Guided bone regeneration: materials and biological mechanisms revisited

Ibrahim Elgali, Omar Omar, Christer Dahlin, Peter Thomsen, Ibrahim Elgali, Omar Omar, Christer Dahlin, Peter Thomsen

Abstract

Guided bone regeneration (GBR) is commonly used in combination with the installment of titanium implants. The application of a membrane to exclude non-osteogenic tissues from interfering with bone regeneration is a key principle of GBR. Membrane materials possess a number of properties which are amenable to modification. A large number of membranes have been introduced for experimental and clinical verification. This prompts the need for an update on membrane properties and the biological outcomes, as well as a critical assessment of the biological mechanisms governing bone regeneration in defects covered by membranes. The relevant literature for this narrative review was assessed after a MEDLINE/PubMed database search. Experimental data suggest that different modifications of the physicochemical and mechanical properties of membranes may promote bone regeneration. Nevertheless, the precise role of membrane porosities for the barrier function of GBR membranes still awaits elucidation. Novel experimental findings also suggest an active role of the membrane compartment per se in promoting the regenerative processes in the underlying defect during GBR, instead of being purely a passive barrier. The optimization of membrane materials by systematically addressing both the barrier and the bioactive properties is an important strategy in this field of research.

Keywords: biocompatible materials; growth factors; guided bone regeneration; membrane; osseointegration.

© 2017 The Authors. Eur J Oral Sci published by John Wiley & Sons Ltd.

Figures

Figure 1
Figure 1
Schematic illustration of the principle of guided bone regeneration (GBR).
Figure 2
Figure 2
Horizontal bone augmentation by guided bone regeneration (GBR) in the anterior maxilla. (A) Horizontal bone defect after trauma to the upper jaw. (B) Placement of expanded polytetrafluoroethylene (e‐PTFE) barrier membrane after filling the defect with Bio‐Oss bone substitute. (C) Insertion of implant in the regenerated bone 7 months after the GBR procedure. (D, E) Photograph and radiograph show the final restoration after 1 yr in function (Courtesy of Drs hatano & dahlin).
Figure 3
Figure 3
Vertical bone augmentation by guided bone regeneration (GBR) in the posterior mandible. (A–D) The defect is filled with autogenous bone particles and blocks and covered with titanium (Ti)‐reinforced expanded polytetrafluoroethylene (e‐PTFE) membrane. (E) Surgical re‐entry showing the regenerated bone site. (F) The prosthetic construction in place. (G) Panoramic radiograph at the re‐entry. Published by permission from the Clin Implant Dent Relat Res229.
Figure 4
Figure 4
Structural, cellular, and molecular events governing the mechanism of guided bone regeneration (GBR). The application of a GBR collagen membrane on a trabecular bone defect (A) promotes structural restitution of the defect with newly regenerated bone compared with the untreated sham defect (B) where soft‐tissue collapse and poor defect restitution is prominent. Quantitative histomorphometric measurements of the different zones of the defect (C) demonstrate higher area percentages of regenerated bone in the membrane‐treated defect compared with the sham defect, particularly in the top zone directly underneath the membrane (D). The asterisk (*) denotes a statistically significant difference. Immunohistochemical analyses of the membrane compartment reveal that during GBR healing (here exemplified at 3 d) the membrane recruits and hosts different cell types, including CD68‐positive monocytes/macrophages (E) as well as periostin‐positive osteoprogenitors (F). Furthermore, the immunohistochemical evaluation shows positive protein reactivity for major bone‐promoting growth factors, fibroblast growth factor 2 (FGF‐2) (G) and bone morphogenetic protein 2 (BMP‐2) (H), within the membrane. The quantitative polymerase chain reaction (qPCR) analysis of the membrane confirms the progressive expression of the pro‐osteogenic growth factors, FGF‐2 and BMP‐2 (I and J, respectively), in parallel with a time‐dependent reduction in the vascularization‐related factor, vascular endothelial growth factor (VEGF) (K), in the membrane compartment. The qPCR analysis of the underlying defect shows that the presence of the membrane modulates the molecular activities denoting the early inflammation (L) as well as bone formation (M) and remodeling, which provides molecular evidence for the enhanced bone regeneration in the membrane‐treated defect. Furthermore, the correlation analysis (insert Table) demonstrates that the molecular activities in the defect are linked to the molecular activities in the overlying membrane. CatK, cathepsin K; OC, osteocalcin. The montage is adapted on the basis of data from turri a and coworkers 180.
Figure 5
Figure 5
A schematic illustration of the cellular and molecular cascades during guided bone regeneration. The experimentally induced bone defect is covered with porcine collagen membrane (with inherent proteins). The cellular and molecular cascades include: migration of different cells (e.g. CD68‐positive monocytes/macrophages and periostin‐positive osteoprogenitors) from the surrounding tissue into the membrane. The cells which have migrated into the membrane express and secrete factors pivotal for bone formation and bone remodeling. This promotes the development of mature remodeled bone in the underlying defect, by stimulating the activity of osteoblasts and osteoclasts, the main cells of bone formation and remodeling. The cellular and molecular activities inside the membrane correlate with the pro‐osteogenic and bone‐remodeling molecular pattern in the bone defect underneath the membrane. The presence of the membrane and its bioactive properties promote a higher degree of bone regeneration and restitution of the defect in comparison with the defect without membrane. BMP‐2, bone morphogenetic protein 2; CatK, cathepsin K; CD68, cluster of differentiation 68; CR, calcitonin receptor; FGF‐2, fibroblast growth factor 2; OC, osteocalcin; RANKL, receptor activator of nuclear factor kappa‐B ligand; TGF‐β, transforming growth factor‐β; VEGF, vascular endothelial growth factor.

References

    1. Chiapasco M, Zaniboni M, Boisco M. Augmentation procedures for the rehabilitation of deficient edentulous ridges with oral implants. Clin Oral Implants Res 2006; 17(Suppl): 136–159.
    1. Bernstein S, Cooke J, Fotek P, Wang HL. Vertical bone augmentation: where are we now? Implant Dent 2006; 15: 219–228.
    1. Donos N, Mardas N, Chadha V. Clinical outcomes of implants following lateral bone augmentation: systematic assessment of available options (barrier membranes, bone grafts, split osteotomy). J Clin Periodontol 2008; 35: 173–202.
    1. Rocchietta I, Fontana F, Simion M. Clinical outcomes of vertical bone augmentation to enable dental implant placement: a systematic review. J Clin Periodontol 2008; 35: 203–215.
    1. Hammerle CH, Jung RE. Bone augmentation by means of barrier membranes. Periodontol 2000 2003; 33: 36–53.
    1. Rakhmatia YD, Ayukawa Y, Furuhashi A, Koyano K. Current barrier membranes: titanium mesh and other membranes for guided bone regeneration in dental applications. J Prosthodont Res 2013; 57: 3–14.
    1. Chiapasco M, Zaniboni M. Clinical outcomes of GBR procedures to correct peri‐implant dehiscences and fenestrations: a systematic review. Clin Oral Implants Res 2009; 20(Suppl): 113–123.
    1. Benic GI, Hammerle CH. Horizontal bone augmentation by means of guided bone regeneration. Periodontol 2000 2014; 66: 13–40.
