192
Views
5
CrossRef citations to date
0
Altmetric
Perspectives

Risk of Bacteriophage Therapeutics to Transfer Genetic Material and Contain Contaminants Beyond Endotoxins with Clinically Relevant Mitigation Strategies

ORCID Icon
Pages 5629-5637 | Published online: 23 Dec 2021

References

  • Doub JB, Ng VY, Johnson A, Amoroso A, Kottilil S, Wilson E. Potential use of adjuvant bacteriophage therapy with debridement, antibiotics, and implant retention surgery to treat chronic prosthetic joint infections. Open Forum Infect Dis. 2021;8(6):ofab277. doi:10.1093/ofid/ofab27734159220
  • Trend S, Fonceca AM, Ditcham WG, Kicic A, Cf A. The potential of phage therapy in cystic fibrosis: essential human-bacterial-phage interactions and delivery considerations for use in Pseudomonas aeruginosa-infected airways. J Cyst Fibros. 2017;16(6):663–670. doi:10.1016/j.jcf.2017.06.01228720345
  • Dickey J, Perrot V, Becker K. Adjunct phage treatment enhances the effectiveness of low antibiotic concentration against Staphylococcus aureus biofilms in vitro. PLoS One. 2019;14(1):e0209390. doi:10.1371/journal.pone.020939030650088
  • Yilmaz C, Colak M, Yilmaz BC, Ersoz G, Kutateladze M, Gozlugol M. Bacteriophage therapy in implant-related infections: an experimental study. J Bone Joint Surg Am. 2013;95(2):117–125. doi:10.2106/JBJS.K.0113523324958
  • Chaudhry WN, Concepción-Acevedo J, Park T, Andleeb S, Bull JJ, Levin BR. Synergy and order effects of antibiotics and phages in killing pseudomonas aeruginosa biofilms. PLoS One. 2017;12(1):e0168615. doi:10.1371/journal.pone.016861528076361
  • Kaur S, Harjai K, Chhibber S. Bacteriophage mediated killing of Staphylococcus aureus in vitro on orthopaedic K wires in presence of linezolid prevents implant colonization. PLoS One. 2014;9:e90411. doi:10.1371/journal.pone.009041124594764
  • Ferry T, Kolenda C, Batailler C, et al. Phage therapy as adjuvant to conservative surgery and antibiotics to salvage patients with relapsing S. aureus prosthetic knee infection. Front Med (Lausanne). 2020;7:570572. doi:10.3389/fmed.2020.57057233304911
  • Onsea J, Soentjens P, Djebara S, et al. Bacteriophage application for difficult-to-treat musculoskeletal infections: development of a standardized multidisciplinary treatment protocol. Viruses. 2019;11(10):891. doi:10.3390/v11100891
  • Aslam S, Lampley E, Wooten D, 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(9):ofaa389. doi:10.1093/ofid/ofaa38933005701
  • Doub JB. Bacteriophage therapy for clinical biofilm infections: parameters that influence treatment protocols and current treatment approaches. Antibiotics (Basel). 2020;9(11):799. doi:10.3390/antibiotics9110799
  • Jault P, Leclerc T, Jennes S, et al. Efficacy and tolerability of a cocktail of bacteriophages to treat burn wounds infected by Pseudomonas aeruginosa (PhagoBurn): a randomised, controlled, double-blind Phase 1/2 trial. Lancet Infect Dis. 2019;19(1):35–45. doi:10.1016/S1473-3099(18)30482-130292481
  • Leitner L, Ujmajuridze A, Chanishvili N, et al. Intravesical bacteriophages for treating urinary tract infections in patients undergoing transurethral resection of the prostate: a randomised, placebo-controlled, double-blind clinical trial. Lancet Infect Dis. 2021;21(3):427–436. doi:10.1016/S1473-3099(20)30330-332949500
  • Rhoads DD, Wolcott RD, Kuskowski MA, Wolcott BM, Ward LS, Sulakvelidze A. Bacteriophage therapy of venous leg ulcers in humans: results of a Phase I safety trial. J Wound Care. 2009;18(6):237–243. doi:10.12968/jowc.2009.18.6.4280119661847
  • Mašlaňová I, Doškař J, Varga M, et al. Bacteriophages of Staphylococcus aureus efficiently package various bacterial genes and mobile genetic elements including SCCmec with different frequencies. Environ Microbiol Rep. 2013;5(1):66–73. doi:10.1111/j.1758-2229.2012.00378.x23757132
  • Birge EA. Bacterial and Bacteriophage Genetics. 4th ed. New York: Springer; 2000.
