J Knee Surg 2020; 33(02): 119-131
DOI: 10.1055/s-0040-1701214
Special Focus Section
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Biofilms in Periprosthetic Joint Infections: A Review of Diagnostic Modalities, Current Treatments, and Future Directions

Monica M. Shoji
1   Department of Orthopaedic Surgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts
,
Antonia F. Chen
1   Department of Orthopaedic Surgery, Brigham and Women's Hospital, Harvard Medical School, Boston, Massachusetts
› Author Affiliations
Further Information

Publication History

16 July 2019

27 December 2019

Publication Date:
14 January 2020 (online)

Abstract

As the number of total joint arthroplasties continues to rise, periprosthetic joint infection (PJI), a significant and devastating complication of total joint arthroplasty, may also increase. In PJI, bacterial biofilms are formed by causative pathogens surrounded by extracellular matrix with relatively dormant cells that can persist, resulting in a barrier against the host immune system and antibiotics. These biofilms not only contribute to the pathogenesis of PJI but also result in diagnostic challenges, antibiotic resistance, and PJI treatment failure. This review discusses the development of biofilms and key features associated with biofilm pathogenicity in PJI, current PJI diagnostic methods and their limitations, and current treatment options. Additionally, this article explores novel approaches to treat PJI, including targeting persister bacteria, immunotherapy, antimicrobial peptides, nanoparticles, and bacteriophage therapy. Biofilm eradication can also be achieved through enzymatic therapy, photodynamic therapy, and ultrasound. Finally, this review discusses novel techniques to prevent PJI, including improved irrigation solutions, smart implants with antimicrobial properties, inhibition of quorum sensing, and vaccines, which may revolutionize PJI management in the future by eradicating a devastating problem.

 
  • References

  • 1 Sloan M, Premkumar A, Sheth NP. Projected volume of primary total joint arthroplasty in the U.S., 2014 to 2030. J Bone Joint Surg Am 2018; 100 (17) 1455-1460
  • 2 Phillips JE, Crane TP, Noy M, Elliott TSJ, Grimer RJ. The incidence of deep prosthetic infections in a specialist orthopaedic hospital: a 15-year prospective survey. J Bone Joint Surg Br 2006; 88 (07) 943-948
  • 3 Gbejuade HO, Lovering AM, Webb JC. The role of microbial biofilms in prosthetic joint infections. Acta Orthop 2015; 86 (02) 147-158
  • 4 Tzeng A, Tzeng TH, Vasdev S. , et al. Treating periprosthetic joint infections as biofilms: key diagnosis and management strategies. Diagn Microbiol Infect Dis 2015; 81 (03) 192-200
  • 5 Aggarwal VK, Bakhshi H, Ecker NU, Parvizi J, Gehrke T, Kendoff D. Organism profile in periprosthetic joint infection: pathogens differ at two arthroplasty infection referral centers in Europe and in the United States. J Knee Surg 2014; 27 (05) 399-406
  • 6 Schinsky MF, Della Valle CJ, Sporer SM, Paprosky WG. Perioperative testing for joint infection in patients undergoing revision total hip arthroplasty. J Bone Joint Surg Am 2008; 90 (09) 1869-1875
  • 7 Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis 2002; 8 (09) 881-890
  • 8 Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 2006; 17 (Suppl. 02) 68-81