    1. Laney WR. Glossary of oral and maxillofacial implants. Berlin: Quintessence Publishing Co Ltd, 2007; 1–212.
    1. Retzepi M, Donos N. Guided Bone Regeneration: biological principle and therapeutic applications. Clin Oral Implants Res 2010; 21: 567–576.
    1. Dimitriou R, Mataliotakis GI, Calori GM, Giannoudis PV. The role of barrier membranes for guided bone regeneration and restoration of large bone defects: current experimental and clinical evidence. BMC Med 2012; 10: 1–24.
    1. Bornstein MM, Halbritter S, Harnisch H, Weber HP, Buser D. A retrospective analysis of patients referred for implant placement to a specialty clinic: indications, surgical procedures, and early failures. Int J Oral Maxillofac Implants 2008; 23: 1109–1116.
    1. Clementini M, Morlupi A, Canullo L, Agrestini C, Barlattani A. Success rate of dental implants inserted in horizontal and vertical guided bone regenerated areas: a systematic review. Int J Oral Maxillofac Surg 2012; 41: 847–852.
    1. Jensen SS, Terheyden H. Bone augmentation procedures in localized defects in the alveolar ridge: clinical results with different bone grafts and bone‐substitute materials. Int J Oral Maxillofac Implants 2009; 24(Suppl): 218–236.
    1. Hammerle CH, Jung RE, Feloutzis A. A systematic review of the survival of implants in bone sites augmented with barrier membranes (guided bone regeneration) in partially edentulous patients. J Clin Periodontol 2002; 29(Suppl): 226–231; discussion 232–223.
    1. Liu J, Kerns DG. Mechanisms of guided bone regeneration: a review. Open Dent J 2014; 8: 56–65.
    1. Bottino MC, Thomas V, Schmidt G, Vohra YK, Chu TM, Kowolik MJ, Janowski GM. Recent advances in the development of GTR/GBR membranes for periodontal regeneration–a materials perspective. Dent Mater 2012; 28: 703–721.
    1. Sam G, Pillai BR. Evolution of barrier membranes in periodontal regeneration‐”are the third generation membranes really here?”. J Clin Diagn Res 2014; 8: Ze14–Ze17.
    1. Aghaloo TL, Moy PK. Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants 2007; 22(Suppl): 49–70.
    1. Tan WL, Wong TL, Wong MC, Lang NP. A systematic review of post‐extractional alveolar hard and soft tissue dimensional changes in humans. Clin Oral Implants Res 2012; 23(Suppl): 1–21.
    1. Esposito M, Grusovin MG, Felice P, Karatzopoulos G, Worthington HV, Coulthard P. The efficacy of horizontal and vertical bone augmentation procedures for dental implants ‐ a Cochrane systematic review. Eur J Oral Implantol 2009; 2: 167–184.
    1. Zitzmann NU, Naef R, Scharer P. Resorbable versus nonresorbable membranes in combination with Bio‐Oss for guided bone regeneration. Int J Oral Maxillofac Implants 1997; 12: 844–852.
    1. McAllister BS, Haghighat K. Bone augmentation techniques. J Periodontol 2007; 78: 377–396.
    1. Chiapasco M, Zaniboni M. Clinical outcomes of GBR procedures to correct peri‐implant dehiscences and fenestrations: a systematic review. Clin Oral Implants Res 2009; 20(Suppl 4): 113–123.
    1. Merli M, Migani M, Bernardelli F, Esposito M. Vertical bone augmentation with dental implant placement: efficacy and complications associated with 2 different techniques. A retrospective cohort study. Int J Oral Maxillofac Implants 2006; 21: 600–606.
    1. Simion M, Jovanovic SA, Trisi P, Scarano A, Piattelli A. Vertical ridge augmentation around dental implants using a membrane technique and autogenous bone or allografts in humans. Int J Periodontics Restorative Dent 1998; 18: 8–23.
    1. Simion M, Fontana F, Rasperini G, Maiorana C. Vertical ridge augmentation by expanded‐polytetrafluoroethylene membrane and a combination of intraoral autogenous bone graft and deproteinized anorganic bovine bone (Bio Oss). Clin Oral Implants Res 2007; 18: 620–629.
    1. Canullo L, Malagnino VA. Vertical ridge augmentation around implants by e‐PTFE titanium‐reinforced membrane and bovine bone matrix: a 24‐ to 54‐month study of 10 consecutive cases. Int J Oral Maxillofac Implants 2008; 23: 858–866.
    1. Langer B, Langer L, Sullivan RM. Vertical ridge augmentation procedure using guided bone regeneration, demineralized freeze‐dried bone allograft, and miniscrews: 4‐ to 13‐year observations on loaded implants. Int J Periodontics Restorative Dent 2010; 30: 227–235.
    1. Tinti C, Parma‐Benfenati S. Vertical ridge augmentation: surgical protocol and retrospective evaluation of 48 consecutively inserted implants. Int J Periodontics Restorative Dent 1998; 18: 434–443.
    1. Keestra JA, Barry O, Jong L, Wahl G. Long‐term effects of vertical bone augmentation: a systematic review. J Appl Oral Sci 2016; 24: 3–17.
    1. Urban IA, Monje A, Lozada JL, Wang HL. Long‐term evaluation of peri‐implant bone level after reconstruction of severely atrophic edentulous maxilla via vertical and horizontal guided bone regeneration in combination with sinus augmentation: a case series with 1 to 15 years of loading. Clin Implant Dent Relat Res 2017; 19: 46–55.
    1. Soldatos NK, Stylianou P, Koidou VP, Angelov N, Yukna R, Romanos GE. Limitations and options using resorbable versus nonresorbable membranes for successful guided bone regeneration. Quintessence Int 2017; 48: 131–147.
    1. Jung RE, Thoma DS, Hammerle CH. Assessment of the potential of growth factors for localized alveolar ridge augmentation: a systematic review. J Clin Periodontol 2008; 35: 255–281.
    1. Pilipchuk SP, Plonka AB, Monje A, Taut AD, Lanis A, Kang B, Giannobile WV. Tissue engineering for bone regeneration and osseointegration in the oral cavity. Dent Mater 2015; 31: 317–338.
    1. Amorfini L, Migliorati M, Signori A, Silvestrini‐Biavati A, Benedicenti S. Block allograft technique versus standard guided bone regeneration: a randomized clinical trial. Clin Implant Dent Relat Res 2014; 16: 655–667.
    1. Miron RJ, Zucchelli G, Pikos MA, Salama M, Lee S, Guillemette V, Fujioka‐Kobayashi M, Bishara M, Zhang Y, Wang HL, Chandad F, Nacopoulos C, Simonpieri A, Aalam AA, Felice P, Sammartino G, Ghanaati S, Hernandez MA, Choukroun J. Use of platelet‐rich fibrin in regenerative dentistry: a systematic review. Clin Oral Investig 2017; 21: 1913–1927.
    1. Chen TL, Lu HJ, Liu GQ, Tang DH, Zhang XH, Pan ZL, Wang SF, Zhang QF. Effect of autologous platelet‐rich plasma in combination with bovine porous bone mineral and bio‐guide membrane on bone regeneration in mandible bicortical bony defects. J Craniofac Surg 2014; 25: 215–223.
    1. Eskan MA, Greenwell H, Hill M, Morton D, Vidal R, Shumway B, Girouard ME. Platelet‐rich plasma‐assisted guided bone regeneration for ridge augmentation: a randomized, controlled clinical trial. J Periodontol 2014; 85: 661–668.
