In vivo efficacy of single phage versus phage cocktail in resolving burn wound infection in BALB/c mice

Microbial Pathogenesis

Volumn 99, Issue , 2016, Pages 68-77

  Chadha, Parul ^a   Katare, Om Prakash ^b   Chhibber, Sanjay ^a  

^a PANJAB UNIVERSITY   (India)

^b PANJAB UNIVERSITY   (India)

Author keywords

Bacteriophage; Burn wound infection; Cocktail; Klebsiella pneumoniae

Indexed keywords

COLLAGEN; MYELOPEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL LOAD; BACTERIOPHAGE; BAGG ALBINO MOUSE; BIOLOGICAL THERAPY; BURN INFECTION; CLINICAL EFFECTIVENESS; COLLAGEN SYNTHESIS; COLONY FORMING UNIT; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIZATION; HISTOPATHOLOGY; HOST RANGE; IN VIVO STUDY; KLEBSIELLA PNEUMONIAE; MOUSE; NONHUMAN; PHAGE COCKTAIL; PHAGE THERAPY; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; ANIMAL; BURN; COMPLICATION; DISEASE MODEL; GROWTH, DEVELOPMENT AND AGING; KLEBSIELLA INFECTIONS; PROCEDURES; TIME FACTOR; TREATMENT OUTCOME; WOUND INFECTION;

ANIMALS; BACTERIAL LOAD; BACTERIOPHAGES; BURNS; DISEASE MODELS, ANIMAL; KLEBSIELLA INFECTIONS; MICE, INBRED BALB C; PHAGE THERAPY; TIME FACTORS; TREATMENT OUTCOME; WOUND INFECTION;

EID: 84981489410     PISSN: 08824010     EISSN: 10961208     Source Type: Journal    
DOI: 10.1016/j.micpath.2016.08.001     Document Type: Article

References (62)

