Skip to main content
Log in

Sinus mucosa thinning and perforation after sinus augmentation. A histological study in rabbits

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

Abstract

Aim

To evaluate the modifications and possible perforations of the sinus mucosa lining graft particles and implant surfaces after sinus lifting.

Material and methods

Twelve New Zealand rabbits underwent a bilateral sinus lifting using either autogenous bone harvested from the tibia (AB; autogenous bone group) or deproteinized bovine bone mineral (DBBM group) as filler. Implants were simultaneously installed. Thinned sites (<40 μm) and perforations were histologically evaluated at the sinus mucosa in contact with the graft and with the implant after 7 and 40 days of healing.

Results

The mean width of the pristine mucosa was ~70–80 μm. After 7 days of healing, the sinus mucosa in contact with the graft presented fourteen thinned sites in the AB group (mean width 28.8±12.8 μm) and fifty-nine in the DBBM group (mean width 22.2±5.2 μm). No perforations of the mucosa were seen in the AB group while six perforations distributed in two sinuses were found in the DBBM group. After 40 days, only one thinned mucosa and no perforations were observed in the AB group while ninety-six thinned mucosa sites were shared by six sinuses (19.2±3.8 μm), and 3 perforations by two sinuses in the DBBM group. Few sites of the mucosa were in contact with the implant apex and threads after 7 days of healing. However, after 40 days, twelve thinned mucosa sites were seen in four sinuses in the AB groups (mean width ~19 μm) and 5 in two sinuses in the DBBM group (mean width ~20 μm). Perforations were seen in two sinuses in the AB group, and in one sinus in the DBBM group.

Conclusions

The sinus mucosa might be damaged by a close contact with graft particles and implant surface.

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

Similar content being viewed by others

References

  1. Del Fabbro M, Wallace SS, Testori T (2013) Long-term implant survival in the grafted maxillary sinus: a systematic review. Int J Periodontics Restorative Dent 33(6):773–783. https://doi.org/10.11607/prd.1288 Review

    Article  PubMed  Google Scholar 

  2. Kim J, Jang H (2019) A review of complications of maxillary sinus augmentation and available treatment methods. J Korean Assoc Oral Maxillofac Surg. 45(4):220–224. https://doi.org/10.5125/jkaoms.2019.45.4.220

    Article  PubMed  PubMed Central  Google Scholar 

  3. Stacchi C, Andolsek F, Berton F, Perinetti G, Navarra CO, Di Lenarda R (2017) Intraoperative complications during sinus floor elevation with lateral approach: a systematic review. Int J Oral Maxillofac Implants 32(3):e107–e118. https://doi.org/10.11607/jomi.4884

    Article  PubMed  Google Scholar 

  4. Testori T, Yu SH, Tavelli L, Wang HL (2020) Perforation risk assessment in maxillary sinus augmentation with lateral wall technique. Int J Periodontics Restorative Dent 40(3):373–380. https://doi.org/10.11607/prd.4179 Review

    Article  PubMed  Google Scholar 

  5. Nolan PJ, Freeman K, Kraut RA (2014 Jan) Correlation between Schneiderian membrane perforation and sinus lift graft outcome: a retrospective evaluation of 359 augmented sinus. J Oral Maxillofac Surg. 72(1):47–52. https://doi.org/10.1016/j.joms.2013.07.020

    Article  PubMed  Google Scholar 

  6. Boffano P, Forouzanfar T (2014) Current concepts on complications associated with sinus augmentation procedures. J Craniofac Surg. 25(2):e210–e212. https://doi.org/10.1097/SCS.0000000000000438

    Article  PubMed  Google Scholar 

  7. Park WB, Han JY, Kang P, Momen-Heravi F (2019) The clinical and radiographic outcomes of Schneiderian membrane perforation without repair in sinus elevation surgery. Clin Implant Dent Relat Res. 21(5):931–937. https://doi.org/10.1111/cid.12752

