approaches in various models. PT has been evaluated in several recent clinical trials. However, there are still several unanswered concerns due to a lack of appropriate regulation and pharmacokinetic data regarding the application of phages in human therapeutic procedures. In this review, we also presented the current state of PT and considered how animal models can be used to adapt these therapies for humans. The development of realistic solutions to circumvent these constraints is critical for advancing this technology.

Keywords

References

  1. Microbiol Spectr. 2017 Aug;5(4): [PMID: 28840811]
  2. PLoS One. 2013 Aug 16;8(8):e71036 [PMID: 23976975]
  3. J Wound Care. 2009 Jun;18(6):237-8, 240-3 [PMID: 19661847]
  4. Front Microbiol. 2017 Sep 12;8:1754 [PMID: 28955321]
  5. Antibiotics (Basel). 2022 Jul 18;11(7): [PMID: 35884219]
  6. Antimicrob Agents Chemother. 2015 Nov 16;60(2):744-51 [PMID: 26574007]
  7. Pharmacotherapy. 2020 Feb;40(2):153-168 [PMID: 31872889]
  8. Nat Commun. 2022 May 3;13(1):2313 [PMID: 35504908]
  9. Annu Rev Microbiol. 2010;64:475-93 [PMID: 20528693]
  10. Front Cell Infect Microbiol. 2021 Mar 02;11:637313 [PMID: 33738267]
  11. Antimicrob Agents Chemother. 2005 Mar;49(3):1220-1 [PMID: 15728933]
  12. Methods Mol Biol. 2014;1149:709-21 [PMID: 24818945]
  13. Clin Exp Dermatol. 2005 Jan;30(1):23-6 [PMID: 15663496]
  14. Viruses. 2018 May 06;10(5): [PMID: 29734776]
  15. Front Microbiol. 2019 Jun 05;10:1251 [PMID: 31231338]
  16. Vet Sci. 2020 Mar 06;7(1): [PMID: 32155751]
  17. Front Cell Infect Microbiol. 2021 Feb 26;11:631585 [PMID: 33718279]
  18. J Appl Microbiol. 2014 Sep;117(3):627-33 [PMID: 24916438]
  19. Methods Mol Biol. 2009;501:287-92 [PMID: 19066828]
  20. Antimicrob Agents Chemother. 2007 Aug;51(8):2765-73 [PMID: 17517843]
  21. Sci Rep. 2017 Aug 1;7(1):7043 [PMID: 28765534]
  22. Antimicrob Agents Chemother. 2018 May 25;62(6): [PMID: 29581113]
  23. Appl Microbiol Biotechnol. 2018 Sep;102(18):7901-7912 [PMID: 30008020]
  24. J Infect Dis. 2003 Feb 15;187(4):613-24 [PMID: 12599078]
  25. Antimicrob Agents Chemother. 2019 Mar 27;63(4): [PMID: 30642930]
  26. J Infect Dis. 2010 Apr 1;201(7):1096-104 [PMID: 20196657]
  27. Viruses. 2019 Aug 05;11(8): [PMID: 31387285]
  28. Open Forum Infect Dis. 2020 Aug 27;7(9):ofaa389 [PMID: 33005701]
  29. J Med Microbiol. 2017 Jul;66(7):874-883 [PMID: 28671537]
  30. Front Microbiol. 2018 Jan 09;8:2659 [PMID: 29375524]
  31. Antimicrob Agents Chemother. 2019 Dec 20;64(1): [PMID: 31527029]
  32. EBioMedicine. 2016 Jan 05;4:124-37 [PMID: 26981577]
  33. Antimicrob Agents Chemother. 2018 May 25;62(6): [PMID: 29555626]
  34. Front Microbiol. 2016 Oct 04;7:1590 [PMID: 27757110]
  35. Emerg Top Life Sci. 2017 Apr 21;1(1):93-103 [PMID: 33525818]
  36. Antibiotics (Basel). 2022 Sep 30;11(10): [PMID: 36289998]
