Strategies for combating bacterial biofilm infections

Hong Wu, Claus Moser, Heng-Zhuang Wang, Niels Høiby, Zhi-Jun Song

International Journal of Oral Science ›› 2014, Vol. 6 ›› Issue (1) : 1-7.

International Journal of Oral Science All Journals
International Journal of Oral Science ›› 2014, Vol. 6 ›› Issue (1) : 1-7. DOI: 10.1038/ijos.2014.65
Article

Strategies for combating bacterial biofilm infections

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Abstract

Antibiotics alone are often ineffective in the treatment of bacterial biofilm infections and new strategies are needed. Once bacteria shift from their free-swimming state to the structured community of a biofilm, they become much harder to kill with conventional antibiotic regimens. A review by Zhi-Jun Song and colleagues at Denmark’s University Hospital of Copenhagen explores the challenges of diagnosing and eliminating biofilms that form on the surface of implanted medical devices. At present, the best solution is early detection followed by aggressive treatment with multiple antibiotics and removal of the device in question. However, recent research suggests other possible solutions, including drugs that interfere with communication between bacteria or disrupt their ability to anchor to surfaces, and viruses that specifically infect and kill biofilm-forming microbes.

Keywords

antibiotic resistance / antimicrobial treatments / bacterial biofilm / chronic infection

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Hong Wu, Claus Moser, Heng-Zhuang Wang, Niels Høiby, Zhi-Jun Song. Strategies for combating bacterial biofilm infections. International Journal of Oral Science, 2014, 6(1): 1‒7 https://doi.org/10.1038/ijos.2014.65

