In vitro efficacy of bismuth thiols against biofilms formed by bacteria isolated from human chronic wounds

Journal of Applied Microbiology

Volumn 111, Issue 4, 2011, Pages 989-996

  Folsom, J P ^a   Baker, B ^b   Stewart, P S ^a  

^a MONTANA STATE UNIVERSITY   (United States)

^b Microbion Corporation   (United States)

Author keywords

Antibiotic; Antimicrobial; Biofilm; Bismuth; Chronic wound; MRSA

Indexed keywords

ANTIMICROBIAL AGENTS; BACTERIA; BIOFILMS; BISMUTH;

ANTIMICROBIAL; BACTERICIDAL ACTIVITY; BIOFILM MODELS; CHRONIC WOUNDS; IN-VITRO; LOG REDUCTIONS; MICRO-ORGANISMS; MRSA; PSEUDOMONAS AERUGINOSA; SINGLE SPECIES;

ANTIBIOTICS;

AMIKACIN; AMPICILLIN; BISMUTH DERIVATIVE; BISMUTH THIOL; CEFEPIME; CIPROFLOXACIN; DAPTOMYCIN; IMIPENEM; RIFAMPICIN; SULFADIAZINE SILVER; TOBRAMYCIN; UNCLASSIFIED DRUG; VANCOMYCIN;

ANTIBIOTICS; ANTIMICROBIAL ACTIVITY; BACTERIUM; BIOFILM; BIOREACTOR; BISMUTH; COLONY; THIOL;

ANTIBIOTIC SENSITIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BACTERIAL GROWTH; BACTERICIDAL ACTIVITY; BACTERIUM COLONY; BACTERIUM ISOLATION; BIOFILM; CHRONIC WOUND; COLONY FORMATION; DRUG EFFICACY; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; NONHUMAN; PSEUDOMONAS AERUGINOSA;

BACTERIA (MICROORGANISMS); METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; PSEUDOMONAS AERUGINOSA;

EID: 80052810743     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2011.05110.x     Document Type: Article

References (42)

