Skip to main content
Erschienen in: Archives of Virology 9/2019

14.06.2019 | Original Article

Elimination of multidrug-resistant Proteus mirabilis biofilms using bacteriophages

verfasst von: Salwa Gomaa, Fathy Serry, Hemmat Abdellatif, Hisham Abbas

Erschienen in: Archives of Virology | Ausgabe 9/2019

Einloggen, um Zugang zu erhalten

Abstract

Proteus mirabilis is responsible for a wide range of infections that affect the urinary tract, the respiratory tract, burns, wounds and the feet of individuals with diabetes. They are highly resistant to antimicrobial agents, and new therapeutic options are therefore needed to combat this pathogen. The use of bacteriophages is one option that may be useful in treating multidrug-resistant (MDR) Proteus mirabilis infections, especially biofilm-based infections. The aim of this study was to control biofilms formed by MDR Proteus mirabilis using bacteriophages. Proteus mirabilis isolates were identified based on biochemical tests, and their resistance profiles were determined by the disk diffusion method. The biofilm-forming capacity of the isolates was assessed by the spectrophotometric method. Bacteriophages attacking Proteus mirabilis were isolated from sewage. The effect of phage on biofilm formation was investigated by the viable count method. A high rate of drug resistance was found (87.2%). Strong biofilm formation was observed in 80.5% of isolates, while moderate production was found in 19.5%. Five bacteriophages were isolated from sewage and were tested for their ability to eliminate biofilms. Significant disruption of pre-formed biofilms was observed that reached up to 99.9% decrease in the number of viable cells. The use of bacteriophages is considered a promising strategy against the biofilm infections caused by MDR Proteus mirabilis isolates.
Literatur
1.
Zurück zum Zitat Abbas HA, Gad AI (2014) Eradication of biofilms formed by bacteria isolated from diabetic foot infections by potential antibiofilm agents alone and in combination with ciprofloxacin. Afr J Microbiol Res 8:3882–3892 Abbas HA, Gad AI (2014) Eradication of biofilms formed by bacteria isolated from diabetic foot infections by potential antibiofilm agents alone and in combination with ciprofloxacin. Afr J Microbiol Res 8:3882–3892
2.
Zurück zum Zitat Abbas HA, El-Saysed MA, Ganiny AM, Fattah AA (2018) Antimicrobial resistance patterns of Proteus mirabilis isolates from urinary tract, burn wound and diabetic foot infections. Res J Pharm Tech 11:249–252CrossRef Abbas HA, El-Saysed MA, Ganiny AM, Fattah AA (2018) Antimicrobial resistance patterns of Proteus mirabilis isolates from urinary tract, burn wound and diabetic foot infections. Res J Pharm Tech 11:249–252CrossRef
3.
Zurück zum Zitat Adeolu M, Alnajar S, Naushad S, Gupta RS (2016) Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 66:5575–5599CrossRefPubMed Adeolu M, Alnajar S, Naushad S, Gupta RS (2016) Genome-based phylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 66:5575–5599CrossRefPubMed
4.
Zurück zum Zitat Afriani R, Rusmana I, Budiarti S (2014) Characterization of Proteus mirabilis lytic phage from Situ Letik River Bogor Indonesia. Int J Innovat Res Sci Eng 2:2347–3207 Afriani R, Rusmana I, Budiarti S (2014) Characterization of Proteus mirabilis lytic phage from Situ Letik River Bogor Indonesia. Int J Innovat Res Sci Eng 2:2347–3207
6.
Zurück zum Zitat Azeredo J, Sutherland IW (2008) The use of phages for the removal of infectious biofilms. Curr Pharm Biotechnol 9:261–266CrossRefPubMed Azeredo J, Sutherland IW (2008) The use of phages for the removal of infectious biofilms. Curr Pharm Biotechnol 9:261–266CrossRefPubMed
7.
Zurück zum Zitat Carey-Smith GV, Billington C, Cornelius AJ, Hudson JA, Heinemann JA (2006) Isolation and characterization of bacteriophages infecting Salmonella spp. FEMS Microbiol Lett 258:182–186CrossRefPubMed Carey-Smith GV, Billington C, Cornelius AJ, Hudson JA, Heinemann JA (2006) Isolation and characterization of bacteriophages infecting Salmonella spp. FEMS Microbiol Lett 258:182–186CrossRefPubMed
8.