References

[1]
de Fuente-Núñez C, Reffuveille F, Fernandez L. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol, 2013, 16(5): 580-589.
CrossRef Google scholar
[2]
Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol, 2004, 2(2): 95-108.
CrossRef Google scholar
[3]
Yang L, Liu Y, Wu H. Combating biofilms. FEMS Immunol Med Microbiol, 2012, 65(2): 146-157.
CrossRef Google scholar
[4]
Høiby N, Ciofu O, Johansen HK. The clinical impact of bacterial biofilms. Int J Oral Sci, 2011, 3(2): 55-65.
CrossRef Google scholar
[5]
Hengzhuang W, Wu H, Ciofu O. Pharmacokinetics/pharmacodynamics of colistin and imipenem on mucoid and nonmucoid Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother, 2011, 55(9): 4469-4474.
CrossRef Google scholar
[6]
Hengzhuang W, Wu H, Ciofu O. In vivo pharmacokinetics/pharmacodynamics of colistin and imipenem in Pseudomonas aeruginosa biofilm infection. Antimicrob Agents Chemother, 2012, 56(5): 2683-2690.
CrossRef Google scholar
[7]
Høiby N, Bjarnsholt T, Givskov M. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents, 2010, 35(4): 322-332.
CrossRef Google scholar
[8]
Høiby N. Recent advances in the treatment of Pseudomonas aeruginosa infections in cystic fibrosis. BMC Med, 2011, 9: 32.
CrossRef Google scholar
[9]
Tran PL, Lowry N, Campbell T. An organoselenium compound inhibits Staphylococcus aureus biofilms on hemodialysis catheters in vivo. Antimicrob Agents Chemother, 2012, 56(2): 972-978.
CrossRef Google scholar
[10]
Tollefson DF, Bandyk DF, Kaebnick HW. Surface biofilm disruption. Enhanced recovery of microorganisms from vascular prostheses. Arch Surg, 1987, 122(1): 38-43.
CrossRef Google scholar
[11]
Fux CA, Quigley M, Worel AM. Biofilm-related infections of cerebrospinal fluid shunts. Clin Microbiol Infect, 2006, 12(4): 331-337.
CrossRef Google scholar
[12]
Donlan RM. Biofilms and device-associated infections. Emerg Infect Dis, 2001, 7(2): 277-281.
CrossRef Google scholar
[13]
Song Z, Borgwardt L, Høiby N. Prosthesis infections after orthopedic joint replacement: the possible role of bacterial biofilms. Orthop Rev (Pavia), 2013, 5(2): 65-71.
CrossRef Google scholar
[14]
Santos AP, Watanabe E, Andrade D. Biofilm on artificial pacemaker: fiction or reality. Arq Bras Cardiol, 2011, 97(5): e113-e120.
CrossRef Google scholar
[15]
Dasgupta MK. Biofilms and infection in dialysis patients. Semin Dial, 2002, 15(5): 338-346.
CrossRef Google scholar
[16]
Auler ME, Morreira D, Rodrigues FF. Biofilm formation on intrauterine devices in patients with recurrent vulvovaginal candidiasis. Med Mycol, 2010, 48(1): 211-216.
CrossRef Google scholar
[17]
Donelli G, Vuotto C, Cardines R. Biofilm-growing intestinal anaerobic bacteria. FEMS Immunol Med Microbiol, 2012, 65(2): 318-325.
CrossRef Google scholar
[18]
Murakami M, Nishi Y, Seto K et al. Dry mouth and denture plaque microflora in complete denture and palatal obturator prosthesis wearers. Gerodontology 2013; doi: 10.1111/ger.12073.
[19]
Rieger UM, Mesina J, Kalbermatten DF. Bacterial biofilms and capsular contracture in patients with breast implants. Br J Surg, 2013, 100(6): 768-774.
CrossRef Google scholar
[20]
Abidi SH, Sherwani SK, Siddiqui TR. Drug resistance profile and biofilm forming potential of Pseudomonas aeruginosa isolated from contact lenses in Karachi-Pakistan. BMC Ophthalmol, 2013, 13: 57.
CrossRef Google scholar
[21]
Høiby N, Ciofu O, Bjarnsholt T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol, 2010, 5(11): 1663-1674.
CrossRef Google scholar
[22]
Martinez-Solano L, Macia MD, Fajardo A. Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. Clin Infect Dis, 2008, 47(12): 1526-1533.
CrossRef Google scholar
[23]
Wessman M, Bjarnsholt T, Eickhardt-Sorensen SR et al. Mucosal biofilm detection in chronic otitis media: a study of middle ear biopsies from Greenlandic patients. Eur Arch Otorhinolaryngol 2014; doi: 10.1007/s00405-014-2886-9.
[24]
Jain R, Douglas R. When and how should we treat biofilms in chronic sinusitis. Curr Opin Otolaryngol Head Neck Surg, 2014, 22(1): 16-21.
CrossRef Google scholar
[25]
Percival SL, Hill KE, Williams DW. A review of the scientific evidence for biofilms in wounds. Wound Repair Regen, 2012, 20(5): 647-657.