    1. He L, Lin Y, Hu X, Zhang Y, Wu H. A comparative study of platelet‐rich fibrin (PRF) and platelet‐rich plasma (PRP) on the effect of proliferation and differentiation of rat osteoblasts in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009; 108: 707–713.
    1. Ozdemir H, Ezirganli S, Isa Kara M, Mihmanli A, Baris E. Effects of platelet rich fibrin alone used with rigid titanium barrier. Arch Oral Biol 2013; 58: 537–544.
    1. Pieri F, Lucarelli E, Corinaldesi G, Fini M, Aldini NN, Giardino R, Donati D, Marchetti C. Effect of mesenchymal stem cells and platelet‐rich plasma on the healing of standardized bone defects in the alveolar ridge: a comparative histomorphometric study in minipigs. J Oral Maxillofac Surg 2009; 67: 265–272.
    1. Dhurat R, Sukesh M. Principles and methods of preparation of platelet‐rich plasma: a review and author's perspective. J Cutan Aesthet Surg 2014; 7: 189–197.
    1. Kang YH, Jeon SH, Park JY, Chung JH, Choung YH, Choung HW, Kim ES, Choung PH. Platelet‐rich fibrin is a Bioscaffold and reservoir of growth factors for tissue regeneration. Tissue Eng Part A 2011; 17: 349–359.
    1. Naik B, Karunakar P, Jayadev M, Marshal VR. Role of Platelet rich fibrin in wound healing: A critical review. J Conserv Dent 2013; 16: 284–293.
    1. Agarwal A, Gupta ND, Jain A. Platelet rich fibrin combined with decalcified freeze‐dried bone allograft for the treatment of human intrabony periodontal defects: a randomized split mouth clinical trail. Acta Odontol Scand 2016; 74: 36–43.
    1. Toffler M, Toscano N, Holtzclaw D. Osteotome‐mediated sinus floor elevation using only platelet‐rich fibrin: an early report on 110 patients. Implant Dent 2010; 19: 447–456.
    1. Vijayalakshmi R, Rajmohan CS, Deepalakshmi D, Sivakami G. Use of platelet rich fibrin in a fenestration defect around an implant. J Indian Soc Periodontol 2012; 16: 108–112.
    1. Kawase T, Kamiya M, Kobayashi M, Tanaka T, Okuda K, Wolff LF, Yoshie H. The heat‐compression technique for the conversion of platelet‐rich fibrin preparation to a barrier membrane with a reduced rate of biodegradation. J Biomed Mater Res B Appl Biomater 2015; 103: 825–831.
    1. Sheikh Z, Abdallah M, Hamdan N, Javaid M, Khurshid Z, Matilinna K. Barrier membranes for tissue regeneration and bone augmentation techniques in dentistry In: Matinlinna J, ed. Handbook of oral biomaterials. Singapore: Pan Stanford Publishing, 2014; 605–636.
    1. Carbonell JM, Martin IS, Santos A, Pujol A, Sanz‐Moliner JD, Nart J. High‐density polytetrafluoroethylene membranes in guided bone and tissue regeneration procedures: a literature review. Int J Oral Maxillofac Surg 2014; 43: 75–84.
    1. Gentile P, Chiono V, Tonda‐Turo C, Ferreira AM, Ciardelli G. Polymeric membranes for guided bone regeneration. Biotechnol J 2011; 6: 1187–1197.
    1. Ali SA, Karthigeyan S, Deivanai M, Kumar A. Implant rehabilitation for atrophic maxilla: a review. J Indian Prosthodont Soc 2014; 14: 196–207.
    1. Hutmacher D, Hurzeler MB, Schliephake H. A review of material properties of biodegradable and bioresorbable polymers and devices for GTR and GBR applications. Int J Oral Maxillofac Implants 1996; 11: 667–678.
    1. Piattelli A, Scarano A, Coraggio F, Matarasso S. Early tissue reactions to polylactic acid resorbable membranes: a histological and histochemical study in rabbit. Biomaterials 1998; 19: 889–896.
    1. Hurzeler MB, Quinones CR, Schupbach P. Guided bone regeneration around dental implants in the atrophic alveolar ridge using a bioresorbable barrier. An experimental study in the monkey. Clin Oral Implants Res 1997; 8: 323–331.
    1. Lekovic V, Camargo PM, Klokkevold PR, Weinlaender M, Kenney EB, Dimitrijevic B, Nedic M. Preservation of alveolar bone in extraction sockets using bioabsorbable membranes. J Periodontol 1998; 69: 1044–1049.
    1. Meinig RP. Clinical use of resorbable polymeric membranes in the treatment of bone defects. Orthop Clin North Am 2010; 41: 39–47.
    1. 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.
    1. Liu SH, Yang RS, al‐Shaikh R, Lane JM. Collagen in tendon, ligament, and bone healing. A current review. Clin Orthop Relat Res 1995; 318: 265–278.
    1. Bunyaratavej P, Wang H‐L. Collagen membranes: a review. J Periodontol 2001; 72: 215–229.
    1. Rothamel D, Schwarz F, Sager M, Herten M, Sculean A, Becker J. Biodegradation of differently cross‐linked collagen membranes: an experimental study in the rat. Clin Oral Implants Res 2005; 16: 369–378.
    1. Jorge‐Herrero E, Fernandez P, Turnay J, Olmo N, Calero P, García R, Freile I, Castillo‐Olivares J. Influence of different chemical cross‐linking treatments on the properties of bovine pericardium and collagen. Biomaterials 1999; 20: 539–545.
    1. Speer DP, Chvapil M, Eskelson CD, Ulreich J. Biological effects of residual glutaraldehyde in glutaraldehyde‐tanned collagen biomaterials. J Biomed Mater Res 1980; 14: 753–764.
    1. 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.
    1. Tal H, Kozlovsky A, Nemcovsky C, Moses O. Bioresorbable collagen membranes for guided bone regeneration In: Tal H, ed. Bone regeneration. Croatia: InTech, 2012; 111–139.
    1. Zubery Y, Nir E, Goldlust A. Ossification of a collagen membrane cross‐linked by sugar: a human case series. J Periodontol 2008; 79: 1101–1107.
    1. Bottino MC, Thomas V, Jose MV, Dean DR, Janowski GM. Acellular dermal matrix graft: synergistic effect of rehydration and natural crosslinking on mechanical properties. J Biomed Mater Res B Appl Biomater 2010; 95: 276–282.
    1. Friedmann A, Gissel K, Soudan M, Kleber BM, Pitaru S, Dietrich T. Randomized controlled trial on lateral augmentation using two collagen membranes: morphometric results on mineralized tissue compound. J Clin Periodontol 2011; 38: 677–685.
    1. Fernandes PG, Novaes AB Jr, de Queiroz AC, de Souza SL, Taba M Jr, Palioto DB, Grisi MF. Ridge preservation with acellular dermal matrix and anorganic bone matrix cell‐binding peptide P‐15 after tooth extraction in humans. J Periodontol 2011; 82: 72–79.
    1. Bondioli E, Fini M, Veronesi F, Giavaresi G, Tschon M, Cenacchi G, Cerasoli S, Giardino R, Melandri D. Development and evaluation of a decellularized membrane from human dermis. J Tissue Eng Regen Med 2014; 8: 325–336.
    1. Wainwright DJ. Use of an acellular allograft dermal matrix (AlloDerm) in the management of full‐thickness burns. Burns 1995; 21: 243–248.