1. Akiyama, H., Yamasaki, O., Kanzaki, H., Tada, J. and Arata, J. (1998) Effects of sucrose and silver on Staphylococcus aureus biofilms. J Antimicrob Chemother 42, 629-634.
2. Alipour, M., Suntres, Z.E., Lafrenie, R.M. and Omri, A. (2010) Attenuation of Pseudomonas aeruginosa virulence factors and biofilms by co-encapsulation of bismuth-ethanedithiol with tobramycin in liposomes. J Antimicrob Chemother 65, 684-693.
3. Anderl, J.N., Franklin, M.J. and Stewart, P.S. (2000) Role of antibiotic penetration limitation in Klebsiella pneumoniae biofilm resistance to ampicillin and ciprofloxacin. Antimicrob Agents Chemother 44, 1818-1824.
4. Badireddy, A.R., Chellam, S., Yanina, S., Gassman, P. and Rosso, K.M. (2008a) Bismuth dimercaptopropanol (BisBAL) inhibits the expression of extracellular polysaccharides and proteins by Brevundimonas diminuta: implications for membrane microfiltration. Biotechnol Bioeng 99, 634-643.
5. Badireddy, A.R., Korpol, B.R., Chellam, S., Gassman, P.L., Engelhard, M.H., Lea, A.S. and Rosso, K.M. (2008b) Spectroscopic characterization of extracellular polymeric substances from Escherichia coli and Serratia marcescens: suppression using sub-inhibitory concentrations of bismuth thiols. Biomacromolecules 9, 3079-3089.
6. Bickers, D.R., Lim, H.W., Margolis, D., Weinstock, M.A., Goodman, C., Faulkner, E., Gould, C., Gemmen, E. et al. (2004) The burden of skin diseases: 2004: a joint project of the American Academy of Dermatology Association and the Society for Investigative Dermatology. J Am Acad Dermatol 55, 490-500.
7. Bjarnsholt, T., Kirketerp-Møller, K., Kristiansen, S., Phipps, R., Nielsen, A.K., Jensen, P.Ø., Høiby, N. and Givskov, M. (2007) Silver against Pseudomonas aeruginosa biofilms. APMIS 115, 921-928.
8. Bjarnsholt, T., Kirketerp-Moller, K., Jensen, P.O., Madsen, K.G., Phipps, R., Krogfelt, K., Hoiby, N. and Givskov, M. (2008) Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen 16, 2-10.
9. Buckingham-Meyer, K., Goeres, D.M. and Hamilton, M. (2007) Comparative evaluation of biofilm disinfectant efficacy tests. J Microbiol Methods 70, 236-244.
10. Codony, F., Domenico, P. and Mas, J. (2003) Assessment of bismuth thiols and conventional disinfectants on drinking water biofilms. J Appl Microbiol 95, 288-293.
11. Costerton, J.W., Stewart, P.S. and Greenberg, E.P. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322.
12. Davis, S.C., Ricotti, C., Cazzaniga, A., Welsh, E., Eaglstein, W.H. and Mertz, P.M. (2008) Microscopic and physiologic evidence for biofilm-associated wound colonization in vivo. Wound Repair Regen 16, 23-29.
13. Domenico, P., Salo, R.J., Novick, S.G., Schoch, P.E., Van Horn, K. and Cunha, B.A. (1997) Enhancement of bismuth antibacterial activity with lipophilic thiol chelators. Antimicrob Agents Chemother 41, 1697-1703.
14. Domenico, P., Tomas, J.M., Merino, S., Rubires, X. and Cunha, B.A. (1999) Surface antigen exposure by bismuth dimercaprol suppression of Klebsiella pneumoniae capsular polysaccharide. Infect Immun 67, 664-669.
15. Domenico, P., Baldassarri, L., Schoch, P.E., Kaehler, K., Sasatsu, M. and Cunha, B.A. (2001) Activities of Bismuth Thiols against Staphylococci and Staphylococcal Biofilms. Antimicrob Agents Chemother 45, 1417-1421.
16. Dowd, S.E., Sun, Y., Secor, P.R., Rhoads, D.D., Wolcott, B.M., James, G.A. and Wolcott, R.D. (2008) Survey of bacterial diversity in chronic wounds using pyrosequencing, DGGE, and full ribosome shotgun sequencing. BMC Microbiol 8, 43.
17. Fazli, M., Bjarnsholt, T., Kirketerp-Møller, K., Jørgensen, B., Andersen, A.S., A., K.K., Givskov, M. and Tolker-Nielsen, T. (2009) Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 47, 4084-4089.
18. Frank, D.N., Wysocki, A., Specht-Glick, D.D., Rooney, A., Feldman, R.A., St Amand, A.L., Pace, N.R. and Trent, J.D. (2009) Microbial diversity in chronic open wounds. Wound Repair Regen 17, 163-172.
19. Goeres, D.M., Hamilton, M.A., Beck, N.A., Buckingham-Meyer, K., Hilyard, J.D., Loetterle, L.R., Lorenz, L.A., Walker, D.K. et al. (2009) A method for growing a biofilm under low shear at the air-liquid interface using the drip flow biofilm reactor. Nat Protoc 4, 783-788.
20. Herigstad, B., Hamilton, M. and Heersink, J. (2001) How to optimize the drop plate method for enumerating bacteria. J Microbiol Methods 44, 121-129.