CrossRef Google scholar
[26]
Malic S, Hill KE, Hayes A. Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA FISH). Microbiology, 2009, 155(Pt 8): 2603-2611.
CrossRef Google scholar
[27]
Paredes J, Onso-Arce M, Schmidt C. Smart central venous port for early detection of bacterial biofilm related infections. Biomed Microdevices, 2014, 16(3): 365-374.
[28]
Jost GF, Wasner M, Taub E. Sonication of catheter tips for improved detection of microorganisms on external ventricular drains and ventriculo-peritoneal shunts. J Clin Neurosci, 2013, 21(4): 578-582.
CrossRef Google scholar
[29]
Portillo ME, Salvado M, Trampuz A. Sonication versus vortexing of implants for diagnosis of prosthetic joint infection. J Clin Microbiol, 2013, 51(2): 591-594.
CrossRef Google scholar
[30]
Guembe M, Marin M, Martin-Rabadan P. Use of universal 16S rRNA gene PCR as a diagnostic tool for venous access port-related bloodstream infections. J Clin Microbiol, 2013, 51(3): 799-804.
CrossRef Google scholar
[31]
Khot PD, Ko DL, Fredricks DN. Sequencing and analysis of fungal rRNA operons for development of broad-range fungal PCR assays. Appl Environ Microbiol, 2009, 75(6): 1559-1565.
CrossRef Google scholar
[32]
Bjarnsholt T, Nielsen XC, Johansen U. Methods to classify bacterial pathogens in cystic fibrosis. Methods Mol Biol, 2011, 742: 143-171.
CrossRef Google scholar
[33]
Rickerts V, Khot PD, Myerson D. Comparison of quantitative real time PCR with Sequencing and ribosomal RNA-FISH for the identification of fungi in formalin fixed, paraffin-embedded tissue specimens. BMC Infect Dis, 2011, 11: 202.
CrossRef Google scholar
[34]
Zimmerli W, Waldvogel FA, Vaudaux P. Pathogenesis of foreign body infection: description and characteristics of an animal model. J Infect Dis, 1982, 146(4): 487-497.
CrossRef Google scholar
[35]
Zimmerli W, Lew PD, Waldvogel FA. Pathogenesis of foreign body infection. Evidence for a local granulocyte defect. J Clin Invest, 1984, 73(4): 1191-1200.
CrossRef Google scholar
[36]
Raad II, Hanna HA. Intravascular catheter-related infections: new horizons and recent advances. Arch Intern Med, 2002, 162(8): 871-878.
CrossRef Google scholar
[37]
Mermel LA, Allon M, Bouza E. Clinical practice guidelines for the diagnosis and management of intravascular catheter-related infection: 2009 Update by the Infectious Diseases Society of America. Clin Infect Dis, 2009, 49(1): 1-45.
CrossRef Google scholar
[38]
Fernandez-Hidalgo N, Almirante B. Antibiotic-lock therapy: a clinical viewpoint. Expert Rev Anti Infect Ther, 2014, 12(1): 117-129.
CrossRef Google scholar
[39]
Vandenhende MA, Buret J, Camou F. Successful daptomycin lock therapy for implantable intra-arterial catheter infection in a patient with liver metastases of colon cancer. Diagn Microbiol Infect Dis, 2014, 78(4): 497-498.
CrossRef Google scholar
[40]
Tan M, Lau J, Guglielmo BJ. Ethanol locks in the prevention and treatment of catheter-related bloodstream infections. Ann Pharmacother, 2014, 48(5): 607-615.
CrossRef Google scholar
[41]
Madsen M, Rosthoj S. Impact of hydrochloric acid instillation on salvage of infected central venous catheters in children with acute lymphoblastic leukaemia. Scand J Infect Dis, 2013, 45(1): 38-44.
CrossRef Google scholar
[42]
Zimmerli W, Moser C. Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunol Med Microbiol, 2012, 65(2): 158-168.
CrossRef Google scholar
[43]
Mocchegiani R, Nataloni M. Complications of infective endocarditis. Cardiovasc Hematol Disord Drug Targets, 2009, 9(4): 240-248.
CrossRef Google scholar
[44]
Nataloni M, Pergolini M, Rescigno G. Prosthetic valve endocarditis. J Cardiovasc Med (Hagerstown), 2010, 11(12): 869-883.
CrossRef Google scholar
[45]
May JG, Shah P, Sachdeva L. Potential role of biofilms in deep cervical abscess. Int J Pediatr Otorhinolaryngol, 2014, 78(1): 10-13.
CrossRef Google scholar
[46]
Høiby N, Krogh JH, Moser C. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect, 2001, 3(1): 23-35.
CrossRef Google scholar
[47]
Laub R, Schneider YJ, Trouet A. Antibiotic susceptibility of Salmonella spp. at different pH values. J Gen Microbiol, 1989, 135(6): 1407-1416.
[48]