    1. Luczyszyn SM, Papalexiou V, Novaes AB Jr, Grisi MF, Souza SL, Taba M Jr. Acellular dermal matrix and hydroxyapatite in prevention of ridge deformities after tooth extraction. Implant Dent 2005; 14: 176–184.
    1. Fotek PD, Neiva RF, Wang HL. Comparison of dermal matrix and polytetrafluoroethylene membrane for socket bone augmentation: a clinical and histologic study. J Periodontol 2009; 80: 776–785.
    1. Park SH, Lee KW, Oh TJ, Misch CE, Shotwell J, Wang HL. Effect of absorbable membranes on sandwich bone augmentation. Clin Oral Implants Res 2008; 19: 32–41.
    1. Piattelli M, Scarano A, Piattelli A. Histological evaluation of freeze‐dried dura mater (FDDMA) used in guided bone regeneration (GBR): a time course study in man. Biomaterials 1996; 17: 2319–2323.
    1. Vidyadharan AK, Ravindran A. Localized ridge defect augmentation using human pericardium membrane and demineralized bone matrix. Indian J Dent Res 2014; 25: 445–448.
    1. Gomes MF, dos Anjos MJ, Nogueira TO, Guimaraes SA. Histologic evaluation of the osteoinductive property of autogenous demineralized dentin matrix on surgical bone defects in rabbit skulls using human amniotic membrane for guided bone regeneration. Int J Oral Maxillofac Implants 2001; 16: 563–571.
    1. Li W, Ma G, Brazile B, Li N, Dai W, Butler JR, Claude AA, Wertheim JA, Liao J, Wang B. Investigating the potential of amnion‐based scaffolds as a barrier membrane for guided bone regeneration. Langmuir 2015; 31: 8642–8653.
    1. Pillai C, Paul W, Sharma CP. Chitin and chitosan polymers: Chemistry, solubility and fiber formation. Prog Polym Sci 2009; 34: 641–678.
    1. Ma S, Chen Z, Qiao F, Sun Y, Yang X, Deng X, Cen L, Cai Q, Wu M, Zhang X, Gao P. Guided bone regeneration with tripolyphosphate cross‐linked asymmetric chitosan membrane. J Dent 2014; 42: 1603–1612.
    1. Lee KY, Mooney DJ. Alginate: properties and biomedical applications. Prog Polym Sci 2012; 37: 106–126.
    1. 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.
    1. Kuo SM, Chang SJ, Chen TW, Kuan TC. Guided tissue regeneration for using a chitosan membrane: an experimental study in rats. J Biomed Mater Res A 2006; 76: 408–415.
    1. 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.
    1. Teng SH, Lee EJ, Yoon BH, Shin DS, Kim HE, Oh JS. Chitosan/nanohydroxyapatite composite membranes via dynamic filtration for guided bone regeneration. J Biomed Mater Res A 2009; 88: 569–580.
    1. Song JM, Shin SH, Kim YD, Lee JY, Baek YJ, Yoon SY, Kim HS. Comparative study of chitosan/fibroin‐hydroxyapatite and collagen membranes for guided bone regeneration in rat calvarial defects: micro‐computed tomography analysis. Int J Oral Sci 2014; 6: 87–93.
    1. 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.
    1. 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.
    1. 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.
    1. He H, Huang J, Shi J, Ping F, Chen G, Dong Y. Haversian remodeling in guided bone regeneration with calcium alginate film in circular bone defect model of rabbit. Artif Cells Blood Substit Immobil Biotechnol 2007; 35: 533–542.
    1. He H, Huang J, Ping F, Sun G, Chen G. Calcium alginate film used for guided bone regeneration in mandible defects in a rabbit model. Cranio 2008; 26: 65–70.
    1. Brunette DM. Titanium in medicine: material science, surface science, engineering, biological responses and medical applications. Berlin: Springer, 2001.
    1. Boyne PJ. Restoration of osseous defects in maxillofacial casualities. J Am Dent Assoc 1969; 78: 767–776.
    1. Artzi Z, Dayan D, Alpern Y, Nemcovsky CE. Vertical ridge augmentation using xenogenic material supported by a configured titanium mesh: clinicohistopathologic and histochemical study. Int J Oral Maxillofac Implants 2003; 18: 440–446.
    1. Degidi M, Scarano A, Piattelli A. Regeneration of the alveolar crest using titanium micromesh with autologous bone and a resorbable membrane. J Oral Implantol 2003; 29: 86–90.
    1. Proussaefs P, Lozada J, Kleinman A, Rohrer MD, McMillan PJ. The use of titanium mesh in conjunction with autogenous bone graft and inorganic bovine bone mineral (bio‐oss) for localized alveolar ridge augmentation: a human study. Int J Periodontics Restorative Dent 2003; 23: 185–195.
    1. Roccuzzo M, Ramieri G, Spada MC, Bianchi SD, Berrone S. Vertical alveolar ridge augmentation by means of a titanium mesh and autogenous bone grafts. Clin Oral Implants Res 2004; 15: 73–81.
    1. Proussaefs P, Lozada J. Use of titanium mesh for staged localized alveolar ridge augmentation: clinical and histologic‐histomorphometric evaluation. J Oral Implantol 2006; 32: 237–247.
    1. Roccuzzo M, Ramieri G, Bunino M, Berrone S. Autogenous bone graft alone or associated with titanium mesh for vertical alveolar ridge augmentation: a controlled clinical trial. Clin Oral Implants Res 2007; 18: 286–294.
    1. Louis PJ, Gutta R, Said‐Al‐Naief N, Bartolucci AA. Reconstruction of the maxilla and mandible with particulate bone graft and titanium mesh for implant placement. J Oral Maxillofac Surg 2008; 66: 235–245.
    1. Corinaldesi G, Pieri F, Sapigni L, Marchetti C. Evaluation of survival and success rates of dental implants placed at the time of or after alveolar ridge augmentation with an autogenous mandibular bone graft and titanium mesh: a 3‐ to 8‐year retrospective study. Int J Oral Maxillofac Implants 2009; 24: 1119–1128.
    1. Funato A, Ishikawa T, Kitajima H, Yamada M, Moroi H. A novel combined surgical approach to vertical alveolar ridge augmentation with titanium mesh, resorbable membrane, and rhPDGF‐BB: a retrospective consecutive case series. Int J Periodontics Restorative Dent 2013; 33: 437–445.
    1. Poli PP, Beretta M, Cicciu M, Maiorana C. Alveolar ridge augmentation with titanium mesh. A retrospective clinical study. Open . Dent J 2014; 8: 148–158.
    1. Misch CM, Jensen OT, Pikos MA, Malmquist JP. Vertical bone augmentation using recombinant bone morphogenetic protein, mineralized bone allograft, and titanium mesh: a retrospective cone beam computed tomography study. Int J Oral Maxillofac Implants 2015; 30: 202–207.
    1. von Arx T, Kurt B. Implant placement and simultaneous ridge augmentation using autogenous bone and a micro titanium mesh: a prospective clinical study with 20 implants. Clin Oral Implants Res 1999; 10: 24–33.
    1. Assenza B, Piattelli M, Scarano A, Lezzi G, Petrone G, Piattelli A. Localized ridge augmentation using titanium micromesh. J Oral Implantol 2001; 27: 287–292.
