Phage Therapy in the Twenty-First Century: Facing the Decline of the Antibiotic Era; Is It Finally Time for the Age of the Phage?

Literature Cited

1. 1. 

   Ando H, Lemire S, Pires DP, Lu TK 2015. Engineering modular viral scaffolds for targeted bacterial population editing. Cell Syst 1:187–96
   [Google Scholar]
2. 2. 

   Bai J, Kim YT, Ryu S, Lee JH 2016. Biocontrol and rapid detection of food-borne pathogens using bacteriophages and endolysins. Front. Microbiol. 7:474
   [Google Scholar]
3. 3. 

   Banks PA, Freeman ML, Pract. Parameters Comm. Am. Coll. Gastroenterol. 2006. Practice guidelines in acute pancreatitis. Am. J. Gastroenterol. 101:2379–400
   [Google Scholar]
4. 4. 

   Billard-Pomares T, Fouteau S, Jacquet ME, Roche D, Barbe V et al. 2014. Characterization of a P1-like bacteriophage carrying an SHV-2 extended-spectrum β-lactamase from an Escherichia coli strain. Antimicrob. Agents Chemother. 58:6550–57
   [Google Scholar]
5. 5. 

   Boyd EF. 2012. Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions. Adv. Virus Res. 82:91–118
   [Google Scholar]
6. 6. 

   Bren L. 2007. Bacteria-eating virus approved as food additive. FDA Consum 41:20–22
   [Google Scholar]
7. 7. 

   Chan BK, Turner PE, Kim S, Mojibian HR, Elefteriades JA, Narayan D 2018. Phage treatment of an aortic graft infected with Pseudomonas aeruginosa. Evol. Med. Public Health 2018:60–66
   [Google Scholar]
8. 8. 

   Chart H, Row B, Threlfall EJ, Ward LR 1989. Conversion of Salmonella enteritidis phage type 4 to phage type 7 involves loss of lipopolysaccharide with concomitant loss of virulence. FEMS Microbiol. Lett. 60:37–40
   [Google Scholar]
9. 9. 

   Citorik RJ, Mimee M, Lu TK 2014. Bacteriophage-based synthetic biology for the study of infectious diseases. Curr. Opin. Microbiol. 19:59–69
   [Google Scholar]
10. 10. 

    Clokie MR, Millard AD, Letarov AV, Heaphy S 2011. Phages in nature. Bacteriophage 1:31–45
    [Google Scholar]
11. 11. 

    Commercial aspects of bacteriophage therapy 1933. JAMA 100:1603–4
12. 12. 

    de la Cruz VF, Lal AA, McCutchan TF 1988. Immunogenicity and epitope mapping of foreign sequences via genetically engineered filamentous phage. J. Biol. Chem. 263:4318–22
    [Google Scholar]
13. 13. 

    d'Herelle F. 1917. Sur un microbe invisible antagoniste des bacilles dysentèriques. C. R. Hebd. Séanc. Acad. Sci. Paris 165:373–75
    [Google Scholar]
14. 14. 

    Didelot X, Bowden R, Wilson DJ, Peto TEA, Crook DW 2012. Transforming clinical microbiology with bacterial genome sequencing. Nat. Rev. Genet. 13:601–12
    [Google Scholar]
15. 15. 

    DiMasi JA, Grabowski HG, Hansen RW 2016. Innovation in the pharmaceutical industry: new estimates of R&D costs. J. Health Econ. 47:20–33
    [Google Scholar]
16. 16. 

    Donelli G, Dore E, Frontali C, Grandolfo ME 1975. Structure and physico-chemical properties of bacteriophage G. III. A homogeneous DNA of molecular weight 5 × 10⁸. J. Mol. Biol. 94:555–65
    [Google Scholar]
17. 17. 

    Eaton MD, Bayne-Jones S. 1934. Bacteriophage therapy—review of the principles and results of the use of bacteriophage in the treatment of infections. JAMA 103:1934–39
    [Google Scholar]
18. 18. 

