Clinical Oral Investigations

, Volume 21, Issue 3, pp 787–794 | Cite as

Histological and radiological evaluation of sintered and non-sintered deproteinized bovine bone substitute materials in sinus augmentation procedures. A prospective, randomized-controlled, clinical multicenter study

  • Tim Fienitz
  • Ofer Moses
  • Christoph Klemm
  • Arndt Happe
  • Daniel Ferrari
  • Matthias Kreppel
  • Zeev Ormianer
  • Moti Gal
  • Daniel RothamelEmail author
Original Article



The objective of this study is to histologically and radiologically compare a sintered and a non-sintered bovine bone substitute material in sinus augmentation procedures.

Materials and methods

Thirty-three patients were included in the clinically controlled randomized multicentre study resulting in a total of 44 treated sinuses. After lateral approach, sinuses were filled with either a sintered (SBM, Alpha Bio’s Graft®) or a non-sintered (NSBM, Bio Oss®) deproteinized bovine bone substitute material. The augmentation sites were radiologically assessed before and immediately after the augmentation procedure as well as prior to implant placement. Bone trephine biopsies for histological analysis were harvested 6 months after augmentation whilst preparing the osteotomies for implant placement.


Healing was uneventful in all patients. After 6 months, radiological evaluation of 43 sinuses revealed a residual augmentation height of 94.65 % (±2.74) for SBM and 95.76 % (±2.15) for NSBM. One patient left the study for personal reasons. Histological analysis revealed a percentage of new bone of 29.71 % (±13.67) for SBM and 30.57 % (±16.07) for NSBM. Residual bone substitute material averaged at 40.68 % (±16.32) for SBM compared to 43.43 % (±19.07) for NSBM. All differences between the groups were not statistically significant (p > 0.05, Student’s t test).


Both xenogeneic bone substitute materials showed comparable results regarding new bone formation and radiological height changes in external sinus grafting procedures.

Clinical relevance

Both bone substitute materials allow for a predictable new bone formation following sinus augmentation procedures.


Xenograft Augmentation Implantology Sinuslift Bone substitute Sintering 


Compliance with ethical standards


This study was supported by Alpha Bio, Petach Tikva, Israel.

Conflict of interest

Tim Fienitz, Christoph Klemm, Arndt Happe, Daniel Ferrari, Zeev Ormianer and Joachim E. Zoeller declare that they have no conflict of interest. Ofer Moses declares that he serves as an external consultant for Alpha Bio. Moti Gal declares that he was employed at Alpha Bio until June 2015. Daniel Rothamel declares that he has received speaker honorariums from Alpha Bio and is a consultant of Botiss Biomaterials, the manufacturer of the collagen membrane and one of the bone substitute materials that were investigated.