Herrmann G, Yang L, Wu H. Colistin–tobramycin combinations are superior to monotherapy concerning the killing of biofilm Pseudomonas aeruginosa. J Infect Dis, 2010, 202(10): 1585-1592.
CrossRef Google scholar
[49]
Song Z, Wu H, Mygind P. Effects of intratracheal administration of novispirin G10 on a rat model of mucoid Pseudomonas aeruginosa lung infection. Antimicrob Agents Chemother, 2005, 49(9): 3868-3874.
CrossRef Google scholar
[50]
Ceri H, Olson ME, Stremick C. The calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol, 1999, 37(6): 1771-1776.
[51]
Moskowitz SM, Foster JM, Emerson J. Clinically feasible biofilm susceptibility assay for isolates of Pseudomonas aeruginosa from patients with cystic fibrosis. J Clin Microbiol, 2004, 42(5): 1915-1922.
CrossRef Google scholar
[52]
DeRyke CA, Lee SY, Kuti JL. Optimising dosing strategies of antibacterials utilising pharmacodynamic principles: impact on the development of resistance. Drugs, 2006, 66(1): 1-14.
CrossRef Google scholar
[53]
Neu HC. The crisis in antibiotic resistance. Science, 1992, 257(5073): 1064-1073.
CrossRef Google scholar
[54]
Hengzhuang W, Ciofu O, Yang L. High beta-lactamase levels change the pharmacodynamics of beta-lactam antibiotics in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother, 2013, 57(1): 196-204.
CrossRef Google scholar
[55]
Dubern JF, Diggle SP. Quorum sensing by 2-alkyl-4-quinolones in Pseudomonas aeruginosa and other bacterial species. Mol Biosyst, 2008, 4(9): 882-888.
CrossRef Google scholar
[56]
Kalia D, Merey G, Nakayama S. Nucleotide, c-di-GMP, c-di-AMP, cGMP, cAMP, (p)ppGpp signaling in bacteria and implications in pathogenesis. Chem Soc Rev, 2013, 42(1): 305-341.
CrossRef Google scholar
[57]
Hengge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol, 2009, 7(4): 263-273.
CrossRef Google scholar
[58]
Romling U, Galperin MY, Gomelsky M. Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev, 2013, 77(1): 1-52.
CrossRef Google scholar
[59]
Romero D, Aguilar C, Losick R. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A, 2010, 107(5): 2230-2234.
CrossRef Google scholar
[60]
Wu H, Song Z, Hentzer M. Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother, 2004, 53(6): 1054-1061.
CrossRef Google scholar
[61]
O′Loughlin CT, Miller LC, Siryaporn A. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci U S A, 2013, 110(44): 17981-17986.
CrossRef Google scholar
[62]
Cevizci R, Duzlu M, Dundar Y et al. Preliminary results of a novel quorum sensing inhibitor against pneumococcal infection and biofilm formation with special interest to otitis media and cochlear implantation. Eur Arch Otorhinolaryngol 2014. doi: 10.1007/s00405-014-2942-5. [Epub ahead of print].
[63]
Cirioni O, Mocchegiani F, Cacciatore I. Quorum sensing inhibitor FS3-coated vascular graft enhances daptomycin efficacy in a rat model of staphylococcal infection 2. Peptides, 2013, 40: 77-81.
CrossRef Google scholar
[64]
Balaban N, Cirioni O, Giacometti A. Treatment of Staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP. Antimicrob Agents Chemother, 2007, 51(6): 2226-2229.
CrossRef Google scholar
[65]
LoVetri K, Madhyastha S. Antimicrobial and antibiofilm activity of quorum sensing peptides and Peptide analogues against oral biofilm bacteria. Methods Mol Biol, 2010, 618: 383-392.
CrossRef Google scholar
[66]
Bjarnsholt T, Jensen PO, Rasmussen TB. Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology, 2005, 151(Pt 12): 3873-3880.
CrossRef Google scholar
[67]
Hoffmann N, Lee B, Hentzer M. Azithromycin blocks quorum sensing and alginate polymer formation and increases the sensitivity to serum and stationary-growth-phase killing of Pseudomonas aeruginosa and attenuates chronic P. aeruginosa lung infection in Cftr−/− mice. Antimicrob Agents Chemother, 2007, 51(10): 3677-3687.
CrossRef Google scholar
[68]
Song Z, Kong KF, Wu H. Panax ginseng has anti-infective activity against opportunistic pathogen Pseudomonas aeruginosa by inhibiting quorum sensing, a bacterial communication process critical for establishing infection. Phytomedicine, 2010, 17(13): 1040-1046.
CrossRef Google scholar
[69]
Wu H, Song Z, Givskov M. Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology, 2001, 147(Pt 5): 1105-1113.
