Deproteinized Bovine Bone Xenograft

  • Andreas Stavropoulos
Chapter
Part of the Orthopedic Biology and Medicine book series (OBM)

Abstract

Deproteinized bovine bone (DBB) has a chemical composition and architectural geometry that is almost identical to that of human bone and can support new bone formation in direct contact to the graft. DBB grafts are widely used in dentistry in a variety of applications, and positive results have been generally observed after their application. However, an added clinical benefi t from their use in association with dental implants and/or when used as adjuncts to guided tissue regeneration (GTR) in the treatment of periodontal intrabony defects cannot unequivocally be confi rmed. It seems that DBB should be regarded as an osteocompatible fi ller material that may act as a space provision device rather than as a bone promoting substance, and the outcome of DBB grafting in terms of bone fill seems greatly dependent on the confi guration and dimensions of the defect. Relevant in vitro and animal experiments, as well as human clinical studies in a variety of applications, are presented and discussed. The chapter also briefly describes the processing method of xenograft bone and its properties, and discusses the risk of disease transmission.

Keywords

Bone bovine devitalized deproteinized grafts GTR implants osteoconduction periodontology regeneration xenograft xenotransplantation 
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References

  1. 1.
    1. Gorer PA, Loutit JF, Micklem HS. Proposed revision of “transplantese”. Nature. 1961;189:1024–25.PubMedGoogle Scholar
  2. 2.
    van Meekeren J. Heel en geneeskonstige aanmerkingen. Commelijn. 1668.Google Scholar
  3. 3.
    3. Ricard MA. Réparation d'une perte de substance de la voûte cranienne par la greffe osseuse immédiate. Gaz Hopitaux. 1891;64:785–86.Google Scholar
  4. 4.
    4. Küttner D. Die Transplantation aus dem Affen und ihre Dauererfolge. Wien Med Wochenschr. 1917;64:1449–52.Google Scholar
  5. 5.
    5. Reynier MP. Réparation des pertes osseuses craniennes dans les plaies de guerre, greffes hétéroplastiques. Bull Acad Med. 1915;73:753–67.Google Scholar
  6. 6.
    6. Senn N. On the healing of aseptic bone cavities by implantation of antiseptic decal cified bone. J Med Sci (Am). 1889;98:219–43.Google Scholar
  7. 7.
    7. Grekoff J. Über die Deckung von Schädeldefekten mit ausgeglühtem Knochen. Zentralbl Chir. 1898;39:969–73.Google Scholar
  8. 8.
    8. Babcock WW. “Soup Bone” implant for the correction of defects of the skull and face. JAMA 69, 352–355. 1917. Ref Type: GenericGoogle Scholar
  9. 9.
    9. Jaksch R. Zur Frage der Deckung von Knochendefekten des Schädels nach der Trepanation. Wien Med Wochenschr. 1889;38:1435–37.Google Scholar
  10. 10.
    10. Rehn E. Über halbe Gelenktransplantation mit Horn. Zentralbl Chir. 1913;40:1185–86.Google Scholar
  11. 11.
    11. Hughes CW. Rate of absorption and callus stimulating properties of cow horn, ivory, beef bone and autogenous bone. Surg Gynecol Obstet. 1943;76:665.Google Scholar
  12. 12.
    12. Magnusson PB. Holding fractures with absorbable materials-ivory plates and screws. JAMA. 1913;61:1514.Google Scholar
  13. 13.
    13. Mauclaire P. Prosthese d&ivoire pour réparer les pertes de substance du crâne. Soc Chir Bull Mem. 1916;42:1191.Google Scholar
  14. 14.
    14. Weibrich G, Gnoth SH, Kunkel M, Trettin R, Werner HD, Wagner W. Röntgenspektrometrischer Vergleich der aktuell verfügbaren Knochenersatzmateri alien. Mund Kiefer Gesichtschir. 1999;3:92–97.PubMedGoogle Scholar
  15. 15.
    15. Holmes RE. Bone regeneration within a coraline hydroxyapatite implant. Plast Reconstr Surg. 1979;63:626–33.PubMedGoogle Scholar
  16. 16.
    16. Holmes RE. A coralline hydroxyapatite bone graft substitute: preliminary report. Clin Orthop. 1984;188:252–62.PubMedGoogle Scholar
  17. 17.
    17. Burchardt H. The biology of bone graft repair. Clin Orthop. 1983;174:28–42.PubMedGoogle Scholar
  18. 18.
    18. Salama R. Xenogeneic bone grafting in humans. Clin Orthop. 1983;174:113–21.PubMedGoogle Scholar
  19. 19.
    19. Heiple KG, Kendrick RE, Herndon CH, Chase SW. A critical evaluation of proc essed calf bone. J Bone Joint Surg Am. 1967;49:1119–27.PubMedGoogle Scholar
  20. 20.
    20. Pieron AP, Bigelow D, Hamonic M. Bone grafting with Boplant. Results in thirty three cases. J Bone Joint Surg Br. 1968;50:364–68.PubMedGoogle Scholar
  21. 21.
    21. Elves MW, Salama R. A study of the development of cytotoxic antibodies pro duced in recipients of xenografts (heterografts) of iliac bone. J Bone Joint Surg Br. 1974;56:331–l39.PubMedGoogle Scholar
  22. 22.
    22. Cantore G, Fortuna A. Intersomatic fusion with calf bone “Kiel bone splint” in the anterior surgical approaach for the treatment of myelopathy in cervical spondylosis. Acta Neurochir (Wien). 1969;20:59–61.Google Scholar
  23. 23.
    23. Goran A, Murthy KK. Fracture dislocation of the cervical spine. Value of anterior approach with bovine bone interbody fusion. Spine. 1978;3:95–102.PubMedGoogle Scholar
  24. 24.
    24. Jackson JW. Surgical approaches to the anterior aspect of the spinal column. Ann R Coll Surg Engl. 1971;48:83–98.PubMedGoogle Scholar
  25. 25.
    25. Salama R, Weissman SL. The clinical use of combined xenografts of bone and autologous red marrow. A preliminary report. J Bone Joint Surg Br. 1978;60:111–15.PubMedGoogle Scholar
  26. 26.
    26. Siqueira EB, Kranzler LI. Cervical Interbody fusion using calf bone. Surg Neurol. 1982;18:37–39.PubMedGoogle Scholar
  27. 27.
  28. 28.
    28. Nielsen IM, Ellegaard B, Karring T. Kielbone in new attachment attempts in Humans. J Periodontol. 1981;52:723–28.PubMedGoogle Scholar
  29. 29.
    29. Older LB. The use of heterogenous bovine bone implants in the treatment of peri odontal pockets. An experimental study in humans. J Periodontol. 1967;38:539–.PubMedGoogle Scholar
  30. 30.
    30. Sigurdson A. Orala benimplantat. Sven Tandlak Tidskr. 1972;65:33–40.PubMedGoogle Scholar
  31. 31.
    31. Christiansen JV, Hindmarsh T, Levander B, Lofgren H, Olsson T, ReinholtFP. Comparative vascular evaluation by MRI of autologous and bovine grafts. In: Schoutens A, Arlet J, Gardeniers JWM, Hughes SPF, eds. Bone Circulation in Normal and Pathological Condition. New York: Plenum Press; 1993: 137–40.Google Scholar
  32. 32.
    32. Espersen JO, Buhl M, Eriksen EF, Fode K, Klaerke A, Kroyer L et al. Treatment of cervical disc disease using Cloward&s technique. I. General results, effect of different operative methods and complications in 1,106 patients. Acta Neurochir (Wien). 1984;70:97–114.Google Scholar
  33. 33.