  37. Viruses. 2018 Jun 30;10(7): [PMID: 29966329]
  38. Expert Opin Drug Discov. 2015 Jun;10(6):651-69 [PMID: 25910798]
  39. Adv Drug Deliv Rev. 2019 May;145:4-17 [PMID: 30659855]
  40. Front Microbiol. 2022 Mar 25;13:884176 [PMID: 35401457]
  41. Antimicrob Agents Chemother. 2020 Jun 23;64(7): [PMID: 32340988]
  42. Front Microbiol. 2019 Apr 04;10:689 [PMID: 31019499]
  43. Evol Med Public Health. 2018 Mar 08;2018(1):60-66 [PMID: 29588855]
  44. Viruses. 2018 Dec 25;11(1): [PMID: 30585199]
  45. Microbes Infect. 2014 Jun;16(6):512-7 [PMID: 24631574]
  46. Microorganisms. 2020 Sep 22;8(9): [PMID: 32971807]
  47. Appl Environ Microbiol. 2020 Dec 11;87(5): [PMID: 33310718]
  48. Front Microbiol. 2022 Jan 27;13:820572 [PMID: 35154059]
  49. Vet Microbiol. 2014 Jul 16;171(3-4):460-9 [PMID: 24315040]
  50. Front Microbiol. 2019 Dec 17;10:2877 [PMID: 31921055]
  51. Antimicrob Agents Chemother. 2003 Apr;47(4):1301-7 [PMID: 12654662]
  52. PLoS One. 2012;7(10):e47742 [PMID: 23082205]
  53. World J Gastrointest Pharmacol Ther. 2017 Aug 6;8(3):162-173 [PMID: 28828194]
  54. J Am Coll Nutr. 2019 Jan;38(1):68-75 [PMID: 30157383]
  55. Cell Physiol Biochem. 2017;44(6):2337-2345 [PMID: 29258062]
  56. FEMS Microbiol Lett. 2016 Feb;363(3): [PMID: 26691737]
  57. PLoS One. 2019 Jul 10;14(7):e0219599 [PMID: 31291645]
  58. Pharmaceuticals (Basel). 2018 Apr 19;11(2): [PMID: 29671806]
  59. Virol J. 2012 Jan 10;9:9 [PMID: 22234269]
  60. J Med Microbiol. 2011 Feb;60(Pt 2):205-210 [PMID: 20965914]
  61. J Infect Dis. 2017 Mar 1;215(5):703-712 [PMID: 28007922]
  62. J Antimicrob Chemother. 2016 Aug;71(8):2071-4 [PMID: 27068400]
  63. Curr Pharm Biotechnol. 2010 Jan;11(1):48-57 [PMID: 20214607]
  64. Virus Res. 2022 Nov;321:198909 [PMID: 36057417]
  65. Viruses. 2018 Jun 07;10(6): [PMID: 29875339]
  66. Viruses. 2018 Jul 20;10(7): [PMID: 30036941]
  67. Antimicrob Agents Chemother. 2016 Sep 23;60(10):5806-16 [PMID: 27431214]
  68. Arch Immunol Ther Exp (Warsz). 2014 Apr;62(2):117-29 [PMID: 24500660]
  69. Front Microbiol. 2018 Apr 30;9:850 [PMID: 29760690]
  70. Genome Announc. 2018 Jan 4;6(1): [PMID: 29301897]
  71. Sci Rep. 2019 Apr 30;9(1):6643 [PMID: 31040333]
  72. Antimicrob Agents Chemother. 2006 Sep;50(9):2912-8 [PMID: 16940081]
  73. Antimicrob Agents Chemother. 2009 May;53(5):2205-8 [PMID: 19223640]
  74. Antimicrob Agents Chemother. 2019 Jun 24;63(7): [PMID: 31010858]
  75. Adv Appl Microbiol. 2010;70:217-48 [PMID: 20359459]
  76. Indian J Med Res. 2016 Jan;143(1):87-94 [PMID: 26997019]
  77. J Virol. 2014 Nov;88(21):12551-7 [PMID: 25142581]
  78. Sci Rep. 2017 Jan 09;7:40182 [PMID: 28067286]
  79. Arch Virol. 2019 Oct;164(10):2599-2603 [PMID: 31278422]
  80. Int J Food Microbiol. 2010 Jul 15;141(3):151-5 [PMID: 20537744]
  81. Sci Rep. 2015 Nov 26;5:17257 [PMID: 26607832]
  82. Microbiol Spectr. 2022 Feb 23;10(1):e0139321 [PMID: 35171008]