    Article  PubMed  Google Scholar 

  8. Doud Galli SK, Lebowitz RA, Giacchi RJ, Glickman R, Jacobs JB (2001) Chronic sinusitis complicating sinus lift surgery. Am J Rhinol. 15(3):181–186

    Article  CAS  Google Scholar 

  9. Berengo M, Sivolella S, Majzoub Z, Cordioli G (2004) Endoscopic evaluation of the bone-added osteotome sinus floor elevation procedure. Int J Oral Maxillofac Surg. 33(2):189–194. https://doi.org/10.1054/ijom.2002.0459

    Article  CAS  PubMed  Google Scholar 

  10. Nkenke E, Schlegel A, Schultze-Mosgau S, Neukam FW, Wiltfang J (2002) The endoscopically controlled osteotome sinus floor elevation: a preliminary prospective study. Int J Oral Maxillofac Implants. 17(4):557–566

    PubMed  Google Scholar 

  11. Anavi Y, Allon DM, Avishai G, Calderon S (2008) Complications of maxillary sinus augmentations in a selective series of patients. Oral Surg Oral Med Oral Patho Oral RadiolEndod 106(1):34–38. https://doi.org/10.1016/j.tripleo.2007.09.021 [CrossRef] [Google Scholar]

    Article  Google Scholar 

  12. Ragucci GM, Elnayef B, Suárez-López Del Amo F, Wang HL, Hernández-Alfaro F, Gargallo-Albiol J (2019) Influence of exposing dental implants into the sinus cavity on survival and complications rate: a systematic review. Int J Implant Dent 5(1):6. Published 2019 Feb 5. https://doi.org/10.1186/s40729-019-0157-7

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ellegaard B, Kølsen-Petersen J, Baelum V (1997) Implant therapy involving maxillary sinus lift in periodontally compromised patients. Clin Oral Implants Res. 8(4):305–315. https://doi.org/10.1034/j.1600-0501.1997.080409.x

    Article  CAS  PubMed  Google Scholar 

  14. Lundgren S, Andersson S, Gualini F, Sennerby L (2004) Bone reformation with sinus membrane elevation: a new surgical technique for maxillary sinus floor augmentation. Clin Implant Dent Relat Res. 6(3):165–173

    Article  Google Scholar 

  15. Starch-Jensen T, Schou S (2017) Maxillary sinus membrane elevation with simultaneous installation of implants without the use of a graft material: a systematic review. Implant Dent. 26(4):621–633. https://doi.org/10.1097/ID.0000000000000617

    Article  PubMed  Google Scholar 

  16. Rammelsberg P, Kilian S, Büsch C, Kappel S (2020) The effect of transcrestal sinus-floor elevation without graft on the long-term prognosis of maxillary implants. J Clin Periodontol. 47(5):640–648. https://doi.org/10.1111/jcpe.13278

    Article  PubMed  Google Scholar 

  17. De Santis E, Lang NP, Ferreira S, Rangel Garcia I Jr, Caneva M, Botticelli D (2017) Healing at implants installed concurrently to maxillary sinus floor elevation with Bio-Oss® or autologous bone grafts. A histo-morphometric study in rabbits. Clin Oral Implants Res. 28(5):503–511. https://doi.org/10.1111/clr.12825

    Article  PubMed  Google Scholar 

  18. Reiser GM, Rabinovitz Z, Bruno J, Damoulis PD, Griffin TJ (2001) Evaluation of maxillary sinus membrane response following elevation with the crestal osteotome technique in human cadavers. Int J Oral Maxillofac Implants. 16(6):833–840

    CAS  PubMed  Google Scholar 

  19. Gargallo-Albiol J, Tattan M, Sinjab KH, Chan HL, Wang HL (2019) Schneiderian membrane perforation via transcrestal sinus floor elevation: a randomized ex vivo study with endoscopic validation. Clin Oral Implants Res. 30(1):11–19. https://doi.org/10.1111/clr.13388

