Abstract
The demand for joint replacement surgery is continuously increasing with rising costs for hospitals and healthcare systems. Staphylococci are the most prevalent etiological agents of orthopedic infections. After an initial adhesin-mediated implant colonization, Staphylococcus aureus and Staphylococcus epidermidis produce biofilm. Biofilm formation proceeds as a four-step process: (1) initial attachment of bacterial cells; (2) cell aggregation and accumulation in multiple cell layers; (3) biofilm maturation and (4) detachment of cells from the biofilm into a planktonic state to initiate a new cycle of biofilm formation elsewhere. The encasing of bacteria in biofilms gives rise to insuperable difficulties not only in the treatment of the infection, but also in assessing the state and the nature of the infection using traditional cultural methods. Therefore, DNA-based molecular methods have been developed to provide rapid identification of all microbial pathogens. To combat biofilm-centered implant infections, new strategies are being developed, among which anti-infective or infective-resistant materials are at the forefront. Infection-resistant materials can be based on different approaches: (i) modifying the biomaterial surface to give anti-adhesive properties, (ii) doping the material with antimicrobial substances, (iii) combining anti-adhesive and antimicrobial effects in the same coating, (iv) designing materials able to oppose biofilm formation and support bone repair.
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References
Allesen-Holm M, Barken KB, Yang L et al (2006) A characterization of DNA release in Pseudomonas aeruginosa cultures and biofilms. Mol Microbiol 59(4):1114–1128
Arciola CR, Radin L, Alvergna P, Cenni E, Pizzoferrato A (1993) Heparin surface treatment of poly(methylmethacrylate) alters adhesion of a Staphylococcus aureus strain: utility of bacterial fatty acid analysis. Biomaterials 14(15):1161–1164
Arciola CR, Caramazza R, Pizzoferrato A (1994) In vitro adhesion of Staphylococcus epidermidis on heparin-surface-modified intraocular lenses. J Cataract Refract Surg 20(2):158–161
Arciola CR, Maltarello MC, Cenni E, Pizzoferrato A (1995) Disposable contact lenses and bacterial adhesion. In vitro comparison between ionic/high-water content and non-ionic/low-water content lenses. Biomaterials 16:685–690
Arciola CR, Montanaro L, Caramazza R, Sassoli V, Cavedagna D (1998) Inhibition of bacterial adherence to a high-water-content polymer by a water-soluble, nonsteroidal, anti-inflammatory drug. J Biomed Mater Res 42(1):1–5
Arciola CR, Montanaro L, Moroni A, Giordano M, Pizzoferrato A, Donati ME (1999) Hydroxyapatite-coated orthopaedic screws as infection resistant materials: in vitro study. Biomaterials 20(4):323–327
Arciola CR, Baldassarri L, Montanaro L (2001) Presence of icaA and icaD genes and slime production in a collection of staphylococcal strains from catheter associated infections. J Clin Microbiol 39(6):2151–2156
Arciola CR, Bustanji Y, Conti M, Campoccia D, Baldassarri L, Samorì B, Montanaro L (2003) Staphylococcus epidermidis-fibronectin binding and its inhibition by heparin. Biomaterials 24(18):3013–3019
Arciola CR, An YH, Campoccia D, Donati ME, Montanaro L (2005) Etiology of implant orthopedic infections: a survey on 1027 clinical isolates. Int J Artif Organs 28:1091–1100
Arciola CR, Baldassarri L, Campoccia D et al (2008) Strong biofilm production, antibiotic multi-resistance and high gelE expression in epidemic clones of Enterococcus faecalis from orthopaedic implant infections. Biomaterials 29(5):580–586
