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Mechanisms of Bacterial Colonization of Implants and Host Response

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A Modern Approach to Biofilm-Related Orthopaedic Implant Infections

Part of the book series: Advances in Experimental Medicine and Biology ((AMIDPH,volume 971))

Abstract

The review focuses on the current knowledge and the most pertinent hypotheses regarding the local host immune response as the key factor for the pathogenesis of implant-associated infections. Although bacterial biofilms have long been recognized as causative agents, the link between the infection and the devastating inflammatory response, particularly the localized tissue destruction and bone degradation is less well understood. Understanding these consequences of infection, however, is of utmost importance, because suppressing inflammation and preventing bone destruction could be a novel, alternative therapeutic option in cases when eradicating the infections fails.

The authors state that there is no actual or potential conflict of interest regarding the study.

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References

  • Agarwal A, Singh KP, Jain A (2010) Medical significance and management of staphylococcal biofilm. FEMS Immunol Med Microbiol 58:147–160

    Article  CAS  PubMed  Google Scholar 

  • Arciola CR (2009) New concepts and new weapons in implant infections. Int J Artif Organs 32:533–536

    PubMed  Google Scholar 

  • Armengaud M (1976) Bacterial infections and immunosuppression. Sem Hop 52(2):91–97

    CAS  PubMed  Google Scholar 

  • Beloin C, Renard S, Ghigo JM et al (2014) Novel approaches to combat bacterial biofilms. Curr Opin Pharmacol 18:61–68

    Article  CAS  PubMed  Google Scholar 

  • Berliner N, Horwitz M, Loughran TP (2004) Congenital and acquired neutropenia. Hematology Am Soc Hematol Educ Program, 63–79

    Google Scholar 

  • Bjarnsholt T, Høiby N, Donelli G et al (2012) Understanding biofilms – are we there yet? FEMS Immunol Med Microbiol 65(2):125–126

    Article  CAS  PubMed  Google Scholar 

  • Bjarnsholt T, Alhede M, Eickhardt-Sørensen SR et al (2013) The in vivo biofilm. Trends Microbiol 21(9):466–474

    Article  CAS  PubMed  Google Scholar 

  • Bowler PG (2002) Wound pathophysiology, infection and therapeutic options. Ann Med 34(6):419–427

    Article  CAS  PubMed  Google Scholar 

  • Busscher HJ, van der Mei HC, Subbiahdoss G (2012) Biomaterial-associated infection: locating the finish line in the race for the surface. Sci Transl Med 4(153):153rv10

    Article  PubMed  Google Scholar 

  • Büttner H, Mack D, Rohde H (2015) Structural basis of Staphylococcus epidermidis biofilm formation: mechanisms and molecular interactions. Front Cell Infect Microbiol. doi:10.3389/fcimb.2015.00014

    PubMed  PubMed Central  Google Scholar 

  • Chun CK, Ozer EA, Welsh MJ et al (2004) Inactivation of a pseudomonas aeruginosa quorum-sensing signal by human airway epithelia. Proc Natl Acad Sci U S A 101(10):3587–3590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costerton JW, Stewart PS, Greenberg EP (1999) Bacterial biofilms: a common cause of persistent infections. Science 284:1318–1326

    Article  CAS  PubMed  Google Scholar 

  • Costerton JW, Montanaro L, Arciola CR (2005) Biofilm in implant infections: its production and regulation. Int J Artif Organs 28:1062–1068

    CAS  PubMed  Google Scholar 

  • Dallegri F, Ottonello L (1997) Tissue injury in neutrophilic inflammation. Inflamm Res 46:382–391

    Article  CAS  PubMed  Google Scholar 

  • Dapunt U, Giese T, Lasitschka F et al (2014a) Osteoclast generation and cytokine profile at prosthetic interface: a study on tissue of patients with aseptic loosening or implant-associated infections. Eur J Inflamm 12:147–159

    Article  CAS  Google Scholar 

  • Dapunt U, Lehner B, Burckhardt I et al (2014b) Evaluation of implant sonication as a diagnostic tool in implant-associated infections. J Appl Biomat Funct Mater 12:135–140

    Google Scholar 

  • Dapunt U, Giese T, Maurer S et al (2015) Neutrophil-derived MRP-14 is up-regulated in infectious osteomyelitis and stimulates osteoclast generation. J Leukoc Biol 98(4):575–582