    1. Maiorana C, Santoro F, Rabagliati M, Salina S. Evaluation of the use of iliac cancellous bone and anorganic bovine bone in the reconstruction of the atrophic maxilla with titanium mesh: a clinical and histologic investigation. Int J Oral Maxillofac Implants 2001; 16: 427–432.
    1. Malchiodi L, Scarano A, Quaranta M, Piattelli A. Rigid fixation by means of titanium mesh in edentulous ridge expansion for horizontal ridge augmentation in the maxilla. Int J Oral Maxillofac Implants 1998; 13: 701–705.
    1. von Arx T, Kurt B. Implant placement and simultaneous peri‐implant bone grafting using a micro titanium mesh for graft stabilization. Int J Periodontics Restorative Dent 1998; 18: 117–127.
    1. Di Stefano DA, Greco GB, Cinci L, Pieri L. Horizontal‐guided bone regeneration using a titanium mesh and an equine bone graft. J Contemp Dent Pract 2015; 16: 154–162.
    1. von Arx T, Hardt N, Wallkamm B. The TIME technique: a new method for localized alveolar ridge augmentation prior to placement of dental implants. Int J Oral Maxillofac Implants 1996; 11: 387–394.
    1. Torres J, Tamimi F, Alkhraisat MH, Manchon A, Linares R, Prados‐Frutos JC, Hernandez G, Lopez Cabarcos E. Platelet‐rich plasma may prevent titanium‐mesh exposure in alveolar ridge augmentation with anorganic bovine bone. J Clin Periodontol 2010; 37: 943–951.
    1. Her S, Kang T, Fien MJ. Titanium mesh as an alternative to a membrane for ridge augmentation. J Oral Maxillofac Surg 2012; 70: 803–810.
    1. Ricci L, Perrotti V, Ravera L, Scarano A, Piattelli A, Iezzi G. Rehabilitation of deficient alveolar ridges using titanium grids before and simultaneously with implant placement: a systematic review. J Periodontol 2013; 84: 1234–1242.
    1. Lundgren AK, Sennerby L, Lundgren D. Guided jaw‐bone regeneration using an experimental rabbit model. Int J Oral Maxillofac Surg 1998; 27: 135–140.
    1. Gaggl A, Schultes G. Titanium foil‐guided tissue regeneration in the treatment of periimplant bone defects. Implant Dent 1999; 8: 368–375.
    1. Watzinger F, Luksch J, Millesi W, Schopper C, Neugebauer J, Moser D, Ewers R. Guided bone regeneration with titanium membranes: a clinical study. Br J Oral Maxillofac Surg 2000; 38: 312–315.
    1. Van Steenberghe D, Johansson C, Quirynen M, Molly L, Albrektsson T, Naert I. Bone augmentation by means of a stiff occlusive titanium barrier. Clin Oral Implants Res 2003; 14: 63–71.
    1. Molly L, Quirynen M, Michiels K, van Steenberghe D. Comparison between jaw bone augmentation by means of a stiff occlusive titanium membrane or an autologous hip graft: a retrospective clinical assessment. Clin Oral Implants Res 2006; 17: 481–487.
    1. Shah FA, Trobos M, Thomsen P, Palmquist A. Commercially pure titanium (cp‐Ti) versus titanium alloy (Ti6Al4V) materials as bone anchored implants ‐ Is one truly better than the other? Mater Sci Eng C Mater Biol Appl 2016; 62: 960–966.
    1. Rosengren A, Johansson BR, Danielsen N, Thomsen P, Ericson LE. Immunohistochemical studies on the distribution of albumin, fibrinogen, fibronectin, IgG and collagen around PTFE and titanium implants. Biomaterials 1996; 17: 1779–1786.
    1. Decco O, Cura A, Beltran V, Lezcano M, Engelke W. Bone augmentation in rabbit tibia using microfixed cobalt‐chromium membranes with whole blood, tricalcium phosphate and bone marrow cells. Int J Clin Exp Med 2015; 8: 135–144.
    1. Di Alberti L, Tamborrino F, Lo Muzio L, D'Agostino A, Trevisiol L, De Santis D, Nocini PF, Bertossi D. Calcium sulfate barrier for regeneration of human bone defects. 3 years randomized controlled study. Minerva Stomatol 2013; [Epub ahead of print].
    1. Harris RJ. Clinical evaluation of a composite bone graft with a calcium sulfate barrier. J Periodontol 2004; 75: 685–692.
    1. Pecora G, Andreana S, Margarone JE 3rd, Covani U, Sottosanti JS. Bone regeneration with a calcium sulfate barrier. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1997; 84: 424–429.
    1. Melo LG, Nagata MJ, Bosco AF, Ribeiro LL, Leite CM. Bone healing in surgically created defects treated with either bioactive glass particles, a calcium sulfate barrier, or a combination of both materials. A histological and histometric study in rat tibias. Clin Oral Implants Res 2005; 16: 683–691.
    1. Camargo PM, Lekovic V, Weinlaender M, Klokkevold PR, Kenney EB, Dimitrijevic B, Nedic M, Jancovic S, Orsini M. Influence of bioactive glass on changes in alveolar process dimensions after exodontia. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000; 90: 581–586.
    1. Couri CJ, Maze GI, Hinkson DW, Collins BH 3rd, Dawson DV. Medical grade calcium sulfate hemihydrate versus expanded polytetrafluoroethylene in the treatment of mandibular class II furcations. J Periodontol 2002; 73: 1352–1359.
    1. Anderud J, Jimbo R, Abrahamsson P, Isaksson SG, Adolfsson E, Malmstrom J, Kozai Y, Hallmer F, Wennerberg A. Guided bone augmentation using a ceramic space‐maintaining device. Oral Surg Oral Med Oral Pathol Oral Radiol 2014; 118: 532–538.
    1. Li J, Man Y, Zuo Y, Zhang L, Huang C, Liu M, Li Y. In vitro and in vivo evaluation of a nHA/PA66 composite membrane for guided bone regeneration. J Biomater Sci Polym Ed 2011; 22: 263–275.
    1. Basile MA, d'Ayala GG, Malinconico M, Laurienzo P, Coudane J, Nottelet B, Ragione FD, Oliva A. Functionalized PCL/HA nanocomposites as microporous membranes for bone regeneration. Mater Sci Eng C Mater Biol Appl 2015; 48: 457–468.
    1. Ribeiro N, Sousa SR, van Blitterswijk CA, Moroni L, Monteiro FJ. A biocomposite of collagen nanofibers and nanohydroxyapatite for bone regeneration. Biofabrication 2014; 6: 035015.
    1. Veríssimo DM, Leitão RF, Figueiró SD, Góes JC, Lima V, Silveira CO, Brito GA. Guided bone regeneration produced by new mineralized and reticulated collagen membranes in critical‐sized rat calvarial defects. Experimental Biology and Medicine 2015; 240: 175–184.
    1. Kitayama S, Wong LO, Ma L, Hao J, Kasugai S, Lang NP, Mattheos N. Regeneration of rabbit calvarial defects using biphasic calcium phosphate and a strontium hydroxyapatite‐containing collagen membrane. Clin Oral Implants Res 2016; 27: e206–e214.
    1. Hao J, Acharya A, Chen K, Chou J, Kasugai S, Lang NP. Novel bioresorbable strontium hydroxyapatite membrane for guided bone regeneration. Clin Oral Implants Res 2015; 26: 1–7.