    Esvelt KM, Carlson JC, Liu DR 2011. A system for the continuous directed evolution of biomolecules. Nature 472:499–503
    [Google Scholar]
19. 19. 

    Frenkel D, Katz O, Solomon B 2000. Immunization against Alzheimer's β-amyloid plaques via EFRH phage administration. PNAS 97:11455–59
    [Google Scholar]
20. 20. 

    Geier MR, Trigg ME, Merril CR 1973. Fate of bacteriophage lambda in non-immune germ-free mice. Nature 246:221–23
    [Google Scholar]
21. 21. 

    Gill JJ, Hyman P. 2010. Phage choice, isolation, and preparation for phage therapy. Curr. Pharm. Biotechnol. 11:2–14
    [Google Scholar]
22. 22. 

    Golden MR, Marra CM, Holmes KK 2003. Update on syphilis: resurgence of an old problem. JAMA 290:1510–14
    [Google Scholar]
23. 23. 

    Griffiths AJF. 2000. An Introduction to Genetic Analysis New York: W.H. Freeman
24. 24. 

    Henry M, Biswas B, Vincent L, Mokashi V, Schuch R et al. 2012. Development of a high throughput assay for indirectly measuring phage growth using the OmniLog™ system. Bacteriophage 2:159–67
    [Google Scholar]
25. 25. 

    Hotchkiss RS, Karl IE. 2003. The pathophysiology and treatment of sepsis. N. Engl. J. Med. 348:138–50
    [Google Scholar]
26. 26. 

    Hsieh SE, Lo HH, Chen ST, Lee MC, Tseng YH 2011. Wide host range and strong lytic activity of Staphylococcus aureus lytic phage Stau2. Appl. Environ. Microbiol. 77:756–61
    [Google Scholar]
27. 27. 

    Jerne NK. 1956. The presence in normal serum of specific antibody against bacteriophage T4 and its increase during the earliest stages of immunization. J. Immunol. 76:209–16
    [Google Scholar]
28. 28. 

    Knouf EG, Ward WE Reichle PA, Bower AG, Hamilton PM 1946. Treatment of typhoid fever with type specific bacteriophage. JAMA 132:134–38
    [Google Scholar]
29. 29. 

    Kristensen DM, Cai X, Mushegian A 2011. Evolutionarily conserved orthologous families in phages are relatively rare in their prokaryotic hosts. J. Bacteriol. 193:1806–14
    [Google Scholar]
30. 30. 

    Kutateladze M. 2015. Experience of the Eliava Institute in bacteriophage therapy. Virol. Sin. 30:80–81
    [Google Scholar]
31. 31. 

    Kutateladze M, Adamia R. 2008. Phage therapy experience at the Eliava Institute. Med. Mal. Infect. 38:426–30
    [Google Scholar]
32. 32. 

    Labrie SJ, Samson JE, Moineau S 2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317–27
    [Google Scholar]
33. 33. 

    LaVergne S, Hamilton T, Biswas B, Kumaraswamy M, Schooley RT, Wooten D 2018. Phage therapy for a multidrug-resistant Acinetobacter baumannii craniectomy site infection. Open. Forum. Infect. Dis. 5:ofy064
    [Google Scholar]
34. 34. 

    Laxminarayan R, Powers JH. 2011. Antibacterial R&D incentives. Nat. Rev. Drug Discov. 10:727–28
    [Google Scholar]
35. 35. 

    Lee YT, Kuo SC, Yang SP, Lin YT, Tseng FC et al. 2012. Impact of appropriate antimicrobial therapy on mortality associated with Acinetobacter baumannii bacteremia: relation to severity of infection. Clin. Infect. Dis. 55:209–15
    [Google Scholar]
36. 36. 

    Leon M, Bastias R. 2015. Virulence reduction in bacteriophage resistant bacteria. Front. Microbiol. 6:343
    [Google Scholar]
37. 37. 

    Levison ME, Levison JH. 2009. Pharmacokinetics and pharmacodynamics of antibacterial agents. Infect. Dis. Clin. N. Am. 23:791–815
    [Google Scholar]
38. 38. 