    Article  CAS  PubMed  Google Scholar 

  • Dapunt U, Giese T, Stegmaier S et al (2016) The osteoblast as an inflammatory cell: production of cytokines in response to bacteria and components of bacterial biofilms. BMC Musculoskelet Disord. doi:10.1186/s12891-016-1091-y

    PubMed  PubMed Central  Google Scholar 

  • Dickschat JS (2010) Quorum sensing and bacterial biofilms. Nat Prod Rep 27(3):343–369

    Article  CAS  PubMed  Google Scholar 

  • Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Doria A, Canova M, Tonon M et al (2008) Infections as triggers and complications of systemic lupus erythematosus. Autoimm Rev 8(1):24–28

    Article  CAS  Google Scholar 

  • Drago L, De Vecchi E, Mattina R et al (2013) Activity of N-acetyl-L-cysteine against biofilm of Staphylococcus aureus and Pseudomonas aeruginosa on orthopaedic prosthetic materials. Int J Artif Organs 36(1):39–46

    Article  PubMed  Google Scholar 

  • Dumville JC, McFarlane E, Edwards P et al (2015) Preoperative skin antiseptics for preventing surgical wound infections after clean surgery. Cochrane Database Syst Rev. doi:10.1002/14651858.CD003949.pub4

    Google Scholar 

  • Faurschou M, Borregaard N (2003) Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 5(14):1317–1327

    Article  CAS  PubMed  Google Scholar 

  • Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633

    CAS  PubMed  Google Scholar 

  • Foster TJ, Geoghegan JA, Ganesh VK et al (2014) Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nat Rev Microbiol 12(1):49–62

    Article  CAS  PubMed  Google Scholar 

  • Francolini I, Donelli G, Crisante F (2015) Antimicrobial polymers for anti-biofilm medical devices: state-of-art and perspectives. Adv Exp Med Biol 831:93–117

    Article  PubMed  Google Scholar 

  • Gaida MM, Mayer B, Stegmaier S (2012) Polymorphonuclear neutrophils in osteomyelitis: link to osteoclast generation and bone resorption. Eur J Inflamm 10:413–426

    Article  CAS  Google Scholar 

  • Garg N, Manchanda G, Kumar A (2014) Bacterial quorum sensing: circuits and apllications. Antonie Van Leeuwenhoek 105(2):289–305

    Article  PubMed  Google Scholar 

  • Gbejuade HO, Lovering AM, Webb JC (2015) The role of microbial biofilms in prosthetic joint infections. Acta Orthop 86:147–158

    Article  PubMed  PubMed Central  Google Scholar 

  • Goodman SB, Yao Z, Keeney M et al (2013) The future of biologic coatings for orthopaedic implants. Biomaterials 34:3174–3183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenberg EP (2003) Bacterial communication and group behavior. J Clin Invest 112(9):1288–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gristina AG (1987) Biomaterial-centered infection: microbial adhesion versus tissue integration. Science 237:1588–1595

    Article  CAS  PubMed  Google Scholar 

  • Günther F, Wabnitz G, Stroh P et al (2009) Host defence against Staphylococcus aureus biofilm infection: phagocytosis of biofilms by polymorphonuclear neutrophils (PMN). Mol Immunol 46:1805–1813

    Article  PubMed  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108

    Article  CAS  PubMed  Google Scholar 

  • Hänsch GM (2012a) Host defence against bacterial biofilms: “mission impossible”? ISRN Immunol. doi:10.5402/2012/853123

    Google Scholar 

  • Hänsch GM (2012b) Molecular eavesdropping: phagocytic cells spy on bacterial communication. J Leukoc Biol 91:3–5

    Article  PubMed  Google Scholar 

  • Harmsen M, Yang L, Pamp SJ et al (2010) An update on Pseudomonas aeruginosa biofilm formation, tolerance, and dispersal. FEMS Immunol Med Microbiol 59:253–268

    Article  CAS  PubMed  Google Scholar 

  • Hastings JW (2004) Bacterial quorum-sensing signals are inactivated by mammalian cells. Proc Natl Acad Sci U S A 101(12):3993–3994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heilmann C (2011) Adhesion mechanisms of staphylococci. Adv Exp Med Biol 715:105–123