  83. J Transl Med. 2019 Nov 14;17(1):373 [PMID: 31727099]
  84. Viruses. 2018 Nov 15;10(11): [PMID: 30445722]
  85. Antibiotics (Basel). 2021 Apr 19;10(4): [PMID: 33921682]
  86. PLoS One. 2019 Dec 26;14(12):e0226574 [PMID: 31877146]
  87. Appl Environ Microbiol. 2015 Jul;81(14):4841-9 [PMID: 25956778]
  88. Viruses. 2019 Apr 17;11(4): [PMID: 30999559]
  89. Int J Antimicrob Agents. 2008 Feb;31(2):152-7 [PMID: 18082374]
  90. Appl Microbiol Biotechnol. 2019 Sep;103(18):7751-7765 [PMID: 31388727]
  91. J Glob Antimicrob Resist. 2020 Sep;22:32-39 [PMID: 32006750]
  92. Viral Immunol. 2014 Aug;27(6):295-304 [PMID: 24893003]
  93. Bacteriophage. 2014 Dec 15;4(4):e964081 [PMID: 26713221]
  94. Nat Microbiol. 2020 Mar;5(3):465-472 [PMID: 32066959]
  95. Crit Care Med. 2015 Jun;43(6):e190-8 [PMID: 25803649]
  96. Front Microbiol. 2019 Jan 18;9:3227 [PMID: 30713528]
  97. Viruses. 2019 Jan 21;11(1): [PMID: 30669652]
  98. Arch Virol. 2020 Jun;165(6):1289-1297 [PMID: 32246283]
  99. Thorax. 2017 Jul;72(7):666-667 [PMID: 28265031]
  100. Sci Rep. 2017 Sep 13;7(1):11477 [PMID: 28904355]
  101. Front Microbiol. 2016 Aug 31;7:1383 [PMID: 27630633]
  102. Appl Environ Microbiol. 2008 Jul;74(13):4149-63 [PMID: 18456848]
  103. Int J Pharm. 2019 Dec 15;572:118779 [PMID: 31740093]
  104. PLoS One. 2017 Jul 25;12(7):e0181671 [PMID: 28742812]
  105. Cell Mol Life Sci. 2003 Nov;60(11):2356-70 [PMID: 14625682]
  106. JAMA Otolaryngol Head Neck Surg. 2019 Aug 01;145(8):723-729 [PMID: 31219531]
  107. Appl Microbiol Biotechnol. 2017 Nov;101(21):7977-7985 [PMID: 28914348]
  108. Sci Rep. 2017 Jan 25;7:41441 [PMID: 28120922]
  109. Front Microbiol. 2016 Oct 24;7:1681 [PMID: 27822205]
  110. Curr Pharm Biotechnol. 2010 Jan;11(1):15-27 [PMID: 20214605]
  111. J Infect Dis. 2010 Jan 15;201(2):264-71 [PMID: 20001604]
  112. Molecules. 2022 Mar 13;27(6): [PMID: 35335222]
  113. Biomed Res Int. 2015;2015:752930 [PMID: 25879036]
  114. Rev Soc Bras Med Trop. 2019 Nov 14;52:e20190290 [PMID: 31778422]
  115. Front Microbiol. 2019 Jan 09;9:3302 [PMID: 30687281]
  116. Front Microbiol. 2018 Feb 28;9:326 [PMID: 29541067]
  117. Arch Virol. 2013 Aug;158(8):1733-41 [PMID: 23515875]
  118. Front Microbiol. 2016 Sep 26;7:1515 [PMID: 27725811]
  119. Future Microbiol. 2018 Sep;13:1215-1223 [PMID: 30238774]
  120. BMC Microbiol. 2018 Aug 31;18(1):97 [PMID: 30170558]
  121. Sci Rep. 2020 Apr 28;10(1):7163 [PMID: 32346029]
  122. Microbiol Spectr. 2019 May;7(3): [PMID: 31111820]
  123. Int J Mol Sci. 2020 May 25;21(10): [PMID: 32466194]
  124. Appl Environ Microbiol. 2019 May 16;85(11): [PMID: 30902858]
  125. Lancet Infect Dis. 2021 Mar;21(3):427-436 [PMID: 32949500]
  126. J Biosci Bioeng. 2020 Jun;129(6):693-699 [PMID: 32107153]
  127. APMIS. 2017 Jun;125(6):579-584 [PMID: 28418081]
  128. Biochimie. 2015 Oct;117:119-28 [PMID: 25868999]