    33. Lofgren H, Johannsson V, Olsson T, Ryd L, Levander B. Rigid fusion after cloward operation for cervical disc disease using autograft, allograft, or xenograft: a ran domized study with radiostereometric and clinical follow-up assessment. Spine. 2000;25:1908–16.PubMedGoogle Scholar
  34. 34.
    34. McMurray GN. The evaluation of Kiel bone in spinal fusions. J Bone Joint Surg Br. 1982;64:101–4.PubMedGoogle Scholar
  35. 35.
    35. Ramani PS, Kalbag RM, Sengupta RP. Cervical spinal interbody fusion with Kiel bone. Br J Surg. 1975;62:147–50.PubMedGoogle Scholar
  36. 36.
    36. Rawlinson JN. Morbidity after anterior cervical decompression and fusion. The influence of the donor site on recovery, and the results of a trial of surgibone com pared to autologous bone. Acta Neurochir (Wien). 1994;131:106–18.Google Scholar
  37. 37.
    37. Sutter B, Friehs G, Pendl G, Tolly E. Bovine dowels for anterior cervical fusion: experience in 66 patients with a note on postoperative CT and MRI appearance. Acta Neurochir (Wien). 1995;137:192–98.Google Scholar
  38. 38.
    38. Melcher AH. The use of heterogenous anorganic bone as an implant material in oral procedures. Oral Surg Oral Med Oral Pathol. 1962;15:996–1000.PubMedGoogle Scholar
  39. 39.
    39. Nielsen IM, Ellegaard B, Karring T. Kielbone in healing interradicular lesions in monkeys. J Periodontal Res. 1980;15:328–37.PubMedGoogle Scholar
  40. 40.
    40. Baer W, Schaller P, Carl HD. Spongy hydroxyapatite in hand surgery–a five year follow-up. J Hand Surg [Br]. 2002;27:101–3.Google Scholar
  41. 41.
    41. Briem D, Linhart W, Lehmann W, Meenen NM, Rueger JM. Langzeitergebnisse nach Anwendung einer porösen Hydroxylapatitkeramik (Endobon) zur operativen Versorgung von Tibiakopffrakturen. Unfallchirurg. 2002;105:128–33.PubMedGoogle Scholar
  42. 42.
    42. Helber MU, Ulrich C. Metaphysärer Defektersatz mit Hydroxylapatitkeramik - 3-bis 4-Jahresnachuntersuchungsergebnisse. Unfallchirurg. 2000;103:749–53.PubMedGoogle Scholar
  43. 43.
    43. Werber KD, Brauer RB, Weiss W, Becker K. Osseous integration of bovine hydroxyapatite ceramic in metaphyseal bone defects of the distal radius. J Hand Surg [Am]. 2000;25:833–41.Google Scholar
  44. 44.
    Jarcho M. Calcium phosphate ceramics as hard tissue prosthetics. Clin Orthop Relat Res. 1981;259–78.Google Scholar
  45. 45.
    LeGeros RZ. Properties of osteoconductive biomaterials: calcium phosphates. Clin Orthop Relat Res. 2002;81–98.Google Scholar
  46. 46.
    46. LeGeros RZ. Apatites in biological systems. ProgCrystal Growth Charact. 1981;4:1–45.Google Scholar
  47. 47.
    LeGeros RZ. CaP in Oral Biology and Medicine. In: Meyers H, ed. Monographs in Oral Sciences. Basel: Karger; 1991.Google Scholar
  48. 48.
    48. Peters F, Schwarz K, Epple M. The structure of bone studied with synchrotron X-ray diffraction, X-ray absorption spectroscopy and thermal analysis. Thermochim Acta. 2000;361:131–38.Google Scholar
  49. 49.
    49. Jensen SS, Aaboe M, Pinholt EM, Hjorting-Hansen E, Melsen F, Ruyter IE. Tissue reaction and material characteristics of four bone substitutes. Int J Oral Maxillofac Implants. 1996;11:55–66.PubMedGoogle Scholar
  50. 50.
    50. Benke D, Olah A, Mohler H. Protein-chemical analysis of Bio-Oss bone substitute and evidence on its carbonate content. Biomaterials. 2001;22:1005–12.PubMedGoogle Scholar
  51. 51.
    51. Peetz M. Characterization of xenogeneic bone mineral. In: Boyne PJ, ed. Osseous Reconstruction of the Maxilla and the Mandible: Surgical Techniques using Titanium Mesh and Bone Mineral. Carol Stream, IL: Quintessence Publishing; 1997: 87–93.Google Scholar
  52. 52.
    52. Spector M. Basic principles of tissue engineering. In: Lynch SEGRJMRE, ed. Tissue engineering: applications in maxillofacial surgery and periodontics. Carol Stream, IL, USA: Quintessence Publishing Co. Inc.; 1998: 3–16.Google Scholar
  53. 53.
    53. Weibrich G, Trettin R, Gnoth SH, Gotz H, Duschner H, Wagner W. Bestimmung der Größe der spezifischen Oberfläche von Knochenersatzmaterialien mittels Gasadsorption. Mund Kiefer Gesichtschir. 2000;4:148–52.PubMedGoogle Scholar
  54. 54.
    54. LeGeros RZ. Biodegradation and bioresorption of calcium phosphate ceramics. Clin Mater. 1993;14:65–88.PubMedGoogle Scholar
  55. 55.
    55. Koerten HK, van der MJ. Degradation of calcium phosphate ceramics. J Biomed Mater Res. 1999;44:78–86.PubMedGoogle Scholar
  56. 56.
    Bauer TW, Muschler GF. Bone graft materials. An overview of the basic science. Clin Orthop Relat Res. 2000;10–27.Google Scholar
  57. 57.
    57. Hofman S, Sidqui M, Abensur D, Valentini P, Missika P. Effects of Laddec on the formation of calcified bone matrix in rat calvariae cells culture. Biomaterials. 1999;20:1155–66.PubMedGoogle Scholar
  58. 58.
    58. Stephan EB, Jiang D, Lynch S, Bush P, Dziak R. Anorganic bovine bone supports osteoblastic cell attachment and proliferation. J Periodontol. 1999;70:364–69.PubMedGoogle Scholar
  59. 59.
    59. Acil Y, Terheyden H, Dunsche A, Fleiner B, Jepsen S. Three-dimensional cul tivation of human osteoblast-like cells on highly porous natural bone mineral. J Biomed Mater Res. 2000;51:703–10.PubMedGoogle Scholar
  60. 60.
    60. Matsumoto T, Kawakami M, Kuribayashi K, Takenaka T, Minamide A, Tamaki T. Effects of sintered bovine bone on cell proliferation, collagen synthesis, and oste-oblastic expression in MC3T3-E1 osteoblast-like cells. J Orthop Res. 1999;17:586–92.PubMedGoogle Scholar
  61. 61.
    61. Qian JJ, Bhatnagar RS. Enhanced cell attachment to anorganic bone mineral in the presence of a synthetic peptide related to collagen. J Biomed Mater Res. 1996;31:545–54.PubMedGoogle Scholar
  62. 62.
    62. Bhatnagar RS, Qian JJ, Wedrychowska A, Sadeghi M, Wu YM, Smith N. Design of biomimetic habitats for tissue engineering with P-15, a synthetic peptide analogue of collagen. Tissue Eng. 1999;5:53–65.PubMedGoogle Scholar
  63. 63.
    63. Kubler A, Neugebauer J, Oh JH, Scheer M, Zoller JE. Growth and proliferation of human osteoblasts on different bone graft substitutes: an in vitro study. Implant Dent. 2004;13:171–79.PubMedGoogle Scholar
  64. 64.
