Advertisement

Odontology

, Volume 105, Issue 1, pp 1–12 | Cite as

Collagen based barrier membranes for periodontal guided bone regeneration applications

  • Zeeshan Sheikh
  • Javairia Qureshi
  • Abdullah M. Alshahrani
  • Heba Nassar
  • Yuichi Ikeda
  • Michael Glogauer
  • Bernhard GanssEmail author
Review Article

Abstract

Certain cell populations within periodontal tissues possess the ability to induce regeneration, provided they have the opportunity to populate the wound or defect. Guided regeneration techniques have been investigated for regenerating periodontal tissues and such therapies usually utilize barrier membranes. Various natural and synthetic barrier membranes have been fabricated and tested to prevent epithelial and connective tissue cells from invading while allowing periodontal cells to selectively migrate into the defect. This paper focuses on the literature relevant to the use and potential of resorbable collagen membranes in GBR procedures, sites of periodontal and intrabony defects, in cases of socket and alveolar ridge preservation and at implant sites. The results of their use in GBR procedures has shown them to be effective and comparable with non-resorbable membranes with regards to clinical attachment gain, probing depth reduction and defect bone filling. They have also shown to prevent epithelial ingrowth into the defect space during the initial wound healing phase postsurgically. Collagen membranes have also been used for root coverage and GBR procedures and have shown good success rates comparable to subepithelial connective tissue grafts and expanded-polytetrafluoroethylene (e-PTFE) membranes. The future for periodontal tissue engineering is very exciting with the use of barrier membranes expected to continue playing a critical role. However, long-term clinical trials are required to further evaluate and confirm the efficacy of the available collagen barrier membranes for periodontal and bone regeneration use.