  129. PLoS Negl Trop Dis. 2019 Aug 19;13(8):e0007113 [PMID: 31425525]
  130. PLoS One. 2010 Nov 22;5(11):e13904 [PMID: 21124920]
  131. Res Microbiol. 2008 Jun;159(5):349-57 [PMID: 18565737]
  132. FEMS Microbiol Lett. 2009 Feb;291(2):201-8 [PMID: 19087204]
  133. BMC Genomics. 2015 Nov 18;16:972 [PMID: 26582495]
  134. Viruses. 2019 Aug 22;11(9): [PMID: 31443379]
  135. Appl Environ Microbiol. 2011 Feb;77(3):756-61 [PMID: 21148689]
  136. Methods Mol Biol. 2019;1898:183-190 [PMID: 30570733]
  137. Antibiotics (Basel). 2019 Jul 25;8(3): [PMID: 31349628]
  138. Antimicrob Agents Chemother. 2007 Jun;51(6):1934-8 [PMID: 17387151]
  139. Curr Pharm Biotechnol. 2010 Jan;11(1):69-86 [PMID: 20214609]
  140. J Glob Antimicrob Resist. 2019 Dec;19:255-261 [PMID: 31100499]
  141. Food Sci Biotechnol. 2016 Feb 29;25(1):355-360 [PMID: 30263278]
  142. J Infect Dev Ctries. 2016 Nov 24;10(11):1208-1213 [PMID: 27886033]
  143. Antimicrob Agents Chemother. 2015 Dec 07;60(2):968-81 [PMID: 26643348]
  144. Viruses. 2019 Jan 21;11(1): [PMID: 30669600]
  145. Biomed Res Int. 2014;2014:793242 [PMID: 24999476]
  146. Front Pharmacol. 2021 May 07;12:675440 [PMID: 34025436]
  147. Front Microbiol. 2019 Aug 06;10:1783 [PMID: 31447809]
  148. Antimicrob Agents Chemother. 2019 Sep 23;63(10): [PMID: 31358593]
  149. Antimicrob Agents Chemother. 2014;58(4):2084-8 [PMID: 24449776]
  150. Infect Immun. 2019 Oct 18;87(11): [PMID: 31451618]
  151. Infect Immun. 2002 Jul;70(7):3904-14 [PMID: 12065534]
  152. Curr Opin Biotechnol. 2021 Apr;68:151-159 [PMID: 33310655]
  153. FEMS Microbiol Lett. 2014 Jul;356(1):113-7 [PMID: 24893888]
  154. Lancet Infect Dis. 2018 Mar;18(3):318-327 [PMID: 29276051]
  155. Cell. 2022 May 26;185(11):1860-1874.e12 [PMID: 35568033]
  156. Antimicrob Agents Chemother. 2017 Sep 22;61(10): [PMID: 28739792]
  157. Clin Otolaryngol. 2009 Aug;34(4):349-57 [PMID: 19673983]
  158. Curr Opin Microbiol. 2011 Oct;14(5):524-31 [PMID: 21868281]
  159. Nat Commun. 2017 Feb 01;8:14187 [PMID: 28146150]
  160. Antimicrob Agents Chemother. 2018 Jan 25;62(2): [PMID: 29158280]
  161. Nat Rev Immunol. 2014 Dec;14(12):796-810 [PMID: 25421701]
  162. Viruses. 2020 Feb 09;12(2): [PMID: 32050494]
  163. Front Microbiol. 2018 Nov 27;9:2927 [PMID: 30538696]
  164. J Virol Methods. 2004 Jan;115(1):99-104 [PMID: 14656466]
  165. Front Microbiol. 2016 Aug 10;7:1251 [PMID: 27558214]
  166. Front Cell Infect Microbiol. 2019 Feb 18;9:22 [PMID: 30834237]
  167. Expert Rev Anti Infect Ther. 2017 Feb;15(2):167-179 [PMID: 27885865]
  168. Curr Pharm Biotechnol. 2010 Jan;11(1):2-14 [PMID: 20214604]
  169. Front Cell Infect Microbiol. 2017 Sep 22;7:418 [PMID: 29018773]
  170. Sci Total Environ. 2022 Jun 10;824:153842 [PMID: 35183626]
  171. Curr Pharm Biotechnol. 2010 Jan;11(1):28-47 [PMID: 20214606]
  172. Antimicrob Agents Chemother. 2017 Sep 22;61(10): [PMID: 28807909]