Zurück zum Zitat Carlton RM (1999) Phage therapy: past history and future prospects. Arch Immunol Ther Exp (Warsz) 47:267–274 Carlton RM (1999) Phage therapy: past history and future prospects. Arch Immunol Ther Exp (Warsz) 47:267–274
9.
Zurück zum Zitat Carson L, Gorman SP, Gilmore BF (2010) The use of lytic bacteriophages in the prevention and eradication of biofilms of Proteus mirabilis and Escherichia coli. FEMS Immunol Med Microbiol 59:447–455CrossRefPubMed Carson L, Gorman SP, Gilmore BF (2010) The use of lytic bacteriophages in the prevention and eradication of biofilms of Proteus mirabilis and Escherichia coli. FEMS Immunol Med Microbiol 59:447–455CrossRefPubMed
10.
Zurück zum Zitat Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A (1999) The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776PubMedPubMedCentral Ceri H, Olson ME, Stremick C, Read RR, Morck D, Buret A (1999) The Calgary Biofilm Device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 37:1771–1776PubMedPubMedCentral
11.
Zurück zum Zitat Cerveny KE, DePaola A, Duckworth DH, Gulig PA (2002) Phage therapy of local and systemic disease caused by Vibrio vulnificus in iron-dextran-treated mice. Infect Immun 70:6251–6262CrossRefPubMedPubMedCentral Cerveny KE, DePaola A, Duckworth DH, Gulig PA (2002) Phage therapy of local and systemic disease caused by Vibrio vulnificus in iron-dextran-treated mice. Infect Immun 70:6251–6262CrossRefPubMedPubMedCentral
12.
Zurück zum Zitat Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Fut Microbiol 8:769–783CrossRef Chan BK, Abedon ST, Loc-Carrillo C (2013) Phage cocktails and the future of phage therapy. Fut Microbiol 8:769–783CrossRef
13.
Zurück zum Zitat Chen C-Y, Chen Y-H, Lu P-L, Lin W-R, Chen T-C, Lin C-Y (2012) Proteus mirabilis urinary tract infection and bacteremia: risk factors, clinical presentation, and outcomes. J Microbiol Immunol Infect 45:228–236CrossRefPubMed Chen C-Y, Chen Y-H, Lu P-L, Lin W-R, Chen T-C, Lin C-Y (2012) Proteus mirabilis urinary tract infection and bacteremia: risk factors, clinical presentation, and outcomes. J Microbiol Immunol Infect 45:228–236CrossRefPubMed
14.
Zurück zum Zitat Clark JR, March JB (2006) Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol 24:212–218CrossRefPubMed Clark JR, March JB (2006) Bacteriophages and biotechnology: vaccines, gene therapy and antibacterials. Trends Biotechnol 24:212–218CrossRefPubMed
15.
Zurück zum Zitat CLSI-Clinical and Laboratory Standards Institute (2016) Performance standards for antimicrobial susceptibility testing, CLSI document M100-S-26. CLSI-Clinical and Laboratory Standards Institute, Wayne CLSI-Clinical and Laboratory Standards Institute (2016) Performance standards for antimicrobial susceptibility testing, CLSI document M100-S-26. CLSI-Clinical and Laboratory Standards Institute, Wayne
16.
Zurück zum Zitat Coker C, Poore CA, Li X, Mobley HL (2000) Pathogenesis of Proteus mirabilis urinary tract infection. Microb Infect 2:1497–1505CrossRef Coker C, Poore CA, Li X, Mobley HL (2000) Pathogenesis of Proteus mirabilis urinary tract infection. Microb Infect 2:1497–1505CrossRef
17.
Zurück zum Zitat Cornelissen A, Ceyssens P-J, T’syen J, Van Praet H, Noben J-P, Shaburova OV, Krylov VN, Volckaert G, Lavigne R (2011) The T7-related Pseudomonas putida phage φ15 displays virionassociated biofilm degradation properties. PLoS One 6:e18597CrossRefPubMedPubMedCentral Cornelissen A, Ceyssens P-J, T’syen J, Van Praet H, Noben J-P, Shaburova OV, Krylov VN, Volckaert G, Lavigne R (2011) The T7-related Pseudomonas putida phage φ15 displays virionassociated biofilm degradation properties. PLoS One 6:e18597CrossRefPubMedPubMedCentral
18.
