The role of barrier membranes for guided bone regeneration and restoration of large bone defects: current experimental and clinical evidence

BMC Medicine

Peter V Giannoudis²  Giorgio Maria Calori³  George I Mataliotakis¹  Rozalia Dimitriou¹ 

[1] Department of Trauma and Orthopaedics, Academic Unit, Clarendon Wing, Leeds Teaching Hospitals NHS Trust, Great George Street, Leeds LS1 3EX, UK;Leeds NIHR Biomedical Research Unit, Leeds Institute of Molecular Medicine, Beckett Street, Leeds, LS9 7TF UK;Department of Trauma and Orthopedics, University of Milan, Orthopedic Institute, G. Pini, University of Milan, Italy

关键词: bioresorbable/absorbable membranes;    non-resorbable membranes;    barrier membranes;    bone defect;    bone regeneration;   

Others  :  1125909
DOI  :  10.1186/1741-7015-10-81

 received in 2011-11-10, accepted in 2012-07-26,  发布年份 2012

【 摘 要 】

Treatment of large bone defects represents a great challenge in orthopedic and craniomaxillofacial surgery. Although there are several methods for bone reconstruction, they all have specific indications and limitations. The concept of using barrier membranes for restoration of bone defects has been developed in an effort to simplify their treatment by offering a sinlge-staged procedure. Research on this field of bone regeneration is ongoing, with evidence being mainly attained from preclinical studies. The purpose of this review is to summarize the current experimental and clinical evidence on the use of barrier membranes for restoration of bone defects in maxillofacial and orthopedic surgery. Although there are a few promising preliminary human studies, before clinical applications can be recommended, future research should aim to establish the 'ideal' barrier membrane and delineate the need for additional bone grafting materials aiming to 'mimic' or even accelerate the normal process of bone formation. Reproducible results and long-term observations with barrier membranes in animal studies, and particularly in large animal models, are required as well as well-designed clinical studies to evaluate their safety, efficacy and cost-effectiveness.

【 授权许可】

   
2012 Dimitriou et al; licensee BioMed Central Ltd.

【 参考文献 】

• [1]Dimitriou R, Jones E, McGonagle D, Giannoudis PV: Bone regeneration: current concepts and future directions. BMC Med 2011, 9:66. BioMed Central Full Text
• [2]Gugala Z, Lindsey RW, Gogolewski S: New approaches in the treatment of critical-size segmental defects in long bones. Macromol Symp 2007, 253:147-161.
• [3]Schmitz JP, Hollinger JO: The critical size defect as an experimental model for craniomandibulofacial nonunions. Clin Orthop Relat Res 1986, 205:299-308.
• [4]Aronson J: Limb-lengthening, skeletal reconstruction, and bone transport with the Ilizarov method. J Bone Joint Surg Am 1997, 79:1243-1258.
• [5]Bauer TW, Muschler GF: Bone graft materials. An overview of the basic science. Clin Orthop Relat Res 2000, 371:10-27.
• [6]Giannoudis PV, Dinopoulos H, Tsiridis E: Bone substitutes: an update. Injury 2005, 36(Suppl 3):S20-27.
• [7]Giannoudis PV, Einhorn TA: Bone morphogenetic proteins in musculoskeletal medicine. Injury 2009, 40(Suppl 3):S1-3.
• [8]Pederson WC, Person DW: Long bone reconstruction with vascularized bone grafts. Orthop Clin North Am 2007, 38:23-35.
• [9]Masquelet AC, Begue T: The concept of induced membrane for reconstruction of long bone defects. Orthop Clin North Am 2010, 41:27-37.
• [10]Pelissier P, Masquelet AC, Bareille R, Pelissier SM, Amedee J: Induced membranes secrete growth factors including vascular and osteoinductive factors and could stimulate bone regeneration. J Orthop Res 2004, 22:73-79.
• [11]Viateau V, Guillemin G, Calando Y, Logeart D, Oudina K, Sedel L, Hannouche D, Bousson V, Petite H: Induction of a barrier membrane to facilitate reconstruction of massive segmental diaphyseal bone defects: an ovine model. Vet Surg 2006, 35:445-452.
• [12]Giannoudis PV, Faour O, Goff T, Kanakaris N, Dimitriou R: Masquelet technique for the treatment of bone defects: tips-tricks and future directions. Injury 2011, 42:591-598.
• [13]Meinig RP: Clinical use of resorbable polymeric membranes in the treatment of bone defects. Orthop Clin North Am 2010, 41:39-47.
• [14]Retzepi M, Donos N: Guided bone regeneration: biological principle and therapeutic applications. Clin Oral Implants Res 2010, 21:567-576.
• [15]Gottlow J: Guided tissue regeneration using bioresorbable and nonresorbable devices: initial healing and long-term results. J Periodontol 1993, 64(11 Suppl):1157-1165.
• [16]Hurley L, Stinchfield F, Bassett A, Lyon W: The role of soft tissues in osteogenesis. An experimental study of canine spine fusions. J Bone Joint Surg Am 1959, 41:1243-1254.