1. [1] Williams, F.N., Herndon, D.N., Hawkins, H.K., Lee, J.O., Cox, R.A., Kulp, G.A., Finnerty, C.C., Chinkes, D.L., Jeschke, M.G., The leading causes of death after burn injury in a single pediatric burn center. Crit. Care, 13, 2009, 183.
2. [2] Mann, E.A., Baun, M.M., Meininger, J.C., Wade, C.E., Comparison of mortality associated with sepsis in the burn, trauma, and general intensive care unit patient: a systematic review of the literature. Shock 37 (2012), 4–16.
3. [3] Schwacha, M.G., Holland, L.T., Chaudry, I.H., Messina, J.L., Genetic variability in the immune-inflammatory response after major burn injury. Shock 23 (2005), 123–128.
4. [4] Mundhada, S.G., Waghmare, P.H., Rathod, P.G., Ingole, K.V., Bacterial and fungal profile of burn wound infections in Tertiary Care Center. Ind. J. Burns 23 (2015), 71–75.
5. [5] Malik, R., Chhibber, S., Protection with bacteriophage KØ1 against fatal Klebsiella, pneumoniae-induced burn wound infection in mice. J. Microbiol. Immunol. Infect. 42 (2009), 134–140.
6. [6] Nasser, S., Mabrouk, A., Maher, A., Colonization of burn wounds in Ain Shams university burn unit. Burns 29 (2003), 229–233.
7. [7] Brusselaers, N., Vogelaers, D., Blot, S., The rising problem of antimicrobial resistance in the intensive care unit. Ann. Intensive. Care, 1, 2011, 47.
8. [8] Chung The, H., Karkey, A., Phan Thanh, D., Boinett, C.J., Cain, A.K., Ellington, M., Baker, K.S., Dongol, S., Thompson, C., Harris, S.R., Jombart, T., Le Thi Phuong, T., Tran Do Hoang, N., Ha Thanh, T., Shretha, S., Joshi, S., Basnyat, B., Thwaites, G., Thomson, N.R., Rabaa, M.A., Baker, S., A high resolution genomic analysis of multidrug-resistant hospital outbreaks of Klebsiella pneumonia. EMBO Mol. Med. 7 (2015), 227–239.
9. [9] Sakandelidze, V.M., The combined use of specific phages and antibiotics in different infectious allergoses. Vrach. Delo 3 (1991), 60–63.
10. [10] Cislo, M., Dabrowski, M., Weber-Dabrowska, B., Woyton, A., Bacteriophage treatment of suppurative skin infections. Arch. Immunol. Ther. Exp. 2 (1987), 175–183.
11. [11] Weber-Dabrowska, B., Dabrowski, M., Slopek, S., Studies on bacteriophage penetration in patients subjected to phage therapy. Arch. Immunol. Ther. Exp. 35 (1987), 563–568.
12. [12] Chhibber, S., Kaur, T., Kaur, S., Co-Therapy using lytic bacteriophage and linezolid: effective treatment in eliminating methicillin resistant Staphylococcus aureus (MRSA) from diabetic foot infections. PLoS One, 8, 2013, 56022.
13. [13] Mathur, M.D., Bidhani, S., Mehndiratta, P.L., Bacteriophage therapy: an alternative to conventional antibiotics. J. Assoc. Phys. India 51 (2003), 593–596.
14. [14] Kumari, S., Harjai, K., Chhibber, S., Topical treatment of Klebsiella pneumoniae B5055 induced burn wound infection in mice using natural products. J. Infect. Dev. Ctries. 4 (2010), 367–377.
15. [15] Singla, S., Harjai, K., Katare, O.P., Chhibber, S., Bacteriophage-loaded nanostructured lipid carrier: improved pharmacokinetics mediates effective resolution of Klebsiella pneumoniae induced lobar pneumonia. J. Infect. Dis., 2015, 10.1093/infdis/jiv029.
16. [16] Soothill, J.S., Bacteriophage prevents destruction of skin grafts by Pseudomonas aeruginosa. Burns 3 (1994), 209–211.
17. [17] Letkiewicz, S., Międzybrodzki, R., Klak, M., Jonczyk, E., Weber-Dabrowska, B., Gorski, A., The perspectives of the application of phage therapy in chronic bacterial prostatitis. FEMS. Immunol. Med. Microbiol. 60 (2010), 99–112.
18. [18] Wright, A., Hawkins, C.H., Anggård, E.E., Harper, D.R., A controlled clinical trial of a therapeutic bacteriophage preparation in chronic otitis due to antibiotic-resistant Pseudomonas aeruginosa; a preliminary report of efficacy. Clin. Otolaryngol. 34 (2009), 349–357.
19. [19] Mathur, M.D., Vidhani, S., Mehndiratta, P.L., Bacteriophage therapy: an alternative to conventional antibiotics. J. Assoc. Phys. India 51 (2003), 593–596.