  173. Antimicrob Agents Chemother. 2022 Mar 15;66(3):e0207121 [PMID: 35041506]
  174. Genome Announc. 2017 Jul 13;5(28): [PMID: 28705957]
  175. Antimicrob Agents Chemother. 2014;58(1):536-42 [PMID: 24189265]
  176. Appl Environ Microbiol. 2012 Apr;78(7):2264-71 [PMID: 22287009]
  177. Nat Protoc. 2020 Sep;15(9):2867-2890 [PMID: 32709990]
  178. Appl Environ Microbiol. 2008 Aug;74(15):4799-805 [PMID: 18515488]
  179. Biomed Res Int. 2018 Jul 11;2018:7569645 [PMID: 30105246]
  180. Bacteriophage. 2015 Aug 28;5(4):e1088124 [PMID: 26909243]
  181. Virol J. 2017 Sep 16;14(1):179 [PMID: 28915819]
  182. Annu Rev Med. 2022 Jan 27;73:197-211 [PMID: 34428079]
  183. Nat Microbiol. 2020 Mar;5(3):391-392 [PMID: 32103171]
  184. Front Microbiol. 2016 Aug 09;7:1253 [PMID: 27555842]
  185. Nat Rev Microbiol. 2010 May;8(5):317-27 [PMID: 20348932]
  186. Viruses. 2018 Feb 06;10(2): [PMID: 29415431]
  187. Nat Med. 2019 May;25(5):730-733 [PMID: 31068712]
  188. Cell Host Microbe. 2017 Jul 12;22(1):38-47.e4 [PMID: 28704651]
  189. Lancet Infect Dis. 2022 Aug;22(8):e208-e220 [PMID: 35248167]
  190. Lancet Infect Dis. 2019 Jan;19(1):35-45 [PMID: 30292481]
  191. Appl Microbiol Biotechnol. 2019 Jun;103(11):4279-4289 [PMID: 30997551]
  192. Antimicrob Agents Chemother. 2012 Jul;56(7):3568-75 [PMID: 22491690]
  193. Front Immunol. 2021 Jun 14;12:639570 [PMID: 34194425]
  194. Sci Rep. 2019 Feb 6;9(1):1527 [PMID: 30728389]
  195. Antimicrob Agents Chemother. 2019 May 24;63(6): [PMID: 30962344]
  196. Appl Microbiol Biotechnol. 2020 Feb;104(4):1609-1619 [PMID: 31900556]
  197. Appl Biochem Biotechnol. 2014 Nov;174(6):2031-47 [PMID: 25163882]
  198. Antimicrob Agents Chemother. 2020 Jan 27;64(2): [PMID: 31767724]
  199. ACS Infect Dis. 2021 Dec 10;7(12):3336-3344 [PMID: 34788533]
  200. Antimicrob Agents Chemother. 2009 Jun;53(6):2469-74 [PMID: 19364866]
  201. Antibiotics (Basel). 2021 Jan 28;10(2): [PMID: 33525684]
  202. Front Microbiol. 2020 Jan 23;11:7 [PMID: 32038593]
  203. Front Cell Infect Microbiol. 2018 Oct 23;8:376 [PMID: 30406049]
  204. Microb Pathog. 2019 Dec;137:103770 [PMID: 31586662]
  205. Bacteriophage. 2013 Apr 1;3(2):e24872 [PMID: 24228220]
  206. Adv Sci (Weinh). 2022 Feb;9(4):e2103645 [PMID: 34914854]
  207. Folia Microbiol (Praha). 2020 Apr;65(2):339-351 [PMID: 31256341]
  208. Res Microbiol. 2018 Nov;169(9):531-539 [PMID: 29777835]
  209. Int J Antimicrob Agents. 2020 Feb;55(2):105844 [PMID: 31715257]
  210. Nat Commun. 2022 Sep 29;13(1):5725 [PMID: 36175406]
  211. Crit Rev Microbiol. 2020 Feb;46(1):78-99 [PMID: 32091280]

MeSH Term

Animals
Humans
Phage Therapy
Bacterial Infections
Bacteriophages
Drug Resistance, Multiple, Bacterial
Models, Animal
Anti-Bacterial Agents

Chemicals

Anti-Bacterial Agents

Word Cloud

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