CrossRef Google scholar
[70]
Brackman G, Cos P, Maes L. Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob Agents Chemother, 2011, 55(6): 2655-2661.
CrossRef Google scholar
[71]
Sambanthamoorthy K, Luo C, Pattabiraman N. Identification of small molecules inhibiting diguanylate cyclases to control bacterial biofilm development. Biofouling, 2014, 30(1): 17-28.
CrossRef Google scholar
[72]
Lieberman OJ, Orr MW, Wang Y. High-throughput screening using the differential radial capillary action of ligand assay identifies ebselen as an inhibitor of diguanylate cyclases. ACS Chem Biol, 2014, 9(1): 183-192.
CrossRef Google scholar
[73]
Wu H, Lee B, Yang L. Effects of ginseng on Pseudomonas aeruginosa motility and biofilm formation. FEMS Immunol Med Microbiol, 2011, 62(1): 49-56.
CrossRef Google scholar
[74]
Connolly KL, Roberts AL, Holder RC. Dispersal of Group A streptococcal biofilms by the cysteine protease SpeB leads to increased disease severity in a murine model. PLoS One, 2011, 6(4): e18984.
CrossRef Google scholar
[75]
Park JH, Lee JH, Cho MH. Acceleration of protease effect on Staphylococcus aureus biofilm dispersal. FEMS Microbiol Lett, 2012, 335(1): 31-38.
CrossRef Google scholar
[76]
Cegelski L, Pinkner JS, Hammer ND. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol, 2009, 5(12): 913-919.
CrossRef Google scholar
[77]
Romero D, Sanabria-Valentin E, Vlamakis H. Biofilm inhibitors that target amyloid proteins. Chem Biol, 2013, 20(1): 102-110.
CrossRef Google scholar
[78]
Sintim HO, Smith JA, Wang J. Paradigm shift in discovering next-generation anti-infective agents: targeting quorum sensing, c-di-GMP signaling and biofilm formation in bacteria with small molecules. Future Med Chem, 2010, 2(6): 1005-1035.
CrossRef Google scholar
[79]
Soothill J. Use of bacteriophages in the treatment of Pseudomonas aeruginosa infections. Expert Rev Anti Infect Ther, 2013, 11(9): 909-915.
CrossRef Google scholar
[80]
Burrowes B, Harper DR, Anderson J. Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev Anti Infect Ther, 2011, 9(9): 775-785.
CrossRef Google scholar
[81]
Seth AK, Geringer MR, Nguyen KT. Bacteriophage therapy for Staphylococcus aureus biofilm-infected wounds: a new approach to chronic wound care. Plast Reconstr Surg, 2013, 131(2): 225-234.
CrossRef Google scholar
[82]
Yilmaz C, Colak M, Yilmaz BC. Bacteriophage therapy in implant-related infections: an experimental study. J Bone Joint Surg Am, 2013, 95(2): 117-125.
CrossRef Google scholar
[83]
Alemayehu D, Casey PG, McAuliffe O. Bacteriophages phiMR299-2 and phiNH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fibrosis lung airway cells. MBio, 2012, 3(2): e00029-12.
CrossRef Google scholar
[84]
Brussow H. Bacteriophage–host interaction: from splendid isolation into a messy reality. Curr Opin Microbiol, 2013, 16(4): 500-506.
CrossRef Google scholar
[85]
Singh PK, Parsek MR, Greenberg EP. A component of innate immunity prevents bacterial biofilm development. Nature, 2002, 417(6888): 552-555.
CrossRef Google scholar
[86]
Iwase T, Uehara Y, Shinji H. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature, 2010, 465(7296): 346-349.
CrossRef Google scholar
[87]
He N, Hu J, Liu H. Enhancement of vancomycin activity against biofilms by using ultrasound-targeted microbubble destruction. Antimicrob Agents Chemother, 2011, 55(11): 5331-5337.
CrossRef Google scholar
[88]
Hoen B, Duval X. Clinical practice. Infective endocarditis. N Engl J Med, 2013, 368(15): 1425-1433.
CrossRef Google scholar
[89]
Baddour LM, Wilson WR, Bayer AS. Infective endocarditis: diagnosis, antimicrobial therapy, and management of complications: a statement for healthcare professionals from the Committee on Rheumatic Fever, Endocarditis, and Kawasaki Disease, Council on Cardiovascular Disease in the Young, and the Councils on Clinical Cardiology, Stroke, and Cardiovascular Surgery and Anesthesia, American Heart Association: endorsed by the Infectious Diseases Society of America. Circulation, 2005, 111(23): e394-e434.
[90]
Smith RN, Nolan JP. Central venous catheters. BMJ, 2013, 347: f6570.
CrossRef Google scholar

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