Arciola CR, Montanaro L, Costerton JW (2011) New trends in diagnosis and control strategies for implant infections. Int J Artif Organs 34(9):727–736
Arciola CR, Hänsch GM, Visai L, Testoni F, Maurer S, Campoccia D, Selan L, Montanaro L (2012a) Interactions of staphylococci with osteoblasts and phagocytes in the pathogenesis of implant-associated osteomyelitis. Int J Artif Organs 35(10):713–726
Arciola CR, Campoccia D, Speziale P, Montanaro L, Costerton JW (2012b) Biofilm formation in Staphylococcus implant infections. A review of molecular mechanisms and implications for biofilm-resistant materials. Biomaterials 33(26):5967–5982
Bagheri M, Beyermann M, Dathe M (2012) Mode of action of cationic antimicrobial peptides defines the tethering position and the efficacy of biocidal surfaces. Bioconjug Chem 23(1):66–74
Bustanji Y, Arciola CR, Conti M, Mandello E, Montanaro L, Samorí B (2003) Dynamics of the interaction between a fibronectin molecule and a living bacterium under mechanical force. Proc Natl Acad Sci U S A 100(23):13292–13297
Campoccia D, Arciola CR, Cervellati M, Maltarello MC, Montanaro L (2003) In vitro behaviour of bone marrow-derived mesenchymal cells cultured on fluorohydroxyapatite-coated substrata with different roughness. Biomaterials 24:587–596
Campoccia D, Speziale P, Ravaioli S, Cangini I, Rindi S, Pirini V, Montanaro L, Arciola CR (2009) The presence of both bone sialoprotein-binding protein gene and collagen adhesin gene as a typical virulence trait of the major epidemic cluster in isolates from orthopedic implant infections. Biomaterials 30(34):6621–6628
Campoccia D, Montanaro L, Speziale P, Arciola CR (2010) Antibiotic-loaded biomaterials and the risks for the spread of antibiotic resistance following their prophylactic and therapeutic clinical use. Biomaterials 31(25):6363–6377
Campoccia D, Montanaro L, Arciola CR (2013) A review of the biomaterials technologies for infection-resistant surfaces. Biomaterials 34(34):8533–8554
Chavakis T, Wiechmann K, Preissner KT, Herrmann M (2005) Staphylococcus aureus interactions with the endothelium: the role of bacterial “secretable expanded repertoire adhesive molecules” (SERAM) in disturbing host defense systems. Thromb Haemost 94(2):278–285
Corvec S, Portillo ME, Pasticci BM, Borens O, Trampuz A (2012) Epidemiology and new developments in the diagnosis of prosthetic joint infection. Int J Artif Organs 35(10):923–934
Costerton JW, DeMeo P (2011) Discussion. The role of biofilms: are we hitting the right target? Plast Reconstr Surg 127(Suppl 1):36S–37S
Costerton JW, Veeh R, Shirtliff M, Pasmore M, Post JC, Ehrlich GD (2003) The application of biofilm science to the study and control of chronic bacterial infections. J Clin Investig 112(10):1466–1477
Costerton JW, Montanaro L, Arciola CR (2005) Biofilm in implant infections: its production and regulation. Int J Artif Organs 28(11):1062–1068
Costerton JW, Post JC, Ehrlich GD, Hu FZ, Kreft R, Nistico L, Kathju S, Stoodley P, Hall-Stoodley L, Maale G, James G, Sotereanos N, DeMeo P (2011) New methods for the detection of orthopedic and other biofilm infections. FEMS Immunol Med Microbiol 61(2):133–140
Cramton SE, Gerke C, Schnell NF, Nichols WW, Götz F (1999) The intercellular adhesion (ica) locus is present in Staphylococcus aureus and is required for biofilm formation. Infect Immun 67(10):5427–5433
Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penadés JR (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 83:2888–2896