    64. Turhani D, Weissenbock M, Watzinger E, Yerit K, Cvikl B, Ewers R et al. Invitro study of adherent mandibular osteoblast-like cells on carrier materials. Int J Oral Maxillofac Surg. 2005;34:543–50.PubMedGoogle Scholar
  65. 65.
    65. Taylor JC, Cuff SE, Leger JP, Morra A, Anderson GI. In vitro osteoclast resorption of bone substitute biomaterials used for implant site augmentation: a pilot study. Int J Oral Maxillofac Implants. 2002;17:321–30.PubMedGoogle Scholar
  66. 66.
    66. Schwartz Z, Weesner T, van DS, Cochran DL, Mellonig JT, Lohmann CH et al. Ability of deproteinized cancellous bovine bone to induce new bone formation. J Periodontol. 2000;71:1258–69.PubMedGoogle Scholar
  67. 67.
    67. Honig JF, Merten HA, Heinemann DE. Risk of transmission of agents associ ated with Creutzfeldt-Jakob disease and bovine spongiform encephalopathy. Plast Reconstr Surg. 1999;103:1324–25.PubMedGoogle Scholar
  68. 68.
    68. Will RG, Ironside JW, Zeidler M, Cousens SN, Estibeiro K, Alperovitch A et al. A new variant of Creutzfeldt-Jakob disease in the UK. Lancet. 1996;347:921–25.PubMedGoogle Scholar
  69. 69.
    69. Asher DM, Gibbs CJ, Jr., Sulima MP, Bacote A, Amyx H, Gajdusek DC. Transmission of human spongiform encephalopathies to experimental animals: comparison of the chimpanzee and squirrel monkey. Dev Biol Stand. 1993;80:9–13.PubMedGoogle Scholar
  70. 70.
    70. Lantos PL. From slow virus to prion: a review of transmissible spongiform enceph-alopathies. Histopathology. 1992;20:1–11.PubMedGoogle Scholar
  71. 71.
    c WHO. Public health issues related to animal and human spongiform encepha-lopathies: Memorandum from a WHO meeting. Bulletin of the World Health Organization. 1992;70:183–90.Google Scholar
  72. 72.
    72. Wenz B, Oesch B, Horst M. Analysis of the risk of transmitting bovine spongiform encephalopathy through bone grafts derived from bovine bone. Biomaterials. 2001;22:1599–606.PubMedGoogle Scholar
  73. 73.
    Bundesgesundheitsamt. Bekanntmachung der Sicherheitsanforderungen an Arzneimittel aus KoK rperbestandteilen von Rind, Schaf oder Ziege zur Vemeidung des Risikos einer UG bertragung von BSE bzw. Scrapie. Bundesanzeiger. 1994;40:1851–55.Google Scholar
  74. 74.
    Bundesgesundheitsamt. Bekanntmachung über die Zulassung und Registrierung von Arzneimitteln. Bundesanzeiger. 1996;67:4158–62.Google Scholar
  75. 75.
    75. Sogal A, Tofe AJ. Risk assessment of bovine spongiform encephalopathy transmis sion through bone graft material derived from bovine bone used for dental applica tions. J Periodontol. 1999;70:1053–63.PubMedGoogle Scholar
  76. 76.
    76. Artzi Z, Nemcovsky CE. The application of deproteinized bovine bone mineral for ridge preservation prior to implantation. Clinical and histological observations in a case report. J Periodontol. 1998;69:1062–67.PubMedGoogle Scholar
  77. 77.
    77. Artzi Z, Tal H, Dayan D. Porous bovine bone mineral in healing of human extrac tion sockets. Part 1: histomorphometric evaluations at 9 months. J Periodontol. 2000;71:1015–23.PubMedGoogle Scholar
  78. 78.
    78. Artzi Z, Tal H, Dayan D. Porous bovine bone mineral in healing of human extraction sockets: 2. Histochemical observations at 9 months. J Periodontol. 2001;72:152–59.PubMedGoogle Scholar
  79. 79.
    79. van Steenberghe D., Callens A, Geers L, Jacobs R. The clinical use of deprotein-ized bovine bone mineral on bone regeneration in conjunction with immediate implant installation. Clin Oral Implants Res. 2000;11:210–216.PubMedGoogle Scholar
  80. 80.
    80. Schlegel AK, Donath K. BIO-OSS–a resorbable bone substitute? J Long Term Eff Med Implants. 1998;8:201–9.PubMedGoogle Scholar
  81. 81.
    81. Maiorana C, Santoro F, Rabagliati M, Salina S. Evaluation of the use of iliac can-cellous 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;16:427–32.PubMedGoogle Scholar
  82. 82.
    82. Skoglund A, Hising P, Young C. A clinical and histologic examination in humans of the osseous response to implanted natural bone mineral. Int J Oral Maxillofac Implants. 1997;12:194–99.PubMedGoogle Scholar
  83. 83.
    83. Froum SJ, Tarnow DP, Wallace SS, Rohrer MD, Cho SC. Sinus floor elevation using anorganic bovine bone matrix (OsteoGraf/N) with and without autogenous bone: a clinical, histologic, radiographic, and histomorphometric analysis–Part 2 of an ongoing prospective study. Int J Periodontics Restorative Dent. 1998;18:528–43.PubMedGoogle Scholar
  84. 84.
    84. Krauser JT, Rohrer MD, Wallace SS. Human histologic and histomorphometric analysis comparing OsteoGraf/N with PepGen P-15 in the maxillary sinus eleva tion procedure: a case report. Implant Dent. 2000;9:298–302.PubMedGoogle Scholar
  85. 85.
    85. Fugazzotto PA, Vlassis J. Long-term success of sinus augmentation using vari ous surgical approaches and grafting materials. Int J Oral Maxillofac Implants. 1998;13:52–58.PubMedGoogle Scholar
  86. 86.
    86. Hallman M, Lundgren S, Sennerby L. Histologic analysis of clinical biopsies taken 6 months and 3 years after maxillary sinus floor augmentation with 80 percent bovine hydroxyapatite and 20 percent autogenous bone mixed with fibrin glue. Clin Implant Dent Relat Res. 2001;3:87–96.PubMedGoogle Scholar
  87. 87.
    87. Hallman M, Cederlund A, Lindskog S, Lundgren S, Sennerby L. A clinical his-tologic study of bovine hydroxyapatite in combination with autogenous bone and fibrin glue for maxillary sinus floor augmentation. Results after 6 to 8 months of healing. Clin Oral Implants Res. 2001;12:135–43.PubMedGoogle Scholar
  88. 88.
    88. Hurzeler MB, Kirsch A, Ackermann KL, Quinones CR. Reconstruction of the severely resorbed maxilla with dental implants in the augmented maxillary sinus: a 5-year clinical investigation. Int J Oral Maxillofac Implants. 1996;11:466–75.PubMedGoogle Scholar
  89. 89.
    89. Maiorana C, Redemagni M, Rabagliati M, Salina S. Treatment of maxillary ridge resorption by sinus augmentation with iliac cancellous bone, anorganic bovine bone, and endosseous implants: a clinical and histologic report. Int J Oral Maxillofac Implants. 2000;15:873–78.PubMedGoogle Scholar
  90. 90.
    90. Tawil G, Mawla M. Sinus floor elevation using a bovine bone mineral (Bio-Oss) with or without the concomitant use of a bilayered collagen barrier (Bio-Gide): a clinical report of immediate and delayed implant placement. Int J Oral Maxillofac Implants. 2001;16:713–21.PubMedGoogle Scholar
  91. 91.
