Isolation and characterization of lytic bacteriophages against Pseudomonas aeruginosa isolates from human infections in the north-west of Iran
,
Abstract
Background and Objectives: With the emergence of Pseudomonas aeruginosa antibiotic-resistant strains, using the antibacterial potential of bacteriophages could be an effective approach to combat bacterial infections.
Materials and Methods: In this study, after evaluation of antibiotic sensitivity of 20 clinical bacterial isolates of Pseudomonas aeruginosa, isolation of lytic phages was performed against 15 isolates using double-layer agar overlay technique. Molecular analysis of isolated phages was carried out using EcoRV and HindIII endonucleases. Then, the host range of the phages was evaluated and the phage with the broadest host range (PPaMa1/18) was selected to morphological characteristics by TEM. Also, its one-step growth curve was determined and the stability of the phage to environmental parameters (temperature and pH) was evaluated.
Results: All isolates of Pseudomonas aeruginosa were resistant to five antibiotics. In total, 15 phages were successfully isolated from the sewage sources against each of 15 used bacterial isolates. Molecular analysis of the phages showed a high rate of genomic variation. In the morphological analysis of the selected phage (PPaMa1/18) using TEM, an icosahedral head with a size of 90 nm × 75 nm and a long contractile tail (215 nm) were observed which indicated its similarity to the Myoviridae family. The latent period of the PPaMa1/18 was about 20 minutes and its burst size was estimated to be 58 PFU/cell. Also, the PPaMa1/18 phage antibacterial activity was not significantly affected at pH 4-10 and temperature 4-40C°.
Conclusion: Findings demonstrated that isolated bacteriophage (PPaMa1/18) with wide host range, strong lytic effect and high stability can be used as a promising candidate for the treatment of antibiotic-resistant infections caused by Pseudomonas aeruginosa.
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2. Hancock RE, Speert DP. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updat 2000; 3: 247-255.
3. Battle SE, Rello J, Hauser AR. Genomic islands of Pseudomonas aeruginosa. FEMS Microbiol Lett 2009; 290: 70-78.
4. Pires DP, Boas DV, Sillankorva S, Azeredo J. Phage therapy: a step forward in the treatment of Pseudomonas aeruginosa infections. J Virol 2015; 89: 7449-7456.
5. Snyder LA, Loman NJ, Faraj LA, Levi K, Weinstock G, Boswell TC, et al. Epidemiological investigation of Pseudomonas aeruginosa isolates from a six-year-long hospital outbreak using high-throughput whole genome sequencing. Euro Surveill 2013; 18: 20611.
6. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-193.
7. Essoh C, Blouin Y, Loukou G, Cablanmian A, Lathro S, Kutter E, et al. The susceptibility of Pseudomonas aeruginosa strains from cystic fibrosis patients to bacteriophages. PLoS One 2013; 8(4): e60575.
8. Lister PD, Wolter DJ, Hanson ND. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin Microbiol Rev 2009; 22: 582-610.
9. Lambert PA. Mechanisms of antibiotic resistance in Pseudomonas aeruginosa. J R Soc Med 2002; 95 Suppl 41(Suppl 41): 22-26.
10. Aloush V, Navon-Venezia S, Seigman-Igra Y, Cabili S, Carmeli Y. Multidrug-resistant Pseudomonas aeruginosa: risk factors and clinical impact. Antimicrob Agents Chemother 2006; 50: 43-48.
11. Hall AR, De Vos D, Friman VP, Pirnay JP, Buckling A. Effects of sequential and simultaneous applications of bacteriophages on populations of Pseudomonas aeruginosa in vitro and in wax moth larvae. Appl Environ Microbiol 2012; 78: 5646-5652.
12. Clark JR, March JB. Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol 2006; 24: 212-218.
13. Ackermann HW. 5500 Phages examined in the electron microscope. Arch Virol 2007; 152: 227-243.
Chaudhry WN, Akhtar MN, Andleeb S, Qadri I. Bacteriophages and their implications on future biotechnology: a review. Virol J 2012; 9: 9.
15. Henry M, Debarbieux L. Tools from viruses: bacteriophage successes and beyond. Virology 2012; 434: 151-161.
16. Endersen L, O'Mahony J, Hill C, Ross RP, McAuliffe O, Coffey A. Phage therapy in the food industry. Annu Rev Food Sci Technol 2014; 5: 327-349.