Ethical approval

All procedures performed in this study were in accordance with the 1964 Helsinki Declaration and its later amendments and the ethical standards of the institutional research committee of the University of Cologne and the local ethical committees of Duesseldorf and Muenster.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Ali SA, Karthigeyan S, Deivanai M, Kumar A (2014) Implant rehabilitation for atrophic maxilla: a review. J Indian Prosthodont Soc 14(3):196–207CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Barbeck M, Udeabor S, Lorenz J, Schlee M, Grosse Holthaus M, Raetscho N, Choukroun J, Sader R, Kirkpatrick CJ and Ghanaati S (2014) High-temperature sintering of xenogeneic bone substitutes leads to increased multinucleated giant cell formation: In vivo and preliminary clinical results. J Oral Implantol 41(5):e212–e222Google Scholar
  3. 3.
    Beretta M, Cicciu M, Bassi G, Rancitelli D, Poli P, Grossi GB and Maiorana C (2015) A retrospective evaluation of 192 implants placed in augmented bone: a six-year mean follow-up study. J Oral Implantol 41(6):669–674Google Scholar
  4. 4.
    Butz SJ, Huys LW (2005) Long-term success of sinus augmentation using a synthetic alloplast: a 20 patients, 7 years clinical report. Implant Dent 14(1):36–42CrossRefPubMedGoogle Scholar
  5. 5.
    Chiapasco M, Zaniboni M, Boisco M (2006) Augmentation procedures for the rehabilitation of deficient edentulous ridges with oral implants. Clin Oral Implants Res 17(Suppl 2):136–159CrossRefPubMedGoogle Scholar
  6. 6.
    Gomes KU, Carlini JL, Biron C, Rapoport A, Dedivitis RA (2008) Use of allogeneic bone graft in maxillary reconstruction for installation of dental implants. J Oral Maxillofac Surg 66(11):2335–2338CrossRefPubMedGoogle Scholar
  7. 7.
    Jensen T, Schou S, Stavropoulos A, Terheyden H, Holmstrup P (2012) Maxillary sinus floor augmentation with Bio-Oss or Bio-Oss mixed with autogenous bone as graft in animals: a systematic review. Int J Oral Maxillofac Surg 41(1):114–120CrossRefPubMedGoogle Scholar
  8. 8.
    Jung RE, Fenner N, Hammerle CH, Zitzmann NU (2013) Long-term outcome of implants placed with guided bone regeneration (GBR) using resorbable and non-resorbable membranes after 12-14 years. Clin Oral Implants Res 24(10):1065–1073CrossRefPubMedGoogle Scholar
  9. 9.
    Klein MO, Kammerer PW, Gotz H, Duschner H, Wagner W (2013) Long-term bony integration and resorption kinetics of a xenogeneic bone substitute after sinus floor augmentation: histomorphometric analyses of human biopsy specimens. Int J Periodontics Restorative Dent 33(4):e101–e110CrossRefPubMedGoogle Scholar
  10. 10.
    McAllister BS, Haghighat K (2007) Bone augmentation techniques. J Periodontol 78(3):377–396CrossRefPubMedGoogle Scholar
  11. 11.
    Moses O, Nemcovsky CE, Langer Y, Tal H (2007) Severely resorbed mandible treated with iliac crest autogenous bone graft and dental implants: 17-year follow-up. Int J Oral Maxillofac Implants 22(6):1017–1021PubMedGoogle Scholar
  12. 12.
    Murugan R, Panduranga Rao K, Sampath Kumar TS (2003) Heat-deproteinated xenogeneic bone from slaughterhouse waste: physico-chemical properties. Bull Mater Sci 26(5):523–528Google Scholar
  13. 13.
    Nedir R, Nurdin N, Khoury P and Bischof M (2015) Short Implants Placed with or without Grafting in Atrophic Sinuses: The 3-Year Results of a Prospective Randomized Controlled Study. Clin Implant Dent Relat Res 18(1):10–18Google Scholar
  14. 14.
    Nkenke E, Radespiel-Troger M, Wiltfang J, Schultze-Mosgau S, Winkler G, Neukam FW (2002) Morbidity of harvesting of retromolar bone grafts: a prospective study. Clin Oral Implants Res 13(5):514–521CrossRefPubMedGoogle Scholar
  15. 15.
    Nkenke E, Schultze-Mosgau S, Radespiel-Troger M, Kloss F, Neukam FW (2001) Morbidity of harvesting of chin grafts: a prospective study. Clin Oral Implants Res 12(5):495–502CrossRefPubMedGoogle Scholar
  16. 16.
    Panagiotou D, Ozkan Karaca E, Dirikan Ipci S, Cakar G, Olgac V and Yilmaz S (2015) “Comparison of two different xenografts in bilateral sinus augmentation: Radiographic and histologic findings.” Quintessence Int 46(7):611–619Google Scholar
  17. 17.
    Pinchasov G, Juodzbalys G (2014) Graft-free sinus augmentation procedure: a literature review. J Oral Maxillofac Res 5(1):e1CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Raghoebar GM, Batenburg RH, Vissink A, Reintsema H (1996) Augmentation of localized defects of the anterior maxillary ridge with autogenous bone before insertion of implants. J Oral Maxillofac Surg 54(10):1180–1185, discussion 1185-1186CrossRefPubMedGoogle Scholar
  19. 19.
    Riachi F, Naaman N, Tabarani C, Aboelsaad N, Aboushelib MN, Berberi A, Salameh Z (2012) Influence of material properties on rate of resorption of two bone graft materials after sinus lift using radiographic assessment. Int J Dent 2012:737262CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Shanbhag S, Shanbhag V, Stavropoulos A (2014) Volume changes of maxillary sinus augmentations over time: a systematic review. Int J Oral Maxillofac Implants 29(4):881–892CrossRefPubMedGoogle Scholar
  21. 21.
    Smiler DG, Johnson PW, Lozada JL, Misch C, Rosenlicht JL, Tatum OH Jr, Wagner JR (1992) Sinus lift grafts and endosseous implants. Treatment of the atrophic posterior maxilla. Dent Clin North Am 36(1):151–186, discussion 187-158PubMedGoogle Scholar
  22. 22.
    Tatum OH Jr, Lebowitz MS, Tatum CA, Borgner RA (1993) Sinus augmentation. Rationale, development, long-term results. N Y State Dent J 59(5):43–48PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Tim Fienitz
    • 1
  • Ofer Moses
    • 2
  • Christoph Klemm
    • 1
  • Arndt Happe
    • 3
  • Daniel Ferrari
    • 4
  • Matthias Kreppel
    • 1
  • Zeev Ormianer
    • 5
  • Moti Gal
    • 6
  • Daniel Rothamel
    • 1
    Email author
  1. 1.Department of Craniomaxillofacial and Plastic SurgeryUniversity Hospital of CologneCologneGermany
  2. 2.Department of Periodontology and Dental ImplantologyTel-Aviv UniversityTel AvivIsrael
  3. 3.Private PracticeMuensterGermany
  4. 4.Private PracticeDuesseldorfGermany
  5. 5.Department of Oral Rehabilitation, School of Dental MedicineTel Aviv UniversityTel AvivIsrael
  6. 6.Faculty of Life SciencesBar Ilan University Ramat GanRamat GanIsrael

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