  • Goh S. Phage Transduction. Methods Mol Biol. 2016;1476:177–185.27507341
  • Chen J, Quiles-Puchalt N, Chiang YN, et al. Genome hypermobility by lateral transduction. Science. 2018;362(6411):207–212. doi:10.1126/science.aat586730309949
  • Volkova VV, Lu Z, Besser T, Gröhn YT. Modeling the infection dynamics of bacteriophages in enteric Escherichia coli: estimating the contribution of transduction to antimicrobial gene spread. Appl Environ Microbiol. 2014;80(14):4350–4362. doi:10.1128/AEM.00446-1424814786
  • Nanda AM, Thormann K, Frunzke J. Impact of spontaneous prophage induction on the fitness of bacterial populations and host-microbe interactions. J Bacteriol. 2015;197(3):410–419. doi:10.1128/JB.02230-1425404701
  • Chiang YN, Penadés JR, Chen J. Genetic transduction by phages and chromosomal islands: the new and noncanonical. PLoS Pathog. 2019;15:e1007878. doi:10.1371/journal.ppat.100787831393945
  • Fillol-Salom A, Alsaadi A, Sousa JAM, et al. Bacteriophages benefit from generalized transduction. PLoS Pathog. 2019;15(7):e1007888. doi:10.1371/journal.ppat.100788831276485
  • Schmidt H, Hensel M. Pathogenicity islands in bacterial pathogenesis [published correction appears in Clin Microbiol Rev. 2006 Jan;19(1):257]. Clin Microbiol Rev. 2004;17(1):14–56. doi:10.1128/CMR.17.1.14-56.200414726454
  • Cervera-Alamar M, Guzmán-Markevitch K, Žiemytė M, et al. Mobilisation mechanism of pathogenicity islands by endogenous phages in Staphylococcus aureus clinical strains. Sci Rep. 2018;8(1):16742. doi:10.1038/s41598-018-34918-230425253
  • Karaolis DK, Somara S, Maneval DR, Johnson JA, Kaper JB. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria. Nature. 1999;399(6734):375–379. doi:10.1038/2071510360577
  • Novick RP, Ram G. Staphylococcal pathogenicity islands-movers and shakers in the genomic firmament. Curr Opin Microbiol. 2017;38:197–204. doi:10.1016/j.mib.2017.08.00129100762
  • Ram G, Chen J, Kumar K, et al. Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. Proc Natl Acad Sci U S A. 2012;109(40):16300–16305. doi:10.1073/pnas.120461510922991467
  • Chen J, Novick RP. Phage-mediated intergeneric transfer of toxin genes. Science. 2009;323(5910):139–141. doi:10.1126/science.116478319119236
  • Tsao YF, Taylor VL, Kala S, et al. Phage morons play an important role in Pseudomonas aeruginosa phenotypes. J Bacteriol. 2018;200(22):e00189–18. doi:10.1128/JB.00189-1830150232
  • Asadulghani M, Ogura Y, Ooka T, et al. The defective prophage pool of Escherichia coli O157: prophage-prophage interactions potentiate horizontal transfer of virulence determinants. PLoS Pathog. 2009;5(5):e1000408. doi:10.1371/journal.ppat.100040819412337
  • Johnson HM, Russell JK, Pontzer CH. Staphylococcal enterotoxin microbial superantigens. FASEB J. 1991;5(12):2706–2712. doi:10.1096/fasebj.5.12.19160931916093
  • Krakauer T, Stiles BG. The staphylococcal enterotoxin (SE) family: SEB and siblings. Virulence. 2013;4(8):759–773. doi:10.4161/viru.2390523959032
  • Doub JB, Wilson E. Observed transaminitis with a unique bacteriophage therapy protocol to treat recalcitrant Staphylococcal biofilm infections [published online ahead of print, 2021 Jul 30]. Infection. 2021. doi:10.1007/s15010-021-01675-w