17. Pires D, Sillankorva S, Faustino A, Azeredo J. Use of newly isolated phages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. Res Microbiol 2011; 162: 798-806.
18. Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother 2010; 54: 397-404.
19. Wright A, Hawkins CH, Änggård EE, Harper DR. 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 2009; 34: 349-357.
20. Watanabe R, Matsumoto T, Sano G, Ishii Y, Tateda K, Sumiyama Y, et al. Efficacy of bacteriophage therapy against gut-derived sepsis caused by Pseudomonas aeruginosa in mice. Antimicrob Agents Chemother 2007; 51: 446-452.
21. Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1996; 45: 493-496.
22. Wayne PA. Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute. CLSI M100-S27. 2017.
23. Pallavali RR, Degati VL, Lomada D, Reddy MC, Durbaka VRP. Isolation and in vitro evaluation of bacteriophages against MDR-bacterial isolates from septic wound infections. PLoS One 2017; 12(7): e0179245.24. Cao Z, Zhang J, Niu
YD, Cui N, Ma Y, Cao F, et al. Isolation and characterization of a “phiKMV-like” bacteriophage and its therapeutic effect on mink hemorrhagic pneumonia. PLoS One 2015; 10(1): e0116571.
25. Pajunen M, Kiljunen S, Skurnik M. Bacteriophage phiYeO3-12, specific for Yersinia enterocolitica serotype O: 3, is related to coliphages T3 and T7. J Bacteriol 2000; 182: 5114-5120.
26. Bao H, Zhang H, Wang R. Isolation and characterization of bacteriophages of Salmonella enterica serovar Pullorum. Poult Sci 2011; 90: 2370-2377.
27. Verma V, Harjai K, Chhibber S. Characterization of a T7-like lytic bacteriophage of Klebsiella pneumoniae B5055: a potential therapeutic agent. Curr Microbiol 2009; 59: 274-281.
28. Breidenstein EB, de la Fuente-Núñez C, Hancock RE. Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol 2011; 19: 419-426.
29. Vieira A, Silva YJ, Cunha A, Gomes NC, Ackermann HW, Almeida A. Phage therapy to control multidrug-resistant Pseudomonas aeruginosa skin infections: in vitro and ex vivo experiments. Eur J Clin Microbiol Infect Dis 2012; 31: 3241-3249.
30. kouchaksaraei FM, Shahandashti EF, Molana Z, kouchaksaraei MM, Asgharpour F, Mojtahedi A, et al. Molecular detection of Integron genes and pattern of antibiotic resistance in Pseudomonas aeruginosa strains isolated from intensive care unit, Shahid Beheshti Hospital, North of Iran. Int J Mol Cell Med 2012; 1: 209-217.
31. Hosu MC, Vasaikar S, Okuthe GE, Apalata T. Molecular detection of antibiotic-resistant genes in Pseudomonas aeruginosa from nonclinical environment: public health implications in Mthatha, Eastern Cape province, South Africa. Int J Microbiol 2021; 2021: 8861074.
32. Brzozowski M, Krukowska Ż, Galant K, Jursa-Kulesza J, Kosik-Bogacka D. Genotypic characterisation and antimicrobial resistance of Pseudomonas aeruginosa strains isolated from patients of different hospitals and medical centres in Poland. BMC Infect Dis 2020; 20: 693.33. Chan BK, Abedon ST, Loc-Carrillo C. Phage cocktails and the future of phage
therapy. Future Microbiol 2013; 8: 769-783.
34. Goodridge LW (2008). Phages, bacteria and food. In: bacteriophage ecology: population growth, evolution and impact of bacterial viruses. Ed, ST Abedon. Cambridge University Press, 1st ed, Cambridge, UK, pp. 302-305.
35. Yu X, Xu Y, Gu Y, Zhu Y, Liu X. Characterization and genomic study of “phiKMV-Like” phage PAXYB1 infecting Pseudomonas aeruginosa. Sci Rep 2017; 7: 13068.
36. Jamal M, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, et al. Isolation and characterization of a bacteriophage and its utilization against multi-drug resistant Pseudomonas aeruginosa-2995. Life Sci 2017; 190: 21-28.
