Skip to main content

Advertisement

Log in

Sinus Augmentation Using Mineralized Bone Allografts: A 6-Month Histological and Histomorphometric Analysis

  • Original Article
  • Published:
Journal of Maxillofacial and Oral Surgery Aims and scope Submit manuscript

A Correction to this article was published on 01 April 2024

This article has been updated

Abstract

Purpose

The aim of this study was to evaluate, after a six-month healing period, the histological and histomorphometric results of mineralized bone allograft used in lateral sinus augmentation procedures.

Materials and Methods

Twenty-one pneumatized maxillary sinuses with residual bone height ≤ 4 mm were grafted with a mixture of 1/1 cortical and cancellous mineralized bone allograft using lateral sinus floor elevation. Six months later, during implant placement, a core biopsy was retrieved for histological and histomorphometric evaluation.

Results

Biopsies showed mature cancellous bone with no signs of acute or chronic inflammatory reactions. Higher magnification revealed new lamellar bone, active osteocytes and normal lamellar arrangement around Haversian canals interspersed with osteocytes in lacunae. At grafted bone periphery, a high concentration of osteoblastic/osteoclastic couple was noted, indicating active bone remodeling. Histomorphometric evaluation revealed an average vital bone content of 30.32% (25.00–44.00%), and a percentage of residual non-vital bone of 18.06% (14.05–25.00%).

Conclusions

Histological and histomorphometric evaluation indicated that the mixture of 1 to 1 cortical and cancellous mineralized bone allograft promoted de-novo bone formation and can be predictably used for sinus augmentation procedures.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14
Fig. 15
Fig. 16
Fig. 17
Fig. 18

Similar content being viewed by others

Change history

References

  1. Seong W-J, Barczak M, Jung J, Basu S, Olin PS, Conrad HJ (2013) Prevalence of sinus augmentation associated with maxillary posterior implants. J Oral Implantol 39(6):680–688

    Article  PubMed  Google Scholar 

  2. Misch CE, Judy KW (1987) Classification of partially edentulous arches for implant dentistry. Int J Oral Implantol Implantol 4(2):7–13

    CAS  Google Scholar 

  3. Parr GR (1985) Tissue-integrated prostheses: Osseointegration in clinical dentistry: Per-Ingvar Branemark, MD, Ph. D., George A. Zarb, DSS, MS, FRCD (C), and Thomas Albrektsson, MD, Ph. D. Chicago, 1985, Quintessence Publishing Company

  4. Boyne PJ, James RA (1980) Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg Am Dent Assoc 1965 38(8):613–616

    CAS  Google Scholar 

  5. Tatum H Jr (1986) Maxillary and sinus implant reconstructions. Dent Clin North Am 30(2):207–229

    Article  PubMed  Google Scholar 

  6. Del Fabbro M, Testori T, Francetti L, Weinstein R (2005) Systematic review of survival rates for implants placed in the grafted maxillary sinus. J Prosthet Dent 94(3):266

    Article  Google Scholar 

  7. Pjetursson BE, Tan WC, Zwahlen M, Lang NP (2008) A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontol 35(s8):216–240

    Article  PubMed  Google Scholar 

  8. Summers RB (1994) The osteotome technique: part 3–Less invasive methods of elevating the sinus floor. Compend Newtown Pa 15(6):702–704 (passim; quiz 710)

    Google Scholar 

  9. Del Fabbro M, Rosano G, Taschieri S (2008) Implant survival rates after maxillary sinus augmentation. Eur J Oral Sci 116(6):497–506

    Article  PubMed  Google Scholar 

  10. Chao Y-L, Chen H-H, Mei C-C, Tu Y-K, Lu H-K (2010) Meta-regression analysis of the initial bone height for predicting implant survival rates of two sinus elevation procedures. J Clin Periodontol 37(5):456–465