    Article  CAS  PubMed  Google Scholar 

  • Jefferson KK (2004) What drives bacteria to produce a biofilm? FEMS Microbiol Lett 236(2):163–173

    Article  CAS  PubMed  Google Scholar 

  • Karatan E, Watnick P (2009) Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol Mol Biol Rev 73:310–347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karauzum H, Datta K (2016) Adaptive immunity against staphylococcus aureus. Curr Top Microbiol Immunol. doi:10.1007/82_2016_1

    PubMed  Google Scholar 

  • Kobayashi SD, Voyich JM, DeLeo FR (2003) Regulation of the neutrophil-mediated inflammatory response to infection. Microbes Infect 5(14):1317–1327

    Article  Google Scholar 

  • Lee WL, Harrison RE, Grinstein S (2003) Phagocytosis by neutrophils. Microbes Infect 5(14):1299–1306

    Article  CAS  PubMed  Google Scholar 

  • Levy DM, Wetters NG, Levine BR (2016) Prevention of periprosthetic joint infections of the hip and knee. Am J Orthop 45(5):E299–E307

    PubMed  Google Scholar 

  • Lourenco A, Coenye T, Goeres DM et al (2014) Minimum information about a biofilm experiment (MIABiE): standards for reporting experiments and data on sessile microbial communities living at interfaces. Pathog Dis 70(3):250–256

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch SA, Robertson GT (2008) Bacterial and fungal biofilm infections. Ann Rev Med 59:415–428

    Article  CAS  PubMed  Google Scholar 

  • Marriott I (2004) Osteoblast responses to bacterial pathogens. Immunol Res 30(3):291–308

    Article  CAS  PubMed  Google Scholar 

  • Maurer S, Wabnitz GH, Kahle NA et al (2015) Tasting Pseudomonas aeruginosa biofilms: human neutrophils express the bitter receptor T2R38 as sensor for the quorum sensing molecule N-(3.oxododecanoyl)-I-homoserine lactone. Front Immunol. doi:10.3389/fimmu.2015.00369

    PubMed  PubMed Central  Google Scholar 

  • McLean RJ, Lam JS, Graham LL (2012) Training the biofilm generation – a tribute to J.W. Costerton. J Bacteriol 194:6706–6711

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyle E, Stroh P, Günther F et al (2010) Destruction of bacterial biofilms by polymorphonuclear neutrophils: relative contribution of phagocytosis, DNA release, and degranulation. Int J Artif Organs 33:608–620

    CAS  PubMed  Google Scholar 

  • Moermann M, Thederan M, Nackchbandi I et al (2008) Lipopolysaccharides (LPS) induce the differentiation of human monocytes to osteoclasts in a tumour necrosis factor (TNF) α-dependent manner: a link between infection and pathological bone resorption. Mol Immunol 45:3330–3337

    Article  CAS  Google Scholar 

  • Nagar E, Schwarz R (2015) To be or not to be planktonic? Self-inhibition of biofilm development. Environ Microbiol 17(5):1477–1486

    Article  CAS  PubMed  Google Scholar 

  • Neut D, van Horn JR, van Kooten TG (2003) Detection of biomaterial-associated infections in orthopaedic joint implants. Clin Orthop 413:261–268

    Article  Google Scholar 

  • Obst U, Marten SM, Niessner C et al (2012) Diversity of patients microflora on orthopaedic and dental implants. Int J Artif Organs 35:727–734

    CAS  PubMed  Google Scholar 

  • Olsen I (2015) Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis 34:877–886

    Article  CAS  PubMed  Google Scholar 

  • O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79

    Article  PubMed  Google Scholar 

  • Otto M (2009) Staphylococcus epidermidis – the “accidental” pathogen. Nat Rev Microbiol 7:555–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Otto M (2014) Physical stress and bacterial colonization. FEMS Microbiol Rev 38(6):1250–1257

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pavithra D, Doble M (2008) Biofilm formation, bacterial adhesion and host response on polymeric implants – issues and prevention. Biomed Mater. doi:10.1088/1748-6041/3/3/034003

    PubMed  Google Scholar 

  • Percival SL, McCarty SM, Lipsky B (2015) Biofilms and wounds: an overview of the evidence. Adv Wound Care (New Rochelle) 4(7):373–381