37. Azizian R, Nasser A, Askari H, Kalani MT, Sadeghifard N, Pakzad I, et al. Sewage as a rich source of phage study against Pseudomonas aeruginosa PAO. Biologicals 2015; 43: 238-241.
38. Akhwale JK, Rohde M, Rohde C, Bunk B, Spröer C, Boga HI, et al. Isolation, characterization and analysis of bacteriophages from the haloalkaline lake Elmenteita, Kenya. PLoS One 2019; 14(4): e0215734.
39. Kwiatek M, Mizak L, Parasion S, Gryko R, Olender A, Niemcewicz M. Characterization of five newly isolated bacteriophages active against Pseudomonas aeruginosa clinical strains. Folia Microbiol (Praha) 2015; 60: 7-14.
40. Garbe J, Wesche A, Bunk B, Kazmierczak M, Selezska K, Rohde C, et al. Characterization of JG024, a Pseudomonas aeruginosa PB1-like broad host range phage under simulated infection conditions. BMC Microbiol 2010; 10: 301.
41. Essoh C, Latino L, Midoux C, Blouin Y, Loukou G, Nguetta SP, et al. Investigation of a large collection of Pseudomonas aeruginosa bacteriophages collected from a single environmental source in Abidjan, Côte d’Ivoire. PLoS One 2015 ;10(6): e0130548.
42. de Melo ACC, da Mata Gomes A, Melo FL, Ardisson-Araújo DMP, de Vargas AP, Ely VL, et al. Characterization of a bacteriophage with broad host range against strains of Pseudomonas aeruginosa isolated from domestic animals. BMC Microbiol 2019; 19: 134.
43. Amarillas L, Rubí-Rangel L, Chaidez C, González-Robles A, Lightbourn-Rojas L, León-Félix J. Isolation and characterization of phiLLS, a novel phage with potential biocontrol agent against multidrug-resistant Escherichia coli. Front Microbiol 2017; 8: 1355.
44. El Didamony G, Askora A, Shehata AA. Isolation and characterization of T7-like lytic bacteriophages infecting multidrug resistant Pseudomonas aeruginosa isolated from Egypt. Curr Microbiol 2015; 70: 786-791.
45. Müller-Merbach M, Kohler K, Hinrichs J. Environmental factors for phage-induced fermentation problems: replication and adsorption of the Lactococcus lactis phage P008 as influenced by temperature and pH. Food Microbiol 2007; 24: 695-702.
46. Jurczak-Kurek A, Gąsior T, Nejman-Faleńczyk B, Bloch S, Dydecka A, Topka G, et al. Biodiversity of bacteriophages: morphological and biological properties of a large group of phages isolated from urban sewage. Sci Rep 2016; 6: 34338.
47. Cui X, You J, Sun L, Yang X, Zhang T, Huang K, et al. Characterization of Pseudomonas aeruginosa phage C11 and identification of host genes required for virion maturation. Sci Rep 2016; 6: 39130.
48. Latz S, Krüttgen A, Häfner H, Buhl EM, Ritter K, Horz HP. Differential effect of newly isolated phages belonging to PB1-Like, phiKZ-Like and LUZ24-Like Viruses against Multi-Drug Resistant Pseudomonas aeruginosa under varying growth conditions. Viruses 2017; 9: 315.
49. Heo YJ, Lee YR, Jung HH, Lee J, Ko G, Cho YH. Antibacterial efficacy of phages against Pseudomonas aeruginosa infections in mice and Drosophila melanogaster. Antimicrob Agents Chemother 2009; 53: 2469-2474.50. Ahmadi M,
Karimi Torshizi MA, Rahimi S, Dennehy JJ. Prophylactic bacteriophage administration more effective than post-infection administration in reducing Salmonella enterica serovar Enteritidis shedding in Quail. Front Microbiol 2016; 7: 1253.
51. Hazem A. Effects of temperatures, pH-values, ultra-violet light, ethanol and chloroform on the growth of isolated thermophilic Bacillus phages. New Microbiol 2002; 25: 469-476.
52. Tan CW, Rukayadi Y, Hasan H, Abdul-Mutalib NA, Jambari NN, Hara H, et al. Isolation and characterization of six Vibrio parahaemolyticus lytic bacteriophages from seafood samples. Front Microbiol 2021; 12: 616548.