  • 9 Malhotra R, Dhawan B, Garg B, Shankar V, Nag TC. A comparison of bacterial adhesion and biofilm formation on commonly used orthopaedic metal implant materials: an in vitro study. Indian J Orthop 2019; 53 (01) 148-153
  • 10 Høiby N, Bjarnsholt T, Givskov M, Molin S, Ciofu O. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 2010; 35 (04) 322-332
  • 11 Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother 2001; 45 (04) 999-1007
  • 12 Driffield K, Miller K, Bostock JM, O'Neill AJ, Chopra I. Increased mutability of Pseudomonas aeruginosa in biofilms. J Antimicrob Chemother 2008; 61 (05) 1053-1056
  • 13 Ciofu O. Pseudomonas aeruginosa chromosomal beta-lactamase in patients with cystic fibrosis and chronic lung infection. Mechanism of antibiotic resistance and target of the humoral immune response. APMIS Suppl 2003; (116) 1-47
  • 14 Pamp SJ, Gjermansen M, Johansen HK, Tolker-Nielsen T. Tolerance to the antimicrobial peptide colistin in Pseudomonas aeruginosa biofilms is linked to metabolically active cells, and depends on the pmr and mexAB-oprM genes. Mol Microbiol 2008; 68 (01) 223-240
  • 15 Wolcott RD, Ehrlich GD. Biofilms and chronic infections. JAMA 2008; 299 (22) 2682-2684
  • 16 Tack KJ, Sabath LD. Increased minimum inhibitory concentrations with anaerobiasis for tobramycin, gentamicin, and amikacin, compared to latamoxef, piperacillin, chloramphenicol, and clindamycin. Chemotherapy 1985; 31 (03) 204-210
  • 17 Walters III MC, Roe F, Bugnicourt A, Franklin MJ, Stewart PS. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Chemother 2003; 47 (01) 317-323
  • 18 Ernest EP, Machi AS, Karolcik BA, LaSala PR, Dietz MJ. Topical adjuvants incompletely remove adherent Staphylococcus aureus from implant materials. J Orthop Res 2018; 36 (06) 1599-1604
  • 19 Tsang STJ, Gwynne PJ, Gallagher MP, Simpson AHRW. The biofilm eradication activity of acetic acid in the management of periprosthetic joint infection. Bone Joint Res 2018; 7 (08) 517-523
  • 20 Leid JG, Shirtliff ME, Costerton JW, Stoodley P. Human leukocytes adhere to, penetrate, and respond to Staphylococcus aureus biofilms. Infect Immun 2002; 70 (11) 6339-6345
  • 21 Zimmerli W, Lew PD, Waldvogel FA. Pathogenesis of foreign body infection. Evidence for a local granulocyte defect. J Clin Invest 1984; 73 (04) 1191-1200
  • 22 Gries CM, Kielian T. Staphylococcal biofilms and immune polarization during prosthetic joint infection. J Am Acad Orthop Surg 2017; 25 (Suppl. 01) S20-S24
  • 23 Zimmerli W, Sendi P. Pathogenesis of implant-associated infection: the role of the host. Semin Immunopathol 2011; 33 (03) 295-306
  • 24 Khoury AE, Lam K, Ellis B, Costerton JW. Prevention and control of bacterial infections associated with medical devices. ASAIO J 1992; 38 (03) M174-M178
  • 25 Hall-Stoodley L, Hu FZ, Gieseke A. , et al. Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 2006; 296 (02) 202-211
  • 26 Parvizi J, Zmistowski B, Berbari EF. , et al. New definition for periprosthetic joint infection: from the Workgroup of the Musculoskeletal Infection Society. Clin Orthop Relat Res 2011; 469 (11) 2992-2994
  • 27 Koh IJ, Cho W-S, Choi NY, Parvizi J, Kim TK. ; Korea Knee Research Group. How accurate are orthopedic surgeons in diagnosing periprosthetic joint infection after total knee arthroplasty?: a multicenter study. Knee 2015; 22 (03) 180-185