    Article  PubMed  Google Scholar 

  11. Wallace SS, Froum SJ (2003) Effect of maxillary sinus augmentation on the survival of endosseous dental implants. A systematic review. Ann Periodontol Am Acad Periodontol 8(1):328–343

    Article  Google Scholar 

  12. Wang W, Yeung KWK (2017) Bone grafts and biomaterials substitutes for bone defect repair: a review. Bioact Mater 2(4):224–247

    PubMed  PubMed Central  Google Scholar 

  13. Nedir R, Nurdin N, Szmukler-Moncler S, Bischof M (2009) Osteotome sinus floor elevation technique without grafting material and immediate implant placement in atrophic posterior maxilla: report of 2 cases. J Oral Maxillofac Surg Off J Am Assoc Oral Maxillofac Surg 67(5):1098–1103

    Article  Google Scholar 

  14. Nkenke E, Radespiel-Tröger 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):514–521

    Article  PubMed  Google Scholar 

  15. Nkenke E, Schultze-Mosgau S, Radespiel-Tröger M, Kloss F, Neukam FW (2001) Morbidity of harvesting of chin grafts: a prospective study. Clin Oral Implants Res 12(5):495–502

    Article  CAS  PubMed  Google Scholar 

  16. Galindo-Moreno P, Avila G, Fernández-Barbero JE, Aguilar M, Sánchez-Fernández E, Cutando A et al (2007) Evaluation of sinus floor elevation using a composite bone graft mixture. Clin Oral Implants Res 18(3):376–382

    Article  PubMed  Google Scholar 

  17. Klijn RJ, van den Beucken JJJP, Bronkhorst EM, Berge SJ, Meijer GJ, Jansen JA (2012) Predictive value of ridge dimensions on autologous bone graft resorption in staged maxillary sinus augmentation surgery using cone-beam CT. Clin Oral Implants Res 23(4):409–415

    Article  CAS  PubMed  Google Scholar 

  18. Nkenke E, Stelzle F (2009) Clinical outcomes of sinus floor augmentation for implant placement using autogenous bone or bone substitutes: a systematic review. Clin Oral Implants Res 20(Suppl 4):124–133

    Article  PubMed  Google Scholar 

  19. Del Fabbro M, Testori T, Francetti L, Weinstein R (2004) Systematic review of survival rates for implants placed in the grafted maxillary sinus. Int J Periodontics Restorative Dent 24(6):565–577

    PubMed  Google Scholar 

  20. Klijn RJ, Meijer GJ, Bronkhorst EM, Jansen JA (2010) A meta-analysis of histomorphometric results and graft healing time of various biomaterials compared to autologous bone used as sinus floor augmentation material in humans. Tissue Eng Part B Rev 16(5):493–507

    Article  CAS  PubMed  Google Scholar 

  21. Klijn RJ, Meijer GJ, Bronkhorst EM, Jansen JA (2010) Sinus floor augmentation surgery using autologous bone grafts from various donor sites: a meta-analysis of the total bone volume. Tissue Eng Part B Rev 16(3):295–303

    Article  PubMed  Google Scholar 

  22. Schlegel KA, Fichtner G, Schultze-Mosgau S, Wiltfang J (2003) Histologic findings in sinus augmentation with autogenous bone chips versus a bovine bone substitute. Int J Oral Maxillofac Implants 18(1):53–58

    PubMed  Google Scholar 

  23. Wheeler SL, Holmes RE, Calhoun CJ (1996) Six-year clinical and histologic study of sinus-lift grafts. Int J Oral Maxillofac Implants 11(1):26–34

    CAS  PubMed  Google Scholar 

  24. Carson JS, Bostrom MPG (2007) Synthetic bone scaffolds and fracture repair. Injury 38(Suppl 1):S33-37

    Article  PubMed  Google Scholar 

  25. Donath K, Breuner G (1982) A method for the study of undecalcified bones and teeth with attached soft tissues. The Säge-Schliff (sawing and grinding) technique. J Oral Pathol 11(4):318–326