53. Santos TM, Ledbetter EC, Caixeta LS, Bicalho ML, Bicalho RC. Isolation and characterization of two bacteriophages with strong in vitro antimicrobial activity against Pseudomonas aeruginosa isolated from dogs with ocular infections. Am J Vet Res 2011; 72: 1079-1086.
2. Hancock RE, Speert DP. Antibiotic resistance in Pseudomonas aeruginosa: mechanisms and impact on treatment. Drug Resist Updat 2000; 3: 247-255.
3. Battle SE, Rello J, Hauser AR. Genomic islands of Pseudomonas aeruginosa. FEMS Microbiol Lett 2009; 290: 70-78.
4. Pires DP, Boas DV, Sillankorva S, Azeredo J. Phage therapy: a step forward in the treatment of Pseudomonas aeruginosa infections. J Virol 2015; 89: 7449-7456.
5. Snyder LA, Loman NJ, Faraj LA, Levi K, Weinstock G, Boswell TC, et al. Epidemiological investigation of Pseudomonas aeruginosa isolates from a six-year-long hospital outbreak using high-throughput whole genome sequencing. Euro Surveill 2013; 18: 20611.
6. Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 2002; 15: 167-193.
7. Essoh C, Blouin Y, Loukou G, Cablanmian A, Lathro S, Kutter E, et al. The susceptibility of Pseudomonas aeruginosa strains from cystic fibrosis patients to bacteriophages. PLoS One 2013; 8(4): e60575.
8. Lister PD, Wolter DJ, Hanson ND. Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms. Clin Microbiol Rev 2009; 22: 582-610.
9. Lambert PA. Mechanisms of antibiotic resistance in Pseudomonas aeruginosa. J R Soc Med 2002; 95 Suppl 41(Suppl 41): 22-26.
10. Aloush V, Navon-Venezia S, Seigman-Igra Y, Cabili S, Carmeli Y. Multidrug-resistant Pseudomonas aeruginosa: risk factors and clinical impact. Antimicrob Agents Chemother 2006; 50: 43-48.
11. Hall AR, De Vos D, Friman VP, Pirnay JP, Buckling A. Effects of sequential and simultaneous applications of bacteriophages on populations of Pseudomonas aeruginosa in vitro and in wax moth larvae. Appl Environ Microbiol 2012; 78: 5646-5652.
12. Clark JR, March JB. Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol 2006; 24: 212-218.
13. Ackermann HW. 5500 Phages examined in the electron microscope. Arch Virol 2007; 152: 227-243.
Chaudhry WN, Akhtar MN, Andleeb S, Qadri I. Bacteriophages and their implications on future biotechnology: a review. Virol J 2012; 9: 9.
15. Henry M, Debarbieux L. Tools from viruses: bacteriophage successes and beyond. Virology 2012; 434: 151-161.
16. Endersen L, O'Mahony J, Hill C, Ross RP, McAuliffe O, Coffey A. Phage therapy in the food industry. Annu Rev Food Sci Technol 2014; 5: 327-349.
17. Pires D, Sillankorva S, Faustino A, Azeredo J. Use of newly isolated phages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. Res Microbiol 2011; 162: 798-806.
18. Fu W, Forster T, Mayer O, Curtin JJ, Lehman SM, Donlan RM. Bacteriophage cocktail for the prevention of biofilm formation by Pseudomonas aeruginosa on catheters in an in vitro model system. Antimicrob Agents Chemother 2010; 54: 397-404.
19. Wright A, Hawkins CH, Änggård EE, Harper DR. 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 2009; 34: 349-357.
20. Watanabe R, Matsumoto T, Sano G, Ishii Y, Tateda K, Sumiyama Y, et al. Efficacy of bacteriophage therapy against gut-derived sepsis caused by Pseudomonas aeruginosa in mice. Antimicrob Agents Chemother 2007; 51: 446-452.
21. Bauer AW, Kirby WM, Sherris JC, Turck M. Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1996; 45: 493-496.
22. Wayne PA. Performance Standards for Antimicrobial Susceptibility Testing. Clinical and Laboratory Standards Institute. CLSI M100-S27. 2017.