    91. Valentini P, Abensur D. Maxillary sinus floor elevation for implant placement with demineralized freeze-dried bone and bovine bone (Bio-Oss): a clinical study of 20 patients. Int J Periodontics Restorative Dent. 1997;17:232–41.PubMedGoogle Scholar
  92. 92.
    92. Valentini P, Abensur D, Densari D, Graziani JN, Hammerle C. Histological eval uation of Bio-Oss in a 2-stage sinus floor elevation and implantation procedure. A human case report. Clin Oral Implants Res. 1998;9:59–64.PubMedGoogle Scholar
  93. 93.
    93. Hallman M, Sennerby L, Lundgren S. A clinical and histologic evaluation of implant integration in the posterior maxilla after sinus floor augmentation with autogenous bone, bovine hydroxyapatite, or a 20:80 mixture. Int J Oral Maxillofac Implants. 2002;17:635–43.PubMedGoogle Scholar
  94. 94.
    94. Hising P, Bolin A, Branting C. Reconstruction of severely resorbed alveolar ridge crests with dental implants using a bovine bone mineral for augmentation. Int J Oral Maxillofac Implants. 2001;16:90–97.PubMedGoogle Scholar
  95. 95.
    95. Valentini P, Abensur DJ. Maxillary sinus grafting with an organic bovine bone: a clinical report of long-term results. Int J Oral Maxillofac Implants. 2003;18:556–60.PubMedGoogle Scholar
  96. 96.
    96. Maiorana C, Sigurta D, Mirandola A, Garlini G, Santoro F. Sinus elevation with alloplasts or xenogenic materials and implants: an up-to-4-year clinical and radio-logic follow-up. Int J Oral Maxillofac Implants. 2006;21:426–32.PubMedGoogle Scholar
  97. 97.
    97. Del Fabbro M, Testori T, Francetti L, Weinstein R. Systematic review of sur vival rates for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent. 2004;24:565–77.PubMedGoogle Scholar
  98. 98.
    98. Wallace SS, Froum SJ. Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol. 2003;8:328–43.PubMedGoogle Scholar
  99. 99.
    99. Mayfield LJ, Skoglund A, Hising P, Lang NP, Attstrom R. Evaluation following functional loading of titanium fixtures placed in ridges augmented by deproteinized bone mineral. A human case study. Clin Oral Implants Res. 2001;12:508–14.PubMedGoogle Scholar
  100. 100.
    100. Zitzmann NU, Scharer P, Marinello CP. Long-term results of implants treated with guided bone regeneration: a 5-year prospective study. Int J Oral Maxillofac Implants. 2001;16:355–66.PubMedGoogle Scholar
  101. 101.
    101. Dies F, Etienne D, Abboud NB, Ouhayoun JP. Bone regeneration in extraction sites after immediate placement of an e-PTFE membrane with or without a bioma-terial. A report on 12 consecutive cases. Clin Oral Implants Res. 1996;7:277–85.PubMedGoogle Scholar
  102. 102.
    102. Lorenzoni M, Pertl C, Keil C, Wegscheider WA. Treatment of peri-implant defects with guided bone regeneration: a comparative clinical study with various mem branes and bone grafts. Int J Oral Maxillofac Implants. 1998;13:639–46.PubMedGoogle Scholar
  103. 103.
    103. 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;12:844–52.PubMedGoogle Scholar
  104. 104.
    104. Carpio L, Loza J, Lynch S, Genco R. Guided bone regeneration around endosseous implants with anorganic bovine bone mineral. A randomized controlled trial com paring bioabsorbable versus non-resorbable barriers. J Periodontol. 2000;71:1743–49.PubMedGoogle Scholar
  105. 105.
    105. Hammerle CH, Lang NP. Single stage surgery combining transmucosal implant placement with guided bone regeneration and bioresorbable materials. Clin Oral Implants Res. 2001;12:9–18.PubMedGoogle Scholar
  106. 106.
    106. Zitzmann NU, Scharer P, Marinello CP, Schupbach P, Berglundh T. Alveolar ridge augmentation with Bio-Oss: a histologic study in humans. Int J Periodontics Restorative Dent. 2001;21:288–95.PubMedGoogle Scholar
  107. 107.
    107. Cornelini R, Cangini F, Martuscelli G, Wennstrom J. Deproteinized bovine bone and biodegradable barrier membranes to support healing following immediate placement of transmucosal implants: a short-term controlled clinical trial. Int J Periodontics Restorative Dent. 2004;24:555–63.PubMedGoogle Scholar
  108. 108.
    108. Moses O, Pitaru S, Artzi Z, Nemcovsky CE. Healing of dehiscence-type defects in implants placed together with different barrier membranes: a comparative clinical study. Clin Oral Implants Res. 2005;16:210–219.PubMedGoogle Scholar
  109. 109.
    109. Norton MR, Odell EW, Thompson ID, Cook RJ. Efficacy of bovine bone mineral for alveolar augmentation: a human histologic study. Clin Oral Implants Res. 2003;14:775–83.PubMedGoogle Scholar
  110. 110.
    110. Nemcovsky CE, Artzi Z, Moses O, Gelernter I. Healing of marginal defects at implants placed in fresh extraction sockets or after 4–6 weeks of healing. A com parative study. Clin Oral Implants Res. 2002;13:410–419.PubMedGoogle Scholar
  111. 111.
    111. De Boever AL, De Boever JA. Guided bone regeneration around non-submerged implants in narrow alveolar ridges: a prospective long-term clinical study. Clinical Oral Implants Research. 2005;16:549–56.PubMedGoogle Scholar
  112. 112.
    112. Yildirim M, Spiekermann H, Biesterfeld S, Edelhoff D. Maxillary sinus aug mentation using xenogenic bone substitute material Bio-Oss in combination with venous blood. A histologic and histomorphometric study in humans. Clin Oral Implants Res. 2000;11:217–29.PubMedGoogle Scholar
  113. 113.
    113. Artzi Z, Nemcovsky CE, Tal H, Dayan D. Histopathological morphometric evalu ation of 2 different hydroxyapatite-bone derivatives in sinus augmentation proce dures: a comparative study in humans. J Periodontol. 2001;72:911–20.PubMedGoogle Scholar
  114. 114.
    114. Rodoni LR, Glauser R, Feloutzis A, Hammerle CH. Implants in the posterior maxilla: a comparative clinical and radiologic study. Int J Oral Maxillofac Implants. 2005;20:231–37.PubMedGoogle Scholar
  115. 115.
    115. Hallman M, Nordin T. Sinus floor augmentation with bovine hydroxyapatite mixed with fibrin glue and later placement of nonsubmerged implants: a retro spective study in 50 patients. Int J Oral Maxillofac Implants. 2004;19:222–27.PubMedGoogle Scholar
  116. 116.
    116. John HD, Wenz B. Histomorphometric analysis of natural bone mineral for maxillary sinus augmentation. Int J Oral Maxillofac Implants. 2004;19:199–207.PubMedGoogle Scholar
  117. 117.
  118. 118.
    118. Artzi Z, Dayan D, Alpern Y, Nemcovsky CE. Vertical ridge augmentation using xenogenic material supported by a configured titanium mesh: clinicohistopatho logic and histochemical study. Int J Oral Maxillofac Implants. 2003;18:440–446.PubMedGoogle Scholar
  119. 119.
  120. 120.
    120. Philippart P, Daubie V, Pochet R. Sinus grafting using recombinant human tis sue factor, platelet-rich plasma gel, autologous bone, and anorganic bovine bone mineral xenograft: histologic analysis and case reports. Int J Oral Maxillofac Implants. 2005;20:274–81.PubMedGoogle Scholar
  121. 121.
