Strategies for combating bacterial biofilm infections

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

Abstract

Formation of biofilm is a survival strategy for bacteria and fungi to adapt to their living environment, especially in the hostile environment. Under the protection of biofilm, microbial cells in biofilm become tolerant and resistant to antibiotics and the immune responses, which increases the difficulties for the clinical treatment of biofilm infections. Clinical and laboratory investigations demonstrated a perspicuous correlation between biofilm infection and medical foreign bodies or indwelling devices. Clinical observations and experimental studies indicated clearly that antibiotic treatment alone is in most cases insufficient to eradicate biofilm infections. Therefore, to effectively treat biofilm infections with currently available antibiotics and evaluate the outcomes become important and urgent for clinicians. The review summarizes the latest progress in treatment of clinical biofilm infections and scientific investigations, discusses the diagnosis and treatment of different biofilm infections and introduces the promising laboratory progress, which may contribute to prevention or cure of biofilm infections. We conclude that, an efficient treatment of biofilm infections needs a well-established multidisciplinary collaboration, which includes removal of the infected foreign bodies, selection of biofilm-active, sensitive and well-penetrating antibiotics, systemic or topical antibiotic administration in high dosage and combinations, and administration of anti-quorum sensing or biofilm dispersal agents.

References

    1. de Fuente-Núñez C, Reffuveille F, Fernandez L et al. Bacterial biofilm development as a multicellular adaptation: antibiotic resistance and new therapeutic strategies. Curr Opin Microbiol 2013; 16(5): 580–589.
    1. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2004; 2(2): 95–108.
    1. Yang L, Liu Y, Wu H et al. Combating biofilms. FEMS Immunol Med Microbiol 2012; 65(2): 146–157.
    1. Høiby N, Ciofu O, Johansen HK et al. The clinical impact of bacterial biofilms. Int J Oral Sci 2011; 3(2): 55–65.
    1. Hengzhuang W, Wu H, Ciofu O et al. Pharmacokinetics/pharmacodynamics of colistin and imipenem on mucoid and nonmucoid Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2011; 55(9): 4469–4474.
    1. Hengzhuang W, Wu H, Ciofu O et al. In vivo pharmacokinetics/pharmacodynamics of colistin and imipenem in Pseudomonas aeruginosa biofilm infection. Antimicrob Agents Chemother 2012; 56(5): 2683–2690.
    1. Høiby N, Bjarnsholt T, Givskov M et al. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 2010; 35(4): 322–332.
    1. Høiby N. Recent advances in the treatment of Pseudomonas aeruginosa infections in cystic fibrosis. BMC Med 2011; 9: 32.
    1. Tran PL, Lowry N, Campbell T et al. An organoselenium compound inhibits Staphylococcus aureus biofilms on hemodialysis catheters in vivo. Antimicrob Agents Chemother 2012; 56(2): 972–978.
    1. Tollefson DF, Bandyk DF, Kaebnick HW et al. Surface biofilm disruption. Enhanced recovery of microorganisms from vascular prostheses. Arch Surg 1987; 122(1): 38–43.
    1. Fux CA, Quigley M, Worel AM et al. Biofilm-related infections of cerebrospinal fluid shunts. Clin Microbiol Infect 2006; 12(4): 331–337.
    1. Donlan RM. Biofilms and device-associated infections. Emerg Infect Dis 2001; 7(2): 277–281.
    1. Song Z, Borgwardt L, Høiby N et al. Prosthesis infections after orthopedic joint replacement: the possible role of bacterial biofilms. Orthop Rev (Pavia) 2013; 5(2): 65–71.
    1. Santos AP, Watanabe E, Andrade D. Biofilm on artificial pacemaker: fiction or reality? Arq Bras Cardiol 2011; 97(5): e113–e120.
    1. Dasgupta MK. Biofilms and infection in dialysis patients. Semin Dial 2002; 15(5): 338–346.
    1. Auler ME, Morreira D, Rodrigues FF et al. Biofilm formation on intrauterine devices in patients with recurrent vulvovaginal candidiasis. Med Mycol 2010; 48(1): 211–216.
    1. Donelli G, Vuotto C, Cardines R et al. Biofilm-growing intestinal anaerobic bacteria. FEMS Immunol Med Microbiol 2012; 65(2): 318–325.
    1. 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.
    1. Rieger UM, Mesina J, Kalbermatten DF et al. Bacterial biofilms and capsular contracture in patients with breast implants. Br J Surg 2013; 100(6): 768–774.
    1. Abidi SH, Sherwani SK, Siddiqui TR et al. Drug resistance profile and biofilm forming potential of Pseudomonas aeruginosa isolated from contact lenses in Karachi-Pakistan. BMC Ophthalmol 2013; 13: 57.