    Article  Google Scholar 

  • Persat A, Nadell CD, Kim MK et al (2015) The mechanical world of bacteria. Cell 161(5):988–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rendueles O, Ghigo JM (2012) Multi-species biofilms: how to avoid unfriendly neighbors. FEMS Microbiol Rev 36(5):972–989

    Article  CAS  PubMed  Google Scholar 

  • Roberts AE, Kragh KN, Bjarnsholt T (2015) The limitations of in vitro experimentation in understanding biofilms and chronic infection. J Mol Biol 427(23):3646–3661

    Article  CAS  PubMed  Google Scholar 

  • Robins EV (1989) Immunosuppression of the burned patient. Crit Care Nurs Clin North Am 1(4):767–774

    CAS  PubMed  Google Scholar 

  • Rochford ET, Richards RG, Moriarty TF (2012) Influence of material on the development of device-associated infections. Clin Microbiol Infect 18(12):1162–1167

    Article  CAS  PubMed  Google Scholar 

  • Romano CL, Scarponi S, Gallazzi E et al (2015) Antibacterial coating of implant in orthopaedics and trauma: a classification proposal in an evolving panorama. J Orthop Surg Res. doi:10.1186/s13018-015-0294-5

    PubMed  PubMed Central  Google Scholar 

  • Sanchez CJ Jr, Ward CL, Romano DR et al (2013) Staphylococcus aureus biofilms decrease osteoblast viability, inhibits osteogenic differentiation, and increases bone resorption in vitro. BMC Musculoskelet Disord. doi:10.1186/1471-2474-14-187

    PubMed  PubMed Central  Google Scholar 

  • Savill J (1997) Apoptosis in resolution of inflammation. J Leukoc Biol 61(4):375–380

    CAS  PubMed  Google Scholar 

  • Schierholz JM, Beuth J (2001) Implant infections: a haven for opportunistic bacteria. J Hosp Infect 49:87–93

    Article  CAS  PubMed  Google Scholar 

  • Schmidmaier G, Lucke M, Wildemann B et al (2006) Prophylaxis and treatment of implant-related infections by antibiotic-coated implants: a review. Injury 37(Suppl2):S105–S112

    Article  PubMed  Google Scholar 

  • Shadyab AH, Crum-Cianflone NF (2012) Methicillin-Resistant Staphylococcus Aureus (MRSA) infections among HIV-infected persons in the era of highly active antiretroviral therapy. A review of the literature. HIV Med 13(6):319–332

    Article  CAS  PubMed  Google Scholar 

  • Sherry L, Rajendran R, Lappin DF et al (2014) Biofilms formed by Candida albicans bloodstream isolates display phenotypic and transcriptional heterogeneity that are associated with resistance and pathogenicity. BMC Microbiol. doi:10.1186/1471-2180-14-182

    Google Scholar 

  • Shunmugaperumal T (2010) Microbial colonization of medical devices and novel preventive strategies. Recent Pat Drug Deliv Formul 4(2):153–173

    Article  CAS  PubMed  Google Scholar 

  • Stoodley P, Sauer K, Davies D et al (2002) Biofilms as complex differential communities. Ann Rev Microbiol 56:187–209

    Article  CAS  Google Scholar 

  • Sutherland IW (2001) The biofilm matrix – an immobilized but dynamic microbial environment. Trends Microbiol 9(5):222–227

    Article  CAS  PubMed  Google Scholar 

  • Tande AJ, Patel R (2014) Prosthetic joint infection. Clin Microbiol Rev 27:302–345

    Article  PubMed  PubMed Central  Google Scholar 

  • Tanner J, Dumville JC, Norman G et al (2016) Surgical hand antisepsis to reduce surgical site infection. Cochrane Database Syst Rev. doi:10.1002/14651858.CD004288.pub3

    Google Scholar 

  • Trampuz A, Piper KE, Jacobson MJ et al (2007) Sonication of removed hip and knee prostheses for diagnosis of infection. N Engl J Med 357:654–663

    Article  CAS  PubMed  Google Scholar 

  • Van der Mei HC, Busscher HJ (2012) Bacterial cell surface heterogeneity: a pathogen’s disguise. PLoS Path. doi:10.1371/journal.ppat.1002821