• [17]Boyne PJ: Regeneration of alveolar bone beneath cellulose acetate filter implants. J Dent Res 1964, 43:827.
• [18]Boyne PJ: Restoration of osseous defects in maxillofacial casualties. J Am Dent Assoc 1969, 78:767-776.
• [19]Ogiso B, Hughes FJ, Melcher AH, McCulloch CA: Fibroblasts inhibit mineralised bone nodule formation by rat bone marrow stromal cells in vitro. J Cell Physiol 1991, 146:442-450.
• [20]Dahlin C, Linde A, Gottlow J, Nyman S: Healing of bone defects by guided tissue regeneration. Plast Reconstr Surg 1988, 81:672-676.
• [21]Pitaru S, Tal H, Soldinger M, Grosskopf A, Noff M: Partial regeneration of periodontal tissues using collagen barriers. Initial observations in the canine. J Periodontol 1988, 59:380-386.
• [22]Schenk RK, Buser D, Hardwick WR, Dahlin C: Healing pattern of bone regeneration in membrane-protected defects: a histologic study in the canine mandible. Int J Oral Maxillofac Implants 1994, 9:13-29.
• [23]McAllister BS, Haghighat K: Bone augmentation techniques. J Periodontol 2007, 78:377-396.
• [24]Nyman R, Magnusson M, Sennerby L, Nyman S, Lundgren D: Membrane-guided bone regeneration. Segmental radius defects studied in the rabbit. Acta Orthop Scand 1995, 66:169-173.
• [25]Scantlebury TV: 1982-1992: a decade of technology development for guided tissue regeneration. J Periodontol 1993, 64(11 Suppl):1129-1137.
• [26]Aaboe M, Pinholt EM, Hjørting-Hansen E: Healing of experimentally created defects: a review. Br J Oral Maxillofac Surg 1995, 33:312-318.
• [27]Wiltfang J, Merten HA, Peters JH: Comparative study of guided bone regeneration using absorbable and permanent barrier membranes: a histologic report. Int J Oral Maxillofac Implants 1998, 13:416-421.
• [28]Marouf HA, El-Guindi HM: Efficacy of high-density versus semipermeable PTFE membranes in an elderly experimental model. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000, 89:164-170.
• [29]Ostermann PA, Haase N, Rübberdt A, Wich M, Ekkernkamp A: Management of a long segmental defect at the proximal meta-diaphyseal junction of the tibia using a cylindrical titanium mesh cage. J Orthop Trauma 2002, 16:597-601.
• [30]Hardwick R, Hayes BK, Flynn C: Devices for dentoalveolar regeneration: an up-to-date literature review. J Periodontol 1995, 66:495-505.
• [31]Gielkens PF, Schortinghuis J, de Jong JR, Raghoebar GM, Stegenga B, Bos RR: Vivosorb, Bio-Gide, and Gore-Tex as barrier membranes in rat mandibular defects: an evaluation by microradiography and micro-CT. Clin Oral Implants Res 2008, 19:516-521.
• [32]Gielkens PF, Schortinghuis J, de Jong JR, Paans AM, Ruben JL, Raghoebar GM, Stegenga B, Bos RR: The influence of barrier membranes on autologous bone grafts. J Dent Res 2008, 87:1048-1052.
• [33]Kinoshita Y: Regenerative medicine for jawbone. JMAJ 2004, 47:294-297.
• [34]Thomaidis V, Kazakos K, Lyras DN, Dimitrakopoulos I, Lazaridis N, Karakasis D, Botaitis S, Agrogiannis G: Comparative study of 5 different membranes for guided bone regeneration of rabbit mandibular defects beyond critical size. Med Sci Monit 2008, 14:BR67-73.
• [35]Needleman IG, Worthington HV, Giedrys-Leeper E, Tucker RJ: Guided tissue regeneration for periodontal infra-bony defects. Cochrane Database Syst Rev 2006, 2:CD001724.
• [36]Sculean A, Nikolidakis D, Schwarz F: Regeneration of periodontal tissues: combinations of barrier membranes and grafting materials - biological foundation and preclinical evidence: a systematic review. J Clin Periodontol 2008, 35(8 Suppl):106-116.
• [37]Nakajima S, Fukuda T, Hasue M, Sengoku Y, Haraoka J, Uchida T: New technique for application of fibrin sealant: rubbing method devised to prevent cerebrospinal fluid leakage from dura mater sites repaired with expanded polytetrafluoroethylene surgical membranes. Neurosurgery 2001, 49:117-123.
• [38]Schmidmaier G, Baehr K, Mohr S, Kretschmar M, Beck S, Wildemann B: Biodegradable polylactide membranes for bone defect coverage: biocompatibility testing, radiological and histological evaluation in a sheep model. Clin Oral Implants Res 2006, 17:439-444.
• [39]Klaue K, Knothe U, Masquelet A: Effet biologique des membranes à corps etranger induites in situ sur la consolidation des greffes d'os spongieux. Rev Chir Orthop Suppl 1995, 70:109-110.