Keywords

Collagen Barrier membranes Periodontal regeneration GBR GTR 

Notes

Acknowledgments

A special thanks to the following people for helping and contributing towards this article: Ms. Esraa Khalil, Amman, Jordan for providing with the illustrations for Fig. 1; Dr. Thomas T. Nguyen, Assistant Professor in Periodontics, Faculty of Dentistry, University of Montreal, Canada for providing the clinical photographs for Fig. 2; of Dr. Nader Hamdan, Periodontist, Canada for providing the clinical photographs for Figs. 3 and 4; and Dr. Faisal Qayyum, Consultant Prosthodontist, Aga Khan University Hospital for providing the clinical photographs for Fig. 5.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. 1.
    Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human periodontal disease. J Clin Periodontol. 1982;9(4):290–6.PubMedCrossRefGoogle Scholar
  2. 2.
    Nyman S, Gottlow J, Karring T, Lindhe J. The regenerative potential of the periodontal ligament. J Clin Periodontol. 1982;9(3):257–65.PubMedCrossRefGoogle Scholar
  3. 3.
    Dahlin C, Linde A, Gottlow J, Nyman S. Healing of bone defects by guided tissue regeneration. Plast Reconstr Surg. 1988;81(5):672–6.PubMedCrossRefGoogle Scholar
  4. 4.
    Buser D, Dula K, Hess D, Hirt HP, Belser UC. Localized ridge augmentation with autografts and barrier membranes. Periodontology. 2000;1999(19):151–63.Google Scholar
  5. 5.
    Deshpande S, Deshmukh J, Deshpande S, Khatri R, Deshpande S. Vertical and horizontal ridge augmentation in anterior maxilla using autograft, xenograft and titanium mesh with simultaneous placement of endosseous implants. J Indian Soc Periodontol. 2014;18(5):661–5. doi: 10.4103/0972-124X.142469.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    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 Implant Res. 2007;18(5):620–9. doi: 10.1111/j.1600-0501.2007.01389.x.CrossRefGoogle Scholar
  7. 7.
    Sheikh Z, Sima C, Glogauer M. Bone replacement materials and techniques used for achieving vertical alveolar bone augmentation. Materials. 2015;8(6):2953–93.CrossRefGoogle Scholar
  8. 8.
    Bhola M, Kinaia BM. Chahine K (2008) Guided bone regeneration using an allograft material: review and case presentations. Pract Proced Aesthet Dent PPAD. 2008;20(9):551–7 quiz 8.PubMedGoogle Scholar
  9. 9.
    Zitzmann N, Schärer P, Marinello C. Factors influencing the success of GBR. J Clin Periodontol. 1999;26(10):673–82.PubMedCrossRefGoogle Scholar
  10. 10.
    Sheikh Z, Glogauer M. Successful ridge augmentation: the challenge of periodontal tissue engineering. EC Dent Sci. 2015;2:216–8.Google Scholar
  11. 11.
    Jensen OT, Greer RO Jr, Johnson L, Kassebaum D. Vertical guided bone-graft augmentation in a new canine mandibular model. Int J Oral Maxillofac Implants. 1995;10(3):335–44.PubMedGoogle Scholar
  12. 12.
    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(1):13–29.PubMedGoogle Scholar
  13. 13.
    Sheikh Z, Abdallah MN, Hamdan N, Javaid MA, Khurshid Z. Barrier membranes for tissue regeneration and bone augmentation techniques in dentistry. In: Matilinna KP, editor. Handbook of oral biomaterials. Singapore: Pan Stanford Publishing; 2014.Google Scholar
  14. 14.
    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(1):3–14. doi: 10.1016/j.jpor.2012.12.001.PubMedCrossRefGoogle Scholar
  15. 15.
    Wei J, Igarashi T, Okumori N, Igarashi T, Maetani T, Liu B, et al. Influence of surface wettability on competitive protein adsorption and initial attachment of osteoblasts. Biomed Mater. 2009;4(4):045002.PubMedCrossRefGoogle Scholar
  16. 16.