    Google Scholar 

  • Vikström E, Magnusson KE, Pivoriunas A (2005) The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone stimulates phagocytic activity in human macrophages through the p38 MAPK pathway. Microbes Infect 7(15):1512–1518

    Article  PubMed  Google Scholar 

  • Wagner C, Hänsch GM (2005) Born to kill – bound to die: the role of leukocytes in host defence. Quaderni di Infezioni Osteoarticolari April 3–9

    Google Scholar 

  • Wagner C, Hänsch GM (2015) Pathophysiology of implant-associated infections. From biofilm to osteolysis and septic loosening. Orthopade 44:967–973

    Article  CAS  PubMed  Google Scholar 

  • Wagner C, Kondella K, Bernschneider T et al (2003) Post-traumatic osteomyelitis: analysis of inflammatory cells recruited into the site of infection. Shock 20:501–510

    Article  Google Scholar 

  • Wagner C, Kaksa A, Müller W et al (2004) Polymorphonuclear neutrophils (PMN) in posttraumatic osteomyelitis: cells recovered from the inflamed site lack chemotactic activity but generate superoxides. Shock 22:108–115

    Article  CAS  PubMed  Google Scholar 

  • Wagner C, Obst U, Hänsch GM (2005) The implant-associated posttraumatic osteomyelitis: collateral damage by the local host defence? Int J Artif Organs 28:1172–1180

    CAS  PubMed  Google Scholar 

  • Wagner C, Heck D, Lautenschläger K et al (2006) T-lymphocytes in implant-associated posttraumatic osteomyelitis: identification of cytotoxic T-effector cells at the site of infection. Shock 25:241–246

    Article  CAS  PubMed  Google Scholar 

  • Wagner C, Kotsougiani D, Pioch M et al (2008) T lymphocytes in acute bacterial infection: increased prevalence of CD11b+ cells in the peripheral blood and recruitment to the infected sit. Immunology 125:503–509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagner C, Aytac S, Hänsch GM (2011) Biofilm growth on implants: bacteria prefer plasma coats. Int J Artif Organs 34:811–817

    Article  CAS  PubMed  Google Scholar 

  • Ward PA, Lentsch AB (1999) The acute inflammatory response and its regulation. Arch Surg 134:666–669

    Article  CAS  PubMed  Google Scholar 

  • Wilkins M, Hall-Stoodley L, Allan RN et al (2014) New approaches to the treatment of biofilm-related infections. J Infect 69(Suppl1):S47–S52

    Article  PubMed  Google Scholar 

  • Williams P, Winzer K, Chan WC et al (2007) Look who’s talking: communication and quorum sensing in the bacterial world. Phil Trans R Soc B 362:1119–1134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wolcott R, Costerton JW, Raoult D et al (2013) The polymicrobial nature of biofilm infection. Clin Microbiol Infect 19:107–112

    Article  CAS  PubMed  Google Scholar 

  • Wuertz S, Okabe S, Hausner M (2004) Microbial communities and their interactions in biofilm systems: an overview. Water Sci Technol 49(11–12):327–336

    CAS  PubMed  Google Scholar 

  • Yano MH, Klatau GB, da Silva CB et al (2014) Improved diagnosis of infection associated with osteosynthesis by use of sonication of fracture fixation implants. J Clin Microbiol 52:4176–4182

    Article  PubMed  PubMed Central  Google Scholar 

  • Zimmerli W, Sendi P (2011) Pathogenesis of implant-associated infection: the role of the host. Semin Immunopathol 33(3):295–306

    Article  CAS  PubMed  Google Scholar 

  • Zimmermann S, Wagner C, Müller W et al (2006) Induction of neutrophil chemotaxis by the quorum-sensing molecule N-(3-oxododecanoyl)-L-homoserine lactone. Infect Immun 74(10):5687–5692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Wagner, C., Hänsch, G.M. (2016). Mechanisms of Bacterial Colonization of Implants and Host Response. In: Drago, L. (eds) A Modern Approach to Biofilm-Related Orthopaedic Implant Infections. Advances in Experimental Medicine and Biology(), vol 971. Springer, Cham. https://doi.org/10.1007/5584_2016_173

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