20. [20] Carlton, R.M., Noordman, W.H., Biswas, B., de Meester, E.D., Loessner, M.J., Bacteriophage P100 for control of Listeria monocytogenes in foods: genome sequence, bioinformatic analyses, oral toxicity study, and application. Regul. Toxicol. Pharmacol. 43 (2005), 301–312.
21. [21] Hanlon, G.W., Bacteriophages: an appraisal of their role in the treatment of bacterial infections. Int. J. Antimicrob. Agents 30 (2007), 118–128.
22. [22] Scott, A.E., Timms, A.R., Connerton, P.L., El-Shibiny, A., Connerton, I.F., Bacteriophage influence Campylobacter jejuni types populating broiler chickens. Environ. Microbiol. 9 (2007), 2341–2353.
23. [23] Cairns, B.J., Timms, A.R., Jansen, V.A.A., Connerton, I.F., Payne, R.J.H., Quantitative models of in vitro bacteriophage–host dynamics and their application to phage therapy. PLoS Pathog. 5 (2009), 1–10.
24. [24] Labrie, S.J., Samson, J.E., Moineau, S., Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8 (2010), 317–327.
25. [25] Sulakvelidze, A., Alavidze, Z., Morris, J., Bacteriophage therapy. Antimicrob. Agents. Chemother. 45 (2001), 649–659.
26. [26] Cairns, B.J., Payne, R.J.H., Bacteriophage therapy and the mutant selection window. Antimicrob. Agents. Chemother. 52 (2008), 4344–4350.
27. [27] Kunisaki, H., Tanji, Y., Intercrossing of phage genomes in a phage cocktail and stable coexistence with Escherichia coli 0157:H7 in anaerobic continuous culture. Appl. Microbiol. Biotechnol. 85 (2010), 1533–1540.
28. [28] Kudva, I.T., Jelacic, S., Tarr, P.i., Youderian, P., Hovde, C.J., Biocontrol of Escherichia coli O157 with O157-specific bacteriophages. Appl. Environ. Microbiol. 65 (1999), 3767–3773.
29. [29] Boone, D.R., Castenholz, R.W., Bergey's Manual of Systematic Bacteriology. second ed., 2001, Springer, New York.
30. [30] Cerveny, K.E., Paola, A., Duckworth, D.H., Gulig, P.A., Phage therapy of local and systemic disease caused by Vibrio vulnificus in iron - dextran -treated mice. Infect. Immun. 70 (2002), 6251–6262.
31. [31] Adams, M., Bacteriophages. 1959, Intersciences, New York.
32. [32] Sambrook, J., Fritsch, E.F., Maniatis, T., Molecular Cloning: a Laboratory Manual. second ed., 1989, Cold Spring Habor laboratory Press, Cold Spring Harbor, New York.
33. [33] Chang, H.C., Chen, C.R., Lin, J.W., Shen, G.H., Chang, K.M., Tseng, Y.H., Weng, S.F., Isolation and characterization of novel giant Stenotrophomonas maltophilia phage FSMA5. Appl. Environ. Microbiol. 71 (2005), 1387–1393.
34. [34] Pajunen, M., Kiljunen, S., Skurnik, M., Bacteriophage φYeO3-12, specific for Yersinia enterocolitica serotype O:3, is related to coliphages T3 and T7. J. Bacteriol. 182 (2000), 5114–5120.
35. [35] Goodridge, L., Gallacci, A., Griffiths, M.W., Morphological, host range and genetic characterization of two coliphages. Appl. Environ. Microbiol. 69 (2003), 5364–5371.
36. [36] Hsieh, S.E., Lo, H.H., Chen, S.T., Lee, M.C., Tseng, Y.H., Wide host range and strong lytic activity of Staphylococcus aureus lytic phage Stau2. Appl. Environ. Microbiol. 77 (2011), 756–761.
37. [37] Kaur, S., Harjai, K., Chhibber, S., Bacteriophage-aided intracellular killing of engulfed methicillin-resistant Staphylococcus aureus (MRSA) by murine macrophages. Appl. Microbiol. Biotechnol. 98 (2014), 4653–4661.
38. [38] Dale, R.M.K., Schnell, G., Wong, J.P., Therapeutic efficacy of “Nubiotics” against burn wound infection by Pseudomonas aeruginosa. Antimicrob. Agents. Chemother. 48 (2004), 2918–2923.
39. [39] Greenberger, M.J., Strieter, R.M., Kunkel, S.L., Danforth, J.M., Laichalk, L.L., Mc Gillicuddy, D.C., Standiford, T.J., Neutralization of Macrophage inflammatory protein-2 attenuates neutrophil recruitment and bacterial clearance in murine Klebsiella pneumoniae. J. Infect. Dis. 173 (1996), 159–165.
40. [40] Brans, T.A., Dutrieux, R.P., Hoekstra, M.J., Kreis, R.W., Du Pont, J.S., Histopathological evaluation of scalds and contact burns in the pig model. Burns, 20, 1994, 548.
41. [41] Meena, K., Mohan, A.V., Sharath, B., Somayaji, S.N., Bairy, K.L., Effect of topical phenytoin on burn wound healing in rats. Indian. J. Exp. Biol. 49 (2011), 56–59.