Zurück zum Zitat Danis-Wlodarczyk K, Olszak T, Arabski M, Wasik S, Majkowska-Skrobek G, Augustyniak D, Gula G, Briers Y, Jang HB, Vandenheuvel D, Duda KA, Lavigne R, Drulis-Kawa Z (2015) Characterization of the newly isolated lytic bacteriophages KTN6 and KT28 and their efficacy against Pseudomonas aeruginosa biofilm. PLoS One 10:e0127603CrossRefPubMedPubMedCentral Danis-Wlodarczyk K, Olszak T, Arabski M, Wasik S, Majkowska-Skrobek G, Augustyniak D, Gula G, Briers Y, Jang HB, Vandenheuvel D, Duda KA, Lavigne R, Drulis-Kawa Z (2015) Characterization of the newly isolated lytic bacteriophages KTN6 and KT28 and their efficacy against Pseudomonas aeruginosa biofilm. PLoS One 10:e0127603CrossRefPubMedPubMedCentral
19.
Zurück zum Zitat Endimiani A, Luzzaro F, Brigante G, Perilli M, Lombardi G, Amicosante G, Rossolini GM, Toniolo A (2005) Proteus mirabilis bloodstream infections: risk factors and treatment outcome related to the expression of extended-spectrum beta-lactamases. Antimicrob Agents Chemother 49:2598–2605CrossRefPubMedPubMedCentral Endimiani A, Luzzaro F, Brigante G, Perilli M, Lombardi G, Amicosante G, Rossolini GM, Toniolo A (2005) Proteus mirabilis bloodstream infections: risk factors and treatment outcome related to the expression of extended-spectrum beta-lactamases. Antimicrob Agents Chemother 49:2598–2605CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Fard RMN, Barton MD, Heuzenroeder MW (2010) Novel Bacteriophages in Enterococcus spp. Curr Microbiol 60:400–406CrossRef Fard RMN, Barton MD, Heuzenroeder MW (2010) Novel Bacteriophages in Enterococcus spp. Curr Microbiol 60:400–406CrossRef
21.
Zurück zum Zitat Ghannad MS, Mohammadi A (2012) Bacteriophage: time to re-evaluate the potential of phage therapy as a promising agent to control multidrug-resistant bacteria. Iran J Basic Med Sci 15:693–701 Ghannad MS, Mohammadi A (2012) Bacteriophage: time to re-evaluate the potential of phage therapy as a promising agent to control multidrug-resistant bacteria. Iran J Basic Med Sci 15:693–701
22.
23.
Zurück zum Zitat Gurnev PA, Oppenheim AB, Winterhalter M, Bezrukov SM (2006) Docking of a single phage lambda to its membrane receptor maltoporin as a time-resolved event. J Mol Biol 359:1447–1455CrossRefPubMed Gurnev PA, Oppenheim AB, Winterhalter M, Bezrukov SM (2006) Docking of a single phage lambda to its membrane receptor maltoporin as a time-resolved event. J Mol Biol 359:1447–1455CrossRefPubMed
24.
Zurück zum Zitat Gutiérrez D, Vandenheuvel D, Martínez B, Rodríguez A, Lavigne R, García P (2015) Two phages, phiIPLA-RODI and phiIPLA-C1C, lyse mono-and dual-species Staphylococcal biofilms. Appl Environ Microbiol 81:3336–3348CrossRefPubMedPubMedCentral Gutiérrez D, Vandenheuvel D, Martínez B, Rodríguez A, Lavigne R, García P (2015) Two phages, phiIPLA-RODI and phiIPLA-C1C, lyse mono-and dual-species Staphylococcal biofilms. Appl Environ Microbiol 81:3336–3348CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108CrossRefPubMed Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108CrossRefPubMed
26.