Della Valle C, Visai L, Santin M, Cigada A, Candiani G, Pezzoli D, Arciola CR, Imbriani M, Chiesa R (2012) A novel antibacterial modification treatment of titanium capable to improve osseointegration. Int J Artif Organs 35(10):864–875
Ehrlich GD, DeMeo P, Costerton JW, Winkler H (eds) (2012) Culture-negative orthopedic biofilm infections. Springer Verlag series on biofilms. Berlin Heidelberg
Ehrlich GD, Arciola CR (2012) From Koch’s postulates to biofilm theory. The lesson of Bill Costerton. Int J Artif Organs 35(10):695–699
Ehrlich GD, Post JC (2013) The time is now for gene and genome-based bacterial diagnostics “you say you want a revolution”. JAMA Intern Med 173(15):1405–1406
Ehrlich GD, Hu FZ, Shen K, Stoodley P, Post JC (2005) Bacterial plurality as a general mechanism driving persistence in chronic infections. Clin Orthop Relat Res 437:20–24
Ehrlich GD, Ahmed A, Earl J, Hiller NL, Costerton JW, Stoodley P, Post JC, DeMeo P, Hu FZ (2010) The distributed genome hypothesis as a rubric for understanding evolution in situ during chronic infectious processes. FEMS Immunol Med Microbiol 59(3):269–279
Ehrlich GD, Hu FZ, Sotereanos N, Sewicke J, Parvizi J, Nara PL, Arciola CR (2014) What role do periodontal pathogens play in osteoarthritis and periprosthetic joint infections of the knee? J Appl Biomater Funct Mater 12(1):e13–e20
Esteban J, Sorlí L, Alentorn-Geli E, Puig L, Horcajada JP (2014) Conventional and molecular diagnostic strategies for prosthetic joint infections. Expert Rev Mol Diagn 14(1):83–96
Fitzgerald RH Jr (1995) Infected total hip arthroplasty: diagnosis and treatment. J Am Acad Orthop Surg 3(5):249–262
Foster SJ (1995) Molecular characterization and functional analysis of the major autolysin of Staphylococcus aureus 8325/4. J Bacteriol 177:5723–5725
Fu J, Ji J, Yuan W, Shen J (2005) Construction of anti-adhesive and antibacterial multilayer films via layer-by-layer assembly of heparin and chitosan. Biomaterials 26(33):6684–6692
Ganss B, Kim RH, Sodek J (1999) Bone sialoprotein. Crit Rev Oral Biol Med 10(1):79–98
Geoghegan JA, Corrigan RM, Gruszka DT, Speziale P, O’Gara JP, Potts JR et al (2010) Role of surface protein SasG in biofilm formation by Staphylococcus aureus. J Bacteriol 192:5663–5673
Grandi S, Cassinelli V, Bini M, Saino E, Mustarelli P, Arciola CR, Imbriani M, Visai L (2011) Bone reconstruction: Au nanocomposite bioglasses with antibacterial properties. Int J Artif Organs 34(9):920–928
Greene C, McDevitt D, Francois P, Vaudaux PE, Lew DP, Foster TJ (1995) Adhesion properties of mutants of Staphylococcus aureus defective in fibronectin-binding proteins and studies on the expression of fnb genes. Mol Microbiol 17(6):1143–1152
Hancock REW, Sahl HG (2006) Antimicrobial and host-defense peptides as new anti-infective therapeutic strategies. Nat Biotechol 24:1551–1557
Hansen EN, Zmistowski B, Parvizi J (2012) Periprosthetic joint infection: what is on the horizon? Int J Artif Organs 35(10):935–950
Harris LG, El-Bouri K, Johnston S, Rees E, Frommelt L, Siemssen N, Christner M, Davies AP, Rohde H, Mack D (2010) Rapid identification of staphylococci from prosthetic joint infections using MALDI-TOF mass-spectrometry. Int J Artif Organs 33(9):568–574
Hauck CR, Ohlsen K (2006) Sticky connections: extracellular matrix protein recognition and integrin-mediated cellular invasion by Staphylococcus aureus. Curr Opin Microbiol 9(1):5–11