    1. Høiby N, Ciofu O, Bjarnsholt T. Pseudomonas aeruginosa biofilms in cystic fibrosis. Future Microbiol 2010; 5(11): 1663–1674.
    1. Martinez-Solano L, Macia MD, Fajardo A et al. Chronic Pseudomonas aeruginosa infection in chronic obstructive pulmonary disease. Clin Infect Dis 2008; 47(12): 1526–1533.
    1. 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.
    1. 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.
    1. Percival SL, Hill KE, Williams DW et al. A review of the scientific evidence for biofilms in wounds. Wound Repair Regen 2012; 20(5): 647–657.
    1. Malic S, Hill KE, Hayes A et al. 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.
    1. Paredes J, Onso-Arce M, Schmidt C et al. Smart central venous port for early detection of bacterial biofilm related infections. Biomed Microdevices 2014; 16(3): 365–374.
    1. Jost GF, Wasner M, Taub E et al. 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.
    1. Portillo ME, Salvado M, Trampuz A et al. Sonication versus vortexing of implants for diagnosis of prosthetic joint infection. J Clin Microbiol 2013; 51(2): 591–594.
    1. Guembe M, Marin M, Martin-Rabadan P et al. 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.
    1. 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.
    1. Bjarnsholt T, Nielsen XC, Johansen U et al. Methods to classify bacterial pathogens in cystic fibrosis. Methods Mol Biol 2011; 742: 143–171.
    1. Rickerts V, Khot PD, Myerson D et al. 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.
    1. Zimmerli W, Waldvogel FA, Vaudaux P et al. Pathogenesis of foreign body infection: description and characteristics of an animal model. J Infect Dis 1982; 146(4): 487–497.
    1. 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.
    1. Raad II, Hanna HA. Intravascular catheter-related infections: new horizons and recent advances. Arch Intern Med 2002; 162(8): 871–878.
    1. Mermel LA, Allon M, Bouza E et al. 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.
    1. Fernandez-Hidalgo N, Almirante B. Antibiotic-lock therapy: a clinical viewpoint. Expert Rev Anti Infect Ther 2014; 12(1): 117–129.
    1. Vandenhende MA, Buret J, Camou F et al. 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.
    1. 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.
    1. 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.
    1. Zimmerli W, Moser C. Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunol Med Microbiol 2012; 65(2): 158–168.
    1. Mocchegiani R, Nataloni M. Complications of infective endocarditis. Cardiovasc Hematol Disord Drug Targets 2009; 9(4): 240–248.
    1. Nataloni M, Pergolini M, Rescigno G et al. Prosthetic valve endocarditis. J Cardiovasc Med (Hagerstown) 2010; 11(12): 869–883.
    1. May JG, Shah P, Sachdeva L et al. Potential role of biofilms in deep cervical abscess. Int J Pediatr Otorhinolaryngol 2014; 78(1): 10–13.
    1. Høiby N, Krogh JH, Moser C et al. Pseudomonas aeruginosa and the in vitro and in vivo biofilm mode of growth. Microbes Infect 2001; 3(1): 23–35.
    1. Laub R, Schneider YJ, Trouet A. Antibiotic susceptibility of Salmonella spp. at different pH values. J Gen Microbiol 1989; 135(6): 1407–1416.
    1. Herrmann G, Yang L, Wu H et al. Colistin–tobramycin combinations are superior to monotherapy concerning the killing of biofilm Pseudomonas aeruginosa. J Infect Dis 2010; 202(10): 1585–1592.
    1. Song Z, Wu H, Mygind P et al. 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.
    1. Ceri H, Olson ME, Stremick C et al. The calgary biofilm device: new technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 1999; 37(6): 1771–1776.
    1. Moskowitz SM, Foster JM, Emerson J et al. Clinically feasible biofilm susceptibility assay for isolates of Pseudomonas aeruginosa from patients with cystic fibrosis. J Clin Microbiol 2004; 42(5): 1915–1922.
    1. DeRyke CA, Lee SY, Kuti JL et al. Optimising dosing strategies of antibacterials utilising pharmacodynamic principles: impact on the development of resistance. Drugs 2006; 66(1): 1–14.
    1. Neu HC. The crisis in antibiotic resistance. Science 1992; 257(5073): 1064–1073.
    1. Hengzhuang W, Ciofu O, Yang L et al. High beta-lactamase levels change the pharmacodynamics of beta-lactam antibiotics in Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 2013; 57(1): 196–204.
    1. 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.
    1. Kalia D, Merey G, Nakayama S et al. 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.
    1. Hengge R. Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 2009; 7(4): 263–273.
    1. 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.