23. Pallavali RR, Degati VL, Lomada D, Reddy MC, Durbaka VRP. Isolation and in vitro evaluation of bacteriophages against MDR-bacterial isolates from septic wound infections. PLoS One 2017; 12(7): e0179245.24. Cao Z, Zhang J, Niu
YD, Cui N, Ma Y, Cao F, et al. Isolation and characterization of a “phiKMV-like” bacteriophage and its therapeutic effect on mink hemorrhagic pneumonia. PLoS One 2015; 10(1): e0116571.
25. Pajunen M, Kiljunen S, Skurnik M. Bacteriophage phiYeO3-12, specific for Yersinia enterocolitica serotype O: 3, is related to coliphages T3 and T7. J Bacteriol 2000; 182: 5114-5120.
26. Bao H, Zhang H, Wang R. Isolation and characterization of bacteriophages of Salmonella enterica serovar Pullorum. Poult Sci 2011; 90: 2370-2377.
27. Verma V, Harjai K, Chhibber S. Characterization of a T7-like lytic bacteriophage of Klebsiella pneumoniae B5055: a potential therapeutic agent. Curr Microbiol 2009; 59: 274-281.
28. Breidenstein EB, de la Fuente-Núñez C, Hancock RE. Pseudomonas aeruginosa: all roads lead to resistance. Trends Microbiol 2011; 19: 419-426.
29. Vieira A, Silva YJ, Cunha A, Gomes NC, Ackermann HW, Almeida A. Phage therapy to control multidrug-resistant Pseudomonas aeruginosa skin infections: in vitro and ex vivo experiments. Eur J Clin Microbiol Infect Dis 2012; 31: 3241-3249.
30. kouchaksaraei FM, Shahandashti EF, Molana Z, kouchaksaraei MM, Asgharpour F, Mojtahedi A, et al. Molecular detection of Integron genes and pattern of antibiotic resistance in Pseudomonas aeruginosa strains isolated from intensive care unit, Shahid Beheshti Hospital, North of Iran. Int J Mol Cell Med 2012; 1: 209-217.
31. Hosu MC, Vasaikar S, Okuthe GE, Apalata T. Molecular detection of antibiotic-resistant genes in Pseudomonas aeruginosa from nonclinical environment: public health implications in Mthatha, Eastern Cape province, South Africa. Int J Microbiol 2021; 2021: 8861074.
32. Brzozowski M, Krukowska Ż, Galant K, Jursa-Kulesza J, Kosik-Bogacka D. Genotypic characterisation and antimicrobial resistance of Pseudomonas aeruginosa strains isolated from patients of different hospitals and medical centres in Poland. BMC Infect Dis 2020; 20: 693.33. Chan BK, Abedon ST, Loc-Carrillo C. Phage cocktails and the future of phage
therapy. Future Microbiol 2013; 8: 769-783.
34. Goodridge LW (2008). Phages, bacteria and food. In: bacteriophage ecology: population growth, evolution and impact of bacterial viruses. Ed, ST Abedon. Cambridge University Press, 1st ed, Cambridge, UK, pp. 302-305.
35. Yu X, Xu Y, Gu Y, Zhu Y, Liu X. Characterization and genomic study of “phiKMV-Like” phage PAXYB1 infecting Pseudomonas aeruginosa. Sci Rep 2017; 7: 13068.
36. Jamal M, Andleeb S, Jalil F, Imran M, Nawaz MA, Hussain T, et al. Isolation and characterization of a bacteriophage and its utilization against multi-drug resistant Pseudomonas aeruginosa-2995. Life Sci 2017; 190: 21-28.
37. Azizian R, Nasser A, Askari H, Kalani MT, Sadeghifard N, Pakzad I, et al. Sewage as a rich source of phage study against Pseudomonas aeruginosa PAO. Biologicals 2015; 43: 238-241.
38. Akhwale JK, Rohde M, Rohde C, Bunk B, Spröer C, Boga HI, et al. Isolation, characterization and analysis of bacteriophages from the haloalkaline lake Elmenteita, Kenya. PLoS One 2019; 14(4): e0215734.
39. Kwiatek M, Mizak L, Parasion S, Gryko R, Olender A, Niemcewicz M. Characterization of five newly isolated bacteriophages active against Pseudomonas aeruginosa clinical strains. Folia Microbiol (Praha) 2015; 60: 7-14.
