Abstract
This study is to establish a rabbit model for human prosthetic joint infection and biofilm formation. Thirty-two healthy adult rabbits were randomly divided into four groups and implanted with stainless steel screws and ultra-high molecular weight polyethylene (UHMWPE) washers in the non-articular surface of the femoral lateral condyle of the right hind knees. The rabbit knee joints were inoculated with 1 mL saline containing 0, 102, 103, 104 CFU of Staphylococcus epidermidis (S. epidermidis) isolated from the patient with total knee arthroplasty (TKA) infection, respectively. On the 14th postoperative day, the UHMWPE washers from the optimal 103 CFU group were further examined. The SEM examination showed a typical biofilm construction that circular S. epidermidis were embedded in a mucous-like matrix. In addition, the LCSM examination showed that the biofilm consisted of the polysaccharide stained bright green fluorescence and S. epidermidis radiating red fluorescence. Thus, we successfully create a rabbit model for prosthetic joint infection and biofilm formation, which should be valuable for biofilm studies.
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References
Kurtz S M, Lau E, Watson H, et al. Economic burden of periprosthetic joint infection in the United States. The Journal of Arthroplasty, 2012, 27(8 Suppl): 61–65
Haenle M, Skripitz C, Mittelmeier W, et al. Economic impact of infected total hip arthroplasty in the German diagnosis-related groups system. Der Orthopade, 2012, 41(6): 467–476
Haenle M, Skripitz C, Mittelmeier W, et al. Economic impact of infected total knee arthroplasty. The Scientific World Journal, 2012, (1): 196515
Kurtz S M, Lau E, Schmier J, et al. Infection burden for hip and knee arthroplasty in the United States. The Journal of Arthroplasty, 2008, 23(7): 984–991
Del Pozo J L, Patel R. Clinical practice. Infection associated with prosthetic joints. The New England Journal of Medicine, 2009, 361(8): 787–794
Phillips J E, Crane T P, Noy M, et al. The incidence of deep prosthetic infections in a specialist orthopaedic hospital: a 15-year prospective survey. The Journal of Bone and Joint Surgery (British Volume), 2006, 88B(7): 943–948
Pulido L, Ghanem E, Joshi A, et al. Periprosthetic joint infection: the incidence, timing, and predisposing factors. Clinical Orthopaedics and Related Research, 2008, 466(7): 1710–1715
Jämsen E, Varonen M, Huhtala H, et al. Incidence of prosthetic joint infections after primary knee arthroplasty. The Journal of Arthroplasty, 2010, 25(1): 87–92
Kurtz S, Ong K, Lau E, et al. Projections of primary and revision hip and knee arthroplasty in the United States from 2005 to 2030. The Journal of Bone and Joint Surgery (American Volume), 2007, 89(4): 780–785
Kurtz S M, Lau E, Schmier J, et al. Infection burden for hip and knee arthroplasty in the United States. The Journal of Arthroplasty, 2008, 23(7): 984–991
Vuong C, Otto M. Staphylococcus epidermidis infections. Microbes and Infection, 2002, 4(4): 481–489
Zimmerli W, Trampuz A, Ochsner P E. Prosthetic-joint infections. The New England Journal of Medicine, 2004, 351(16): 1645–1654
Costerton W, Veeh R, Shirtliff M, et al. The application of biofilm science to the study and control of chronic bacterial infections. Journal of Clinical Investigation, 2003, 112(10): 1466–1477
Høiby N, Ciofu O, Johansen H K, et al. The clinical impact of bacterial biofilms. International Journal of Oral Science, 2011, 3 (2): 55–65
Percival S L, Hill K E, Malic S, et al. Antimicrobial tolerance and the significance of persister cells in recalcitrant chronic wound biofilms. Wound Repair and Regeneration, 2011, 19(1): 1–9
Srinivasan A, Uppuluri P, Lopez-Ribot J, et al. Development of a high-throughput Candida albicans biofilm chip. PLoS ONE, 2011, 6(4): e19036
Zimmerli W, Moser C. Pathogenesis and treatment concepts of orthopaedic biofilm infections. FEMS Immunology and Medical Microbiology, 2012, 65(2): 158–168
Geipel U. Pathogenic organisms in hip joint infections. International Journal of Medical Sciences, 2009, 6(5): 234–240
Pandey R, Berendt A R, Athanasou N A. Histological and microbiological findings in non-infected and infected revision arthroplasty tissues. Archives of Orthopaedic and Trauma Surgery, 2000, 120(10): 570–574
Talsma S S. Biofilms on medical devices. Home Healthcare Nurse, 2007, 25(9): 589–594
Otto M. Staphylococcal biofilms. Current Topics in Microbiology and Immunology, 2008, 322: 207–228
Otto M. Staphylococcus epidermidis—the ‘accidental’ pathogen. Nature Reviews: Microbiology, 2009, 7(8): 555–567
Pribaz J R, Bernthal N M, Billi F, et al. Mouse model of chronic post-arthroplasty infection: noninvasive in vivo bioluminescence imaging to monitor bacterial burden for long-term study. Journal of Orthopaedic Research, 2012, 30(3): 335–340
Scherr T D, Lindgren K E, Schaeffer C R, et al. Mouse model of post-arthroplasty Staphylococcus epidermidis joint infection. Methods in Molecular Biology, 2014, 1106: 173–181
Søe N H, Jensen N V, Nürnberg B M, et al. A novel knee prosthesis model of implant-related osteomyelitis in rats. Acta Orthopaedica, 2013, 84(1): 92–97