Heilmann C, Schweitzer O, Gerke C, Vanittanakom N, Mack D, Götz F (1996) Molecular basis of intercellular adhesion in the biofilm-forming Staphylococcus epidermidis. Mol Microbiol 20:1083–1091
Heilmann C, Hussain M, Peters G, Götz F (1997) Evidence for autolysin-mediated primary attachment of Staphylococcus epidermidis to a polystyrene surface. Mol Microbiol 24:1013–1024
Herrmann M, Lai QJ, Albrecht RM, Mosher DF, Proctor RA (1993) Adhesion of Staphylococcus aureus to surface-bound platelets: role of fibrinogen/fibrin and platelet integrins. J Infect Dis 167(2):312–322
Hirschhausen N, Schlesier T, Schmidt MA, Götz F, Peters G, Heilmann C (2010) A novel staphylococcal internalization mechanism involves the major autolysin Atl and heat shock cognate protein Hsc70 as host cell receptor. Cell Microbiol 12:1746–1764
Houston P, Rowe SE, Pozzi C, Waters EM, O’Gara JP (2011) Essential role for the major autolysin in the fibronectin-binding protein-mediated Staphylococcus aureus biofilm phenotype. Infect Immun 79:1153–1165
Hunt LP, Ben-Shlomo Y, Clark EM, Dieppe P, Judge A, MacGregor AJ, Tobias JH, Vernon K, Blom AW, National Joint Registry for England, Wales and Northern Ireland (2013) 90-day mortality after 409,096 total hip replacements for osteoarthritis, from the National Joint Registry for England and Wales: a retrospective analysis. Lancet 382(9898):1097–1104
Jacovides C, Kreft R, Adeli B, Hozack B, Ehrlich GD, Parvizi J (2012) Successful identification of pathogens by polymerase chain reaction (PCR)-based electron spray ionization time-of-flight mass spectrometry (ESI-TOF-MS) in culture-negative periprosthetic joint infection. J Bone Joint Surg 94(24):2247–2254
Kang SJ, Kim DH, Mishig-Ochir T, Lee BJ (2012) Antimicrobial peptides: their physicochemical properties and therapeutic application. Arch Pharm Res 35(3):409–413
Kapadia BH, McElroy MJ, Issa K, Johnson AJ, Bozic KJ, Mont MA (2014) The economic impact of periprosthetic infections following total knee arthroplasty at a specialized tertiary-care center. J Arthroplasty 29(5):929–932
Kurtz SM, Lau E, Schmier J, Ong KL, Zhao K, Parvizi J (2008) Infection burden for hip and knee arthroplasty in the United States. J Arthroplasty 23(7):984–991
Kurtz SM, Lau E, Watson H, Schmier JK, Parvizi J (2012) Economic burden of periprosthetic joint infection in the United States. J Arthroplasty 27(8 Suppl):61–65
Legeay G, Poncin-Epaillard F, Arciola CR (2006) New surfaces with hydrophilic/hydrophobic characteristics in relation to (no)bioadhesion. Int J Artif Organs 29(4):453–461
Leone JM, Hanssen AD (2006) Management of infection at the site of a total knee arthroplasty. Instr Course Lect 55:449–461
Lindeque B, Hartman Z, Noshchenko A, Cruse M (2014) Infection after primary total hip arthroplasty. Orthopedics 37(4):257–265
Mack D, Fischer W, Krokotsch A, Leopold K, Hartmann R, Egge H, Laufs R (1996) The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J Bacteriol 178(1):175
Mack D, Becker P, Chatterjee I, Dobinsky S, Knobloch JK, Peters G, Rohde H, Herrmann M (2004) Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. Int J Med Microbiol 294(2–3):203–212
Montanaro L, Speziale P, Campoccia D, Pirini V, Ravaioli S, Cangini I, Visai L, Arciola CR (2010) Polymorphisms of agr locus correspond to distinct genetic patterns of virulence in Staphylococcus aureus clinical isolates from orthopedic implant infections. J Biomed Mater Res A 94(3):825–832
Montanaro L, Speziale P, Campoccia D, Ravaioli S, Cangini I, Pietrocola G, Giannini S, Arciola CR (2011a) Scenery of Staphylococcus implant infections in orthopedics. Future Microbiol 6(11):1329–1349