    Luchi M, Morrison DC, Opal S, Yoneda K, Slotman G et al. 2000. A comparative trial of imipenem versus ceftazidime in the release of endotoxin and cytokine generation in patients with gram-negative urosepsis. J. Endotoxin. Res. 6:25–31
    [Google Scholar]
39. 39. 

    Lusiak-Szelachowska M, Zaczek M, Weber-Dabrowska B, Miedzybrodzki R, Klak M et al. 2014. Phage neutralization by sera of patients receiving phage therapy. Viral Immunol. 27:295–304
    [Google Scholar]
40. 40. 

    Mancuso F, Shi J, Malik DJ 2018. High throughput manufacturing of bacteriophages using continuous stirred tank bioreactors connected in series to ensure optimum host bacteria physiology for phage production. Viruses 10:E537
    [Google Scholar]
41. 41. 

    Manring MM, Hawk A, Calhoun JH, Andersen RC 2009. Treatment of war wounds: a historical review. Clin. Orthop. Relat. Res. 467:2168–91
    [Google Scholar]
42. 42. 

    Mantus D, Pisano DJ. 2014. FDA Regulatory Affairs Boca Raton, FL: Taylor Francis
43. 43. 

    Marinelli LJ, Piuri M, Swigonova Z, Balachandran A, Oldfield LM et al. 2008. BRED: a simple and powerful tool for constructing mutant and recombinant bacteriophage genomes. PLOS ONE 3:e3957
    [Google Scholar]
44. 44. 

    McKinley EB. 1923. The bacteriophage in the treatment of infections. Arch. Intern. Med. 32:899–910
    [Google Scholar]
45. 45. 

    Merril CR, Biswas B, Carlton R, Jensen NC, Creed GJ et al. 1996. Long-circulating bacteriophage as antibacterial agents. PNAS 93:3188–92
    [Google Scholar]
46. 46. 

    Merril CR, Scholl D, Adhya SL 2003. The prospect for bacteriophage therapy in Western medicine. Nat. Rev. Drug Discov. 2:489–97
    [Google Scholar]
47. 47. 

    Meyer JR, Dobias DT, Weitz JS, Barrick JE, Quick RT, Lenski RE 2012. Repeatability and contingency in the evolution of a key innovation in phage lambda. Science 335:428–32
    [Google Scholar]
48. 48. 

    Miedzybrodzki R, Borysowski J, Weber-Dabrowska B, Fortuna W, Letkiewicz S et al. 2012. Clinical aspects of phage therapy. Adv. Virus Res. 83:73–121
    [Google Scholar]
49. 49. 

    Munford RS. 2016. Endotoxemia—menace, marker, or mistake. ? J. Leukoc. Biol. 100:687–98
    [Google Scholar]
50. 50. 

    O'Flaherty S, Ross RP, Meaney W, Fitzgerald GF, Elbreki MF, Coffey A 2005. Potential of the polyvalent anti-Staphylococcus bacteriophage K for control of antibiotic-resistant staphylococci from hospitals. Appl. Environ. Microbiol. 71:1836–42
    [Google Scholar]
51. 51. 

    Paine AB. 1912. Mark Twain: A Biography New York: Harper Brothers
52. 52. 

    Pan YJ, Lin TL, Chen CC, Tsai YT, Cheng YH et al. 2017. Klebsiella phage ΦK64-1 encodes multiple depolymerases for multiple host capsular types. J. Virol. 91:e02457–16
    [Google Scholar]
53. 53. 

    Pantucek R, Rosypalova A, Doskar J, Kailerova J, Ruzickova V et al. 1998. The polyvalent staphylococcal phage ϕ812: its host-range mutants and related phages. Virology 246:241–52
    [Google Scholar]
54. 54. 

    Patel R. 2016. New developments in clinical bacteriology laboratories. Mayo Clin. Proc. 91:1448–59
    [Google Scholar]
55. 55. 

    Paterson S, Vogwill T, Buckling A, Benmayor R, Spiers AJ et al. 2010. Antagonistic coevolution accelerates molecular evolution. Nature 464:275–78
    [Google Scholar]
56. 56. 