  • 28 Parvizi J, Tan TL, Goswami K. , et al. The 2018 definition of periprosthetic hip and knee infection: an evidence-based and validated criteria. J Arthroplasty 2018; 33 (05) 1309-1314.e2
  • 29 Xu Y, Rudkjøbing VB, Simonsen O. , et al. Bacterial diversity in suspected prosthetic joint infections: an exploratory study using 16S rRNA gene analysis. FEMS Immunol Med Microbiol 2012; 65 (02) 291-304
  • 30 Cazanave C, Greenwood-Quaintance KE, Hanssen AD. , et al. Rapid molecular microbiologic diagnosis of prosthetic joint infection. J Clin Microbiol 2013; 51 (07) 2280-2287
  • 31 Bjerkan G, Witsø E, Nor A. , et al. A comprehensive microbiological evaluation of fifty-four patients undergoing revision surgery due to prosthetic joint loosening. J Med Microbiol 2012; 61 (Pt 4): 572-581
  • 32 Nistico L, Hall-Stoodley L, Stoodley P. Imaging bacteria and biofilms on hardware and periprosthetic tissue in orthopedic infections. Methods Mol Biol 2014; 1147: 105-126
  • 33 Savichtcheva O, Okayama N, Ito T, Okabe S. Application of a direct fluorescence-based live/dead staining combined with fluorescence in situ hybridization for assessment of survival rate of Bacteroides spp. in drinking water. Biotechnol Bioeng 2005; 92 (03) 356-363
  • 34 Ehrlich GD, Costerton JW, Altman D. , et al. Towards a new paradigm in the diagnosis and treatment of orthopedic infections. In: Ehrlich GD, DeMeo PJ, Costerton JW, Winkler H. , eds. Culture Negative Orthopedic Biofilm Infections. Berlin, Germany: Springer-Verlag; 2012: 129-139
  • 35 Huang WE, Stoecker K, Griffiths R. , et al. Raman-FISH: combining stable-isotope Raman spectroscopy and fluorescence in situ hybridization for the single cell analysis of identity and function. Environ Microbiol 2007; 9 (08) 1878-1889
  • 36 Hamady M, Knight R. Microbial community profiling for human microbiome projects: tools, techniques, and challenges. Genome Res 2009; 19 (07) 1141-1152
  • 37 Metso L, Mäki M, Tissari P. , et al. Efficacy of a novel PCR- and microarray-based method in diagnosis of a prosthetic joint infection. Acta Orthop 2014; 85 (02) 165-170
  • 38 Stoodley P, Nistico L, Johnson S. , et al. Direct demonstration of viable Staphylococcus aureus biofilms in an infected total joint arthroplasty. A case report. J Bone Joint Surg Am 2008; 90 (08) 1751-1758
  • 39 Della Valle C, Parvizi J, Bauer TW. , et al; American Academy of Orthopaedic Surgeons. American Academy of Orthopaedic Surgeons clinical practice guideline on: the diagnosis of periprosthetic joint infections of the hip and knee. J Bone Joint Surg Am 2011; 93 (14) 1355-1357
  • 40 Parry JA, Karau MJ, Kakar S, Hanssen AD, Patel R, Abdel MP. Disclosing agents for the intraoperative identification of biofilms on orthopedic implants. J Arthroplasty 2017; 32 (08) 2501-2504
  • 41 Shaw JD, Miller S, Plourde A, Shaw DL, Wustrack R, Hansen EN. Methylene blue-guided debridement as an intraoperative adjunct for the surgical treatment of periprosthetic joint infection. J Arthroplasty 2017; 32 (12) 3718-3723
  • 42 Bereza PL, Ekiel A, Auguściak-Duma A. , et al. Identification of silent prosthetic joint infection: preliminary report of a prospective controlled study. Int Orthop 2013; 37 (10) 2037-2043
  • 43 Trampuz A, Piper KE, Jacobson MJ. , et al. Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 2007; 357 (07) 654-663
  • 44 Rak M, KavčIč M, Trebše R, CőR A. Detection of bacteria with molecular methods in prosthetic joint infection: sonication fluid better than periprosthetic tissue. Acta Orthop 2016; 87 (04) 339-345