    Kralchevsky P, Nagayama K. Particles at fluid interfaces and membranes: attachment of colloid particles and proteins to interfaces and formation of two-dimensional arrays. vol. 10. Elsevier; 2001.Google Scholar
  17. 17.
    Vogler EA. Water and the acute biological response to surfaces. J Biomater Sci Polym Ed. 1999;10(10):1015–45.PubMedCrossRefGoogle Scholar
  18. 18.
    Israelachvili J, Wennerström H. Role of hydration and water structure in biological and colloidal interactions. Nature. 1996;379(6562):219–25.PubMedCrossRefGoogle Scholar
  19. 19.
    Deng M, James R, Laurencin CT, Kumbar SG. Nanostructured polymeric scaffolds for orthopaedic regenerative engineering. IEEE Trans Nanobiosci. 2012;11(1):3–14.CrossRefGoogle Scholar
  20. 20.
    Lundgren D, Sennerby L, Falk H, Friberg B, Nyman S. The use of a new bioresorbable barrier for guided bone regeneration in connection with implant installation. Case reports. Clin Oral Implants Res. 1994;5(3):177–84.PubMedCrossRefGoogle Scholar
  21. 21.
    Nobréus N, Attström R, Linde A. Guided bone regeneration in dental implant treatment using a bioabsorbable membrane. Clin Oral Implant Res. 1997;8(1):10–7.CrossRefGoogle Scholar
  22. 22.
    Ratner BD. Biomaterials science: an introduction to materials in medicine. Academic press; 2004.Google Scholar
  23. 23.
    Sheikh Z, Najeeb S, Khurshid Z, Verma V, Rashid H, Glogauer M. Biodegradable materials for bone repair and tissue engineering applications. Materials. 2015;8(9):5744–94.CrossRefGoogle Scholar
  24. 24.
    Parodi R, Santarelli G, Carusi G. Application of slow-resorbing collagen membrane to periodontal and peri-implant guided tissue regeneration. Int J Periodontics Restor Dent. 1996;16(2):174–85.Google Scholar
  25. 25.
    Avera SP, Stampley WA, McAllister BS. Histologic and clinical observations of resorbable and nonresorbable barrier membranes used in maxillary sinus graft containment. Int J Oral Maxillofac Implants. 1996;12(1):88–94.Google Scholar
  26. 26.
    Gotfredsen K, Nimb L, Hjørting-hansen E. Immediate implant placement using a biodegradable barrier, polyhydroxybutyrate-hydroxyvalerate reinforced with polyglactin 910. An experimental study in dogs. Clin Oral Implant Res. 1994;5(2):83–91.CrossRefGoogle Scholar
  27. 27.
    Simion M, Scarano A, Gionso L, Piattelli A. Guided bone regeneration using resorbable and nonresorbable membranes: a comparative histologic study in humans. Int J Oral Maxillofac Implants. 1996;11(6):735–42.PubMedGoogle Scholar
  28. 28.
    Bunyaratavej P, Wang H-L. Collagen membranes: a review. J Periodontol. 2001;72(2):215–29.PubMedCrossRefGoogle Scholar
  29. 29.
    Parenteau-Bareil R, Gauvin R, Berthod F. Collagen-based biomaterials for tissue engineering applications. Materials. 2010;3(3):1863–87.CrossRefGoogle Scholar
  30. 30.
    Eyre DR, Paz MA, Gallop PM. Cross-linking in collagen and elastin. Annu Rev Biochem. 1984;53(1):717–48.PubMedCrossRefGoogle Scholar
  31. 31.
    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):1–11.PubMedCrossRefGoogle Scholar
  32. 32.
    Wang H-L, MacNeil RL. Guided tissue regeneration. Absorbable barriers. Dent Clin North Am. 1998;42(3):505–22.PubMedGoogle Scholar
  33. 33.
    Lee C, Grodzinsky A, Spector M. The effects of cross-linking of collagen-glycosaminoglycan scaffolds on compressive stiffness, chondrocyte-mediated contraction, proliferation and biosynthesis. Biomaterials. 2001;22(23):3145–54.PubMedCrossRefGoogle Scholar
  34. 34.
    Minabe M, Kodama T, Kogou T, Tamura T, Hori T, Watanabe Y, et al. Different cross-linked types of collagen implanted in rat palatal gingiva. J Periodontol. 1989;60(1):35–43.PubMedCrossRefGoogle Scholar
  35. 35.