    121. Toffler M. Osteotome-mediated sinus floor elevation: a clinical report. Int J Oral Maxillofac Implants. 2004;19:266–73.PubMedGoogle Scholar
  122. 122.
    122. Schwarz F, Bieling K, Latz T, Nuesry E, Becker J. Healing of intrabony peri implantitis defects following application of a nanocrystalline hydroxyapatite (Ostim) or a bovine-derived xenograft (Bio-Oss) in combination with a collagen membrane (Bio-Gide). A case series. J Clin Periodontol. 2006;33:491–99.PubMedGoogle Scholar
  123. 123.
    123. Hislop WS, Finlay PM, Moos KF. A preliminary study into the uses of anorganic bone in oral and maxillofacial surgery. Br J Oral Maxillofac Surg. 1993;31:149–53.PubMedGoogle Scholar
  124. 124.
    124. Maiorana C, Beretta M, Salina S, Santoro F. Reduction of autogenous bone graft resorption by means of bio-oss coverage: a prospective study. Int J Periodontics Restorative Dent. 2005;25:19–25.PubMedGoogle Scholar
  125. 125.
    125. Hammerle CH, Olah AJ, Schmid J, Fluckiger L, Gogolewski S, Winkler JR et al. The biological effect of natural bone mineral on bone neoformation on the rabbit skull. Clin Oral Implants Res. 1997;8:198–207.PubMedGoogle Scholar
  126. 126.
    126. Nasr HF, Aichelmann-Reidy ME, Yukna RA. Bone and bone substitutes. Periodontol 2000. 1999;19:74–86.PubMedGoogle Scholar
  127. 127.
    127. Karring T, Nyman S, Thilander B, Magnusson I. Bone regeneration in orthodonti cally produced alveolar bone dehiscences. J Periodontal Res. 1982;17:309–15.PubMedGoogle Scholar
  128. 128.
    128. Lindhe J, Nyman S, Karring T. Connective tissue reattachment as related to pres ence or absence of alveolar bone. J Clin Periodontol. 1984;11:33–40.PubMedGoogle Scholar
  129. 129.
    129. Nyman S, Karring T. Regeneration of surgically removed buccal alveolar bone in dogs. J Periodontal Res. 1979;14:86–92.PubMedGoogle Scholar
  130. 130.
    130. Thilander B, Nyman S, Karring T, Magnusson I. Bone regeneration in alveolar bone dehiscences related to orthodontic tooth movements. Eur J Orthod. 1983;5:105–14.PubMedGoogle Scholar
  131. 131.
    131. Caton J, Zander HA. Osseous repair of an infrabony pocket without new attach ment of connective tissue. J Clin Periodontol. 1976;3:54–58.PubMedGoogle Scholar
  132. 132.
    132. Caton J, Nyman S, Zander H. Histometric evaluation of periodontal surgery. II. Connective tissue attachment levels after four regenerative procedures. J Clin Periodontol. 1980;7:224–31.PubMedGoogle Scholar
  133. 133.
    133. Listgarten MA, Rosenberg MM. Histological study of repair following new attachment procedures in human periodontal lesions. J Periodontol. 1979;50:333–44.PubMedGoogle Scholar
  134. 134.
    134. Ewers R, Goriwoda W, Schopper C, Moser D, Spassova E. Histologic findings at augmented bone areas supplied with two different bone substitute materials combined with sinus floor lifting. Report of one case. Clin Oral Implants Res. 2004;15:96–100.PubMedGoogle Scholar
  135. 135.
    135. Valentini P, Abensur D, Wenz B, Peetz M, Schenk R. Sinus grafting with porous bone mineral (Bio-Oss) for implant placement: a 5-year study on 15 patients. Int J Periodontics Restorative Dent. 2000;20:245–53.PubMedGoogle Scholar
  136. 136.
    136. Wallace SS, Froum SJ, Tarnow DP. Histologic evaluation of a sinus elevation procedure: a clinical report. Int J Periodontics Restorative Dent. 1996;16:46–51.PubMedGoogle Scholar
  137. 137.
    137. Wallace SS, Froum SJ, Cho SC, Elian N, Monteiro D, Kim BS et al. Sinus aug mentation utilizing anorganic bovine bone (Bio-Oss) with absorbable and non absorbable membranes placed over the lateral window: histomorphometric and clinical analyses. Int J Periodontics Restorative Dent. 2005;25:551–59.PubMedGoogle Scholar
  138. 138.
    138. Yildirim M, Spiekermann H, Handt S, Edelhoff D. Maxillary sinus augmentation with the xenograft Bio-Oss and autogenous intraoral bone for qualitative improve ment of the implant site: a histologic and histomorphometric clinical study in humans. Int J Oral Maxillofac Implants. 2001;16:23–33.PubMedGoogle Scholar
  139. 139.
    139. Merkx MA, Maltha JC, Stoelinga PJ. Assessment of the value of anorganic bone additives in sinus floor augmentation: a review of clinical reports. Int J Oral Maxillofac Surg. 2003;32:1–6.PubMedGoogle Scholar
  140. 140.
    140. Klinge B, Alberius P, Isaksson S, Jonsson J. Osseous response to implanted natural bone mineral and synthetic hydroxylapatite ceramic in the repair of experimental skull bone defects. J Oral Maxillofac Surg. 1992;50:241–49.PubMedGoogle Scholar
  141. 141.
    141. Thaller SR, Hoyt J, Borjeson K, Dart A, Tesluk H. Reconstruction of calvarial defects with anorganic bovine bone mineral (Bio-Oss) in a rabbit model. J Craniofac Surg. 1993;4:79–84.PubMedGoogle Scholar
  142. 142.
    142. Young C, Sandstedt P, Skoglund A. A comparative study of anorganic xenogenic bone and autogenous bone implants for bone regeneration in rabbits. Int J Oral Maxillofac Implants. 1999;14:72–76.PubMedGoogle Scholar
  143. 143.
    143. Schmitt JM, Buck DC, Joh SP, Lynch SE, Hollinger JO. Comparison of porous bone mineral and biologically active glass in critical-sized defects. J Periodontol. 1997;68:1043–53.PubMedGoogle Scholar
  144. 144.
    144. Al Ruhaimi KA. Bone graft substitutes: a comparative qualitative histologic review of current osteoconductive grafting materials. Int J Oral Maxillofac Implants. 2001;16:105–14.PubMedGoogle Scholar
  145. 145.
    145. Scarano A, Iezzi G, Petrone G, Orsini G, Degidi M, Strocchi R et al. Cortical bone regeneration with a synthetic cell-binding peptide: a histologic and histomorpho metric pilot study. Implant Dent. 2003;12:318–24.PubMedGoogle Scholar
  146. 146.
    146. Thorwarth M, Schultze-Mosgau S, Wehrhan F, Kessler P, Srour S, Wiltfang J et al. Bioactivation of an anorganic bone matrix by P-15 peptide for the promotion of early bone formation. Biomaterials. 2005;26:5648–57.PubMedGoogle Scholar
  147. 147.
    Thorwarth M, Wehrhan F, Srour S, Schultze-Mosgau S, Felszeghy E, Bader RD et al. Evaluation of substitutes for bone: Comparison of microradiographic and histological assessments. Br J Oral Maxillofac Surg. 2006.Google Scholar
  148. 148.
    148. Thorwarth M, Schlegel KA, Wehrhan F, Srour S, Schultze-Mosgau S. Acceleration of de novo bone formation following application of autogenous bone to particu-lated anorganic bovine material in vivo. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006;101:309–16.PubMedGoogle Scholar
  149. 149.