Zurück zum Zitat Hall-Stoodley L, Stoodley P (2009) Evolving concepts in biofilm infections. Cell Microbiol 11:1034–1043CrossRefPubMed Hall-Stoodley L, Stoodley P (2009) Evolving concepts in biofilm infections. Cell Microbiol 11:1034–1043CrossRefPubMed
27.
Zurück zum Zitat Harper D, Enright M (2011) Bacteriophages for the treatment of Pseudomonas aeruginosa infections. J Appl Microbiol 111:1–7CrossRefPubMed Harper D, Enright M (2011) Bacteriophages for the treatment of Pseudomonas aeruginosa infections. J Appl Microbiol 111:1–7CrossRefPubMed
28.
Zurück zum Zitat Harrison JJ, Turner RJ, Joo DA, Stan MA, Chan CS, Allan ND, Vrionis HA, Olson ME, Ceri H (2008) Copper and quaternary ammonium cations exert synergistic bactericidal and anti-biofilm activity against Pseudomonas aeruginosa. Antimicrob Agents Chemother 52:2870–2881CrossRefPubMedPubMedCentral Harrison JJ, Turner RJ, Joo DA, Stan MA, Chan CS, Allan ND, Vrionis HA, Olson ME, Ceri H (2008) Copper and quaternary ammonium cations exert synergistic bactericidal and anti-biofilm activity against Pseudomonas aeruginosa. Antimicrob Agents Chemother 52:2870–2881CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Ho K (2001) Bacteriophage therapy for bacterial infections. Rekindling a memory from the pre-antibiotics era. Perspect Biol Med 44:1–16CrossRefPubMed Ho K (2001) Bacteriophage therapy for bacterial infections. Rekindling a memory from the pre-antibiotics era. Perspect Biol Med 44:1–16CrossRefPubMed
30.
Zurück zum Zitat Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332CrossRefPubMed Hoiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332CrossRefPubMed
31.
Zurück zum Zitat Jacobsen SM, Shirtliff ME (2011) Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence 2:460–465CrossRefPubMed Jacobsen SM, Shirtliff ME (2011) Proteus mirabilis biofilms and catheter-associated urinary tract infections. Virulence 2:460–465CrossRefPubMed
32.
Zurück zum Zitat Jun JW, Kim JH, Shin SP, Han JE, Chai JY, Park SC (2013) Characterization and complete genome sequence of the Shigella bacteriophage pSf-1. Res Microbiol 164:979–986CrossRefPubMed Jun JW, Kim JH, Shin SP, Han JE, Chai JY, Park SC (2013) Characterization and complete genome sequence of the Shigella bacteriophage pSf-1. Res Microbiol 164:979–986CrossRefPubMed
33.
Zurück zum Zitat Karaca B, Akcelik N, Akcelik M (2015) Effects of P22 bacteriophage on Salmonella enterica subsp. enterica serovar Typhimurium DMC4 strain biofilm formation and eradication. Arch Biol Sci 67:1361–1367CrossRef Karaca B, Akcelik N, Akcelik M (2015) Effects of P22 bacteriophage on Salmonella enterica subsp. enterica serovar Typhimurium DMC4 strain biofilm formation and eradication. Arch Biol Sci 67:1361–1367CrossRef
34.
Zurück zum Zitat Karumidze N, Kusradze I, Rigvava S, Goderdzishvili M, Rajakumar K, Alavidze Z (2013) Isolation and characterisation of lytic bacteriophages of Klebsiella pneumoniae and Klebsiella oxytoca. Curr Microbiol 66:251–258CrossRefPubMed Karumidze N, Kusradze I, Rigvava S, Goderdzishvili M, Rajakumar K, Alavidze Z (2013) Isolation and characterisation of lytic bacteriophages of Klebsiella pneumoniae and Klebsiella oxytoca. Curr Microbiol 66:251–258CrossRefPubMed
35.
Zurück zum Zitat Koneman E, Winn WC, Allen S, Janda W, Procop G, Schreckenberger P, Woods G (2006) Koneman’s color atlas and textbook of diagnostic microbiology, 6th edn. Lippincott Williams & Wilkins, Pennsylvania Koneman E, Winn WC, Allen S, Janda W, Procop G, Schreckenberger P, Woods G (2006) Koneman’s color atlas and textbook of diagnostic microbiology, 6th edn. Lippincott Williams & Wilkins, Pennsylvania
37.