• [40]Patino MG, Neiders ME, Andreana S, Noble B, Cohen RE: Collagen as an implantable material in medicine and dentistry. J Oral Implantol 2002, 28:220-225.
• [41]Bunyaratavej P, Wang HL: Collagen membranes: a review. J Periodontol 2001, 72:215-229.
• [42]von Arx T, Broggini N, Jensen SS, Bornstein MM, Schenk RK, Buser D: Membrane durability and tissue response of different bioresorbable barrier membranes: a histologic study in the rabbit calvarium. Int J Oral Maxillofac Implants 2005, 20:843-853.
• [43]Alpar B, Leyhausen G, Günay H, Geurtsen W: Compatibility of resorbable and nonresorbable guided tissue regeneration membranes in cultures of primary human periodontal ligament fibroblasts and human osteoblast-like cells. Clin Oral Investig 2000, 4:219-225.
• [44]Behring J, Junker R, Walboomers XF, Chessnut B, Jansen JA: Toward guided tissue and bone regeneration: morphology, attachment, proliferation, and migration of cells cultured on collagen barrier membranes. A systematic review. Odontology 2008, 96:1-11.
• [45]Rothamel D, Schwarz F, Sculean A, Herten M, Scherbaum W, Becker J: Biocompatibility of various collagen membranes in cultures of human PDL fibroblasts and human osteoblast-like cells. Clin Oral Implants Res 2004, 15:443-449.
• [46]Tal H, Kozlovsky A, Artzi Z, Nemcovsky CE, Moses O: Long-term bio-degradation of cross-linked and non-cross-linked collagen barriers in human guided bone regeneration. Clin Oral Implants Res 2008, 19:295-302.
• [47]Lee CK, Koo KT, Kim TI, Seol YJ, Lee YM, Rhyu IC, Ku Y, Chung CP, Park YJ, Lee JY: Biological effects of a porcine-derived collagen membrane on intrabony defects. J Periodontal Implant Sci 2010, 40:232-238.
• [48]Coïc M, Placet V, Jacquet E, Meyer C: Mechanical properties of collagen membranes used in guided bone regeneration: a comparative study of three models. [Article in French]. Rev Stomatol Chir Maxillofac 2010, 111:286-290.
• [49]Gupta KC, Ravi Kumar MN: Drug release behavior of beads and microgranules of chitosan. Biomaterials 2000, 21:1115-1119.
• [50]Klokkevold PR, Subar P, Fukayama H, Bertolami CN: Effect of chitosan on lingual hemostasis in rabbits with platelet dysfunction induced by epoprostenol. J Oral Maxillofac Surg 1992, 50:41-45.
• [51]Shin SY, Park HN, Kim KH, Lee MH, Choi YS, Park YJ, Lee YM, Ku Y, Rhyu IC, Han SB, Lee SJ, Chung CP: Biological evaluation of chitosan nanofiber membrane for guided bone regeneration. J Periodontol 2005, 76:1778-1784.
• [52]Lee EJ, Shin DS, Kim HE, Kim HW, Koh YH, Jang JH: Membrane of hybrid chitosan-silica xerogel for guided bone regeneration. Biomaterials 2009, 30:743-750.
• [53]Kung S, Devlin H, Fu E, Ho KY, Liang SY, Hsieh YD: The osteoinductive effect of chitosan-collagen composites around pure titanium implant surfaces in rats. J Periodontal Res 2011, 46:126-133.
• [54]Asikainen AJ, Noponen J, Lindqvist C, Pelto M, Kellomäki M, Juuti H, Pihlajamäki H, Suuronen R: Tyrosine-derived polycarbonate membrane in treating mandibular bone defects. An experimental study. J R Soc Interface 2006, 3:629-635.
• [55]Gogolewski S, Pineda L, Büsing CM: Bone regeneration in segmental defects with resorbable polymeric membranes: IV. Does the polymer chemical composition affect the healing process? Biomaterials 2000, 21:2513-2520.
• [56]Kaushiva A, Turzhitsky VM, Darmoc M, Backman V, Ameer GA: A biodegradable vascularizing membrane: a feasibility study. Acta Biomater 2007, 3:631-642.
• [57]Kinoshita Y, Kobayashi M, Fukuoka S, Yokoya S, Ikada Y: Functional reconstruction of the jaw bones using poly(l-lactide) mesh and autogenic particulate cancellous bone and marrow. Tissue Eng 1996, 2:327-341.
• [58]Polimeni G, Koo KT, Pringle GA, Agelan A, Safadi FF, Wikesjo UM: Histopathological observations of a polylactic acid-based device intended for guided bone/tissue regeneration. Clin Implant Dent Relat Res 2008, 10:99-105.
• [59]Schliephake H, Kracht D: Vertical ridge augmentation using polylactic membranes in conjunction with immediate implants in periodontally compromised extraction sites: an experimental study in dogs. Int J Oral Maxillofac Implants 1997, 12:325-334.
• [60]Ueyama Y, Ishikawa K, Mano T, Koyama T, Nagatsuka H, Suzuki K, Ryoke K: Usefulness as guided bone regeneration membrane of the alginate membrane. Biomaterials 2002, 23:2027-2033.