    Kodama T, Minabe M, Hori T, Watanabe Y. The effect of various concentrations of collagen barrier on periodontal wound healing. J Periodontol. 1989;60(4):205–10.PubMedCrossRefGoogle Scholar
  36. 36.
    Karring T, Nyman S, Lindhe J, Sirirat M. Potentials for root resorption during periodontal wound healing. J Clin Periodontol. 1984;11(1):41–52.PubMedCrossRefGoogle Scholar
  37. 37.
    Wang H-L, Carroll WJ. Guided bone regeneration using bone grafts and collagen membranes. Quintessence Int. 2001;32(7):504.PubMedGoogle Scholar
  38. 38.
    Brunel G, Piantoni P, Elharar F, Benqué E, Marin P, Zahedi S. Regeneration of rat calvarial defects using a bioabsorbable membrane technique: influence of collagen cross-linking. J Periodontol. 1996;67(12):1342–8.PubMedCrossRefGoogle Scholar
  39. 39.
    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 Implant Res. 2005;16(3):369–78.CrossRefGoogle Scholar
  40. 40.
    Crigger M, Bogle GC, Garrett S, Gantes BG. Repair following treatment of circumferential periodontal defects in dogs with collagen and expanded polytetrafluoroethylene barrier membranes. J Periodontol. 1996;67(4):403–13.PubMedCrossRefGoogle Scholar
  41. 41.
    Becker J, Al-Nawas B, Klein MO, Schliephake H, Terheyden H, Schwarz F. Use of a new cross-linked collagen membrane for the treatment of dehiscence-type defects at titanium implants: a prospective, randomized-controlled double-blinded clinical multicenter study. Clin Oral Implant Res. 2009;20(7):742–9.CrossRefGoogle Scholar
  42. 42.
    Schliephake H, Neukam F, Hutmacher D, Becker J. Enhancement of bone ingrowth into a porous hydroxylapatite-matrix using a resorbable polylactic membrane: an experimental pilot study. J Oral Maxillofac Surg. 1994;52(1):57–63.PubMedCrossRefGoogle Scholar
  43. 43.
    Wang H-L, Carroll M. Guided bone regeneration using bone grafts and collagen membranes. Quintessence Int (Berlin, Germany: 1985). 2000;32(7):504–15.Google Scholar
  44. 44.
    Oh TJ, Meraw SJ, Lee EJ, Giannobile WV, Wang HL. Comparative analysis of collagen membranes for the treatment of implant dehiscence defects. Clin Oral Implant Res. 2003;14(1):80–90.CrossRefGoogle Scholar
  45. 45.
    Lee S-W, Kim S-G. Membranes for the guided bone regeneration. Korean Assoc Maxillofac Plast Reconstr Surg. 2014;36(6):239–46.Google Scholar
  46. 46.
    Vert M. Bioresorbable polymers for temporary therapeutic applications. Die Angewandte Makromolekulare Chemie. 1989;166(1):155–68.CrossRefGoogle Scholar
  47. 47.
    Vert M, Li S, Spenlehauer G, Guérin P. Bioresorbability and biocompatibility of aliphatic polyesters. J Mater Sci Mater Med. 1992;3(6):432–46.CrossRefGoogle Scholar
  48. 48.
    Tanner MG, Solt CW, Vuddhakanok S. An evaluation of new attachment formation using a microfibrillar collagen barrier. J Periodontol. 1988;59(8):524–30.PubMedCrossRefGoogle Scholar
  49. 49.
    Magnusson I, Batich C, Collins B. New attachment formation following controlled tissue regeneration using biodegradable membranes. J Periodontol. 1988;59(1):1–6.PubMedCrossRefGoogle Scholar
  50. 50.
    Jepsen S, Eberhard J, Herrera D, Needleman I. A systematic review of guided tissue regeneration for periodontal furcation defects. What is the effect of guided tissue regeneration compared with surgical debridement in the treatment of furcation defects? J Clin Periodontol. 2002;29(s3):103–16.PubMedCrossRefGoogle Scholar
  51. 51.
    Simion M, Maglione M, Iamoni F, Scarano A, Piattelli A, Salvato A. Bacterial penetration through Resolut® resorbable membrane in vitro. Clin Oral Implant Res. 1997;8(1):23–31.CrossRefGoogle Scholar
  52. 52.