    1. Li J, Zuo Y, Man Y, Mo A, Huang C, Liu M, Jansen JA, Li Y. Fabrication and biocompatibility of an antimicrobial composite membrane with an asymmetric porous structure. J Biomater Sci Polym Ed 2012; 23: 81–96.
    1. Chou J, Komuro M, Hao J, Kuroda S, Hattori Y, Ben‐Nissan B, Milthorpe B, Otsuka M. Bioresorbable zinc hydroxyapatite guided bone regeneration membrane for bone regeneration. Clin Oral Implants Res 2016; 27: 354–360.
    1. Shim JH, Huh JB, Park JY, Jeon YC, Kang SS, Kim JY, Rhie JW, Cho DW. Fabrication of blended polycaprolactone/poly(lactic‐co‐glycolic acid)/beta‐tricalcium phosphate thin membrane using solid freeform fabrication technology for guided bone regeneration. Tissue Eng Part A 2013; 19: 317–328.
    1. Lee HH, Yu HS, Jang JH, Kim HW. Bioactivity improvement of poly(epsilon‐caprolactone) membrane with the addition of nanofibrous bioactive glass. Acta Biomater 2008; 4: 622–629.
    1. Tirri T, Rich J, Wolke J, Seppala J, Yli‐Urpo A, Narhi TO. Bioactive glass induced in vitro apatite formation on composite GBR membranes. J Mater Sci Mater Med 2008; 19: 2919–2923.
    1. Mota J, Yu N, Caridade SG, Luz GM, Gomes ME, Reis RL, Jansen JA, Walboomers XF, Mano JF. Chitosan/bioactive glass nanoparticle composite membranes for periodontal regeneration. Acta Biomater 2012; 8: 4173–4180.
    1. Leal AI, Caridade SG, Ma J, Yu N, Gomes ME, Reis RL, Jansen JA, Walboomers XF, Mano JF. Asymmetric PDLLA membranes containing Bioglass(R) for guided tissue regeneration: characterization and in vitro biological behavior. Dent Mater 2013; 29: 427–436.
    1. 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.
    1. Puumanen K, Kellomaki M, Ritsila V, Bohling T, Tormala P, Waris T, Ashammakhi N. A novel bioabsorbable composite membrane of Polyactive 70/30 and bioactive glass number 13–93 in repair of experimental maxillary alveolar cleft defects. J Biomed Mater Res B Appl Biomater 2005; 75: 25–33.
    1. Jovanovic SA, Schenk RK, Orsini M, Kenney EB. Supracrestal bone formation around dental implants: an experimental dog study. Int J Oral Maxillofac Implants 1995; 10: 23–31.
    1. Strietzel FP, Khongkhunthian P, Khattiya R, Patchanee P, Reichart PA. Healing pattern of bone defects covered by different membrane types–a histologic study in the porcine mandible. J Biomed Mater Res B Appl Biomater 2006; 78: 35–46.
    1. Carpio L, Loza J, Lynch S, Genco R. Guided bone regeneration around endosseous implants with anorganic bovine bone mineral. A randomized controlled trial comparing bioabsorbable versus non‐resorbable barriers. J Periodontol 2000; 71: 1743–1749.
    1. 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.
    1. Hammerle CH, Jung RE, Yaman D, Lang NP. Ridge augmentation by applying bioresorbable membranes and deproteinized bovine bone mineral: a report of twelve consecutive cases. Clin Oral Implants Res 2008; 19: 19–25.
    1. Chasioti E, Chiang TF, Drew HJ. Maintaining space in localized ridge augmentation using guided bone regeneration with tenting screw technology. Quintessence Int 2013; 44: 763–771.
    1. Li J, Zuo Y, Cheng X, Yang W, Wang H, Li Y. Preparation and characterization of nano‐hydroxyapatite/polyamide 66 composite GBR membrane with asymmetric porous structure. J Mater Sci Mater Med 2009; 20: 1031–1038.
    1. Lee SB, Kwon JS, Lee YK, Kim KM, Kim KN. Bioactivity and mechanical properties of collagen composite membranes reinforced by chitosan and beta‐tricalcium phosphate. J Biomed Mater Res B Appl Biomater 2012; 100: 1935–1942.
    1. Zeng S, Fu S, Guo G, Liang H, Qian Z, Tang X, Luo F. Preparation and characterization of nano‐hydroxyapatite/poly(vinyl alcohol) composite membranes for guided bone regeneration. J Biomed Nanotechnol 2011; 7: 549–557.
    1. Duan H, Yang H, Xiong Y, Zhang B, Ren C, Min L, Zhang W, Yan Y, Li H, Pei F, Tu C. Effects of mechanical loading on the degradability and mechanical properties of the nanocalcium‐deficient hydroxyapatite‐multi(amino acid) copolymer composite membrane tube for guided bone regeneration. Int J Nanomedicine 2013; 8: 2801–2807.
    1. 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.
    1. Asano K, Matsuno T, Tabata Y, Satoh T. Preparation of thermoplastic poly(L‐lactic acid) membranes for guided bone regeneration. Int J Oral Maxillofac Implants 2013; 28: 973–981.
    1. Zellin G, Linde A. Effects of different osteopromotive membrane porosities on experimental bone neogenesis in rats. Biomaterials 1996; 17: 695–702.
    1. Lundgren A, Lundgren D, Taylor A. Influence of barrier occlusiveness on guided bone augmentation. An experimental study in the rat. Clin Oral Implants Res 1998; 9: 251–260.
    1. 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.
    1. Polimeni G, Koo KT, Qahash M, Xiropaidis AV, Albandar JM, Wikesjo UM. Prognostic factors for alveolar regeneration: effect of tissue occlusion on alveolar bone regeneration with guided tissue regeneration. J Clin Periodontol 2004; 31: 730–735.
    1. 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.
    1. 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.
    1. Oh SH, Kim JH, Kim JM, Lee JH. Asymmetrically porous PLGA/Pluronic F127 membrane for effective guided bone regeneration. J Biomater Sci Polym Ed 2006; 17: 1375–1387.
    1. Schmid J, Hammerle CH, Olah AJ, Lang NP. Membrane permeability is unnecessary for guided generation of new bone. An experimental study in the rabbit. Clin Oral Implants Res 1994; 5: 125–130.
    1. Bartee BK. The use of high‐density polytetrafluoroethylene membrane to treat osseous defects: clinical reports. Implant Dent 1995; 4: 21–26.
    1. Bartee BK. Evaluation of a new polytetrafluoroethylene guided tissue regeneration membrane in healing extraction sites. Compend Contin Educ Dent 1998; 19: 1256–1258, 1260, 1262–1254.
    1. Bartee BK, Carr JA. Evaluation of a high‐density polytetrafluoroethylene (n‐PTFE) membrane as a barrier material to facilitate guided bone regeneration in the rat mandible. J Oral Implantol 1995; 21: 88–95.
    1. Sela MN, Steinberg D, Klinger A, Krausz AA, Kohavi D. Adherence of periodontopathic bacteria to bioabsorbable and non‐absorbable barrier membranes in vitro. Clin Oral Implants Res 1999; 10: 445–452.
    1. Barber HD, Lignelli J, Smith BM, Bartee BK. Using a dense PTFE membrane without primary closure to achieve bone and tissue regeneration. J Oral Maxillofac Surg 2007; 65: 748–752.