Montanaro L, Testoni F, Poggi A, Visai L, Speziale P, Arciola CR (2011b) Emerging pathogenetic mechanisms of the implant-related osteomyelitis by Staphylococcus aureus. Int J Artif Organs 34(9):781–788
Montanaro L, Poggi A, Visai L, Ravaioli S, Campoccia D, Speziale P, Arciola CR (2011c) Extracellular DNA in biofilms. Int J Artif Organs 34(9):824–831
Nemes S, Gordon M, Rogmark C, Rolfson O (2014) Projections of total hip replacement in Sweden from 2013 to 2030. Acta Orthop [Epub ahead of print] PubMed PMID: 24758323
Neoh KG, Kang ET (2011) Combating bacterial colonization on metals via polymer coatings: relevance to marine and medical applications. ACS Appl Mater Interfaces 3(8):2808–2819
O’Gara JP (2007) ica and beyond: biofilm mechanisms and regulation in Staphylococcus epidermidis and Staphylococcus aureus. FEMS Microbiol Lett 270:179–188
Osmon DR, Berbari EF, Berendt AR, Lew D, Zimmerli W, Steckelberg JM, Rao N, Hanssen A, Wilson WR, Infectious Diseases Society of America (2013) Diagnosis and management of prosthetic joint infection: clinical practice guidelines by the Infectious Diseases Society of America. Clin Infect Dis 56(1):e1–e25
Parvizi J, Walinchus L, Adeli B (2011) Molecular diagnostics in periprosthetic joint infection. Int J Artif Organs 34(9):847–855
Parvizi J, Erkocak OF, Della Valle CJ (2014) Culture-negative periprosthetic joint infection. J Bone Joint Surg Am 96(5):430–436
Patti JM, Allen BL, McGavin MJ, Höök M (1994a) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48:585–617
Patti JM, Bremell T, Krajewska-Pietrasik D, Abdelnour A, Tarkowski A, Ryde’n C et al (1994b) The Staphylococcus aureus collagen adhesin is a virulence determinant in experimental septic arthritis. Infect Immun 62(1):152–161
Potter A, Ceotto H, Giambiagi-Demarval M, dos Santos KR, Nes IF, Bastos Mdo C (2009) The gene bap, involved in biofilm production, is present in Staphylococcus spp. strains from nosocomial infections. J Microbiol 47:319–326
Puig-Verdié L, Alentorn-Geli E, González-Cuevas A, Sorlí L, Salvadó M, Alier A, Pelfort X, Portillo ME, Horcajada JP (2013) Implant sonication increases the diagnostic accuracy of infection in patients with delayed, but not early, orthopaedic implant failure. Bone Joint J 95-B(2):244–249
Qin Z, Ou Y, Yang L et al (2007) Role of autolysin-mediated DNA release in biofilm formation of Staphylococcus epidermidis. Microbiology 153(7):2083–2092
Rak M, Barlič-Maganja D, Kavčič M, Trebše R, Cőr A (2013) Comparison of molecular and culture method in diagnosis of prosthetic joint infection. FEMS Microbiol Lett 343(1):42–48
Rohde H, Burandt EC, Siemssen N, Frommelt L, Burdelski C, Wurster S et al (2007) Polysaccharide intercellular adhesin or protein factors in biofilm accumulation of Staphylococcus epidermidis and Staphylococcus aureus isolated from prosthetic hip and knee joint infections. Biomaterials 28:1711–1720
Ryde’n C, Tung HS, Nikolaev V, Engström A, Oldberg A (1997) Staphylococcus aureus causing osteomyelitis binds to a nonapeptide sequence in bone sialoprotein. Biochem J 327(Pt3):825–829
Schinsky MF, Della Valle CJ, Sporer SM, Paprosky WG (2008) Perioperative testing for joint infection in patients undergoing revision total hip arthroplasty. J Bone Joint Surg Am 90(9):1869–1875
Sculco TP (1993) The economic impact of infected total joint arthroplasty. Instr Course Lect 42:349–351