  • 45 Pitt WG, Ross SA. Ultrasound increases the rate of bacterial cell growth. Biotechnol Prog 2003; 19 (03) 1038-1044
  • 46 Li J, Ma L, Liao X. , et al. Ultrasound-induced Escherichia coli O157:H7 cell death exhibits physical disruption and biochemical apoptosis. Front Microbiol 2018; 9: 2486
  • 47 Ananta E, Voigt D, Zenker M, Heinz V, Knorr D. Cellular injuries upon exposure of Escherichia coli and Lactobacillus rhamnosus to high-intensity ultrasound. J Appl Microbiol 2005; 99 (02) 271-278
  • 48 Singh R, Ray P, Das A, Sharma M. Penetration of antibiotics through Staphylococcus aureus and Staphylococcus epidermidis biofilms. J Antimicrob Chemother 2010; 65 (09) 1955-1958
  • 49 Raad I, Hanna H, Jiang Y. , et al. Comparative activities of daptomycin, linezolid, and tigecycline against catheter-related methicillin-resistant Staphylococcus bacteremic isolates embedded in biofilm. Antimicrob Agents Chemother 2007; 51 (05) 1656-1660
  • 50 John A-K, Baldoni D, Haschke M. , et al. Efficacy of daptomycin in implant-associated infection due to methicillin-resistant Staphylococcus aureus: importance of combination with rifampin. Antimicrob Agents Chemother 2009; 53 (07) 2719-2724
  • 51 Trampuz A, Zimmerli W. Antimicrobial agents in orthopaedic surgery: prophylaxis and treatment. Drugs 2006; 66 (08) 1089-1105
  • 52 Osmon DR, Berbari EF, Berendt AR. , et al; Infectious Diseases Society of America. Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 2013; 56 (01) e1-e25
  • 53 Nguyen M, Sukeik M, Zahar A, Nizam I, Haddad FS. One-stage exchange arthroplasty for periprosthetic hip and knee joint infections. Open Orthop J 2016; 10: 646-653
  • 54 Yoo JJ, Kwon YS, Koo K-H, Yoon KS, Kim Y-M, Kim HJ. One-stage cementless revision arthroplasty for infected hip replacements. Int Orthop 2009; 33 (05) 1195-1201
  • 55 Kuiper JWP, Rustenburg CME, Willems JH, Verberne SJ, Peters EJG, Saouti R. Results and patient reported outcome measures (PROMs) after one-stage revision for periprosthetic joint infection of the hip: a single-centre retrospective study. J Bone Jt Infect 2018; 3 (03) 143-149
  • 56 Wongworawat MD. Clinical faceoff: one- versus two-stage exchange arthroplasty for prosthetic joint infections. Clin Orthop Relat Res 2013; 471 (06) 1750-1753
  • 57 Strange S, Whitehouse MR, Beswick AD. , et al. One-stage or two-stage revision surgery for prosthetic hip joint infection--the INFORM trial: a study protocol for a randomised controlled trial. Trials 2016; 17: 90
  • 58 Kuiper JW, Willink RT, Moojen DJF, van den Bekerom MP, Colen S. Treatment of acute periprosthetic infections with prosthesis retention: review of current concepts. World J Orthop 2014; 5 (05) 667-676
  • 59 Zmistowski B, Fedorka CJ, Sheehan E, Deirmengian G, Austin MS, Parvizi J. Prosthetic joint infection caused by gram-negative organisms. J Arthroplasty 2011; 26 (6, Suppl): 104-108
  • 60 Crotty MP, Krekel T, Burnham CA, Ritchie DJ. New gram-positive agents: the next generation of oxazolidinones and lipoglycopeptides. J Clin Microbiol 2016; 54 (09) 2225-2232
  • 61 Brade KD, Rybak JM, Rybak MJ. Oritavancin: a new lipoglycopeptide antibiotic in the treatment of gram-positive infections. Infect Dis Ther 2016; 5 (01) 1-15