    Lekovic V, Kenney E, Weinlaender M, Han T, Klokkevold P, Nedic M, et al. A bone regenerative approach to alveolar ridge maintenance following tooth extraction. Report of 10 cases. J Periodontol. 1997;68(6):563–70.PubMedCrossRefGoogle Scholar
  53. 53.
    Zitzmann NU, Naef R, Schärer P. Resorbable versus nonresorbable membranes in combination with Bio-Oss for guided bone regeneration. Int J Oral Maxillofac Implants. 1997;12(6):844–52.PubMedGoogle Scholar
  54. 54.
    Chiapasco M, Zaniboni M. Clinical outcomes of GBR procedures to correct peri-implant dehiscences and fenestrations: a systematic review. Clin Oral Implant Res. 2009;20(s4):113–23.CrossRefGoogle Scholar
  55. 55.
    Evans G, Yukna R, Cambre K, Gardiner D. Clinical regeneration with guided tissue barriers. Curr Opin Periodontol. 1996;4:75–81.Google Scholar
  56. 56.
    Retzepi M, Donos N. Guided bone regeneration: biological principle and therapeutic applications. Clin Oral Implant Res. 2010;21(6):567–76.CrossRefGoogle Scholar
  57. 57.
    Blumenthal N, Steinberg J. The use of collagen membrane barriers in conjunction with combined demineralized bone-collagen gel implants in human infrabony defects. J Periodontol. 1990;61(6):319–27.PubMedCrossRefGoogle Scholar
  58. 58.
    Chen C-C, Wang H-L, Smith F, Glickman GN, Shyr Y, O’Neal RB. Evaluation of a collagen membrane with and without bone grafts in treating periodontal intrabony defects. J Periodontol. 1995;66(10):838–47.PubMedCrossRefGoogle Scholar
  59. 59.
    Iasella JM, Greenwell H, Miller RL, Hill M, Drisko C, Bohra AA, et al. Ridge preservation with freeze-dried bone allograft and a collagen membrane compared to extraction alone for implant site development: a clinical and histologic study in humans. J Periodontol. 2003;74(7):990–9.PubMedCrossRefGoogle Scholar
  60. 60.
    Dowell P, Al-Arrayed F, Adam S, Moran J. A comparative clinical study: the use of human type I collagen with and without the addition of metronidazole in the GTR method of treatment of periodontal disease. J Clin Periodontol. 1995;22(7):543–9.PubMedCrossRefGoogle Scholar
  61. 61.
    Pitaru S, Noff M, Grosskopf A, Moses O, Tal H, Savion N. Heparan sulfate and fibronectin improve the capacity of collagen barriers to prevent apical migration of the junctional epithelium. J Periodontol. 1991;62(10):598–601.PubMedCrossRefGoogle Scholar
  62. 62.
    Gassling V, Hedderich J, Açil Y, Purcz N, Wiltfang J, Douglas T. Comparison of platelet rich fibrin and collagen as osteoblast-seeded scaffolds for bone tissue engineering applications. Clin Oral Implant Res. 2013;24(3):320–8.CrossRefGoogle Scholar
  63. 63.
    Caton J, Nyman S, Zander H. Histometric evaluation of periodontal surgery II. Connective tissue attachment levels after four regenerative procedures. J Clin Periodontol. 1980;7(3):224–31.PubMedCrossRefGoogle Scholar
  64. 64.
    Bowers GM, Chadroff B, Carnevale R, Mellonig J, Corio R, Emerson J, et al. Histologic evaluation of new attachment apparatus formation in humans: part III. J Periodontol. 1989;60(12):683–93.PubMedCrossRefGoogle Scholar
  65. 65.
    Garrett S. Periodontal regeneration around natural teeth. Ann Periodontol. 1996;1(1):621–66.PubMedCrossRefGoogle Scholar
  66. 66.
    McAllister BS, Haghighat K. Bone augmentation techniques. J Periodontol. 2007;78(3):377–96.PubMedCrossRefGoogle Scholar
  67. 67.
    Sevor JJ, Meffert RM, Cassingham RJ. Regeneration of dehisced alveolar bone adjacent to endosseous dental implants utilizing a resorbable collagen membrane: clinical and histologic results. Int J Periodontics Restor Dent. 1993;13(1):71.Google Scholar
  68. 68.
    Karring T, Nyman S, Gottlow J, Laurell L. Development of the biological concept of guided tissue regeneration—animal and human studies. Periodontology 2000. 1993;1(1):26-35.Google Scholar