42. [42] Perween, N., Prakash, S.K., Siddiqui, O., Multi drug resistant Klebsiella isolates in burn patients: a comparative study. J. Clin. Diagn. Res. 9 (2015), 14–16.
43. [43] Findlay, J., Hamouda, A., Dancer, S.J., Amyes, S.G., Rapid acquisition of decreased carbapenem susceptibility in a strain of Klebsiella pneumoniae arising during meropenem therapy. Clin. Microbiol. Infect. 18 (2012), 140–146.
44. [44] Donovan, D.M., Bacteriophage and peptidoglycan degrading enzymes with antimicrobial applications. Recent. Pat. Biotechnol. 1 (2007), 113–122.
45. [45] Filippov, A.A., Sergueev, K.V., He, Y., Huang, X.-Z., Gnade, B.T., Mueller, A.J., Fernandez-Prada, C.M., Nikolich, M.P., Bacteriophage-Resistant Mutants in Yersinia pestis: identification of phage receptors and attenuation for mice. PLoS One, 6, 2011, e25486.
46. [46] O'Flynn, G., Ross, R.P., Fitzgerald, G.F., Coffey, A., Evaluation of a cocktail of three bacteriophages for biocontrol of Escherichia coli O157:H7. Appl. Environ. Microbiol. 70 (2004), 3417–3424.
47. [47] Tomat, D., Migliore, L., Aquili, V., Quiberoni, A., Balagué, C., Phage biocontrol of enteropathogenic and shiga toxin-producing Escherichia coli in meat products. Front. Cell. Infect. Microbiol., 3, 2013, 20.
48. [48] Chirico, D., Gorla, A., Verga, V., Pedersen, P.D., Polgatti, E., Cava, A., Dal Bello, F., Bacteriophage-insensitive mutants for high quality Crescenza manufacture. Front. Microbiol., 5, 2014, 201.
49. [49] Uchiyama, J., Takemura, I., Satoh, M., Kato, S., Ujihara, T., Akechi, K., Matsuzaki, S., Daibata, M., Improved adsorption of an Enterococcus faecalis bacteriophage ΦEF24C with a spontaneous point mutation. PLoS One, 6, 2011, e26648.
50. [50] Gu, J., Liu, X., Li, Y., Han, W., Lei, L., Yang, Y., Zhao, H., Gao, Y., Song, J., Lu, R., Sun, C., Feng, X., A method for generation phage cocktail with great therapeutic potential. PLoS One, 7, 2012, e31698.
51. [51] Chan, B.K., Abedon, S.T., Loc-Carrillo, C., Phage cocktails and the future of phage therapy. Future. Microbiol. 8 (2013), 769–783.
52. [52] Kim, M., Ryu, S., Spontaneous and transient defence against bacteriophage by phase-variable glucosylation of O-antigen in Salmonella enterica serovar Typhimurium. Mol. Microbiol. 86 (2012), 411–425.
53. [53] Tanji, Y., Shimada, T., Yoichi, M., Miyanaga, K., Hori, K., Unno, H., Toward rational control of Escherichia coli O157:H7 by a phage cocktail. Appl. Microbiol. Biotechnol. 64 (2004), 270–274.
54. [54] McVay, C.S., Velásquez, M., Fralick, J.A., Phage Therapy of Pseudomonas aeruginosa infection in a mouse burn wound model. Antimicrob. Agents. Chemother. 51 (2007), 1934–1938.
55. [55] Payne, R.J., Jansen, V.A., Evidence for a phage proliferation threshold?. J. Virol., 76, 2002, 13123.
56. [56] Fischer, S., Kittler, S., Klein, G., Glünder, G., Impact of a single phage and a phage cocktail application in broilers on reduction of Campylobacter jejuni and development of resistance. PLoS One, 8, 2013, e78543.
57. [57] Hooton, S.P., Atterbury, R.J., Connerton, I.F., Application of a bacteriophage cocktail to reduce Salmonella Typhimurium U288 contamination on pig skin, Resistance. Int. J. Food. Microbiol. 151 (2011), 157–163.
58. [58] Bennett, M.F., Robinson, M.K., Baron, E.D., Cooper, K.D., Immune Systems, Skin, Inflammation: protector of the skin or promoter of aging?. J. Investig. Dermatol. Symp. Proc. 13 (2008), 15–19.
59. [59] Carlton, R.M., Phage therapy: past history and future prospects. Arch. Immun. Ther. Exp. 47 (1999), 267–274.
60. [60] Sulakvelidze, A., Morris, J.G., Bacteriophages as therapeutic agents. Ann. Med. 33 (2001), 507–509.
61. [61] Kishor, C., Mishra, R.R., Saraf, S.K., Kumar, M., Srivastav, A.K., Nath, G., Phage therapy of staphylococcal chronic osteomyelitis in experimental animal model. Indian. J. Med. Res. 143 (2016), 87–94.
62. [62] Porter, J., Anderson, J., Carter, L., Donjacour, E., Paros, M., In vitro evaluation of a novel bacteriophage cocktail as a preventative for bovine coliform mastitis. J. Dairy. Sci. 99 (2016), 2053–2062.