Bernthal N M, Stavrakis A I, Billi F, et al. A mouse model of postarthroplasty Staphylococcus aureus joint infection to evaluate in vivo the efficacy of antimicrobial implant coatings. PLoS ONE, 2010, 5(9): e12580
Belmatoug N, Crémieux A C, Bleton R, et al. A new model of experimental prosthetic joint infection due to methicillin-resistant Staphylococcus aureus: a microbiologic, histopathologic, and magnetic resonance imaging characterization. The Journal of Infectious Diseases, 1996, 174(2): 414–417
Lucke M, Schmidmaier G, Sadoni S, et al. A new model of implant-related osteomyelitis in rats. Journal of Biomedical Materials Research Part B: Applied Biomaterials, 2003, 67B(1): 593–602
Craig M R, Poelstra K A, Sherrell J C, et al. A novel total knee arthroplasty infection model in rabbits. Journal of Orthopaedic Research, 2005, 23(5): 1100–1104
Isenberg H D. Clinical Microbiology Procedure Handbook. 1st ed. Washington, DC: American Society for Microbiology, 1992
Steckelberg J M, Osmon D R. Prosthetic joint infection. In: Waldvogel F A, ed. Infections Associated with Indwelling Medical Devices. 3rd ed. Washington, DC: ASM Press, 2000, 173–205
Montanaro L, Speziale P, Campoccia D, et al. Scenery of Staphylococcus implant infections in orthopedics. Future Microbiology, 2011, 6(11): 1329–1349
Hellmark B, Söderquist B, Unemo M, et al. Comparison of Staphylococcus epidermidis isolated from prosthetic joint infections and commensal isolates in regard to antibiotic susceptibility, agr type, biofilm production, and epidemiology. International Journal of Medical Microbiology, 2013, 303(1): 32–39
Chen-Charpentier B M, Stanescu D. Biofilm growth on medical implants with randomness. Mathematical and Computer Modelling, 2011, 54(7–8): 1682–1686
Sendi P, Banderet F, Graber P, et al. Clinical comparison between exogenous and haematogenous periprosthetic joint infections caused by Staphylococcus aureus. Clinical Microbiology and Infection, 2011, 17(7): 1098–1100
Berbari E F, Hanssen A D, Duffy M C, et al. Risk factors for prosthetic joint infection: case-control study. Clinical Infectious Diseases, 1998, 27(5): 1247–1254
Zimmerli W, Sendi P. Pathogenesis of implant-associated infection: the role of the host. Seminars in Immunopathology, 2011, 33(3): 295–306
Rodet A. Physiologie pathologique–étudeexpérimentalesurl’ostéomyeliteinfectieuse. C R Acad Sci, 1885, 99: 569–571
Zurexperimentellenerzeugungosteomyelitischerherde L E. Arch Klin Chir, 1894, 48: 181–200
Rissing J P, Buxton T B, Weinstein R S, et al. Model of experimental chronic osteomyelitis in rats. Infection & Immunity, 1985, 47(3): 581–586
Fukushima N, Yokoyama K, Sasahara T, et al. Establishment of rat model of acute staphylococcal osteomyelitis: relationship between inoculation dose and development of osteomyelitis. Archives of Orthopaedic & Trauma Surgery, 2005, 125(3): 169–176
Ofluoglu E A, Zileli M, Aydin D, et al. Implant-related infection model in rat spine. Archives of Orthopaedic and Trauma Surgery, 2007, 127(5): 391–396
Poultsides L A, Papatheodorou L K, Karachalios T S, et al. Novel model for studying hematogenous infection in an experimental setting of implant-related infection by a community-acquired methicillin-resistant S. aureus strain. Journal of Orthopaedic Research, 2008, 26(10): 1355–1362
Vogelyl H C, Dhertl W J A, Fleer A, et al. The infected orthopaedic implant. An animal model to study the mechanisms of haematogenous infection of cementless implant materials. European Journal of Orthopaedic Surgery & Traumatology, 1996, 6(2): 91–95
Boles B R, Horswill A R. Staphylococcal biofilm disassembly. Trends in Microbiology, 2011, 19(9): 449–455
Mack D, Becker P, Chatterjee I, et al. Mechanisms of biofilm formation in Staphylococcus epidermidis and Staphylococcus aureus: functional molecules, regulatory circuits, and adaptive responses. International Journal of Medical Microbiology, 2004, 294(2–3): 203–212
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. The Journal of Bone and Joint Surgery (American Volume), 2012, 94 (15): 1406–1415
Alt V, Lips K S, Henkenbehrens C, et al. A new animal model for implant-related infected non-unions after intramedullary fixation of the tibia in rats with fluorescent in situ hybridization of bacteria in bone infection. Bone, 2011, 48(5): 1146–1153
Montanaro L, Poggi A, Visai L, et al. Extracellular DNA in biofilms. The International Journal of Artificial Organs, 2011, 34 (9): 824–831
Cue D, Lei M G, Lee C Y. Genetic regulation of the intercellular adhesion locus in staphylococci. Frontiers in Cellular and Infection Microbiology, 2012, 2: 38
Foster T J, Geoghegan J A, Ganesh V K, et al. Adhesion, invasion and evasion: the many functions of the surface proteins of Staphylococcus aureus. Nature Reviews: Microbiology, 2013, 12 (1): 49–62
Stoodley P, Kathju S, Hu F Z, et al. Molecular and imaging techniques for bacterial biofilms in joint arthroplasty infections. Clinical Orthopaedics and Related Research, 2005, 437: 31–40
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Chu, CB., Zeng, H., Shen, DX. et al. A new rabbit model of implant-related biofilm infection: development and evaluation. Front. Mater. Sci. 10, 80–89 (2016). https://doi.org/10.1007/s11706-016-0324-1
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DOI: https://doi.org/10.1007/s11706-016-0324-1