  • Abedon ST, Danis-Wlodarczyk KM, Alves DR. Phage therapy in the 21st century: is there modern, clinical evidence of phage-mediated efficacy? Pharmaceuticals. 2021;14(11):1157. doi:10.3390/ph1411115734832939
  • Sander M, Schmieger H. Method for host-independent detection of generalized transducing bacteriophages in natural habitats. Appl Environ Microbiol. 2001;67(4):1490–1493. doi:10.1128/AEM.67.4.1490-1493.200111282595
  • Beumer A, Robinson JB. A broad-host-range, generalized transducing phage (SN-T) acquires 16S rRNA genes from different genera of bacteria. Appl Environ Microbiol. 2005;71(12):8301–8304. doi:10.1128/AEM.71.12.8301-8304.200516332816
  • Del Casale A, Flanagan PV, Larkin MJ, Allen CC, Kulakov LA. Extent and variation of phage-borne bacterial 16S rRNA gene sequences in wastewater environments. Appl Environ Microbiol. 2011;77(15):5529–5532. doi:10.1128/AEM.00457-1121666016
  • Alexeeva S, Guerra Martínez JA, Spus M, Smid EJ. Spontaneously induced prophages are abundant in a naturally evolved bacterial starter culture and deliver competitive advantage to the host. BMC Microbiol. 2018;18(1):120. doi:10.1186/s12866-018-1229-130249194
  • Mašlaňová I, Stříbná S, Doškař J, Pantůček R. Efficient plasmid transduction to Staphylococcus aureus strains insensitive to the lytic action of transducing phage. FEMS Microbiol Lett. 2016;363(19):fnw211. doi:10.1093/femsle/fnw21127609232
  • Yue WF, Du M, Zhu MJ. High temperature in combination with UV irradiation enhances horizontal transfer of stx2 gene from E. coli O157: H7to non-pathogenic E. coli. PLoS One. 2012;7(2):e31308. doi:10.1371/journal.pone.003130822347461
  • Pinchuk IV, Beswick EJ, Reyes VE. Staphylococcal enterotoxins. Toxins (Basel). 2010;2(8):2177–2197. doi:10.3390/toxins208217722069679
  • Van Tyne D, Martin MJ, Gilmore MS. Structure, function, and biology of the Enterococcus faecalis cytolysin. Toxins (Basel). 2013;5(5):895–911. doi:10.3390/toxins505089523628786
  • Lau GW, Hassett DJ, Britigan BE. Modulation of lung epithelial functions by Pseudomonas aeruginosa. Trends Microbiol. 2005;13(8):389–397. doi:10.1016/j.tim.2005.05.01115951179
  • Marshall JC. Endotoxin in the pathogenesis of sepsis. Contrib Nephrol. 2010;167:1–13.20519894
  • Kissner TL, Cisney ED, Ulrich RG, Fernandez S, Saikh KU. Staphylococcal enterotoxin A induction of pro-inflammatory cytokines and lethality in mice is primarily dependent on MyD88. Immunology. 2010;130(4):516–526. doi:10.1111/j.1365-2567.2010.03249.x20465563
  • Janik E, Ceremuga M, Saluk-Bijak J, Bijak M. Biological toxins as the potential tools for bioterrorism. Int J Mol Sci. 2019;20(5):1181. doi:10.3390/ijms20051181
  • Rusnak JM, Kortepeter MG, Ulrich R, et al. Laboratory exposures to staphylococcal enterotoxin B. Emerg Infect Dis. 2004;10(9):1544–1549. doi:10.3201/eid1009.04025015498154
  • Meyrand A, Boutrand-Loei S, Ray-Gueniot S, et al. Growth and enterotoxin production of Staphylococcus aureus during the manufacture and ripening of Camembert-type cheeses from raw goats’ milk. J Appl Microbiol. 1998;85(3):537–544. doi:10.1046/j.1365-2672.1998.853531.x9750284