• [61]Ueyama Y, Koyama T, Ishikawa K, Mano T, Ogawa Y, Nagatsuka H, Suzuki K: Comparison of ready-made and self-setting alginate membranes used as a barrier membrane for guided bone regeneration. J Mater Sci Mater Med 2006, 17:281-288.
• [62]He H, Huang J, Chen G, Dong Y: Application of a new bioresorbable film to guided bone regeneration in tibia defect model of the rabbits. J Biomed Mater Res A 2007, 82:256-262.
• [63]Jianqi H, Hong H, Lieping S, Genghua G: Comparison of calcium alginate film with collagen membrane for guided bone regeneration in mandibular defects in rabbits. J Oral Maxillofac Surg 2002, 60:1449-1454.
• [64]Kim JH, Kim MK, Park JH, Won JE, Kim TH, Kim HW: Performance of Novel Nanofibrous Biopolymer Membrane for Guided Bone Regeneration within Rat Mandibular Defect. In Vivo 2011, 25:589-595.
• [65]Zhang J, Huang C, Xu Q, Mo A, Li J, Zuo Y: Biological properties of a biomimetic membrane for guided tissue regeneration: a study in rat calvarial defects. Clin Oral Implants Res 2010, 21:392-397.
• [66]Humber CC, Sándor GK, Davis JM, Peel SA, Brkovic BM, Kim YD, Holmes HI, Clokie CM: Bone healing with an in situ-formed bioresorbable polyethylene glycol hydrogel membrane in rabbit calvarial defects. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010, 109:372-384.
• [67]Kothiwale SV, Anuroopa P, Gajiwala AL: A clinical and radiological evaluation of DFDBA with amniotic membrane versus bovine derived xenograft with amniotic membrane in human periodontal grade II furcation defects. Cell Tissue Bank 2009, 10:317-326.
• [68]Wu CA, Pettit AR, Toulson S, Grøndahl L, Mackie EJ, Cassady AI: Responses in vivo to purified poly(3-hydroxybutyrate-co-3-hydroxyvalerate) implanted in a murine tibial defect model. J Biomed Mater Res A 2009, 91:845-854.
• [69]Teng SH, Lee EJ, Wang P, Shin DS, Kim HE: Three-layered membranes of collagen/hydroxyapatite and chitosan for guided bone regeneration. J Biomed Mater Res B Appl Biomater 2008, 87:132-138.
• [70]Shabani I, Haddadi-Asl V, Soleimani M, Seyedjafari E, Babaeijandaghi F, Ahmadbeigi N: Enhanced infiltration and biomineralization of stem cells on collagen-grafted three-dimensional nanofibers. Tissue Eng Part A 2011, 17:1209-1218.
• [71]Berner A, Boerckel JD, Saifzadeh S, Steck R, Ren J, Vaquette C, Zhang JQ, Nerlich M, Guldberg RE, Hutmacher DW, Woodruff MA: Biomimetic tubular nanofiber mesh and platelet rich plasma-mediated delivery of BMP-7 for large bone defect regeneration. Cell Tissue Res 2012, 347:603-612.
• [72]Ereno C, Guimarães SA, Pasetto S, Herculano RD, Silva CP, Graeff CF, Tavano O, Baffa O, Kinoshita A: Latex use as an occlusive membrane for guided bone regeneration. J Biomed Mater Res A 2010, 95:932-939.
• [73]Tokuda S, Obata A, Kasuga T: Preparation of poly(lactic acid)/siloxane/calcium carbonate composite membranes with antibacterial activity. Acta Biomater 2009, 5:1163-1168.
• [74]Zhang J, Xu Q, Huang C, Mo A, Li J, Zuo Y: Biological properties of an anti-bacterial membrane for guided bone regeneration: an experimental study in rats. Clin Oral Implants Res 2010, 21:321-327.
• [75]Chaturvedi R, Gill AS, Sikri P: Evaluation of the regenerative potential of 25% doxycycline-loaded biodegradable membrane vs biodegradable membrane alone in the treatment of human periodontal infrabony defects: a clinical and radiological study. Indian J Dent Res 2008, 19:116-123.
• [76]Pineda LM, Busing Mc, Mienig RP, Gogolewski S: Bone regeneration with resorbable polymeric membranes. Effect of pore size on bone healing process in large defects. J Biomed Mater Res 1996, 31:385-394.
• [77]Chvapil M, Holusa R, Kliment K, Stoll M: Some chemical and biological characteristics of a new collagen-polymer compound material. J Biomed Mater Res 1969, 3:315-332.
• [78]Taylor D, Smith F: Porous methyl methacrylate as an implant material. J Biomed Mater Res 1972, 6:467-479.
• [79]Klawitter J, Bagwell J, Weinstein A, Sauer B: An evaluation of bone growth into porous high density polyethylene. J Biomed Mater Res 1976, 10:311-323.
• [80]Spector M, Flemming W, Kreutner A: Bone growth into porous high-density polyethylene. J Biomed Mater Res 1976, 10:595-603.
