Bacteriophage–Host Interactions and the Therapeutic Potential of Bacteriophages
Abstract
:1. Introduction
2. Classification of Bacteriophages
3. Phage–Host Adsorption and Cell Entry Strategies
4. Resistance to Phage Attack
5. Bacterial Immunity to Phage Infections
6. Bacteriophage-Based Therapeutics
6.1. Phage Therapy
Infection(s)/Phage Trial Interest | Causative Agent(s)/ Agents of Interest | Outcomes/Comments | Reference/ Clinical Trial Identifier |
---|---|---|---|
Suppurative skin infections * | Pseudomonas, Staphylococcus, Klebsiella, Proteus, and E. coli | Thirty-one patients were treated orally and locally for chronically infected skin ulcers with a 74% success rate | [107,108,109] |
Acute postoperative empyema in chronic suppurative lung diseases * | Staphylococcus, Streptococcus, E. coli, Proteus, Pseudomonas aeruginosa, Burkholderia dolosa | Phage–antibiotic combinations were used in the successful treatment of 45 patients | [110,111,112] |
Complications due to bacterial infections in cancer patients * | Staphylococcus and Pseudomonas | 82% (65) successful treatment with phages compared to 61% (66) of patients treated with antibiotics | [113] |
Recurrent subphrenic abscess * | Antibiotic-resistant E. coli | A single patient was successfully treated with phages after 33 days | [114] |
Urinary tract infections (UTIs) * | Staphylococcus, E. coli, and Proteus | Forty-six UTI patients were treated with phages with 92% making clinical improvements and 84% achieving bacterial clearance | [115] |
Rhinitis, pharyngitis, dermatitis, and conjunctivitis * | Staphylococcus, Streptococcus, E. coli, Proteus, enterococci, and P. aeruginosa | Patients were treated with phages (360), antibiotics (404), and phage–antibiotic combinations (576). Clinical improvements of 86%, 48%, and 83% across the treatment regimes, respectively | [116] |
Cerebrospinal meningitis * | K. pneumoniae | Successful treatment with orally administered phages in a newborn. | [117] |
Bacterial diarrhea | E. coli | Orally administered coliphages showed no improvement in clinical outcome; some dysbiosis with streptococci was observed | [118] |
Complicated or recurrent UTI patients with transurethral resection of the prostate | Enterococcus, E. coli, streptococci, P. mirabilis, P. aeruginosa, staphylococci | Patients with intravesical-administered pyophage cocktail, orally administered antibiotics, and a placebo bladder irrigation. Success rates of 18%, 28% and 37% were observed, respectively | [85] |
Burn wounds | P. aeruginosa | Phages PP1131 showed no significant difference to standard of care antibiotics—patients treated with PP1131 were found to have phage-resistant P. aeruginosa | [119] |
Prosthetic joint infections | S. aureus, S. epidermidis, S. lugdunensis, Streptococcus sp., E. faecium, E. faecalis, E. coli, P. aeruginosa, and/or K. pneumoniae | Phage treatment, with intraoperative and intravenous PhageBank™ bacteriophages, in conjunction with standard-of-care antibiotics/Debridement, Antibiotics, and Implant Retention (DAIR) procedures. Completion is predicted in 2024 | [87,91,120] |
Diabetic foot ulcers (DFUs) | Staphylococcus spp., wound microbiome | Use of anti-staphylococcal phage gel (Intralytix Inc., Baltimore, MA, USA). Effect on bacterial microbiome of DFU wounds and patient outcomes. Trial was abandoned for funding reasons | [121] |
Probiotic application for overall gut health | Bifidobacterium animalis subsp. lactis BL04 | The use of bacteriophages (PreforPro) increased the survival and efficacy of probiotic bacteria administered vs. probiotics only vs. placebo | [122] |
Phages preventing the acquisition of multidrug-resistant enterobacteria (PHAGE-BMR) | E. coli or K. pneumoniae containing ESBL or carbapenemases | Collection of multidrug-resistant bacteria from patients in intensive care, subsequent search for presence and absence of phages in carriers/non-carriers. Currently active but of unknown status | [123] |
Phage dynamics and influences during human gut microbiome establishment (METAKIDS) | A broad range of bacteriophage and bacterial hosts | Characterize phage and bacterial genomes, abundance, and variations during infant gut development. Terminated | [124] |
Bacterial infection in cystic fibrosis patients | P. aeruginosa | A cocktail of 10 bacteriophages was used to reduce Pseudomonas presence after 6 and 24 h including sensitivity of isolates. Completed with no recorded outcomes | [125] |