    Patterson TL, Semple SJ, Abramovitz D, Harvey-Vera A, Pines HA et al. 2019. Impact of time perspectives on texting intervention to reduce HIV/STI transmission among female sex workers in Tijuana and Ciudad Juarez, Mexico. J. Behav. Med. 42:111–27
    [Google Scholar]
57. 57. 

    Penades JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP 2015. Bacteriophage-mediated spread of bacterial virulence genes. Curr. Opin. Microbiol. 23:171–78
    [Google Scholar]
58. 58. 

    Philipson CW, Voegtly LJ, Lueder MR, Long KA, Rice GK et al. 2018. Characterizing phage genomes for therapeutic applications. Viruses 10:E188
    [Google Scholar]
59. 59. 

    Pines HA, Semple SJ, Strathdee SA, Hendrix CW, Harvey-Vera A et al. 2018. Vaginal washing and lubrication among female sex workers in the Mexico-US border region: implications for the development of vaginal PrEP for HIV prevention. BMC Public Health 18:1009
    [Google Scholar]
60. 60. 

    Pines HA, Strathdee SA, Hendrix CW, Bristow CC, Harvey-Vera A et al. 2019. Oral and vaginal HIV pre-exposure prophylaxis product attribute preferences among female sex workers in the Mexico-US border region. Int. J. STD AIDS 60:45–55
    [Google Scholar]
61. 61. 

    Pitpitan EV, Semple SJ, Aarons GA, Palinkas LA, Chavarin CV et al. 2018. Factors associated with program effectiveness in the implementation of a sexual risk reduction intervention for female sex workers across Mexico: results from a randomized trial. PLOS ONE 13:e0201954
    [Google Scholar]
62. 62. 

    Quiles-Puchalt N, Carpena N, Alonso JC, Novick RP, Marina A, Penades JR 2014. Staphylococcal pathogenicity island DNA packaging system involving cos-site packaging and phage-encoded HNH endonucleases. PNAS 111:6016–21
    [Google Scholar]
63. 63. 

    R Soc 1951. Obit. Not. Fellows R. Soc. 7:20504–17
64. 64. 

    Regeimbal JM, Jacobs AC, Corey BW, Henry MS, Thompson MG et al. 2016. Personalized therapeutic cocktail of wild environmental phages rescues mice from Acinetobacter baumannii wound infections. Antimicrob. Agents Chemother. 60:5806–16
    [Google Scholar]
65. 65. 

    Reindel R, Fiore CR. 2017. Phage therapy: considerations and challenges for development. Clin. Infect. Dis. 64:1589–90
    [Google Scholar]
66. 66. 

    Rhodes A, Evans LE, Alhazzani W, Levy MM, Antonelli M et al. 2017. Surviving sepsis campaign: international guidelines for management of sepsis and septic shock: 2016. Crit. Care Med. 45:486–552
    [Google Scholar]
67. 67. 

    Rice TB. 1930. The use of bacteriophage filtrates in the treatment of suppurative conditions. Am. J. Med. Sci. 179:345–60
    [Google Scholar]
68. 68. 

    Samson JE, Magadan AH, Sabri M, Moineau S 2013. Revenge of the phages: defeating bacterial defences. Nat. Rev. Microbiol. 11:675–87
    [Google Scholar]
69. 69. 

    Scanlan PD, Hall AR, Blackshields G, Friman VP, Davis MR Jr. et al. 2015. Coevolution with bacteriophages drives genome-wide host evolution and constrains the acquisition of abiotic-beneficial mutations. Mol. Biol. Evol. 32:1425–35
    [Google Scholar]
70. 70. 

    Schless RA. 1932. Staphylococcus aureus meningitis: treatment with specific bacteriophage. Am. J. Dis. Child. 44:813–22
    [Google Scholar]
71. 71. 

    Schmieger H, Schicklmaier P. 1999. Transduction of multiple drug resistance of Salmonella enterica serovar typhimurium DT104. FEMS Microbiol. Lett. 170:251–56
    [Google Scholar]
72. 72. 