• [81]Gutta R, Baker RA, Bartolucci AA, Louis PJ: Barrier membranes used for ridge augmentation: is there an optimal pore size? J Oral Maxillofac Surg 2009, 67:1218-1225.
• [82]Kong L, Ao Q, Wang A, Gong K, Wang X, Lu G, Gong Y, Zhao N, Zhang X: Preparation and characterization of a multilayer biomimetic scaffold for bone tissue engineering. J Biomater Appl 2007, 22:223-239.
• [83]de Santana RB, de Mattos CM, Francischone CE, Van Dyke T: Superficial topography and porosity of an absorbable barrier membrane impacts soft tissue response in guided bone regeneration. J Periodontol 2010, 81:926-933.
• [84]Becker W, Becker B, McGuire M: Localized ridge augmentation using absorbable pins and e-PTFE barrier membranes: a new surgical technique. Case reports. Int J Periodont Restor Dent 1994, 14:48-61.
• [85]Jovanovic S, Nevins M: Bone formation utilizing titanium-reinforced barrier membranes. Int J Periodont Restor Dent 1995, 15:56-69.
• [86]Simion M, Trisi P, Piattelli A: Vertical ridge augmentation using a membrane technique associated with osseointegrated implants. Int J Periodont Restor Dent 1994, 14:496-511.
• [87]Ducheyne P, De Meester P, Aernoudt E: Influence of a functional dynamic loading on bone ingrowth into surface pores of orthopedic implants. J Biomed Mater Res 1977, 11:811-838.
• [88]Heck D, Nakajima I, Kelly P, Chao E: The effect of load alteration on the biological and biomechanical performance of a titanium fiber-metal segmental prosthesis. J Bone Joint Surg Am 1986, 68:118-126.
• [89]Pilliar R, Cameron H, Welsh R, Binnington A: Radiographic and morphologic studies of load-bearing porous-surfaced structured implants. Clin Orthop Relat Res 1981, 156:249-257.
• [90]Boerckel JD, Uhrig BA, Willett NJ, Huebsch N, Guldberg RE: Mechanical regulation of vascular growth and tissue regeneration in vivo. Proc Natl Acad Sci USA 2011, 108:E674-680.
• [91]Matsuo A, Chiba H, Takahashi H, Toyoda J, Abukawa H: Clinical application of a custom-made bioresorbable raw particulate hydroxyapatite/poly-L-lactide mesh tray for mandibular reconstruction. Odontology 2010, 98:85-88.
• [92]Amano Y, Ota M, Sekiguchi K, Shibukawa Y, Yamada S: Evaluation of a poly-l-lactic acid membrane and membrane fixing pin for guided tissue regeneration on bone defects in dogs. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2004, 97:155-163.
• [93]Lacroix D, Prendergast PJ: A mechano-regulation model for tissue differentiation during fracture healing: analysis of gap size and loading. J Biomech 2002, 35:1163-1171.
• [94]Stetzer K, Cooper G, Gassner R, Kapucu R, Mundell R, Mooney MP: Effects of fixation type and guided tissue regeneration on maxillary osteotomy healing in rabbits. J Oral Maxillofac Surg 2002, 60:427-436.
• [95]Kazakos K, Lyras DN, Thomaidis V, Agrogiannis G, Botaitis S, Drosos G, Kokka A, Verettas D: Application of PRP gel alone or in combination with guided bone regeneration does not enhance bone healing process: an experimental study in rabbits. J Craniomaxillofac Surg 2011, 39:49-53.
• [96]Hoogeveen EJ, Gielkens PF, Schortinghuis J, Ruben JL, Huysmans MC, Stegenga B: Vivosorb as a barrier membrane in rat mandibular defects. An evaluation with transversal microradiography. Int J Oral Maxillofac Surg 2009, 38:870-875.
• [97]He H, Yan W, Chen G, Lu Z: Acceleration of de novo bone formation with a novel bioabsorbable film: a histomorphometric study in vivo. J Oral Pathol Med 2008, 37:378-382.
• [98]Zahedi S, Legrand R, Brunel G, Albert A, Dewé W, Coumans B, Bernard JP: Evaluation of a diphenylphosphorylazide-crosslinked collagen membrane for guided bone regeneration in mandibular defects in rats. J Periodontol 1998, 69:1238-1246.
• [99]Linde A, Hedner E: Recombinant bone morphogenetic protein-2 enhances bone healing, guided by osteopromotive e-PTFE membranes: an experimental study in rats. Calcif Tissue Int 1995, 56:549-553.
• [100]Zellin G, Gritli-Linde A, Linde A: Healing of mandibular defects with different biodegradable and non-biodegradable membranes: an experimental study in rats. Biomaterials 1995, 16:601-609.
• [101]Dahlin C, Sandberg E, Alberius P, Linde A: Restoration of mandibular nonunion bone defects. An experimental study in rats using an osteopromotive membrane method. Int J Oral Maxillofac Surg 1994, 23:237-242.
• [102]Kostopoulos L, Karring T: Guided bone regeneration in mandibular defects in rats using a bioresorbable polymer. Clin Oral Implants Res 1994, 5:66-74.