Zurück zum Zitat Krylov VN (2001) Phagotherapy in terms of bacteriophage genetics: hopes, perspectives, safety, limitations. Genetika 37:869–887PubMed Krylov VN (2001) Phagotherapy in terms of bacteriophage genetics: hopes, perspectives, safety, limitations. Genetika 37:869–887PubMed
38.
Zurück zum Zitat Kutateladze M, Adamia R (2010) Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28:591–595CrossRefPubMed Kutateladze M, Adamia R (2010) Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends Biotechnol 28:591–595CrossRefPubMed
39.
Zurück zum Zitat Kutter E, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, Abedon ST (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11:69–86CrossRefPubMed Kutter E, De Vos D, Gvasalia G, Alavidze Z, Gogokhia L, Kuhl S, Abedon ST (2010) Phage therapy in clinical practice: treatment of human infections. Curr Pharm Biotechnol 11:69–86CrossRefPubMed
40.
Zurück zum Zitat Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327CrossRefPubMed Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327CrossRefPubMed
41.
Zurück zum Zitat Lehman SM, Donlan RM (2015) Bacteriophage-mediated control of a two-species biofilm formed by microorganisms causing catheter-associated urinary tract infections in an in vitro urinary catheter model. Antimicrob Agents Chemother 59:1127–1137CrossRefPubMedPubMedCentral Lehman SM, Donlan RM (2015) Bacteriophage-mediated control of a two-species biofilm formed by microorganisms causing catheter-associated urinary tract infections in an in vitro urinary catheter model. Antimicrob Agents Chemother 59:1127–1137CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Liu M, Deora R, Doulatov SR, Gingery M, Eiserling FA, Preston A, Maskell DJ, Simons RW, Cotter PA, Parkhill J, Miller JF (2002) Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295:2091–2094CrossRefPubMed Liu M, Deora R, Doulatov SR, Gingery M, Eiserling FA, Preston A, Maskell DJ, Simons RW, Cotter PA, Parkhill J, Miller JF (2002) Reverse transcriptase-mediated tropism switching in Bordetella bacteriophage. Science 295:2091–2094CrossRefPubMed
46.
Zurück zum Zitat Lynch AS, Robertson GT (2008) Bacterial and fungal biofilm infections. Annu Rev Med 59:415–428CrossRefPubMed Lynch AS, Robertson GT (2008) Bacterial and fungal biofilm infections. Annu Rev Med 59:415–428CrossRefPubMed
47.
Zurück zum Zitat Melo LD, Veiga P, Cerca N, Kropinski AM, Almeida C, Azeredo J, Sillankorva S (2016) Development of a phage cocktail to control Proteus mirabilis catheter-associated urinary tract infections. Front Microbiol 7:1024–1035CrossRefPubMedPubMedCentral Melo LD, Veiga P, Cerca N, Kropinski AM, Almeida C, Azeredo J, Sillankorva S (2016) Development of a phage cocktail to control Proteus mirabilis catheter-associated urinary tract infections. Front Microbiol 7:1024–1035CrossRefPubMedPubMedCentral
49.
Zurück zum Zitat Morozova V, Kozlova Y, Shedko E, Kurilshikov A, Babkin I, Tupikin A, Yunusova A, Chernonosov A, Baykov I, Capital Kabul CI, Kabilov M, Ryabchikova E, Vlassov V, Tikunova N (2016) Lytic bacteriophage PM16 specific for Proteus mirabilis: a novel member of the genus Phikmvvirus. Arch Virol 161:2457–2472CrossRefPubMed Morozova V, Kozlova Y, Shedko E, Kurilshikov A, Babkin I, Tupikin A, Yunusova A, Chernonosov A, Baykov I, Capital Kabul CI, Kabilov M, Ryabchikova E, Vlassov V, Tikunova N (2016) Lytic bacteriophage PM16 specific for Proteus mirabilis: a novel member of the genus Phikmvvirus. Arch Virol 161:2457–2472CrossRefPubMed
50.