    Article  CAS  PubMed  Google Scholar 

  26. Egan KP, Brennan TA, Pignolo RJ (2012) Bone histomorphometry using free and commonly available software. Histopathology 61(6):1168–1173

    Article  PubMed  PubMed Central  Google Scholar 

  27. Younes R, Nader N, Khoury G (2015) Sinus grafting techniques: a step-by-step guide. Springer, Cham

    Book  Google Scholar 

  28. Aghaloo TL, Moy PK (2007) Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants 22(Suppl):49–70

    PubMed  Google Scholar 

  29. Del Fabbro M, Wallace SS, Testori T (2013) Long-term implant survival in the grafted maxillary sinus: a systematic review. Int J Periodontics Restor Dent 33(6):773–783

    Article  Google Scholar 

  30. Esposito M, Grusovin MG, Rees J, Karasoulos D, Felice P, Alissa R et al (2010) Interventions for replacing missing teeth: augmentation procedures of the maxillary sinus. Cochrane Database Syst Rev (3):CD008397

  31. Graziani F, Donos N, Needleman I, Gabriele M, Tonetti M (2004) Comparison of implant survival following sinus floor augmentation procedures with implants placed in pristine posterior maxillary bone: a systematic review. Clin Oral Implants Res 15(6):677–682

    Article  PubMed  Google Scholar 

  32. Jensen SS, Terheyden H (2009) 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 24(Suppl):218–236

    PubMed  Google Scholar 

  33. Pjetursson BE, Tan WC, Zwahlen M, Lang NP (2008) A systematic review of the success of sinus floor elevation and survival of implants inserted in combination with sinus floor elevation. J Clin Periodontol 35(8 Suppl):216–240

    Article  PubMed  Google Scholar 

  34. Sehn FP, Dias RR, de Santana ST, Silva ER, Salata LA, Chaushu G et al (2015) Fresh-frozen allografts combined with bovine bone mineral enhance bone formation in sinus augmentation. J Biomater Appl 29(7):1003–1013

    Article  PubMed  Google Scholar 

  35. Xavier SP, Dias RR, Sehn FP, Kahn A, Chaushu L, Chaushu G (2015) Maxillary sinus grafting with autograft vs. fresh frozen allograft: a split-mouth histomorphometric study. Clin Oral Implants Res 26(9):1080–1085

    Article  PubMed  Google Scholar 

  36. Froum SJ, Wallace SS, Elian N, Cho SC, Tarnow DP (2006) Comparison of mineralized cancellous bone allograft (Puros) and anorganic bovine bone matrix (Bio-Oss) for sinus augmentation: histomorphometry at 26 to 32 weeks after grafting. Int J Periodontics Restor Dent 26(6):543–551

    Google Scholar 

  37. Stacchi C, Orsini G, Di Iorio D, Breschi L, Di Lenarda R (2008) Clinical, histologic, and histomorphometric analyses of regenerated bone in maxillary sinus augmentation using fresh frozen human bone allografts. J Periodontol 79(9):1789–1796

    Article  PubMed  Google Scholar 

  38. Acocella A, Bertolai R, Nissan J, Sacco R (2011) Clinical, histological and histomorphometrical study of maxillary sinus augmentation using cortico-cancellous fresh frozen bone chips. J Cranio-Maxillofac Surg 39(3):192–199

    Article  Google Scholar 

  39. Xavier SP, de Santos TS, Sehn FP, Silva ER, de Garcez-Filho JA, Martins-Filho PRS (2016) Maxillary sinus grafting with fresh frozen allograft versus bovine bone mineral: a tomographic and histological study. J Cranio-Maxillo-fac Surg Off Publ Eur Assoc Cranio-Maxillo-fac Surg 44(6):708–714

    Article  Google Scholar 

  40. Contar CMM, Sarot JR, da Costa MB, Bordini J, de Lima AAS, Alanis LRA et al (2011) Fresh-frozen bone allografts in maxillary ridge augmentation: histologic analysis. J Oral Implantol 37(2):223–231