  69. 69.
    Hämmerle CH, Jung RE. Bone augmentation by means of barrier membranes. Periodontology 2001. 2003;33(1):36–53.Google Scholar
  70. 70.
    Bottino MC, Thomas V, Schmidt G, Vohra YK, Chu T-MG, Kowolik MJ, et al. Recent advances in the development of GTR/GBR membranes for periodontal regeneration—a materials perspective. Dent Mater. 2012;28(7):703–21.PubMedCrossRefGoogle Scholar
  71. 71.
    Meffert RM, Langer B, Fritz ME. Dental implants: a review. J Periodontol. 1992;63(11):859–70.PubMedCrossRefGoogle Scholar
  72. 72.
    Lekovic V, Camargo PM, Klokkevold PR, Weinlaender M, Kenney EB, Dimitrijevic B, et al. Preservation of alveolar bone in extraction sockets using bioabsorbable membranes. J Periodontol. 1998;69(9):1044–9.PubMedCrossRefGoogle Scholar
  73. 73.
    Buser D, Dula K, Belser U, Hirt H-P, Berthold H. Localized ridge augmentation using guided bone regeneration. I. Surgical procedure in the maxilla. Int J Periodontics Restor Dent. 1993;13(1):29–45.Google Scholar
  74. 74.
    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(6):844–52.PubMedGoogle Scholar
  75. 75.
    Hürzeler MB, Kohal RJ, Naghshbandl J, Mota LF, Conradt J, Hutmacher D, et al. Evaluation of a new bioresorbable barrier to facilitate guided bone regeneration around exposed implant threads: an experimental study in the monkey. Int J Oral Maxillofac Surg. 1998;27(4):315–20.PubMedCrossRefGoogle Scholar
  76. 76.
    Vance GS, Greenwell H, Miller RL, Hill M, Johnston H, Scheetz JP. Comparison of an allograft in an experimental putty carrier and a bovine-derived xenograft used in ridge preservation: a clinical and histologic study in humans. Int J Oral Maxillofac Implants. 2004;19(4):491–97.PubMedGoogle Scholar
  77. 77.
    Sevor J, Meffert R. Placement of implants into fresh extraction sites using a resorbable collagen membrane: case reports. Pract Periodontics Aesthet Dent PPAD. 1992;4(3):35.PubMedGoogle Scholar
  78. 78.
    Gotfredsen K, Nimb L, Buser D, Hjørting-Hansen E. Evaluation of guided bone generation around implants placed into fresh extraction sockets: an experimental study in dogs. J Oral Maxillofac Surg. 1993;51(8):879–84.PubMedCrossRefGoogle Scholar
  79. 79.
    Chen ST, Darby IB, Adams GG, Reynolds EC. A prospective clinical study of bone augmentation techniques at immediate implants. Clin Oral Implant Res. 2005;16(2):176–84.CrossRefGoogle Scholar
  80. 80.
    Tinti C, Parma-Benfenati S, Polizzi G. Vertical ridge augmentation: what is the limit? Int J Periodontics Restor Dent. 1996;16(3):220–9.Google Scholar
  81. 81.
    Hämmerle CH, Chiantella GC, Karring T, Lang NP. The effect of a deproteinized bovine bone mineral on bone regeneration around titanium dental implants®. Clin Oral Implant Res. 1998;9(3):151–62.CrossRefGoogle Scholar
  82. 82.
    Parodi R, Carusi G, Santarelli G, Nanni F. Implant placement in large edentulous ridges expanded by GBR using a bioresorbable collagen membrane. Int J Periodontics Restor Dent. 1998;18(3):266–75.Google Scholar
  83. 83.
    Von Arx T, Buser D. Horizontal ridge augmentation using autogenous block grafts and the guided bone regeneration technique with collagen membranes: a clinical study with 42 patients. Clin Oral Implant Res. 2006;17(4):359–66.CrossRefGoogle Scholar
  84. 84.
    Dahlin C, Sennerby L, Lekholm U, Linde A, Nyman S. Generation of new bone around titanium implants using a membrane technique: an experimental study in rabbits. Int J Oral Maxillofac Implants. 1989;4(1):19–25.PubMedGoogle Scholar
  85. 85.