Zurück zum Zitat Morozova V, Kozlova Y, Shedko E, Babkin I, Kurilshikov A, Bokovaya O, Bardashova A, Yunusova A, Tikunov A, Tupikin A, Ushakova T, Ryabchikova E, Tikunova N (2018) Isolation and characterization of a group of new Proteus bacteriophages. Arch Virol 163:2189–2197CrossRefPubMed Morozova V, Kozlova Y, Shedko E, Babkin I, Kurilshikov A, Bokovaya O, Bardashova A, Yunusova A, Tikunov A, Tupikin A, Ushakova T, Ryabchikova E, Tikunova N (2018) Isolation and characterization of a group of new Proteus bacteriophages. Arch Virol 163:2189–2197CrossRefPubMed
51.
Zurück zum Zitat Nzakizwanayo J, Hanin A, Alves DR, McCutcheon B, Dedi C, Salvage J, Knox K, Stewart B, Metcalfe A, Clark J (2015) Bacteriophage can prevent encrustation and blockage of urinary catheters by Proteus mirabilis. Antimicrob Agents Chemother 60:1530–1536CrossRefPubMed Nzakizwanayo J, Hanin A, Alves DR, McCutcheon B, Dedi C, Salvage J, Knox K, Stewart B, Metcalfe A, Clark J (2015) Bacteriophage can prevent encrustation and blockage of urinary catheters by Proteus mirabilis. Antimicrob Agents Chemother 60:1530–1536CrossRefPubMed
52.
Zurück zum Zitat Parasion S, Kwiatek M, Gryko R, Mizak L, Malm A (2014) Bacteriophages as an alternative strategy for fighting biofilm development. Pol J Microbiol 63:137–145PubMed Parasion S, Kwiatek M, Gryko R, Mizak L, Malm A (2014) Bacteriophages as an alternative strategy for fighting biofilm development. Pol J Microbiol 63:137–145PubMed
53.
Zurück zum Zitat Perim MC, Borges Jda C, Celeste SR, Orsolin Ede F, Mendes RR, Mendes GO, Ferreira RL, Carreiro SC, Pranchevicius MC (2015) Aerobic bacterial profile and antibiotic resistance in patients with diabetic foot infections. Rev Soc Br Med Trop 48:546–554CrossRef Perim MC, Borges Jda C, Celeste SR, Orsolin Ede F, Mendes RR, Mendes GO, Ferreira RL, Carreiro SC, Pranchevicius MC (2015) Aerobic bacterial profile and antibiotic resistance in patients with diabetic foot infections. Rev Soc Br Med Trop 48:546–554CrossRef
55.
Zurück zum Zitat Różalski A, Sidorczyk Z, Kotelko K (1997) Potential virulence factors of Proteus bacilli. Microbiol Mol Biol Rev 61:65–89PubMedPubMedCentral Różalski A, Sidorczyk Z, Kotelko K (1997) Potential virulence factors of Proteus bacilli. Microbiol Mol Biol Rev 61:65–89PubMedPubMedCentral
57.
Zurück zum Zitat Sekhar S, Vyas N, Unnikrishnan M, Rodrigues G, Mukhopadhyay C (2014) Antimicrobial susceptibility pattern in diabetic foot ulcer: a pilot study. Ann Med Health Sci Res 4:742–745CrossRefPubMedPubMedCentral Sekhar S, Vyas N, Unnikrishnan M, Rodrigues G, Mukhopadhyay C (2014) Antimicrobial susceptibility pattern in diabetic foot ulcer: a pilot study. Ann Med Health Sci Res 4:742–745CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat Shanmugam P, Jeya M, Susan SL (2013) The bacteriology of diabetic foot ulcers, with a special reference to multidrug resistant strains. J Clin Diagn Res 7:441–445PubMedPubMedCentral Shanmugam P, Jeya M, Susan SL (2013) The bacteriology of diabetic foot ulcers, with a special reference to multidrug resistant strains. J Clin Diagn Res 7:441–445PubMedPubMedCentral
59.
Zurück zum Zitat Shapiro OH, Kushmaro A (2011) Bacteriophage ecology in environmental biotechnology processes. Curr Opin Biotechnol 22:449–455CrossRefPubMed Shapiro OH, Kushmaro A (2011) Bacteriophage ecology in environmental biotechnology processes. Curr Opin Biotechnol 22:449–455CrossRefPubMed
60.