    149. Barboza EP, de Souza RO, Caula AL, Neto LG, Caula FO, Duarte ME. Bone regeneration of localized chronic alveolar defects utilizing cell binding peptide associated with anorganic bovine-derived bone mineral: a clinical and histological study. J Periodontol. 2002;73:1153–59.PubMedGoogle Scholar
  150. 150.
    150. Artzi Z, Givol N, Rohrer MD, Nemcovsky CE, Prasad HS, Tal H. Qualitative and quantitative expression of bovine bone mineral in experimental bone defects. Part 2: Morphometric analysis. J Periodontol. 2003;74:1153–60.PubMedGoogle Scholar
  151. 151.
    151. Cardaropoli G, Araujo M, Hayacibara R, Sukekava F, Lindhe J. Healing of extrac tion sockets and surgically produced - augmented and non-augmented - defects in the alveolar ridge. An experimental study in the dog. J Clin Periodontol. 2005;32:435–40.PubMedGoogle Scholar
  152. 152.
    152. Margolin MD, Cogan AG, Taylor M, Buck D, McAllister TN, Toth C et al. Maxillary sinus augmentation in the non-human primate: a comparative radio graphic and histologic study between recombinant human osteogenic protein-1 and natural bone mineral. J Periodontol. 1998;69:911–19.PubMedGoogle Scholar
  153. 153.
    153. McAllister BS, Margolin MD, Cogan AG, Taylor M, Wollins J. Residual lateral wall defects following sinus grafting with recombinant human osteogenic protein-1 or Bio-Oss in the chimpanzee. Int J Periodontics Restorative Dent. 1998;18:227–39.PubMedGoogle Scholar
  154. 154.
    154. McAllister BS, Margolin MD, Cogan AG, Buck D, Hollinger JO, Lynch SE. Eighteen-month radiographic and histologic evaluation of sinus grafting with anorganic bovine bone in the chimpanzee. Int J Oral Maxillofac Implants. 1999;14:361–68.PubMedGoogle Scholar
  155. 155.
    155. Berglundh T, Lindhe J. Healing around implants placed in bone defects treated with Bio-Oss. An experimental study in the dog. Clin Oral Implants Res. 1997;8:117–24.PubMedGoogle Scholar
  156. 156.
    156. Botticelli D, Berglundh T, Lindhe J. The influence of a biomaterial on the closure of a marginal hard tissue defect adjacent to implants. An experimental study in the dog. Clinical Oral Implants Research. 2004;15:285–92.PubMedGoogle Scholar
  157. 157.
    157. Haas R, Mailath G, Dortbudak O, Watzek G. Bovine hydroxyapatite for maxillary sinus augmentation: analysis of interfacial bond strength of dental implants using pull-out tests. Clin Oral Implants Res. 1998;9:117–22.PubMedGoogle Scholar
  158. 158.
    158. Haas R, Donath K, Fodinger M, Watzek G. Bovine hydroxyapatite for maxillary sinus grafting: comparative histomorphometric findings in sheep. Clin Oral Implants Res. 1998;9:107–16.PubMedGoogle Scholar
  159. 159.
    159. Hurzeler MB, Quinones CR, Kirsch A, Gloker C, Schupbach P, Strub JR et al. Maxillary sinus augmentation using different grafting materials and dental implants in monkeys. Part I. Evaluation of anorganic bovine-derived bone matrix. Clin Oral Implants Res. 1997;8:476–86.PubMedGoogle Scholar
  160. 160.
    160. Terheyden H, Jepsen S, Moller B, Tucker MM, Rueger DC. Sinus floor augmen tation with simultaneous placement of dental implants using a combination of deproteinized bone xenografts and recombinant human osteogenic protein-1. A histometric study in miniature pigs. Clin Oral Implants Res. 1999;10:510–521.PubMedGoogle Scholar
  161. 161.
    161. Wetzel AC, Stich H, Caffesse RG. Bone apposition onto oral implants in the sinus area filled with different grafting materials. A histological study in beagle dogs. Clin Oral Implants Res. 1995;6:155–63.PubMedGoogle Scholar
  162. 162.
    162. Schlegel KA, Fichtner G, Schultze-Mosgau S, Wiltfang J. Histologic findings in sinus augmentation with autogenous bone chips versus a bovine bone substitute. Int J Oral Maxillofac Implants. 2003;18:53–58.PubMedGoogle Scholar
  163. 163.
  164. 164.
    164. Pinholt EM, Bang G, Haanaes HR. Alveolar ridge augmentation in rats by Bio-Oss. Scand J Dent Res. 1991;99:154–61.PubMedGoogle Scholar
  165. 165.
    165. Mandelkow HK, Hallfeldt KK, Kessler SB, Gayk M, Siebeck M, Schweiberer L. Knochenneubildung nach Implantation verschiedener Hydroxylapatitkeramiken. Tierexperimentelle Studie am Bohrlochmodell der Schaftstibia. Unfallchirurg. 1990;93:376–79.PubMedGoogle Scholar
  166. 166.
    166. Fukuta K, Har-Shai Y, Collares MV, Lichten JB, Jackson IT. Comparison of inorganic bovine bone mineral particles with porous hydroxyapatite granules and cranial bone dust in the reconstruction of full-thickness skull defect. J Craniofac Surg. 1992;3:25–29.PubMedGoogle Scholar
  167. 167.
    167. Merkx MA, Maltha JC, Freihofer HP, Kuijpers-Jagtman AM. Incorporation of particulated bone implants in the facial skeleton. Biomaterials. 1999;20:2029–35.PubMedGoogle Scholar
  168. 168.
    168. Merkx MA, Maltha JC, Freihofer HP, Kuijpers-Jagtman AM. Incorporation of three types of bone block implants in the facial skeleton. Biomaterials. 1999;20:639–45.PubMedGoogle Scholar
  169. 169.
    169. Aghaloo TL, Moy PK, Freymiller EG. Evaluation of platelet-rich plasma in com bination with anorganic bovine bone in the rabbit cranium: a pilot study. Int J Oral Maxillofac Implants. 2004;19:59–65.PubMedGoogle Scholar
  170. 170.
    170. Merkx MA, Maltha JC, Freihofer HP. Incorporation of composite bone implants in the facial skeleton. Clin Oral Implants Res. 2000;11:422–29.PubMedGoogle Scholar
  171. 171.
    Schmitz JP, Hollinger JO. The critical size defect as an experimental model for craniomandibulofacial nonunions. Clin Orthop Relat Res. 1986;299–308.Google Scholar
  172. 172.
  173. 173.
    173. Stavropoulos A, Kostopoulos L, Mardas N, Nyengaard JR, Karring T. Deproteinized bovine bone used as an adjunct to guided bone augmentation: an experimental study in the rat. Clin Implant Dent Relat Res. 2001;3:156–65.PubMedGoogle Scholar
  174. 174.
    174. Stavropoulos A, Kostopoulos L, Nyengaard JR, Karring T. Deproteinized bovine bone (Bio-Oss) and bioactive glass (Biogran) arrest bone formation when used as an adjunct to guided tissue regeneration (GTR): an experimental study in the rat. J Clin Periodontol. 2003;30:636–43.PubMedGoogle Scholar
  175. 175.
    175. Stavropoulos A, Kostopoulos L, Nyengaard JR, Karring T. Fate of bone formed by guided tissue regeneration with or without grafting of Bio-Oss or Biogran. An experimental study in the rat. J Clin Periodontol. 2004;31:30–39.PubMedGoogle Scholar
  176. 176.