• [103]Sandberg E, Dahlin C, Linde A: Bone regeneration by the osteopromotion technique using bioabsorbable membranes: an experimental study in rats. J Oral Maxillofac Surg 1993, 51:1106-1114.
• [104]Jégoux F, Goyenvalle E, Cognet R, Malard O, Moreau F, Daculsi G, Aguado E: Mandibular segmental defect regenerated with macroporous biphasic calcium phosphate, collagen membrane, and bone marrow graft in dogs. Arch Otolaryngol Head Neck Surg 2010, 136:971-978.
• [105]Borges GJ, Novaes AB Jr, Grisi MF, Palioto DB, Taba M Jr, de Souza SL: Acellular dermal matrix as a barrier in guided bone regeneration: a clinical, radiographic and histomorphometric study in dogs. Clin Oral Implants Res 2009, 20:1105-1115.
• [106]Sverzut CE, Faria PE, Magdalena CM, Trivellato AE, Mello-Filho FV, Paccola CA, Gogolewski S, Salata LA: Reconstruction of mandibular segmental defects using the guided-bone regeneration technique with polylactide membranes and/or autogenous bone graft: a preliminary study on the influence of membrane permeability. J Oral Maxillofac Surg 2008, 66:647-656.
• [107]Bornstein MM, Bosshardt D, Buser D: Effect of two different bioabsorbable collagen membranes on guided bone regeneration: a comparative histomorphometric study in the dog mandible. J Periodontol 2007, 78:1943-1953.
• [108]Zubery Y, Goldlust A, Antoine Alves A, Nir E: Ossification of a novel cross-linked porcine collagen barrier in guided bone regeneration in dogs. J Periodontol 2007, 78:112-121.
• [109]Peled M, Machtei EE, Rachmiel A: Osseous reconstruction using a membrane barrier following marginal mandibulectomy: an animal pilot study. J Periodontol 2002, 73:1451-1456.
• [110]Fritz ME, Jeffcoat MK, Reddy M, Koth D, Braswell LD, Malmquist J, Lemons J: Guided bone regeneration of large mandibular defects in a primate model. J Periodontol 2000, 71:1484-1491.
• [111]Bernabé PF, Melo LG, Cintra LT, Gomes-Filho JE, Dezan E Jr, Nagata MJ: Bone healing in critical-size defects treated with either bone graft, membrane, or a combination of both materials: a histological and histometric study in rat tibiae. Clin Oral Implants Res 2012, 23:384-388.
• [112]Cai YZ, Wang LL, Cai HX, Qi YY, Zou XH, Ouyang HW: Electrospun nanofibrous matrix improves the regeneration of dense cortical bone. J Biomed Mater Res A 2010, 95:49-57.
• [113]Lysiak-Drwal K, Dominiak M, Solski L, Zywicka B, Pielka S, Konopka T, Gerber H: Early histological evaluation of bone defect healing with and without guided bone regeneration techniques: experimental animal studies. Postepy Hig Med Dosw (Online) 2008, 62:282-288.
• [114]Gerbi ME, Pinheiro AL, Marzola C, Limeira Júnior Fde A, Ramalho LM, Ponzi EA, Soares AO, Carvalho LC, Lima HV, Gonçalves TO: Assessment of bone repair associated with the use of organic bovine bone and membrane irradiated at 830 nm. Photomed Laser Surg 2005, 23:382-388.
• [115]Nasser NJ, Friedman A, Friedman M, Moor E, Mosheiff R: Guided bone regeneration in the treatment of segmental diaphyseal defects: a comparison between resorbable and non-resorbable membranes. Injury 2005, 36:1460-1466.
• [116]Moore DC, Pedrozo HA, Crisco JJ, Ehrlich MG: Preformed grafts of porcine small intestine submucosa (SIS) for bridging segmental bone defects. J Biomed Mater Res A 2004, 69:259-266.
• [117]Ip WY: Polylactide membranes and sponges in the treatment of segmental defects in rabbit radii. Injury 2002, 33(Suppl 2):66-70.
• [118]Matsuzaka K, Shimono M, Inoue T: Characteristics of newly formed bone during guided bone regeneration: observations by immunohistochemistry and confocal laser scanning microscopy. Bull Tokyo Dent Coll 2001, 42:225-234.
• [119]Nyman R, Sennerby L, Nyman S, Lundgren D: Influence of bone marrow on membrane-guided bone regeneration of segmental long-bone defects in rabbits. Scand J Plast Reconstr Surg Hand Surg 2001, 35:239-246.
• [120]Caiazza S, Colangelo P, Bedini R, Formisano G, De Angelis G, Barrucci S: Evaluation of guided bone regeneration in rabbit femur using collagen membranes. Implant Dent 2000, 9:219-225.
• [121]Ishikawa K, Ueyama Y, Mano T, Koyama T, Suzuki K, Matsumura T: Self-setting barrier membrane for guided tissue regeneration method: initial evaluation of alginate membrane made with sodium alginate and calcium chloride aqueous solutions. J Biomed Mater Res 1999, 47:111-115.