61.
Zurück zum Zitat Stepanović S, Vuković D, Hola V, Bonaventura GD, Djukić S, Ćirković I, Ruzicka F (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Acta Pathol Microbiol Immunol Scand B Microbiol 115:891–899CrossRef Stepanović S, Vuković D, Hola V, Bonaventura GD, Djukić S, Ćirković I, Ruzicka F (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. Acta Pathol Microbiol Immunol Scand B Microbiol 115:891–899CrossRef
62.
Zurück zum Zitat Stewart PS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292:107–113CrossRefPubMed Stewart PS (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292:107–113CrossRefPubMed
63.
Zurück zum Zitat Stickler DJ (2014) Clinical complications of urinary catheters caused by crystalline biofilms: something needs to be done. J Intern Med 276:120–129CrossRefPubMed Stickler DJ (2014) Clinical complications of urinary catheters caused by crystalline biofilms: something needs to be done. J Intern Med 276:120–129CrossRefPubMed
64.
Zurück zum Zitat Sutherland IW, Hughes KA, Skillman LC, Tait K (2004) The interaction of phage and biofilms. FEMS Microbiol Lett 232:1–6CrossRefPubMed Sutherland IW, Hughes KA, Skillman LC, Tait K (2004) The interaction of phage and biofilms. FEMS Microbiol Lett 232:1–6CrossRefPubMed
65.
Zurück zum Zitat Thompson R (2018) The isolation and characterisation of Proteus mirabilis bacteriophages and their effect on the colonisation and blockage of urinary catheters. (PhD thesis), Faculty of Health and Applied Sciences, University of the West of England, Bristol Thompson R (2018) The isolation and characterisation of Proteus mirabilis bacteriophages and their effect on the colonisation and blockage of urinary catheters. (PhD thesis), Faculty of Health and Applied Sciences, University of the West of England, Bristol
66.
Zurück zum Zitat Trachoo N (2004) Biofilm removal technique using sands as a research tool for accessing microbial attachment on surface. Songklanakarin J Sci Technol 26:109–115 Trachoo N (2004) Biofilm removal technique using sands as a research tool for accessing microbial attachment on surface. Songklanakarin J Sci Technol 26:109–115
67.
Zurück zum Zitat Yah S, Enabulele I, Yusuf E, Eghafona N (2006) Emerging quinolones resistant transfer genes among gram-negative bacteria isolated from faeces of HIV/AIDS patient attending some clinic and hospital in the city of Benin, Edo State, Nigeria. Online J Health Allied Sci 5:61–91 Yah S, Enabulele I, Yusuf E, Eghafona N (2006) Emerging quinolones resistant transfer genes among gram-negative bacteria isolated from faeces of HIV/AIDS patient attending some clinic and hospital in the city of Benin, Edo State, Nigeria. Online J Health Allied Sci 5:61–91
68.
Zurück zum Zitat Yazdi M, Bouzari M, Ghaemi EA (2018) Isolation and characterization of a lytic bacteriophage (vB_PmiS-TH) and its application in combination with ampicillin against planktonic and biofilm forms of Proteus mirabilis isolated from urinary tract infection. J Mol Microbiol Biotechnol 28:37–46CrossRefPubMed Yazdi M, Bouzari M, Ghaemi EA (2018) Isolation and characterization of a lytic bacteriophage (vB_PmiS-TH) and its application in combination with ampicillin against planktonic and biofilm forms of Proteus mirabilis isolated from urinary tract infection. J Mol Microbiol Biotechnol 28:37–46CrossRefPubMed
Metadaten
Titel
Elimination of multidrug-resistant Proteus mirabilis biofilms using bacteriophages
verfasst von
Salwa Gomaa
Fathy Serry
Hemmat Abdellatif
Hisham Abbas
Publikationsdatum
14.06.2019
Verlag
Springer Vienna
Erschienen in
Archives of Virology / Ausgabe 9/2019
Print ISSN: 0304-8608
Elektronische ISSN: 1432-8798
DOI
https://doi.org/10.1007/s00705-019-04305-x

Weitere Artikel der Ausgabe 9/2019

Archives of Virology 9/2019 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.