    Sigurdsson TJ, Hardwick R, Bogle GC, Wikesjö UM. Periodontal repair in dogs: space provision by reinforced ePTFE membranes enhances bone and cementum regeneration in large supraalveolar defects. J Periodontol. 1994;65(4):350–6.PubMedCrossRefGoogle Scholar
  86. 86.
    Becker W, Dahlin C, Becker BE, Lekholm U, Van Steenberghe D, Higuchi K et al. The use of e-PTFE barrier membranes for bone promotion around titanium implants placed into extraction sockets: a prospective multicenter study. Int J Oral Maxillofac Implants. 1994;9(1):31–40.PubMedGoogle Scholar
  87. 87.
    Juodzbalys G, Wang HL. Soft and hard tissue assessment of immediate implant placement: a case series. Clin Oral Implant Res. 2007;18(2):237–43.CrossRefGoogle Scholar
  88. 88.
    Chiapasco M, Zaniboni M. Clinical outcomes of GBR procedures to correct peri-implant dehiscences and fenestrations: a systematic review. Clin Oral Implant Res. 2009;20(Suppl 4):113–23. doi: 10.1111/j.1600-0501.2009.01781.x.CrossRefGoogle Scholar
  89. 89.
    Chung KM, Salkin LM, Stein MD, Freedman AL. Clinical evaluation of a biodegradable collagen membrane in guided tissue regeneration. J Periodontol. 1990;61(12):732–6.PubMedCrossRefGoogle Scholar
  90. 90.
    Mattson JS, McLey LL, Jabro MH. Treatment of intrabony defects with collagen membrane barriers. Case reports. J Periodontol. 1995;66(7):635–45.PubMedCrossRefGoogle Scholar
  91. 91.
    Mattson JS, Gallagher SJ, Jabro MH. The use of 2 bioabsorbable barrier membranes in the treatment of interproximal intrabony periodontal defects. J Periodontol. 1999;70(5):510–7.PubMedCrossRefGoogle Scholar
  92. 92.
    Martin M, Gantes B, Garrett S, Egelberg J. Treatment of periodontal furcation defects. J Clin Periodontol. 1988;15(4):227–31.PubMedCrossRefGoogle Scholar
  93. 93.
    Van Swol RL, Ellinger R, Pfeifer J, Barton NE, Blumenthal N. Collagen membrane barrier therapy to guide regeneration in class II furcations in humans. J Periodontol. 1993;64(7):622–9.PubMedCrossRefGoogle Scholar
  94. 94.
    Selvig KA, Nilveus RE, Fitzmorris L, Kersten B, Khorsandi SS. Scanning electron microscopic observations of cell population and bacterial contamination of membranes used for guided periodontal tissue regeneration in humans. J Periodontol. 1990;61(8):515–20.PubMedCrossRefGoogle Scholar
  95. 95.
    Chen Y-T, Wang H-L, Lopatin DE, O’Neal R, MacNeil RL. Bacterial adherence to guided tissue regeneration barrier membranes exposed to the oral environment. J Periodontol. 1997;68(2):172–9.PubMedCrossRefGoogle Scholar
  96. 96.
    Black BS, Gher ME, Sandifer JB, Fucini SE, Richardson AC. Comparative study of collagen and expanded polytetrafluoroethylene membranes in the treatment of human class ii furcation defects. J Periodontol. 1994;65(6):598–604.PubMedCrossRefGoogle Scholar
  97. 97.
    Wang H-L, Bunyaratavej P, Labadie M, Shyr Y, MacNeil RL. Comparison of 2 clinical techniques for treatment of gingival recession. J Periodontol. 2001;72(10):1301–11.PubMedCrossRefGoogle Scholar
  98. 98.
    Trombelli L, Scabbia A, Tatakis DN, Checchi L, Calura G. Resorbable barrier and envelope flap surgery in the treatment of human gingival recession defects. J Clin Periodontol. 1998;25(1):24–9.PubMedCrossRefGoogle Scholar
  99. 99.
    Ozcan G, Kurtiş B, Baloş K. Combined use of root conditioning, fibrin-fibronectin system and a collagen membrane to treat a localized gingival recession: a 10-case report. J Marmara Univ Dent Fac. 1997;2(4):588–98.PubMedGoogle Scholar
  100. 100.
    Murphy KG, Gunsolley JC. Guided tissue regeneration for the treatment of periodontal intrabony and furcation defects. A systematic review. Ann Periodontol. 2003;8(1):266–302.PubMedCrossRefGoogle Scholar
  101. 101.