21. Hill, K.E., Malic, S., McKee, R., Rennison, T., Harding, K.G., Williams, D.W. and Thomas, D.W. (2010) An in vitro model of chronic wound biofilms to test wound dressings and assess antimicrobial susceptibilities. J Antimicrob Chemother 65, 1195-1206.
22. Hinchliffe, R.J., Valk, V.D., Apelqvist, J., Armstrong, D.G., Bakker, K., Game, F.L., Hartemann-Heurtier, A., Löndahl, M. et al. (2008) A systematic review of the effectiveness of interventions to enhance the healing of chronic ulcers of the foot in diabetes. Diabetes Metab Res Rev 24(Suppl 1), S119-S144.
23. Hoben, H.J. and Somasegaran, P. (1982) Comparison of the pour, spread, and drop plate methods for enumeration of Rhizobium spp. in inoculants made from presterilized peat. Appl Environ Microbiol 44, 1246-1247.
24. Huang, C.-T. and Stewart, P.S. (1999) Reduction of polysaccharide production in Pseudomonas aeruginosa biofilms by bismuth dimercaprol (BisBAL) treatment. J Antimicrob Chemother 44, 601-605.
25. James, G.A., Swogger, E., Wolcott, R., Pulcini, E.D., Secor, P., Sestrich, J., Costerton, J.W. and Stewart, P.S. (2008) Biofilms in chronic wounds. Wound Repair Regen 16, 37-44.
26. Kirketerp-Møller, K., Jensen, P.Ø., Fazli, M., Madsen, K.G., Pedersen, J., Moser, C., Tolker-Nielsen, T., Høiby, N. et al. (2008) Distribution, organization, and ecology of bacteria in chronic wounds. J Clin Microbiol 46, 2717-2722.
27. Körber, A., Schmid, E.N., Buer, J., Klode, J., Schadendorf, D. and Dissemond, J. (2010) Bacterial colonization of chronic leg ulcers: current results compared with data 5years ago in a specialized dermatology department. J Eur Acad Dermatol Venereol 24, 1017-1025.
28. Kuehn, B.M. (2007) Chronic wound care guidelines issued. JAMA (J Am Med Assoc) 297, 938-939.
29. Lipsky, B.A. and Hoey, C. (2009) Topical antimicrobial therapy for treating chronic wounds. Clin Infect Dis 49, 1541-1549.
30. Malic, S., Hill, K.E., Hayes, A., Percival, S.L., Thomas, D.W. and Williams, D.W. (2009) Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA FISH). Microbiology 155, 2603-2611.
31. Melendez, J.H., Frankel, Y.M., An, A.T., Williams, L., Price, L.B., Wang, N.Y., Lazarus, G.S. and Zenilman, J.M. (2010) Real-time PCR assays compared to culture-based approaches for identification of aerobic bacteria in chronic wounds. Clin Microbiol Infect 16, 1762-1769.
32. O'Meara, S.M., Al-Kurdi, D., Ologun, Y. and Ovington, L.G. (2010) Antibiotics and antiseptics for venous leg ulcers. Cochrane Database of Systematic Reviews 2010 Issue 1. Art. no.: CD003557. doi.
33. Percival, S.L., Bowler, P. and Woods, E.J. (2008) Assessing the effect of an antimicrobial wound dressing on biofilms. Wound Repair Regen 16, 52-57.
34. Singer, A.J. and Clark, R.A.F. (1999) Cutaneous wound healing. N Eng J Med 341, 738-746.
35. Stewart, P.S. and Costerton, W.J. (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358, 135-138.
36. Sun, Y., Dowd, S.E., Smith, E., Rhoads, D.D. and Wolcott, R.D. (2008) In vitro multispecies Lubbock chronic wound biofilm model. Wound Repair Regen 16, 805-813.
37. Thomsen, T.R., Aasholm, M.S., Rudkjøbing, V.B., Saunders, A.M., Bjarnsholt, T., Givskov, M., Kirketerp-Møller, K. and Nielsen, P.H. (2010) The bacteriology of chronic venous leg ulcer examined by culture-independent molecular methods. Wound Repair Regen 18, 38-49.
38. Veloira, W.G., Domenico, P., LiPuma, J.J., Davis, J.M., Gurzenda, E. and Kazzaz, J.A. (2003) In vitro activity and synergy of bismuth thiols and tobramycin against Burkholderia cepacia complex. J Antimicrob Chemother 52, 915-919.
39. White, R.J., Cutting, K. and Kingsley, A. (2006) Topical antimicrobials in the control of wound bioburden. Ostomy Wound Manage 52, 26-58.
40. Wu, C.-L., Domenico, P., Hassett, D.J., Beveridge, T.J., Hauser, A.R. and Kazzaz, J.A. (2002) Subinhibitory bismuth-thiols reduce virulence of Pseudomonas aeruginosa. Am J Respir Cell Mol Biol 26, 731-738.
41. Xu, K.D., Stewart, P.S., Xia, F., Huang, C.-T. and McFeters, G.A. (1998) Spatial physiological heterogeneity in Pseudomonas aeruginosa biofilm is determined by oxygen availability. Appl Environ Microbiol 64, 4035-4039.
42. Zhang, H., Tang, J., Meng, X., Tsang, J. and Tsang, T.-K. (2005) Inhibition of bacterial adherence on the surface of stents and bacterial growth in bile by bismuth dimercaprol. Dig Dis Sci 50, 1046-1051.