Prebiotic | Escherichia coli and microbiota | Commercial coliphage cocktail effects on the microbiota and systemic inflammation. No disruption to microbiota and no effect on inflammatory markers | [126] |
Venous leg ulcers | P. aeruginosa, S. aureus, and E. coli | Polyvalent phage preparation of 8 bacteriophages was assessed for their safety and efficacy. No available outcomes but the trial was completed | [127] |
Lower urinary tract colonization | E. coli | Assess the safety, tolerability, pharmacokinetics, and pharmacodynamics of phage cocktail LBP-EC01 | [128,129] |
Safety of topical phage solution intended for wound infections | S. aureus | Evaluating the safety and skin reactions to ascending doses of phages compared to the placebo | [130,131] |
Infection(s) | Bacterial Species | Outcome/Comment | Reference |
---|---|---|---|
Complicated necrotizing pancreatitis | Acinetobacter baumannii | Clearance of A. baumannii and return to health using intravenously (IV) and percutaneously administered (9) phages screened from a phage bank | [86] |
Bacteremia | P. aeruginosa | An IV-administered bacteriophage cocktail comprising two phages cleared the bacteremia, but the patient succumbed to other complications | [132] |
Lung infection and transplant recipient | P. aeruginosa | An IV- and nebulizer-administered bacteriophage cocktail, AB-PA01 and Navy, with the patient recovering from pneumonia | [111] |
Infection of left ventricular assist device | P. aeruginosa | Six-week IV-administered (3) phage cocktail; the patient was clear and then relapsed but a change in antibiotics led to recovery | [133] |
Osteomyelitis | A. baumannii and K. pneumoniae | The patient developed postoperative infection with multidrug-resistant isolates. IV bacteriophage–antibiotic combination led to the patient’s full recovery without the need for amputation | [133] |
UTI | ESBL E. coli | Phage treatment with two phages over 23 days in conjunction with antibiotic treatment led to negative urine cultures and full recovery of the patient | [132] |
CNS infection of a recovering trauma patient | A. baumannii | IV treatment with an A. baumannii phage for 8 days led to CSF cultures coming back negative for A. baumannii but positive for K. pneumoniae and S. aureus. The patient was declared brain dead and later announced deceased | [132] |
Lung infection of cystic fibrosis patient | Achromobacter xylosoxidans | Cefiderocol and phage treatments were performed for 5 days followed by continuous phage therapy. The patient recovered and was discharged | [132,134] |
6.2. Therapeutic Potential of Phage-Derived Proteins
Enzyme Class | Phage/Enzyme | Polymer Substrates | Targeted Genera | References |
---|---|---|---|---|
Hydrolases | ||||
Sialidases | Phi92 | Polysialic acid | E. coli K1 and K92 | [151] |
K1E | E. coli K5 | [162] | ||
K1F | E. coli K1 | [163] | ||
Levanase | SP10 | Levan | Bacillus spp. | [155] |
SPG24 | ||||
Rhamnosidase | Sf6 | O-antigen LPS | Shigella flexneri | [156,164] |
P22 | Rhamnogalacturonan | Salmonella (ser.) Typhimurium | ||
Cellulases | S6 | Cellulose | Erwinia amylovora | [165] |
Peptidases | CHAPK | Pentaglycine cross-bridge peptidoglycan | Staphylococcus aureus | [166,167] |
phiNIT1 | Poly-γ-glutamate | Bacillus spp. | ||
Lyases | ||||
Hyaluronidases | Prophages | Hyaluronan | Streptococcus equi | [168,169] |
H4489A | Streptococcus pyogenes | |||
Alginate lyases | PT 6 | Alginic acid | P. aeruginosa | [14,65] |
AF | P. putida | |||
Pectin/pectate lyases | ΦIPLA7 | Pectin * | Staphylococcal spp. | [170] |
Others | ||||
Colanidase | Phi92 | Colanic acid | E. coli | [63] |
Lipases/triacylglycerol hydrolases | Phi3ST:2 | Carboxyl ester bonds * | Cellulophaga spp. | [171] |
Tf | Pseudomonas spp. |
7. Limitations of Phage Therapy
8. Genomic Engineering of Phages
9. Diagnostic Potential of Phages and Phage-Derived Proteins
10. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Dicks, L.M.T.; Vermeulen, W. Bacteriophage–Host Interactions and the Therapeutic Potential of Bacteriophages. Viruses 2024, 16, 478. https://doi.org/10.3390/v16030478
Dicks LMT, Vermeulen W. Bacteriophage–Host Interactions and the Therapeutic Potential of Bacteriophages. Viruses. 2024; 16(3):478. https://doi.org/10.3390/v16030478
Chicago/Turabian StyleDicks, Leon M. T., and Wian Vermeulen. 2024. "Bacteriophage–Host Interactions and the Therapeutic Potential of Bacteriophages" Viruses 16, no. 3: 478. https://doi.org/10.3390/v16030478