    Schooley RT, Biswas B, Gill JJ, Hernandez-Morales A, Lancaster J et al. 2017. Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob. Agents Chemother 61:e00954-17 Erratum 2018. Antimicrob. Agents Chemother. 62:e02221–18
    [Google Scholar]
73. 73. 

    Schultz I, Neva FA. 1965. Relationship between blood clearance and viruria after intravenous injection of mice and rats with bacteriophage and polioviruses. J. Immunol. 94:833–41
    [Google Scholar]
74. 74. 

    Shin J, Jardine P, Noireaux V 2012. Genome replication, synthesis, and assembly of the bacteriophage T7 in a single cell-free reaction. ACS Synth. Biol. 1:408–13
    [Google Scholar]
75. 75. 

    Shorr AF, Owens RC Jr 2009. Guidelines and quality for community-acquired pneumonia: measures from the Joint Commission and the Centers for Medicare and Medicaid Services. Am. J. Health Syst. Pharm. 66:S2–7
    [Google Scholar]
76. 76. 

    Simpson AJ, Opal SM, Angus BJ, Prins JM, Palardy JE et al. 2000. Differential antibiotic-induced endotoxin release in severe melioidosis. J. Infect. Dis. 181:1014–19
    [Google Scholar]
77. 77. 

    Stent GS. 1963. Molecular Biology of Bacterial Viruses San Francisco: Freeman
78. 78. 

    Storms ZJ, Brown T, Cooper DG, Sauvageau D, Leask RL 2014. Impact of the cell life-cycle on bacteriophage T4 infection. FEMS Microbiol. Lett. 353:63–68
    [Google Scholar]
79. 79. 

    Suffredini AF, Fromm RE, Parker MM, Brenner M, Kovacs JA et al. 1989. The cardiovascular response of normal humans to the administration of endotoxin. N. Engl. J. Med. 321:280–87
    [Google Scholar]
80. 80. 

    Summers WC. 2001. Bacteriophage therapy. Annu. Rev. Microbiol. 55:437–51
    [Google Scholar]
81. 81. 

    Summers WC. 2012. The strange history of phage therapy. Bacteriophage 2:130–33
    [Google Scholar]
82. 82. 

    Tomaras AP, Dunman PM. 2015. In the midst of the antimicrobial discovery conundrum: an overview. Curr. Opin. Microbiol. 27:103–7
    [Google Scholar]
83. 83. 

    Town AE, Frisbee FSC. 1932. Bacteriophage in ophthalmology—a preliminary report. Arch. Ophthalmol. 8:683–89
    [Google Scholar]
84. 84. 

    Twort FW. 1915. An investigation on the nature of ultra-microscopic viruses. Lancet 2:1241–43
    [Google Scholar]
85. 85. 

    Vitiello CL, Merril CR, Adhya S 2005. An amino acid substitution in a capsid protein enhances phage survival in mouse circulatory system more than a 1000-fold. Virus Res 114:101–3
    [Google Scholar]
86. 86. 

    Yen M, Cairns LS, Camilli A 2017. A cocktail of three virulent bacteriophages prevents Vibrio cholerae infection in animal models. Nat. Commun. 8:14187
    [Google Scholar]
87. 87. 

    Young R. 2014. Phage lysis: three steps, three choices, one outcome. J. Microbiol. 52:243–58
    [Google Scholar]
88. 88. 

    Young R, Gill JJ. 2015. Phage therapy redux—What is to be done. ? Science 350:1163–64
    [Google Scholar]
89. 89. 

    Yuan Y, Gao M. 2017. Jumbo bacteriophages: an overview. Front. Microbiol. 8:403
    [Google Scholar]
90. 90. 

    Zhao M, Lepak AJ, Andes DR 2016. Animal models in the pharmacokinetic/pharmacodynamic evaluation of antimicrobial agents. Bioorg. Med. Chem. 24:6390–400
    [Google Scholar]
91. 91. 

    Zinder ND, Lederberg J. 1952. Genetic exchange in Salmonella. J. Bacteriol. 64:679–99
    [Google Scholar]