  • Spinale JM, Ruebner RL, Copelovitch L, Kaplan BS. Long-term outcomes of Shiga toxin hemolytic uremic syndrome. Pediatr Nephrol. 2013;28(11):2097–2105. doi:10.1007/s00467-012-2383-623288350
  • Chesney PJ, Crass BA, Polyak MB, et al. Toxic shock syndrome: management and long-term sequelae. Ann Intern Med. 1982;96(6 Pt 2):847–851. doi:10.7326/0003-4819-96-6-8477091955
  • Löfblom J, Rosenstein R, Nguyen MT, Ståhl S, Götz F. Staphylococcus carnosus: from starter culture to protein engineering platform. Appl Microbiol Biotechnol. 2017;101(23–24):8293–8307. doi:10.1007/s00253-017-8528-628971248
  • Nair D, Memmi G, Hernandez D, et al. Whole-genome sequencing of Staphylococcus aureus strain RN4220, a key laboratory strain used in virulence research, identifies mutations that affect not only virulence factors but also the fitness of the strain. J Bacteriol. 2011;193(9):2332–2335. doi:10.1128/JB.00027-1121378186
  • Rodríguez-Rubio L, Serna C, Ares-Arroyo M, et al. Extensive antimicrobial resistance mobilization via multicopy plasmid encapsidation mediated by temperate phages. J Antimicrob Chemother. 2020;75(11):3173–3180. doi:10.1093/jac/dkaa31132719862
  • Hay ID, Lithgow T. Filamentous phages: masters of a microbial sharing economy. EMBO Rep. 2019;20(6):e47427. doi:10.15252/embr.20184742730952693
  • Faruque SM, Mekalanos JJ. Phage-bacterial interactions in the evolution of toxigenic Vibrio cholerae. Virulence. 2012;3(7):556–565. doi:10.4161/viru.2235123076327
  • Wolcott R, Costerton JW, Raoult D, Cutler SJ. The polymicrobial nature of biofilm infection. Clin Microbiol Infect. 2013;19(2):107–112. doi:10.1111/j.1469-0691.2012.04001.x22925473
  • Orazi G, O’Toole GA. “It takes a village”: mechanisms underlying antimicrobial recalcitrance of polymicrobial biofilms. J Bacteriol. 2019;202(1):e00530–19. doi:10.1128/JB.00530-1931548277
  • Jean-Pierre F, Vyas A, Hampton TH, Henson MA, O’Toole GA. One versus many: polymicrobial communities and the cystic fibrosis airway. mBio. 2021;12(2):e00006–21. doi:10.1128/mBio.00006-2133727344
  • Sibley CD, Surette MG. The polymicrobial nature of airway infections in cystic fibrosis: cangene gold medal lecture. Can J Microbiol. 2011;57(2):69–77. doi:10.1139/W10-10521326348
  • Noor S, Zubair M, Ahmad J. Diabetic foot ulcer–a review on pathophysiology, classification and microbial etiology. Diabetes Metab Syndr. 2015;9(3):192–199. doi:10.1016/j.dsx.2015.04.00725982677
  • Azam AH, Tanji Y. Peculiarities of Staphylococcus aureus phages and their possible application in phage therapy. Appl Microbiol Biotechnol. 2019;103(11):4279–4289. doi:10.1007/s00253-019-09810-230997551
  • Secor PR, Sweere JM, Michaels LA, et al. Filamentous bacteriophage promote biofilm assembly and function. Cell Host Microbe. 2015;18(5):549–559. doi:10.1016/j.chom.2015.10.01326567508
  • Pires DP, Melo LDR, Azeredo J. Understanding the complex phage-host interactions in biofilm communities. Annu Rev Virol. 2021;8(1):73–94. doi:10.1146/annurev-virology-091919-07422234186004
  • Wilson GG, Young KY, Edlin GJ, Konigsberg W. High-frequency generalised transduction by bacteriophage T4. Nature. 1979;280(5717):80–82. doi:10.1038/280080a015305587