    1. Waasdorp J, Feldman S. Bone regeneration around immediate implants utilizing a dense polytetrafluoroethylene membrane without primary closure: a report of 3 cases. J Oral Implantol 2013; 39: 355–361.
    1. Crump TB, Rivera‐Hidalgo F, Harrison JW, Williams FE, Guo IY. Influence of three membrane types on healing of bone defects. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996; 82: 365–374.
    1. Ronda M, Rebaudi A, Torelli L, Stacchi C. Expanded vs. dense polytetrafluoroethylene membranes in vertical ridge augmentation around dental implants: a prospective randomized controlled clinical trial. Clin Oral Implants Res 2014; 25: 859–866.
    1. Linde A, Thoren C, Dahlin C, Sandberg E. Creation of new bone by an osteopromotive membrane technique: an experimental study in rats. J Oral Maxillofac Surg 1993; 51: 892–897.
    1. Wikesjo UM, Qahash M, Thomson RC, Cook AD, Rohrer MD, Wozney JM, Hardwick WR. Space‐providing expanded polytetrafluoroethylene devices define alveolar augmentation at dental implants induced by recombinant human bone morphogenetic protein 2 in an absorbable collagen sponge carrier. Clin Implant Dent Relat Res 2003; 5: 112–123.
    1. Pineda LM, Busing M, Meinig RP, Gogolewski S. Bone regeneration with resorbable polymeric membranes. III. Effect of poly(L‐lactide) membrane pore size on the bone healing process in large defects. J Biomed Mater Res 1996; 31: 385–394.
    1. Gugala Z, Gogolewski S. Regeneration of segmental diaphyseal defects in sheep tibiae using resorbable polymeric membranes: a preliminary study. J Orthop Trauma 1999; 13: 187–195.
    1. Mardas N, Kostopoulos L, Stavropoulos A, Karring T. Evaluation of a cell‐permeable barrier for guided tissue regeneration combined with demineralized bone matrix. Clin Oral Implants Res 2003; 14: 812–818.
    1. Rothamel D, Schwarz F, Fienitz T, Smeets R, Dreiseidler T, Ritter L, Happe A, Zoller J. Biocompatibility and biodegradation of a native porcine pericardium membrane: results of in vitro and in vivo examinations. Int J Oral Maxillofac Implants 2012; 27: 146–154.
    1. Turri A, Elgali I, Vazirisani F, Johansson A, Emanuelsson L, Dahlin C, Thomsen P, Omar O. Guided bone regeneration is promoted by the molecular events in the membrane compartment. Biomaterials 2016; 84: 167–183.
    1. Ortolani E, Quadrini F, Bellisario D, Santo L, Polimeni A, Santarsiero A. Mechanical qualification of collagen membranes used in dentistry. Ann Ist Super Sanita 2015; 51: 229–235.
    1. Willershausen I, Barbeck M, Boehm N, Sader R, Willershausen B, Kirkpatrick CJ, Ghanaati S. Non‐cross‐linked collagen type I/III materials enhance cell proliferation: in vitro and in vivo evidence. J Appl Oral Sci 2014; 22: 29–37.
    1. Donos N, Kostopoulos L, Karring T. Alveolar ridge augmentation using a resorbable copolymer membrane and autogenous bone grafts. An experimental study in the rat. Clin Oral Implants Res 2002; 13: 203–213.
    1. 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.
    1. Bubalo M, Lazic Z, Matic S, Tatic Z, Milovic R, Curcin AP, Djurdjevic D, Loncarevic S. The impact of thickness of resorbable membrane of human origin on the ossification of bone defects: a pathohistologic study. Vojnosanit Pregl 2012; 69: 1076–1083.
    1. Shin SI, Herr Y, Kwon YH, Chung JH. Effect of a collagen membrane combined with a porous titanium membrane on exophytic new bone formation in a rabbit calvarial model. J Periodontol 2013; 84: 110–116.
    1. Busenlechner D, Kantor M, Tangl S, Tepper G, Zechner W, Haas R, Watzek G. Alveolar ridge augmentation with a prototype trilayer membrane and various bone grafts: a histomorphometric study in baboons. Clin Oral Implants Res 2005; 16: 220–227.
    1. Kim SH, Kim DY, Kim KH, Ku Y, Rhyu IC, Lee YM. The efficacy of a double‐layer collagen membrane technique for overlaying block grafts in a rabbit calvarium model. Clin Oral Implants Res 2009; 20: 1124–1132.
    1. Kozlovsky A, Aboodi G, Moses O, Tal H, Artzi Z, Weinreb M, Nemcovsky CE. Bio‐degradation of a resorbable collagen membrane (Bio‐Gide) applied in a double‐layer technique in rats. Clin Oral Implants Res 2009; 20: 1116–1123.
    1. Kostopoulos L, Karring T. Guided bone regeneration in mandibular defects in rats using a bioresorbable polymer. Clin Oral Implants Res 1994; 5: 66–74.
    1. Schlegel AK, Donath K, Weida S. Histological findings in guided bone regeneration (GBR) around titanium dental implants with autogenous bone chips using a new resorbable membrane. J Long Term Eff Med Implants 1998; 8: 211–224.
    1. Lundgren D, Lundgren AK, Sennerby L, Nyman S. Augmentation of intramembraneous bone beyond the skeletal envelope using an occlusive titanium barrier. An experimental study in the rabbit. Clin Oral Implants Res 1995; 6: 67–72.
    1. Zubery Y, Goldlust A, 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.
    1. Simion M, Dahlin C, Rocchietta I, Stavropoulos A, Sanchez R, Karring T. Vertical ridge augmentation with guided bone regeneration in association with dental implants: an experimental study in dogs. Clin Oral Implants Res 2007; 18: 86–94.
    1. Al‐Hezaimi K, Rudek I, Al‐Hamdan KS, Javed F, Nooh N, Wang HL. Efficacy of using a dual layer of membrane (dPTFE placed over collagen) for ridge preservation in fresh extraction sites: a micro‐computed tomographic study in dogs. Clin Oral Implants Res 2013; 24: 1152–1157.
    1. Benic GI, Thoma DS, Munoz F, Sanz Martin I, Jung RE, Hammerle CH. Guided bone regeneration of peri‐implant defects with particulated and block xenogenic bone substitutes. Clin Oral Implants Res 2015; 27: 567–576.
    1. Donos N, Graziani F, Mardas N, Kostopoulos L. The use of human hypertrophic chondrocytes‐derived extracellular matrix for the treatment of critical‐size calvarial defects. Clin Oral Implants Res 2011; 22: 1346–1353.
    1. Jardini MA, De Marco AC, Lima LA. Early healing pattern of autogenous bone grafts with and without e‐PTFE membranes: a histomorphometric study in rats. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2005; 100: 666–673.
    1. Queiroz TP, Hochuli‐Vieira E, Gabrielli MA, Cancian DC. Use of bovine bone graft and bone membrane in defects surgically created in the cranial vault of rabbits. Histologic comparative analysis. Int J Oral Maxillofac Implants 2006; 21: 29–35.
    1. Kim M, Kim JH, Lee JY, Cho K, Kang SS, Kim G, Lee MJ, Choi SH. Effect of bone mineral with or without collagen membrane in ridge dehiscence defects following premolar extraction. In Vivo 2008; 22: 231–236.
    1. Donos N, Lang NP, Karoussis IK, Bosshardt D, Tonetti M, Kostopoulos L. Effect of GBR in combination with deproteinized bovine bone mineral and/or enamel matrix proteins on the healing of critical‐size defects. Clin Oral Implants Res 2004; 15: 101–111.