• [122]Suckow MA, Voytik-Harbin SL, Terril LA, Badylak SF: Enhanced bone regeneration using porcine small intestinal submucosa. J Invest Surg 1999, 12:277-287.
• [123]Meinig RP, Buesing CM, Helm J, Gogolewski S: Regeneration of diaphyseal bone defects using resorbable poly(L/DL-lactide) and poly(D-lactide) membranes in the Yucatan pig model. J Orthop Trauma 1997, 11:551-558.
• [124]Lu S, Zhang Z, Wang J: Guided bone regeneration in long bone. An experimental study. Chin Med J (Engl) 1996, 109:551-554.
• [125]Nyman R, Magnusson M, Sennerby L, Nyman S, Lundgren D: Membrane-guided bone regeneration. Segmental radius defects studied in the rabbit. Acta Orthop Scand 1995, 66:169-173.
• [126]Farso Nielsen F, Karring T, Gogolewski S: Biodegradable guide for bone regeneration. Polyurethane membranes tested in rabbit radius defects. Acta Orthop Scand 1992, 63:66-69.
• [127]Rhodes NP, Hunt JA, Longinotti C, Pavesio A: In Vivo Characterization of Hyalonect, a Novel Biodegradable Surgical Mesh. J Surg Res 2011, 168:e31-38.
• [128]Oh T, Rahman MM, Lim JH, Park MS, Kim DY, Yoon JH, Kim WH, Kikuchi M, Tanaka J, Koyama Y, Kweon OK: Guided bone regeneration with beta-tricalcium phosphate and poly L-lactide-co-glycolide-co-epsilon-caprolactone membrane in partial defects of canine humerus. J Vet Sci 2006, 7:73-77.
• [129]Beniker D, McQuillan D, Livesey S, Urban RM, Turner TM, Blum B, Hughes K, Haggard WO: The use of acellular dermal matrix as a scaffold for periosteum replacement. Orthopedics 2003, 26(5 Suppl):s591-596.
• [130]Gerber A, Gogolewsky S: Reconstruction of large segmental defects in the sheep tibia using polylactide membranes. A clinical and radiographic report. Injury 2002, 33(Suppl 2):43-57.
• [131]Gugala Z, Gogolewski S: Healing of critical-size segmental bone defects in the sheep tibiae using bioresorbable polylactide membranes. Injury 2002, 33(Suppl 2):71-76.
• [132]Gugala Z, Gogolewski S: Regeneration of segmental diaphyseal defects in sheep tibiae using resorbable polymeric membranes: a pilot study. J Orthop Trauma 1999, 13:187-195.
• [133]Kinoshita Y, Yokoya S, Mizutani N, Amagasa T, Kudo K, Nagayama M, Okabe S, Totsuka Y, Furuta I: Reconstruction of the mandible using bioresorbable poly[L-Lactide]mesh and autogenic particulate cancellous bone and marrow and application of dental implant. [http://sciencelinks.jp/j-east/article/200407/000020040704A0146649.php] webciteHead and Neck Cancer 2000, 26:525-530. [Abstract in English]
• [134]Ip WY, Gogolewski S: Clinical application of resorbable polymers in guided bone regeneration. European Cells and Materials 2004, 7(Suppl 1):36. [Abstract]
• [135]Berkovitz KBB: Disarticulated individual bones. In Gray's Anatomy: The Anatomical Basis of Clinical Practice. 39th edition. Edited by Standring S. London: Elsevier Churchill Livingstone; 2005:463-484.
• [136]Pedersen AB, Johnsen SP, Overgaard S, Søballe K, Sørensen HT, Lucht U: Total hip arthroplasty in Denmark: incidence of primary operations and revisions during 1996-2002 and estimated future demands. Acta Orthop 2005, 76:182-189.
• [137]Ulrich SD, Seyler TM, Bennett D, Delanois RE, Saleh KJ, Thongtrangan I, Kuskowski M, Cheng EY, Sharkey PF, Parvizi J, Stiehl JB, Mont MA: Total hip arthroplasties: what are the reasons for revision? Int Orthop 2008, 32:597-604.
• [138]Mavrogenis AF, Coll-Mesa L, Gonzalez-Gaitan M, Ucelay-Gomez R, Fabri N, Ruggieri P, Papagelopoulos PJ: Criteria and outcome of limb salvage surgery. J BUON 2011, 16:617-626.
• [139]Sampo M, Koivikko M, Taskinen M, Kallio P, Kivioja A, Tarkkanen M, Böhling T: Incidence, epidemiology and treatment results of osteosarcoma in Finland - a nationwide population-based study. Acta Oncol 2011, 50:1206-1214.
• [140]Nicoli Aldini N, Fini M, Giavaresi G, Guzzardella GA, Giardino R: Prosthetic devices shaped as tubular chambers for the treatment of large diaphyseal defects by guided bone regeneration. Int J Artif Organs 2005, 28:51-57.
• [141]Jaroma HJ, Ritsilä VA: Behaviour of cancellous bone graft with and without periosteal isolation in striated muscle. An experimental study. Scand J Plast Reconstr Surg Hand Surg 1988, 22:47-51.