    1. Romero D, Aguilar C, Losick R et al. Amyloid fibers provide structural integrity to Bacillus subtilis biofilms. Proc Natl Acad Sci U S A 2010; 107(5): 2230–2234.
    1. Wu H, Song Z, Hentzer M et al. Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 2004; 53(6): 1054–1061.
    1. O′Loughlin CT, Miller LC, Siryaporn A et al. A quorum-sensing inhibitor blocks Pseudomonas aeruginosa virulence and biofilm formation. Proc Natl Acad Sci U S A 2013; 110(44): 17981–17986.
    1. 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].
    1. Cirioni O, Mocchegiani F, Cacciatore I et al. Quorum sensing inhibitor FS3-coated vascular graft enhances daptomycin efficacy in a rat model of staphylococcal infection 2. Peptides 2013; 40: 77–81.
    1. Balaban N, Cirioni O, Giacometti A et al. Treatment of Staphylococcus aureus biofilm infection by the quorum-sensing inhibitor RIP. Antimicrob Agents Chemother 2007; 51(6): 2226–2229.
    1. 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.
    1. Bjarnsholt T, Jensen PO, Rasmussen TB et al. Garlic blocks quorum sensing and promotes rapid clearing of pulmonary Pseudomonas aeruginosa infections. Microbiology 2005; 151(Pt 12): 3873–3880.
    1. Hoffmann N, Lee B, Hentzer M et al. 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.
    1. Song Z, Kong KF, Wu H et al. 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.
    1. Wu H, Song Z, Givskov M et al. Pseudomonas aeruginosa mutations in lasI and rhlI quorum sensing systems result in milder chronic lung infection. Microbiology 2001; 147(Pt 5): 1105–1113.
    1. Brackman G, Cos P, Maes L et al. Quorum sensing inhibitors increase the susceptibility of bacterial biofilms to antibiotics in vitro and in vivo. Antimicrob Agents Chemother 2011; 55(6): 2655–2661.
    1. Sambanthamoorthy K, Luo C, Pattabiraman N et al. Identification of small molecules inhibiting diguanylate cyclases to control bacterial biofilm development. Biofouling 2014; 30(1): 17–28.
    1. Lieberman OJ, Orr MW, Wang Y et al. 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.
    1. Wu H, Lee B, Yang L et al. Effects of ginseng on Pseudomonas aeruginosa motility and biofilm formation. FEMS Immunol Med Microbiol 2011; 62(1): 49–56.
    1. Connolly KL, Roberts AL, Holder RC et al. 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.
    1. Park JH, Lee JH, Cho MH et al. Acceleration of protease effect on Staphylococcus aureus biofilm dispersal. FEMS Microbiol Lett 2012; 335(1): 31–38.
    1. Cegelski L, Pinkner JS, Hammer ND et al. Small-molecule inhibitors target Escherichia coli amyloid biogenesis and biofilm formation. Nat Chem Biol 2009; 5(12): 913–919.
    1. Romero D, Sanabria-Valentin E, Vlamakis H et al. Biofilm inhibitors that target amyloid proteins. Chem Biol 2013; 20(1): 102–110.
    1. Sintim HO, Smith JA, Wang J et al. 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.
    1. Soothill J. Use of bacteriophages in the treatment of Pseudomonas aeruginosa infections. Expert Rev Anti Infect Ther 2013; 11(9): 909–915.
    1. Burrowes B, Harper DR, Anderson J et al. Bacteriophage therapy: potential uses in the control of antibiotic-resistant pathogens. Expert Rev Anti Infect Ther 2011; 9(9): 775–785.
    1. Seth AK, Geringer MR, Nguyen KT et al. Bacteriophage therapy for Staphylococcus aureus biofilm-infected wounds: a new approach to chronic wound care. Plast Reconstr Surg 2013; 131(2): 225–234.
    1. Yilmaz C, Colak M, Yilmaz BC et al. Bacteriophage therapy in implant-related infections: an experimental study. J Bone Joint Surg Am 2013; 95(2): 117–125.
    1. Alemayehu D, Casey PG, McAuliffe O et al. 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.
    1. Brussow H. Bacteriophage–host interaction: from splendid isolation into a messy reality. Curr Opin Microbiol 2013; 16(4): 500–506.
    1. Singh PK, Parsek MR, Greenberg EP et al. A component of innate immunity prevents bacterial biofilm development. Nature 2002; 417(6888): 552–555.
    1. Iwase T, Uehara Y, Shinji H et al. Staphylococcus epidermidis Esp inhibits Staphylococcus aureus biofilm formation and nasal colonization. Nature 2010; 465(7296): 346–349.
    1. He N, Hu J, Liu H et al. Enhancement of vancomycin activity against biofilms by using ultrasound-targeted microbubble destruction. Antimicrob Agents Chemother 2011; 55(11): 5331–5337.
    1. Hoen B, Duval X. Clinical practice. Infective endocarditis. N Engl J Med 2013; 368(15): 1425–1433.
    1. Baddour LM, Wilson WR, Bayer AS et al. 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.
    1. Smith RN, Nolan JP. Central venous catheters. BMJ 2013; 347: f6570.

Source: PubMed

3
Suscribir