    Draenert FG, Huetzen D, Neff A, Mueller WE. Vertical bone augmentation procedures: basics and techniques in dental implantology. J Biomed Mater Res Part A. 2014;102(5):1605–13. doi: 10.1002/jbm.a.34812.CrossRefGoogle Scholar
  102. 102.
    Nkenke E, Weisbach V, Winckler E, Kessler P, Schultze-Mosgau S, Wiltfang J, et al. Morbidity of harvesting of bone grafts from the iliac crest for preprosthetic augmentation procedures: a prospective study. Int J Oral Maxillofac Surg. 2004;33(2):157–63. doi: 10.1054/ijom.2003.0465.PubMedCrossRefGoogle Scholar
  103. 103.
    Murphy KG. Postoperative healing complications associated with gore-tex periodontal material. Part I. Incidence and characterization. Int J Periodontics Restor Dent. 1995;15(4):363–75.Google Scholar
  104. 104.
    Shanaman RH. A retrospective study of 237 sites treated consecutively with guided tissue regeneration. Int J Periodontics Restor Dent. 1994;14(4):292–301.Google Scholar
  105. 105.
    Passariello C, Thaller MC, Selan L, Berlutti F, de Luca M, Renzini G. Periodontal regeneration procedures may induce colonization by glycocalyx-producing bacteria. Med Microbiol Immunol. 1991;180(2):67–72.PubMedCrossRefGoogle Scholar
  106. 106.
    Kornman KS, Robertson PB. Fundamental principles affecting the outcomes of therapy for osseous lesions. Periodontology 2000. 2000;22(1):22–43.PubMedCrossRefGoogle Scholar
  107. 107.
    Mombelli A, Zappa U, Bragger U, Lang NP. Systemic antimicrobial treatment and guided tissue regeneration Clinical and microbiological effects in function defects. J Clin Periodontol. 1996;23(4):386–96.PubMedCrossRefGoogle Scholar
  108. 108.
    Hugoson A, Ravald N, Fornell J, Johard G, Teiwik A, Gottlow J. Treatment of class II furcation involvements in humans with bioresorbable and nonresorbable guided tissue regeneration barriers. A randomized multi-center study. J Periodontol. 1995;66(7):624–34.PubMedCrossRefGoogle Scholar
  109. 109.
    Iwasaki K, Bajenova E, Somogyi-Ganss E, Miller M, Nguyen V, Nourkeyhani H, et al. Amelotin—a novel secreted, ameloblast-specific protein. J Dent Res. 2005;84(12):1127–32.PubMedCrossRefGoogle Scholar
  110. 110.
    Somogyi-Ganss E, Nakayama Y, Iwasaki K, Nakano Y, Stolf D, McKee MD, et al. Comparative temporospatial expression profiling of murine amelotin protein during amelogenesis. Cells Tissues Organs. 2012;195(6):535–49.PubMedCrossRefGoogle Scholar
  111. 111.
    Nakayama Y, Holcroft J, Ganss B. Enamel hypomineralization and structural defects in amelotin-deficient mice. J Dent Res. 2015;0022034514566214.Google Scholar
  112. 112.
    Lacruz RS, Nakayama Y, Holcroft J, Nguyen V, Somogyi-Ganss E, Snead ML, et al. Targeted overexpression of amelotin disrupts the microstructure of dental enamel. PLoS One. 2012;7(4):e35200.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Abbarin N, San Miguel S, Holcroft J, Iwasaki K, Ganss B. The enamel protein amelotin is a promoter of hydroxyapatite mineralization. J Bone Miner Res. 2015;30(5):775–85.PubMedCrossRefGoogle Scholar
  114. 114.
    Oyane A, Kim HM, Furuya T, Kokubo T, Miyazaki T, Nakamura T. Preparation and assessment of revised simulated body fluids. J Biomed Mater Res Part A. 2003;65(2):188–95.CrossRefGoogle Scholar

Copyright information

© The Society of The Nippon Dental University 2016

Authors and Affiliations

  1. 1.Matrix Dynamics Group, Faculty of DentistryUniversity of TorontoTorontoCanada
  2. 2.Lunenfeld-Tanenbaum Research InstituteMt. Sinai HospitalTorontoCanada
  3. 3.Smile Point Dental PracticeKarachiPakistan
  4. 4.Alfarabi Dental CollegeRiyadhKingdom of Saudi Arabia
  5. 5.Fairmont Dental GroupVancouverCanada

Personalised recommendations