  • 62 Lehoux D, Ostiguy V, Cadieux C. , et al. Oritavancin pharmacokinetics and bone penetration in rabbits. Antimicrob Agents Chemother 2015; 59 (10) 6501-6505
  • 63 Dunne MW, Puttagunta S, Sprenger CR, Rubino C, Van Wart S, Baldassarre J. Extended-duration dosing and distribution of dalbavancin into bone and articular tissue. Antimicrob Agents Chemother 2015; 59 (04) 1849-1855
  • 64 Fernández J, Greenwood-Quaintance KE, Patel R. In vitro activity of dalbavancin against biofilms of staphylococci isolated from prosthetic joint infections. Diagn Microbiol Infect Dis 2016; 85 (04) 449-451
  • 65 Fux CA, Wilson S, Stoodley P. Detachment characteristics and oxacillin resistance of Staphyloccocus aureus biofilm emboli in an in vitro catheter infection model. J Bacteriol 2004; 186 (14) 4486-4491
  • 66 Conlon BP, Nakayasu ES, Fleck LE. , et al. Activated ClpP kills persisters and eradicates a chronic biofilm infection. Nature 2013; 503 (7476): 365-370
  • 67 Kwan BW, Chowdhury N, Wood TK. Combatting bacterial infections by killing persister cells with mitomycin C. Environ Microbiol 2015; 17 (11) 4406-4414
  • 68 Chowdhury N, Wood TL, Martínez-Vázquez M, García-Contreras R, Wood TK. DNA-crosslinker cisplatin eradicates bacterial persister cells. Biotechnol Bioeng 2016; 113 (09) 1984-1992
  • 69 Walz JM, Avelar RL, Longtine KJ, Carter KL, Mermel LA, Heard SO. ; 5-FU Catheter Study Group. Anti-infective external coating of central venous catheters: a randomized, noninferiority trial comparing 5-fluorouracil with chlorhexidine/silver sulfadiazine in preventing catheter colonization. Crit Care Med 2010; 38 (11) 2095-2102
  • 70 Soo VWC, Kwan BW, Quezada H. , et al. Repurposing of anticancer drugs for the treatment of bacterial infections. Curr Top Med Chem 2017; 17 (10) 1157-1176
  • 71 Raafat D, Otto M, Reppschläger K, Iqbal J, Holtfreter S. Fighting Staphylococcus aureus biofilms with monoclonal antibodies. Trends Microbiol 2019; 27 (04) 303-322
  • 72 Yang Y, Qian M, Yi S. , et al. Monoclonal antibody targeting Staphylococcus aureus surface protein a (SasA) protect against Staphylococcus aureus sepsis and peritonitis in mice. PLoS One 2016; 11 (02) e0149460
  • 73 Varshney AK, Kuzmicheva GA, Lin J. , et al. A natural human monoclonal antibody targeting Staphylococcus protein A protects against Staphylococcus aureus bacteremia. PLoS One 2018; 13 (01) e0190537
  • 74 Takeda S, Pier GB, Kojima Y. , et al. Protection against endocarditis due to Staphylococcus epidermidis by immunization with capsular polysaccharide/adhesin. Circulation 1991; 84 (06) 2539-2546
  • 75 França A, Vilanova M, Cerca N, Pier GB. Monoclonal antibody raised against PNAG has variable effects on static S. epidermidis biofilm accumulation in vitro. Int J Biol Sci 2013; 9 (05) 518-520
  • 76 Broekhuizen CAN, de Boer L, Schipper K. , et al. The influence of antibodies on Staphylococcus epidermidis adherence to polyvinylpyrrolidone-coated silicone elastomer in experimental biomaterial-associated infection in mice. Biomaterials 2009; 30 (32) 6444-6450
  • 77 Shahrooei M, Hira V, Khodaparast L. , et al. Vaccination with SesC decreases Staphylococcus epidermidis biofilm formation. Infect Immun 2012; 80 (10) 3660-3668
  • 78 Shahrooei M, Hira V, Stijlemans B, Merckx R, Hermans PWM, Van Eldere J. Inhibition of Staphylococcus epidermidis biofilm formation by rabbit polyclonal antibodies against the SesC protein. Infect Immun 2009; 77 (09) 3670-3678