    Article  PubMed  Google Scholar 

  20. Scala A, Botticelli D, Faeda RS, Garcia Rangel I Jr (2012) Américo de Oliveira J, Lang NP. Lack of influence of the Schneiderian membrane in forming new bone apical to implants simultaneously installed with sinus floor elevation: an experimental study in monkeys. Clin Oral Implants Res. 23(2):175–181. https://doi.org/10.1111/j.1600-0501.2011.02227.x

    Article  PubMed  Google Scholar 

  21. 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):881–892. https://doi.org/10.11607/jomi.3472

    Article  PubMed  Google Scholar 

  22. Corbella S, Taschieri S, Weinstein R, Del Fabbro M (2016) Histomorphometric outcomes after lateral sinus floor elevation procedure: a systematic review of the literature and meta-analysis. Clin Oral Implants Res. 27(9):1106–1122. https://doi.org/10.1111/clr.12702

    Article  PubMed  Google Scholar 

  23. Coopman R, Fennis J, Ghaeminia H, Van de Vyvere G, Politis C, Hoppenreijs TJM (2020) Volumetric osseous changes in the completely edentulous maxilla after sinus grafting and lateral bone augmentation: a systematic review. Int J Oral Maxillofac Surg

  24. Asai S, Shimizu Y, Ooya K (2002) Maxillary sinus augmentation model in rabbits: effect of occluded nasal ostium on new bone formation. Clin Oral Implants Res. 13(4):405–409

    Article  Google Scholar 

  25. Xu H, Shimizu Y, Asai S, Ooya K (2004) Grafting of deproteinized bone particles inhibits bone resorption after maxillary sinus floor elevation. Clin Oral Implants Res. 15(1):126–133

    Article  Google Scholar 

  26. Caneva M, Lang NP, Garcia Rangel IJ, Ferreira S, Caneva M, De Santis E, Botticelli D (2017 Jul) Sinus mucosa elevation using Bio-Oss(®) or Gingistat(®) collagen sponge: an experimental study in rabbits. Clin Oral Implants Res. 28(7):e21–e30. https://doi.org/10.1111/clr.12850

    Article  PubMed  Google Scholar 

  27. Kawakami S, Lang NP, Iida T, Ferri M, Apaza Alccayhuaman KA, Botticelli D (2018) Influence of the position of the antrostomy in sinus floor elevation assessed with cone-beam computed tomography: a randomized clinical trial. J Investig Clin Dent. 9(4):e12362. https://doi.org/10.1111/jicd.12362

    Article  PubMed  Google Scholar 

  28. Kawakami S, Lang NP, Ferri M, Apaza Alccayhuaman KA, Botticelli D (2019) Influence of the height of the antrostomy in sinus floor elevation assessed by cone beam computed tomography- a randomized clinical trial. Int J Oral Maxillofac Implants 34(1):223–232. https://doi.org/10.11607/jomi.7112

    Article  PubMed  Google Scholar 

  29. Iida T, Carneiro Martins Neto E, Botticelli D, Apaza Alccayhuaman KA, Lang NP, Xavier SP (2017) Influence of a collagen membrane positioned subjacent the sinus mucosa following the elevation of the maxillary sinus. A histomorphometric study in rabbits. Clin Oral Implants Res 28:1567–1576

    Article  Google Scholar 

  30. Aimetti M, Massei G, Morra M, Cardesi E, Romano F (2008) Correlation between gingival phenotype and Schneiderian membrane thickness. Int J Oral Maxillofacial Implants 23(6):1128–1132

    Google Scholar 

  31. Jiam NT, Goldberg AN, Murr AH, Pletcher SD (2017) Surgical treatment of chronic rhinosinusitis after sinus lift. Am J Rhinol Allergy. 31(4):271–275

    Article  Google Scholar 

  32. Timmenga NM, Raghoebar GM, van Weissenbruch R, Vissink A (2001) Maxillary sinusitis after augmentation of the maxillary sinus floor: a report of 2 cases. J Oral Maxillofac Surg. 59(2):200–204. https://doi.org/10.1053/joms.2001.20494