    176. Xu H, Shimizu Y, Asai S, Ooya K. Grafting of deproteinized bone particles inhibits bone resorption after maxillary sinus floor elevation. Clinical Oral Implants Research. 2004;15:126–33.PubMedGoogle Scholar
  177. 177.
    177. Araujo MG, Sonohara M, Hayacibara R, Cardaropoli G, Lindhe J. Lateral ridge augmentation by the use of grafts comprised of autologous bone or a biomaterial. An experiment in the dog. J Clin Periodontol. 2002;29:1122–31.PubMedGoogle Scholar
  178. 178.
    178. Carmagnola D, Berglundh T, Lindhe J. The effect of a fibrin glue on the integra tion of Bio-Oss with bone tissue. A experimental study in labrador dogs. J Clin Periodontol. 2002;29:377–83.PubMedGoogle Scholar
  179. 179.
  180. 180.
    180. Schmid J, Hammerle CH, Fluckiger L, Winkler JR, Olah AJ, Gogolewski S et al. Blood-filled spaces with and without filler materials in guided bone regeneration. A comparative experimental study in the rabbit using bioresorbable membranes. Clin Oral Implants Res. 1997;8:75–81.PubMedGoogle Scholar
  181. 181.
    181. Slotte C, Lundgren D. Augmentation of calvarial tissue using non-permeable silicone domes and bovine bone mineral. An experimental study in the rat. Clin Oral Implants Res. 1999;10:468–76.PubMedGoogle Scholar
  182. 182.
    182. Hockers T, Abensur D, Valentini P, Legrand R, Hammerle CH. The combined use of bioresorbable membranes and xenografts or autografts in the treatment of bone defects around implants. A study in beagle dogs. Clin Oral Implants Res. 1999;10:487–98.PubMedGoogle Scholar
  183. 183.
    183. 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.PubMedGoogle Scholar
  184. 184.
    184. Polimeni G, Koo KT, Qahash M, Xiropaidis AV, Albandar JM, Wikesjo UM. Prognostic factors for alveolar regeneration: effect of a space-providing biomate-rial on guided tissue regeneration. J Clin Periodontol. 2004;31:725–29.PubMedGoogle Scholar
  185. 185.
    185. Wikesjo UM, Lim WH, Thomson RC, Hardwick WR. Periodontal repair in dogs: gingival tissue occlusion, a critical requirement for GTR? J Clin Periodontol. 2003;30:655–64.PubMedGoogle Scholar
  186. 186.
    186. Hammerle CH, Chiantella GC, Karring T, Lang NP. The effect of a deproteinized bovine bone mineral on bone regeneration around titanium dental implants. Clin Oral Implants Res. 1998;9:151–62.PubMedGoogle Scholar
  187. 187.
    187. Schou S, Holmstrup P, Jorgensen T, Skovgaard LT, Stoltze K, Hjorting-Hansen E et al. Anorganic porous bovine-derived bone mineral (Bio-Oss( (R) ) ) and ePTFE membrane in the treatment of peri-implantitis in cynomolgus monkeys. Clinical Oral Implants Research. 2003;14:535–47.PubMedGoogle Scholar
  188. 188.
    188. Chiapasco M, Ferrini F, Casentini P, Accardi S, Zaniboni M. Dental implants placed in expanded narrow edentulous ridges with the Extension Crest device. A 1-3-year multicenter follow-up study. Clin Oral Implants Res. 2006;17:265–72.PubMedGoogle Scholar
  189. 189.
    189. Patur B, Glickman I. Clinical and roentgenographic evaluation of the post-treatment healing of infrabony pockets. J Periodontol. 1962;33:164–71.Google Scholar
  190. 190.
    190. Beube FE, Silvers HF. Influence of devitalized heterogenous bone-powder on regeneration of alveolar and maxillary bone of dogs. J Dent Res. 1934;14:15–19.Google Scholar
  191. 191.
    191. Beube FE. Observations on the formation of cementum, periodontal membrane and bone, 20 months postperatively, with the use of boiled cow bone powder. J Dent Res. 1942;21:2989–299.Google Scholar
  192. 192.
    192. Scopp IW, Morgan FH, Dooner JJ, Fredrics HJ, Heyman RA. Bovine bone (Boplant) implants for intrabony oral lesions. Periodontics. 1966;4:169–76.Google Scholar
  193. 193.
    193. Clergeau LP, Danan M, Clergeau-Guerithault S, Brion M. Healing response to anorganic bone implantation in periodontal intrabony defects in dogs. Part I. Bone regeneration. A microradiographic study. J Periodontol. 1996;67:140–149.PubMedGoogle Scholar
  194. 194.
    194. Camelo M, Nevins ML, Schenk RK, Simion M, Rasperini G, Lynch SE et al. Clinical, radiographic, and histologic evaluation of human periodontal defects treated with Bio-Oss and Bio-Gide. Int J Periodontics Restorative Dent. 1998;18:321–31.PubMedGoogle Scholar
  195. 195.
    195. Hutchens LH, Jr. The use of a bovine bone mineral in periodontal osseous defects: case reports. Compend Contin Educ Dent. 1999;20:365-4.PubMedGoogle Scholar
  196. 196.
    196. Richardson CR, Mellonig JT, Brunsvold MA, McDonnell HT, Cochran DL. Clinical evaluation of Bio-Oss: a bovine-derived xenograft for the treatment of periodontal osseous defects in humans. J Clin Periodontol. 1999;26:421–28.PubMedGoogle Scholar
  197. 197.
    197. Karring T, Nyman S, Gottlow J, Laurell L. Development of the biological con cept of guided tissue regeneration-animal and human studies. Periodontol 2000. 1993;1:26–35.Google Scholar
  198. 198.
    Stavropoulos A. Guided tissue regeneration in combination with deproteinized bovine bone and gentamicin. PhD thesis ed. Aarhus, Denmark: 2002.Google Scholar
  199. 199.
    199. Caton J, Wagener C, Polson A, Nyman S, Frantz B, Bouwsma O et al. Guided tissue regeneration in interproximal defects in the monkey. Int J Periodontics Restorative Dent. 1992;12:266–77.PubMedGoogle Scholar
  200. 200.
    200. Gottlow J, Nyman S, Karring T, Lindhe J. New attachment formation as the result of controlled tissue regeneration. J Clin Periodontol. 1984;11:494–503.PubMedGoogle Scholar
  201. 201.
    201. Sallum EA, Sallum AW, Nociti FH, Jr., Marcantonio RA, de TS. New attachment achieved by guided tissue regeneration using a bioresorbable polylactic acid mem brane in dogs. Int J Periodontics Restorative Dent. 1998;18:502–10.PubMedGoogle Scholar
  202. 202.
    202. Camelo M, Lekovic V, Weinlaender M, Nedic M, Vasilic N, Wolinsky E et al. A controlled re-entry study on the effectiveness of bovine porous bone mineral used in combination with a collagen membrane of porcine origin in the treatment of intrabony defects in humans. Journal of Clinical Periodontology. 2000;27:889–96.Google Scholar
  203. 203.
    203. Camelo M, Nevins ML, Lynch SE, Schenk RK, Simion M, Nevins M. Periodontal regeneration with an autogenous bone-Bio-Oss composite graft and a Bio-Gide membrane. Int J Periodontics Restorative Dent. 2001;21:109–19.PubMedGoogle Scholar
  204. 204.
    204. Mellonig JT. Human histologic evaluation of a bovine-derived bone xenograft in the treatment of periodontal osseous defects. Int J Periodontics Restorative Dent. 2000;20:19–29.PubMedGoogle Scholar
  205. 205.