  • 79 Patel M, Kaufman DA. Anti-lipoteichoic acid monoclonal antibody (pagibaximab) studies for the prevention of Staphylococcal bloodstream infections in preterm infants. Expert Opin Biol Ther 2015; 15 (04) 595-600
  • 80 Zaidi S, Misba L, Khan AU. Nano-therapeutics: a revolution in infection control in post antibiotic era. Nanomedicine (Lond) 2017; 13 (07) 2281-2301
  • 81 Qayyum S, Khan AU. Biofabrication of broad range antibacterial and antibiofilm silver nanoparticles. IET Nanobiotechnol 2016; 10 (05) 349-357
  • 82 Li Y-J, Harroun SG, Su Y-C. , et al. Synthesis of self-assembled spermidine-carbon quantum dots effective against multidrug-resistant bacteria. Adv Healthc Mater 2016; 5 (19) 2545-2554
  • 83 Donlan RM. Preventing biofilms of clinically relevant organisms using bacteriophage. Trends Microbiol 2009; 17 (02) 66-72
  • 84 Azeredo J, Sutherland IW. The use of phages for the removal of infectious biofilms. Curr Pharm Biotechnol 2008; 9 (04) 261-266
  • 85 Yilmaz C, Colak M, Yilmaz BC, Ersoz G, Kutateladze M, Gozlugol M. Bacteriophage therapy in implant-related infections: an experimental study. J Bone Joint Surg Am 2013; 95 (02) 117-125
  • 86 Rose T, Verbeken G, Vos DD. , et al. Experimental phage therapy of burn wound infection: difficult first steps. Int J Burns Trauma 2014; 4 (02) 66-73
  • 87 Rhoads DD, Wolcott RD, Kuskowski MA, Wolcott BM, Ward LS, Sulakvelidze A. Bacteriophage therapy of venous leg ulcers in humans: results of a phase I safety trial. J Wound Care 2009; 18 (06) 237-238 , 240–243
  • 88 Wright A, Hawkins CH, Anggård 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 (04) 349-357
  • 89 Kishor C, Mishra RR, Saraf SK, Kumar M, Srivastav AK, Nath G. Phage therapy of staphylococcal chronic osteomyelitis in experimental animal model. Indian J Med Res 2016; 143 (01) 87-94
  • 90 Kaur S, Harjai K, Chhibber S. In vivo assessment of phage and linezolid based implant coatings for treatment of methicillin resistant S. aureus (MRSA) mediated orthopaedic device related infections. PLoS One 2016; 11 (06) e0157626
  • 91 Akanda ZZ, Taha M, Abdelbary H. Current review-the rise of bacteriophage as a unique therapeutic platform in treating peri-prosthetic joint infections. J Orthop Res 2018; 36 (04) 1051-1060
  • 92 Schooley RT, Biswas B, Gill JJ. , et al. Development and use of personalized bacteriophage-based therapeutic cocktails to treat a patient with a disseminated resistant Acinetobacter baumannii infection. Antimicrob Agents Chemother 2017; 61 (10) e00954-17
  • 93 Kaplan JB, Ragunath C, Velliyagounder K, Fine DH, Ramasubbu N. Enzymatic detachment of Staphylococcus epidermidis biofilms. Antimicrob Agents Chemother 2004; 48 (07) 2633-2636
  • 94 Vuong C, Kocianova S, Voyich JM. , et al. A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 2004; 279 (52) 54881-54886
  • 95 Arciola CR, Montanaro L, Costerton JW. New trends in diagnosis and control strategies for implant infections. Int J Artif Organs 2011; 34 (09) 727-736
  • 96 Kaplan JB. Therapeutic potential of biofilm-dispersing enzymes. Int J Artif Organs 2009; 32 (09) 545-554
  • 97 Darouiche RO, Mansouri MD, Gawande PV, Madhyastha S. Antimicrobial and antibiofilm efficacy of triclosan and DispersinB combination. J Antimicrob Chemother 2009; 64 (01) 88-93