    Article  PubMed  Google Scholar 

  41. Pazzaglia UE, Zarattini G, Giacomini D, Rodella L, Menti AM, Feltrin G (2010) Morphometric analysis of the canal system of cortical bone: an experimental study in the rabbit femur carried out with standard histology and micro-CT. Anat Histol Embryol 39(1):17–26

    Article  CAS  PubMed  Google Scholar 

  42. Chiapasco M, Giammattei M, Carmagnola D, Autelitano L, Rabbiosi D, Dellavia C (2013) Iliac crest fresh-frozen allografts and autografts in maxillary and mandibular reconstruction: a histologic and histomorphometric evaluation. Minerva Stomatol 62(1–2):3–16

    CAS  PubMed  Google Scholar 

  43. Spin-Neto R, Landazuri Del Barrio RA, Pereira LAVD, Marcantonio RAC, Marcantonio E, Marcantonio E (2013) Clinical similarities and histological diversity comparing fresh frozen onlay bone blocks allografts and autografts in human maxillary reconstruction. Clin Implant Dent Relat Res 15(4):490–497

    Article  PubMed  Google Scholar 

  44. Stacchi C, Berton F, Fiorillo L, Nicolin V, Lombardi T, Cicciù M et al (2019) Fresh frozen allogeneic bone block in maxillary sinus floor elevation: histomorphometric analysis of a bone specimen retrieved 15 years after grafting procedure. Appl Sci 9(6):1119

    Article  Google Scholar 

  45. Noumbissi SS, Lozada JL, Boyne PJ, Rohrer MD, Clem D, Kim JS et al (2005) Clinical, histologic, and histomorphometric evaluation of mineralized solvent-dehydrated bone allograf (Puros) in human maxillary sinus grafts. J Oral Implantol 31(4):171–179

    Article  PubMed  Google Scholar 

  46. Schmitt CM, Doering H, Schmidt T, Lutz R, Neukam FW, Schlegel KA (2013) Histological results after maxillary sinus augmentation with Straumann® BoneCeramic, Bio-Oss®, Puros®, and autologous bone. A randomized controlled clinical trial. Clin Oral Implants Res 24(5):576–585

    Article  PubMed  Google Scholar 

  47. Berberi A, Nader N (2016) Subantral augmentation with mineralized cortical bone allograft material: clinical, histological, and histomorphometric analyses and graft volume assessments. Implant Dent 25(3):353–360

    Article  PubMed  Google Scholar 

  48. Danesh-Sani SA, Engebretson SP, Janal MN (2017) Histomorphometric results of different grafting materials and effect of healing time on bone maturation after sinus floor augmentation: a systematic review and meta-analysis. J Periodontal Res 52(3):301–312

    Article  CAS  PubMed  Google Scholar 

  49. Landi L, Pretel RW, Hakimi NM, Setayesh R (2000) Maxillary sinus floor elevation using a combination of DFDBA and bovine-derived porous hydroxyapatite: a preliminary histologic and histomorphometric report. Int J Periodontics Restor Dent 20(6):574–583

    CAS  Google Scholar 

  50. Yildirim M, Spiekermann H, Biesterfeld S, Edelhoff D (2000) Maxillary sinus augmentation using xenogenic bone substitute material Bio-Oss in combination with venous blood. A histologic and histomorphometric study in humans. Clin Oral Implants Res 11(3):217–229

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pierre Lahoud.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised as the author names were incorrectly written.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lahoud, P., Nader, N. & Younes, R. Sinus Augmentation Using Mineralized Bone Allografts: A 6-Month Histological and Histomorphometric Analysis. J. Maxillofac. Oral Surg. 21, 1180–1190 (2022). https://doi.org/10.1007/s12663-022-01728-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12663-022-01728-z

Keywords

Navigation