    Article  CAS  PubMed  Google Scholar 

  33. Manor Y, Mardinger O, Bietlitum I, Nashef A, Nissan J, Chaushu G (2010) Late signs and symptoms of maxillary sinusitis after sinus augmentation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 110(1):e1–e4. https://doi.org/10.1016/j.tripleo.2010.02.038

    Article  PubMed  Google Scholar 

  34. Beaumont C, Zafiropoulos GG, Rohmann K, Tatakis DN (2005) Prevalence of maxillary sinus disease and abnormalities in patients scheduled for sinus lift procedures. J Periodontol. 76(3):461–467. https://doi.org/10.1902/jop.2005.76.3.461

    Article  PubMed  Google Scholar 

  35. Cricchio G, Palma VC, Faria PE, de Oliveira JA, Lundgren S, Sennerby L, Salata LA (2009) Histological findings following the use of a space-making device for bone reformation and implant integration in the maxillary sinus of primates. Clin Implant Dent Relat Res. 11(Suppl 1):e14–e22. https://doi.org/10.1111/j.1708-8208.2009.00158.x

    Article  PubMed  Google Scholar 

  36. Cricchio G, Palma VC, Faria PE, de Olivera JA, Lundgren S, Sennerby L, Salata LA (2011) Histological outcomes on the development of new space-making devices for maxillary sinus floor augmentation. Clin Implant Dent Relat Res. 13(3):224–230. https://doi.org/10.1111/j.1708-8208.2009.00208.x

    Article  PubMed  Google Scholar 

  37. Schweikert M, Botticelli D, de Oliveira JA, Scala A, Salata LA, Lang NP (2012) Use of a titanium device in lateral sinus floor elevation: an experimental study in monkeys. Clin Oral Implants Res. 23(1):100–105. https://doi.org/10.1111/j.1600-0501.2011.02200.x

    Article  PubMed  Google Scholar 

  38. Janner SF, Caversaccio MD, Dubach P, Sendi P, Buser D, Bornstein MM (2011) Characteristics and dimensions of the Schneiderian membrane: a radiographic analysis using cone beam computed tomography in patients referred for dental implant surgery in the posterior maxilla. Clin Oral Implants Res 22:1446–1453

    Article  Google Scholar 

  39. Botticelli D, Lang NP (2017) Dynamics of osseointegration in various human and animal models - a comparative analysis. Clin Oral Implants Res. 28(6):742–748. https://doi.org/10.1111/clr.12872

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The competent contributions of Mr. Sebastião Bianco (USP - Faculty of Dentistry of Ribeirão Preto - University of São Paulo, SP, Brazil) in the histological processing are highly acknowledged.

Data and materials availability

The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

Funding

This study has been funded by ARDEC Academy, Rimini, Italy. Bio-Oss® granules had been kindly provided by Geistlich Biomaterials AG, Wolhusen, LU, Switzerland, and the implants by Implalife® - industria de produtos médico-odontologicos, Jales, São Paulo, Brazil.

Author information

Authors and Affiliations

Authors

Contributions

Shingo Kato participated in the concept/design, data analysis/interpretation, article writing, and approval of article.

Daniele Botticelli participated in the concept/design, protocol writing, histological measurements, data analysis/interpretation, article writing, and approval of the article.

Enzo De Santis participated in the concept/design, surgical treatment, critical revision of the article, and approval of the article.

Masatsugu Kanayama participated in the concept/design, critical revision of the article, and approval of article.

Sabrina Ferreira participated in the concept/design, surgical treatment, critical revision of the article, and approval of article.

Idelmo Rangel-Garcia Junior participated in the concept/design, protocol writing, data analysis/interpretation, article writing, and approval of the article.

Corresponding author

Correspondence to Daniele Botticelli.

Ethics declarations

Ethics approval and consent to participate

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. This article does not contain any studies with human participants.

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kato, S., Botticelli, D., De Santis, E. et al. Sinus mucosa thinning and perforation after sinus augmentation. A histological study in rabbits. Oral Maxillofac Surg 25, 477–485 (2021). https://doi.org/10.1007/s10006-021-00946-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10006-021-00946-y

Keywords

Navigation