  • 98 Donelli G, Francolini I, Romoli D. , et al. Synergistic activity of dispersin B and cefamandole nafate in inhibition of Staphylococcal biofilm growth on polyurethanes. Antimicrob Agents Chemother 2007; 51 (08) 2733-2740
  • 99 Izano EA, Amarante MA, Kher WB, Kaplan JB. Differential roles of poly-N-acetylglucosamine surface polysaccharide and extracellular DNA in Staphylococcus aureus and Staphylococcus epidermidis biofilms. Appl Environ Microbiol 2008; 74 (02) 470-476
  • 100 Thomas VC, Thurlow LR, Boyle D, Hancock LE. Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 2008; 190 (16) 5690-5698
  • 101 Whitchurch CB, Tolker-Nielsen T, Ragas PC, Mattick JS. Extracellular DNA required for bacterial biofilm formation. Science 2002; 295 (5559): 1487
  • 102 Castano AP, Demidova TN, Hamblin MR. Mechanisms in photodynamic therapy: part two-cellular signaling, cell metabolism and modes of cell death. Photodiagn Photodyn Ther 2005; 2 (01) 1-23
  • 103 Briggs T, Blunn G, Hislop S. , et al. Antimicrobial photodynamic therapy-a promising treatment for prosthetic joint infections. Lasers Med Sci 2018; 33 (03) 523-532
  • 104 Giannelli M, Landini G, Materassi F. , et al. Effects of photodynamic laser and violet-blue led irradiation on Staphylococcus aureus biofilm and Escherichia coli lipopolysaccharide attached to moderately rough titanium surface: in vitro study. Lasers Med Sci 2017; 32 (04) 857-864
  • 105 Hameister R, Lim CT, Lohmann CH, Wang W, Singh G. What is the role of diagnostic and therapeutic sonication in periprosthetic joint infections?. J Arthroplasty 2018; 33 (08) 2575-2581
  • 106 Ensing GT, Roeder BL, Nelson JL. , et al. Effect of pulsed ultrasound in combination with gentamicin on bacterial viability in biofilms on bone cements in vivo. J Appl Microbiol 2005; 99 (03) 443-448
  • 107 Carmen JC, Roeder BL, Nelson JL. , et al. Treatment of biofilm infections on implants with low-frequency ultrasound and antibiotics. Am J Infect Control 2005; 33 (02) 78-82
  • 108 Wanner S, Gstöttner M, Meirer R, Hausdorfer J, Fille M, Stöckl B. Low-energy shock waves enhance the susceptibility of Staphylococcal biofilms to antimicrobial agents in vitro. J Bone Joint Surg Br 2011; 93 (06) 824-827
  • 109 Yu H, Chen S, Cao P. Synergistic bactericidal effects and mechanisms of low intensity ultrasound and antibiotics against bacteria: a review. Ultrason Sonochem 2012; 19 (03) 377-382
  • 110 Roe D, Karandikar B, Bonn-Savage N, Gibbins B, Roullet J-B. Antimicrobial surface functionalization of plastic catheters by silver nanoparticles. J Antimicrob Chemother 2008; 61 (04) 869-876 4
  • 111 Secinti KD, Özalp H, Attar A, Sargon MF. Nanoparticle silver ion coatings inhibit biofilm formation on titanium implants. J Clin Neurosci 2011; 18 (03) 391-395
  • 112 Ueno M, Miyamoto H, Tsukamoto M. , et al. Silver-containing hydroxyapatite coating reduces biofilm formation by methicillin-resistant Staphylococcus aureus in vitro and in vivo. BioMed Res Int 2016; 2016: 8070597
  • 113 Eto S, Kawano S, Someya S, Miyamoto H, Sonohata M, Mawatari M. First clinical experience with thermal-sprayed silver oxide-containing hydroxyapatite coating implant. J Arthroplasty 2016; 31 (07) 1498-1503
  • 114 Inoue D, Kabata T, Kajino Y, Shirai T, Tsuchiya H. Iodine-supported titanium implants have good antimicrobial attachment effects. J Orthop Sci 2019; 24 (03) 548-551
