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.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10006-021-00946-y/MediaObjects/10006_2021_946_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10006-021-00946-y/MediaObjects/10006_2021_946_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10006-021-00946-y/MediaObjects/10006_2021_946_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10006-021-00946-y/MediaObjects/10006_2021_946_Fig4_HTML.png)
Similar content being viewed by others
References
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
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
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
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
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
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
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
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
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
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
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]
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
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
About this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10006-021-00946-y