Sinha B, Francois PP, Nu¨sse O, Foti M, Hartford OM, Vaudaux P et al (1999) Fibronectin-binding protein acts as Staphylococcus aureus invasin via fibronectin bridging to integrin α5β1. Cell Microbiol 1(2):101–117
Sittka A, Vogel J (2008) A glimpse at the evolution of virulence control. Cell Host Microbe 4:310–312
Speziale P, Visai L, Rindi S, Pietrocola G, Provenza G, Provenzano M (2008) Prevention and treatment of Staphylococcus biofilms. Curr Med Chem 15(30):3185–3195
Speziale P, Pietrocola G, Rindi S, Provenzano M, Provenza G, Di Poto A, Visai L, Arciola CR (2009) Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host. Future Microbiol 4(10):1337–1352
Tan H, Peng Z, Li Q, Xu X, Guo S, Tang T (2012) The use of quaternised chitosan-loaded PMMA to inhibit biofilm formation and downregulate the virulence-associated gene expression of antibiotic-resistant Staphylococcus. Biomaterials 33:365–377
Tande AJ, Patel R (2014) Prosthetic joint infection. Clin Microbiol Rev 27(2):302–345
Thomas VC, Hancock LE (2009) Suicide and fratricide in bacterial biofilms. Int J Artif Organs 32(9):537–544, Review
Thomas VC, Thurlow LR, Boyle D, Hancock LE (2008) Regulation of autolysis-dependent extracellular DNA release by Enterococcus faecalis extracellular proteases influences biofilm development. J Bacteriol 190(16):5690–5698
Thurlow LR, Hanke ML, Fritz T et al (2011) Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J Immunol 186(11):6585–6596
Tormo MA, Knecht E, Götz F, Lasa I, Penadés JR (2005) Bap dependent biofilm formation by pathogenic species of Staphylococcus: evidence of horizontal gene transfer? Microbiology 151:2465–2475
Trampuz A, Piper KE, Jacobson MJ, Hanssen AD, Unni KK, Osmon DR, Mandrekar JN, Cockerill FR, Steckelberg JM, Greenleaf JF, Patel R (2006) Sonication of explanted prosthetic components in bags for diagnosis of prosthetic joint infection is associated with risk of contamination. J Clin Microbiol 44(2):628–631
Tsaras G, Osmon DR, Mabry T, Lahr B, St Sauveur J, Yawn B, Kurland R, Berbari EF (2012) Incidence, secular trends, and outcomes of prosthetic joint infection: a population-based study, Olmsted county, Minnesota, 1969–2007. Infect Control Hosp Epidemiol 33:1207–1212
Vergara-Irigaray M, Valle J, Merino N, Latasa C, García B, Ruiz de Los Mozos I et al (2009) Relevant role of fibronectin-binding proteins in Staphylococcus aureus biofilm-associated foreign-body infections. Infect Immun 77:3978–3991
Whitehouse JD, Friedman ND, Kirkland KB, Richardson WJ, Sexton DJ (2002) The impact of surgical-site infections following orthopedic surgery at a community hospital and a university hospital: adverse quality of life, excess length of stay, and extra cost. Infect Control Hosp Epidemiol 23(4):183–189
Wolcott R, Dowd S (2011) The role of biofilms: are we hitting the right target? Plast Reconstr Surg 127(Suppl 1):28S–35S
Zhao L, Hu Y, Xu D, Cai K (2014) Surface functionalization of titanium substrates with chitosan-lauric acid conjugate to enhance osteoblas ts functions and inhibit bacteria adhesion. Colloids Surf B Biointerfaces [Epub ahead of print].
Zimmerli W, Trampuz A, Ochsner PE (2004) Prosthetic-joint infections. N Engl J Med 351:1645–1654
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Arciola, C.R., Campoccia, D., Ehrlich, G.D., Montanaro, L. (2015). Biofilm-Based Implant Infections in Orthopaedics. In: Donelli, G. (eds) Biofilm-based Healthcare-associated Infections. Advances in Experimental Medicine and Biology, vol 830. Springer, Cham. https://doi.org/10.1007/978-3-319-11038-7_2
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