  • 115 Capuano N, Logoluso N, Gallazzi E, Drago L, Romanò CL. One-stage exchange with antibacterial hydrogel coated implants provides similar results to two-stage revision, without the coating, for the treatment of peri-prosthetic infection. Knee Surg Sports Traumatol Arthrosc 2018; 26 (11) 3362-3367
  • 116 Logoluso N, Drago L, Gallazzi E, George DA, Morelli I, Romanò CL. Calcium-based, antibiotic-loaded bone substitute as an implant coating: a pilot clinical study. J Bone Jt Infect 2016; 1: 59-64
  • 117 Thompson K, Petkov S, Zeiter S. , et al. Intraoperative loading of calcium phosphate-coated implants with gentamicin prevents experimental Staphylococcus aureus infection in vivo. PLoS One 2019; 14 (02) e0210402
  • 118 Harris MA, Beenken KE, Smeltzer MS, Haggard WO, Jennings JA. Phosphatidylcholine coatings deliver local antimicrobials and reduce infection in a murine model: a preliminary study. Clin Orthop Relat Res 2017; 475 (07) 1847-1853
  • 119 Gao G, Lange D, Hilpert K. , et al. The biocompatibility and biofilm resistance of implant coatings based on hydrophilic polymer brushes conjugated with antimicrobial peptides. Biomaterials 2011; 32 (16) 3899-3909
  • 120 Stewart S, Barr S, Engiles J. , et al. Vancomycin-modified implant surface inhibits biofilm formation and supports bone-healing in an infected osteotomy model in sheep: a proof-of-concept study. J Bone Joint Surg Am 2012; 94 (15) 1406-1415
  • 121 Yoshinari M, Kato T, Matsuzaka K, Hayakawa T, Shiba K. Prevention of biofilm formation on titanium surfaces modified with conjugated molecules comprised of antimicrobial and titanium-binding peptides. Biofouling 2010; 26 (01) 103-110
  • 122 Steindler L, Venturi V. Detection of quorum-sensing N-acyl homoserine lactone signal molecules by bacterial biosensors. FEMS Microbiol Lett 2007; 266 (01) 1-9
  • 123 Churchill MEA, Chen L. Structural basis of acyl-homoserine lactone-dependent signaling. Chem Rev 2011; 111 (01) 68-85
  • 124 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 (06) 1054-1061
  • 125 Zhu J, Kaufmann GF. Quo vadis quorum quenching?. Curr Opin Pharmacol 2013; 13 (05) 688-698
  • 126 Josefsson E, Hartford O, O'Brien L, Patti JM, Foster T. Protection against experimental Staphylococcus aureus arthritis by vaccination with clumping factor A, a novel virulence determinant. J Infect Dis 2001; 184 (12) 1572-1580
  • 127 Kuklin NA, Clark DJ, Secore S. , et al. A novel Staphylococcus aureus vaccine: iron surface determinant B induces rapid antibody responses in rhesus macaques and specific increased survival in a murine S. aureus sepsis model. Infect Immun 2006; 74 (04) 2215-2223
  • 128 Brady RA, O'May GA, Leid JG, Prior ML, Costerton JW, Shirtliff ME. Resolution of Staphylococcus aureus biofilm infection using vaccination and antibiotic treatment. Infect Immun 2011; 79 (04) 1797-1803
  • 129 Fowler Jr VG, Proctor RA. Where does a Staphylococcus aureus vaccine stand?. Clin Microbiol Infect 2014; 20 (05) (Suppl. 05) 66-75
  • 130 Independent data monitoring committee recommends discontinuation of the phase 2b STRIVE clinical trial of Staphylococcus aureus vaccine following planned interim analysis. Available at: https://www.pfizer.com/news/press-release/press-release-detail/independent_data_monitoring_committee_recommends_discontinuation_of_the_phase_2b_strive_clinical_trial_of_staphylococcus_aureus_vaccine_following_planned_interim_analysis . Accessed October 14, 2019