• [142]Greenstein G, Greenstein B, Cavallaro J, Tarnow D: The role of bone decortication in enhancing the results of guided bone regeneration: a literature review. J Periodontol 2009, 80:175-189.
• [143]Guerra I, Morais Branco F, Vasconcelos M, Afonso A, Figueiral H, Zita R: Evaluation of implant osseointegration with different regeneration techniques in the treatment of bone defects around implants: an experimental study in a rabbit model. Clin Oral Implants Res 2011, 22:314-322.
• [144]Yokoya S, Mochizuki Y, Nagata Y, Deie M, Ochi M: Tendon-bone insertion repair and regeneration using polyglycolic acid sheet in the rabbit rotator cuff injury model. Am J Sports Med 2008, 36:1298-1309.
• [145]Amado S, Simões MJ, Armada da Silva PA, Luís AL, Shirosaki Y, Lopes MA, Santos JD, Fregnan F, Gambarotta G, Raimondo S, Fornaro M, Veloso AP, Varejão AS, Maurício AC, Geuna S: Use of hybrid chitosan membranes and N1E-115 cells for promoting nerve regeneration in an axonotmesis rat model. Biomaterials 2008, 29:4409-4419.
• [146]Jung RE, Windisch SI, Eggenschwiler AM, Thoma DS, Weber FE, Hämmerle CH: A randomized-controlled clinical trial evaluating clinical and radiological outcomes after 3 and 5 years of dental implants placed in bone regenerated by means of GBR techniques with or without the addition of BMP-2. Clin Oral Implants Res 2009, 20:660-666.
• [147]Lee SJ, Park YJ, Park SN, Lee YM, Seol YJ, Ku Y, Chung CP: Molded porous poly (L-lactide) membranes for guided bone regeneration with enhanced effects by controlled growth factor release. J Biomed Mater Res 2001, 55:295-303.
• [148]Hong KS, Kim EC, Bang SH, Chung CH, Lee YI, Hyun JK, Lee HH, Jang JH, Kim TI, Kim HW: Bone regeneration by bioactive hybrid membrane containing FGF2 within rat calvarium. J Biomed Mater Res A 2010, 94:1187-1194.
• [149]Zellin G, Linde A: Importance of delivery systems for growth-stimulatory factors in combination with osteopromotive membranes. An experimental study using rhBMP-2 in rat mandibular defects. J Biomed Mater Res 1997, 35:181-190.
• [150]Kolambkar YM, Dupont KM, Boerckel JD, Huebsch N, Mooney DJ, Hutmacher DW, Guldberg RE: An alginate-based hybrid system for growth factor delivery in the functional repair of large bone defects. Biomaterials 2011, 32:65-74.
• [151]Kolambkar YM, Boerckel JD, Dupont KM, Bajin M, Huebsch N, Mooney DJ, Hutmacher DW, Guldberg RE: Spatiotemporal delivery of bone morphogenetic protein enhances functional repair of segmental bone defects. Bone 2011, 49:485-492.
• [152]Pinheiro AL, Limeira Júnior Fde A, Gerbi ME, Ramalho LM, Marzola C, Ponzi EA, Soares AO, De Carvalho LC, Lima HC, Gonçalves TO: Effect of 830-nm laser light on the repair of bone defects grafted with inorganic bovine bone and decalcified cortical osseus membrane. J Clin Laser Med Surg 2003, 21:301-306.
• [153]Dahlin C, Linde A, Röckert H: Stimulation of early bone formation by the combination of an osteopromotive membrane technique and hyperbaric oxygen. Scand J Plast Reconstr Surg Hand Surg 1993, 27:103-108.
• [154]Arisawa EA, Brandão AA, Almeida JD, da Rocha RF: Calcitonin in bone-guided regeneration of mandibles in ovariectomized rats: densitometric, histologic and histomorphometric analysis. Int J Oral Maxillofac Surg 2008, 37:47-53.
• [155]Jung RE, Cochran DL, Domken O, Seibl R, Jones AA, Buser D, Hammerle CH: The effect of matrix bound parathyroid hormone on bone regeneration. Clin Oral Implants Res 2007, 18:319-325.
• [156]Weng D, Poehling S, Pippig S, Bell M, Richter EJ, Zuhr O, Hürzeler MB: The effects of recombinant human growth/differentiation factor-5 (rhGDF-5) on bone regeneration around titanium dental implants in barrier membrane-protected defects: a pilot study in the mandible of beagle dogs. Int J Oral Maxillofac Implants 2009, 24:31-37.
• [157]Donos N, Retzepi M, Wall I, Hamlet S, Ivanovski S: In vivo gene expression profile of guided bone regeneration associated with a microrough titanium surface. Clin Oral Implants Res 2011, 22:390-398.
• [158]Dupont KM, Boerckel JD, Stevens HY, Diab T, Kolambkar YM, Takahata M, Schwarz EM, Guldberg RE: Synthetic scaffold coating with adeno-associated virus encoding BMP2 to promote endogenous bone repair. Cell Tissue Res 2012, 347:575-588.