    1. De Marco AC, Jardini MA, Modolo F, Nunes FD, de Lima LA. Immunolocalization of bone morphogenetic protein 2 during the early healing events after guided bone regeneration. Oral Surg Oral Med Oral Pathol Oral Radiol 2012; 113: 533–541.
    1. Ramalingam S, Al‐Rasheed A, ArRejaie A, Nooh N, Al‐Kindi M, Al‐Hezaimi K. Guided bone regeneration in standardized calvarial defects using beta‐tricalcium phosphate and collagen membrane: a real‐time in vivo micro‐computed tomographic experiment in rats. Odontology 2016; 104: 199–210.
    1. Jung UW, Lee JS, Lee G, Lee IK, Hwang JW, Kim MS, Choi SH, Chai JK. Role of collagen membrane in lateral onlay grafting with bovine hydroxyapatite incorporated with collagen matrix in dogs. J Periodontal Implant Sci 2013; 43: 64–71.
    1. Koerdt S, Ristow O, Wannhoff A, Kubler AC, Reuther T. Expression of growth factors during the healing process of alveolar ridge augmentation procedures using autogenous bone grafts in combination with GTR and an anorganic bovine bone substitute: an immunohistochemical study in the sheep. Clin Oral Investig 2014; 18: 179–188.
    1. 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; discussion 436–427.
    1. Taga ML, Granjeiro JM, Cestari TM, Taga R. Healing of critical‐size cranial defects in guinea pigs using a bovine bone‐derived resorbable membrane. Int J Oral Maxillofac Implants 2008; 23: 427–436.
    1. 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–Br73.
    1. Schwarz F, Mihatovic I, Golubovic V, Hegewald A, Becker J. Influence of two barrier membranes on staged guided bone regeneration and osseointegration of titanium implants in dogs: part 1. Augmentation using bone graft substitutes and autogenous bone. Clin Oral Implants Res 2012; 23: 83–89.
    1. Ge Y, Feng H, Wang L. Application of a novel resorbable membrane in the treatment of calvarial defects in rats. J Biomater Sci Polym Ed 2011; 22: 2417–2429.
    1. Bernabe 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.
    1. Ahn YS, Kim SG, Kim CS, Oh JS, Lim SC. Effect of guided bone regeneration with or without pericardium bioabsorbable membrane on bone formation. Oral Surg Oral Med Oral Pathol Oral Radiol 2012; 114: S126–S131.
    1. Guda T, Walker JA, Singleton BM, Hernandez JW, Son JS, Kim SG, Oh DS, Appleford MR, Ong JL, Wenke JC. Guided bone regeneration in long‐bone defects with a structural hydroxyapatite graft and collagen membrane. Tissue Eng Part A 2013; 19: 1879–1888.
    1. Cho KS, Choi SH, Han KH, Chai JK, Wikesjo UM, Kim CK. Alveolar bone formation at dental implant dehiscence defects following guided bone regeneration and xenogeneic freeze‐dried demineralized bone matrix. Clin Oral Implants Res 1998; 9: 419–428.
    1. Weng D, Poehling S, Pippig S, Bell M, Richter EJ, Zuhr O, Hurzeler 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.
    1. Tanaka S, Matsuzaka K, Sato D, Inoue T. Characteristics of newly formed bone during guided bone regeneration: analysis of cbfa‐1, osteocalcin, and VEGF expression. J Oral Implantol 2007; 33: 321–326.
    1. Lima LL, Goncalves PF, Sallum EA, Casati MZ, Nociti FH Jr. Guided tissue regeneration may modulate gene expression in periodontal intrabony defects: a human study. J Periodontal Res 2008; 43: 459–464.
    1. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF‐1 induction of SDF‐1. Nat Med 2004; 10: 858–864.
    1. Karp JM, Leng Teo GS. Mesenchymal stem cell homing: the devil is in the details. Cell Stem Cell 2009; 4: 206–216.
    1. Kitaori T, Ito H, Schwarz EM, Tsutsumi R, Yoshitomi H, Oishi S, Nakano M, Fujii N, Nagasawa T, Nakamura T. Stromal cell‐derived factor 1/CXCR4 signaling is critical for the recruitment of mesenchymal stem cells to the fracture site during skeletal repair in a mouse model. Arthritis Rheum 2009; 60: 813–823.
    1. Binder NB, Niederreiter B, Hoffmann O, Stange R, Pap T, Stulnig TM, Mack M, Erben RG, Smolen JS, Redlich K. Estrogen‐dependent and C‐C chemokine receptor‐2‐dependent pathways determine osteoclast behavior in osteoporosis. Nat Med 2009; 15: 417–424.
    1. Xing Z, Lu C, Hu D, Yu YY, Wang X, Colnot C, Nakamura M, Wu Y, Miclau T, Marcucio RS. Multiple roles for CCR2 during fracture healing. Dis Model Mech 2010; 3: 451–458.
    1. Taguchi Y, Amizuka N, Nakadate M, Ohnishi H, Fujii N, Oda K, Nomura S, Maeda T. A histological evaluation for guided bone regeneration induced by a collagenous membrane. Biomaterials 2005; 26: 6158–6166.
    1. Kuru L, Griffiths GS, Petrie A, Olsen I. Alkaline phosphatase activity is upregulated in regenerating human periodontal cells. J Periodontal Res 1999; 34: 123–127.
    1. Wakabayashi RC, Iha DK, Niu JJ, Johnson PW. Cytokine production by cells adherent to regenerative membranes. J Periodontal Res 1997; 32: 215–224.
    1. Schwarz F, Rothamel D, Herten M, Sager M, Becker J. Angiogenesis pattern of native and cross‐linked collagen membranes: an immunohistochemical study in the rat. Clin Oral Implants Res 2006; 17: 403–409.
    1. Barbeck M, Lorenz J, Holthaus MG, Raetscho N, Kubesch A, Booms P, Sader R, Kirkpatrick CJ, Ghanaati S. Porcine dermis and pericardium‐based, non‐cross‐linked materials induce multinucleated giant cells after their in vivo implantation: a physiological reaction? J Oral Implantol 2015; 41: e267–e281.
    1. Ghanaati S. Non‐cross‐linked porcine‐based collagen I‐III membranes do not require high vascularization rates for their integration within the implantation bed: a paradigm shift. Acta Biomater 2012; 8: 3061–3072.
    1. Rocchietta I, Simion M, Hoffmann M, Trisciuoglio D, Benigni M, Dahlin C. Vertical bone augmentation with an Autogenous block or particles in combination with guided bone regeneration: a clinical and histological preliminary study in humans. Clin Implant Dent Relat Res 2016; 18: 19–29.
    1. Karahaliloglu Z, Ercan B, Taylor EN, Chung S, Denkbas EB, Webster TJ. Antibacterial nanostructured polyhydroxybutyrate membranes for guided bone regeneration. J Biomed Nanotechnol 2015; 11: 2253–2263.
    1. Liao S, Wang W, Uo M, Ohkawa S, Akasaka T, Tamura K, Cui F, Watari F. A three‐layered nano‐carbonated hydroxyapatite/collagen/PLGA composite membrane for guided tissue regeneration. Biomaterials 2005; 26: 7564–7571.

Source: PubMed

3
Suscribir