40. Garbe J, Wesche A, Bunk B, Kazmierczak M, Selezska K, Rohde C, et al. Characterization of JG024, a Pseudomonas aeruginosa PB1-like broad host range phage under simulated infection conditions. BMC Microbiol 2010; 10: 301.
41. Essoh C, Latino L, Midoux C, Blouin Y, Loukou G, Nguetta SP, et al. Investigation of a large collection of Pseudomonas aeruginosa bacteriophages collected from a single environmental source in Abidjan, Côte d’Ivoire. PLoS One 2015 ;10(6): e0130548.
42. de Melo ACC, da Mata Gomes A, Melo FL, Ardisson-Araújo DMP, de Vargas AP, Ely VL, et al. Characterization of a bacteriophage with broad host range against strains of Pseudomonas aeruginosa isolated from domestic animals. BMC Microbiol 2019; 19: 134.
43. Amarillas L, Rubí-Rangel L, Chaidez C, González-Robles A, Lightbourn-Rojas L, León-Félix J. Isolation and characterization of phiLLS, a novel phage with potential biocontrol agent against multidrug-resistant Escherichia coli. Front Microbiol 2017; 8: 1355.
44. El Didamony G, Askora A, Shehata AA. Isolation and characterization of T7-like lytic bacteriophages infecting multidrug resistant Pseudomonas aeruginosa isolated from Egypt. Curr Microbiol 2015; 70: 786-791.
45. Müller-Merbach M, Kohler K, Hinrichs J. Environmental factors for phage-induced fermentation problems: replication and adsorption of the Lactococcus lactis phage P008 as influenced by temperature and pH. Food Microbiol 2007; 24: 695-702.
46. Jurczak-Kurek A, Gąsior T, Nejman-Faleńczyk B, Bloch S, Dydecka A, Topka G, et al. Biodiversity of bacteriophages: morphological and biological properties of a large group of phages isolated from urban sewage. Sci Rep 2016; 6: 34338.
47. Cui X, You J, Sun L, Yang X, Zhang T, Huang K, et al. Characterization of Pseudomonas aeruginosa phage C11 and identification of host genes required for virion maturation. Sci Rep 2016; 6: 39130.
48. Latz S, Krüttgen A, Häfner H, Buhl EM, Ritter K, Horz HP. Differential effect of newly isolated phages belonging to PB1-Like, phiKZ-Like and LUZ24-Like Viruses against Multi-Drug Resistant Pseudomonas aeruginosa under varying growth conditions. Viruses 2017; 9: 315.
49. Heo YJ, Lee YR, Jung HH, Lee J, Ko G, Cho YH. Antibacterial efficacy of phages against Pseudomonas aeruginosa infections in mice and Drosophila melanogaster. Antimicrob Agents Chemother 2009; 53: 2469-2474.50. Ahmadi M,
Karimi Torshizi MA, Rahimi S, Dennehy JJ. Prophylactic bacteriophage administration more effective than post-infection administration in reducing Salmonella enterica serovar Enteritidis shedding in Quail. Front Microbiol 2016; 7: 1253.
51. Hazem A. Effects of temperatures, pH-values, ultra-violet light, ethanol and chloroform on the growth of isolated thermophilic Bacillus phages. New Microbiol 2002; 25: 469-476.
52. Tan CW, Rukayadi Y, Hasan H, Abdul-Mutalib NA, Jambari NN, Hara H, et al. Isolation and characterization of six Vibrio parahaemolyticus lytic bacteriophages from seafood samples. Front Microbiol 2021; 12: 616548.
53. Santos TM, Ledbetter EC, Caixeta LS, Bicalho ML, Bicalho RC. Isolation and characterization of two bacteriophages with strong in vitro antimicrobial activity against Pseudomonas aeruginosa isolated from dogs with ocular infections. Am J Vet Res 2011; 72: 1079-1086.
| Files | ||
| Issue | Vol 14 No 2 (2022) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v14i2.9189 | |
| Keywords | ||
| Phage; Antibiotic resistance; Pseudomonas aeruginosa; Clinical isolates; Bacterial infections | ||
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How to Cite
1.
Majdani R, Shams Ghahfarokhi E. Isolation and characterization of lytic bacteriophages against Pseudomonas aeruginosa isolates from human infections in the north-west of Iran. Iran J Microbiol. 2022;14(2):203-213.