    205. Sculean A, Stavropoulos A, Windisch P, Keglevich T, Karring T, Gera I. Healing of human intrabony defects following regenerative periodontal therapy with a bovine-derived xenograft and guided tissue regeneration. Clin Oral Investig. 2004;8:70–74.PubMedGoogle Scholar
  206. 206.
    206. Lundgren D, Slotte C. Reconstruction of anatomically complicated periodontal defects using a bioresorbable GTR barrier supported by bone mineral. A 6-month follow-up study of 6 cases. J Clin Periodontol. 1999;26:56–62.PubMedGoogle Scholar
  207. 207.
    207. Nevins ML, Camelo M, Lynch SE, Schenk RK, Nevins M. Evaluation of peri-odontal regeneration following grafting intrabony defects with bio-oss collagen: a human histologic report. Int J Periodontics Restorative Dent. 2003;23:9–17.PubMedGoogle Scholar
  208. 208.
    208. Zitzmann NU, Rateitschak-Pluss E, Marinello CP. Treatment of angular bone defects with a composite bone grafting material in combination with a collagen membrane. J Periodontol. 2003;74:687–94.PubMedGoogle Scholar
  209. 209.
    209. Pietruska MD. A comparative study on the use of Bio-Oss and enamel matrix derivative (Emdogain) in the treatment of periodontal bone defects. Eur J Oral Sci. 2001;109:178–81.PubMedGoogle Scholar
  210. 210.
    210. Sculean A, Berakdar M, Chiantella GC, Donos N, Arweiler NB, Brecx M. Healing of intrabony defects following treatment with a bovine-derived xenograft and col lagen membrane. A controlled clinical study. J Clin Periodontol. 2003;30:73–80.PubMedGoogle Scholar
  211. 211.
    211. Stavropoulos A, Karring ES, Kostopoulos L, Karring T. Deproteinized bovine bone and gentamicin as an adjunct to GTR in the treatment of intrabony defects: a randomized controlled clinical study. J Clin Periodontol. 2003;30:486–95.PubMedGoogle Scholar
  212. 212.
    212. Tonetti M, Cortellini P, Lang NP, Suvan E, Adriaens P, Dubravec D et al. Clinical outcomes following treatment of human intrabony defects with GTR/bone replacement material or access flap alone. A multicenter randomized controlled clinical trial. Journal of Clinical Periodontology. 2004;31:770–776.PubMedGoogle Scholar
  213. 213.
    213. Sculean A, Chiantella GC, Windisch P, Arweiler NB, Brecx M, Gera I. Healing of intra-bony defects following treatment with a composite bovine-derived xenograft (Bio-Oss Collagen) in combination with a collagen membrane (Bio-Gide PERIO). J Clin Periodontol. 2005;32:720–724.PubMedGoogle Scholar
  214. 214.
    214. Paolantonio M. Combined periodontal regenerative technique in human intrabony defects by collagen membranes and anorganic bovine bone. A controlled clinical study. J Periodontol. 2002;73:158–66.PubMedGoogle Scholar
  215. 215.
    215. Murphy KG, Gunsolley JC. Guided tissue regeneration for the treatment of peri-odontal intrabony and furcation defects. A systematic review. Ann Periodontol. 2003;8:266–302.PubMedGoogle Scholar
  216. 216.
    216. Paolantonio M, Scarano A, di PG, Tumini V, d'Archivio D, Piattelli A. Periodontal healing in humans using anorganic bovine bone and bovine peritoneum-derived collagen membrane: a clinical and histologic case report. Int J Periodontics Restorative Dent. 2001;21:505–15.PubMedGoogle Scholar
  217. 217.
    217. Sculean A, Windisch P, Keglevich T, Chiantella GC, Gera I, Donos N. Clinical and histologic evaluation of human intrabony defects treated with an enamel matrix protein derivative combined with a bovine-derived xenograft. Int J Periodontics Restorative Dent. 2003;23:47–55.PubMedGoogle Scholar
  218. 218.
    218. Sakata J, Abe H, Ohazama A, Okubo K, Nagashima C, Suzuki M et al. Effects of combined treatment with porous bovine inorganic bone grafts and bilayer porcine collagen membrane on refractory one-wall intrabony defects. Int J Periodontics Restorative Dent. 2006;26:161–69.PubMedGoogle Scholar
  219. 219.
    219. Yamada S, Shima N, Kitamura H, Sugito H. Effect of porous xenographic bone graft with collagen barrier membrane on periodontal regeneration. Int J Periodontics Restorative Dent. 2002;22:389–97.PubMedGoogle Scholar
  220. 220.
    220. Stavropoulos A, Karring T. Five-year results of guided tissue regeneration in com bination with deproteinized bovine bone (Bio-Oss) in the treatment of intrabony periodontal defects: a case series report. Clin Oral Investig. 2005;9:271–77.PubMedGoogle Scholar
  221. 221.
    221. Araujo MG, Carmagnola D, Berglundh T, Thilander B, Lindhe J. Orthodontic movement in bone defects augmented with Bio-Oss. An experimental study in dogs. J Clin Periodontol. 2001;28:73–80.PubMedGoogle Scholar
  222. 222.
    222. Boyne PJ, Shabahang S. An evaluation of bone induction delivery materials in conjunction with root-form implant placement. Int J Periodontics Restorative Dent. 2001;21:333–43.PubMedGoogle Scholar
  223. 223.
    223. Jiang D, Dziak R, Lynch SE, Stephan EB. Modification of an osteoconduc-tive anorganic bovine bone mineral matrix with growth factors. J Periodontol. 1999;70:834–39.PubMedGoogle Scholar
  224. 224.
    224. Terheyden H, Jepsen S, Vogeler S, Tucker M, Rueger DC. Recombinant human osteogenic protein 1 in the rat mandibular augmentation model: differences in morphology of the newly formed bone are dependent on the type of carrier. Mund Kiefer Gesichtschir. 1997;1:272–75.PubMedGoogle Scholar
  225. 225.
    225. Terheyden H, Jepsen S, Rueger DR. Mandibular reconstruction in miniature pigs with prefabricated vascularized bone grafts using recombinant human osteogenic protein-1: a preliminary study. Int J Oral Maxillofac Surg. 1999;28:461–63.PubMedGoogle Scholar
  226. 226.
    226. Lekovic V, Camargo PM, Weinlaender M, Nedic M, Aleksic Z, Kenney EB. A comparison between enamel matrix proteins used alone or in combination with bovine porous bone mineral in the treatment of intrabony periodontal defects in humans. J Periodontol. 2000;71:1110–1116.PubMedGoogle Scholar
  227. 227.
    227. Lekovic V, Camargo PM, Weinlaender M, Vasilic N, Djordjevic M, Kenney EB. The use of bovine porous bone mineral in combination with enamel matrix proteins or with an autologous fibrinogen/fibronectin system in the treatment of intrabony periodontal defects in humans. J Periodontol. 2001;72:1157–63.PubMedGoogle Scholar
  228. 228.
    228. Sigurdsson TJ, Nygaard L, Tatakis DN, Fu E, Turek TJ, Jin L et al. Periodontal repair in dogs: evaluation of rhBMP-2 carriers. Int J Periodontics Restorative Dent. 1996;16:524–37.PubMedGoogle Scholar

Copyright information

© Humana Press, a part of Springer Science+Business Media, LLC 2008

Authors and Affiliations

  • Andreas Stavropoulos
    • 1
  1. 1.Department of Periodontology and Oral Gerontology, School of DentistryUniversity of Aarhus Denmark

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