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Published in: Oral and Maxillofacial Surgery 4/2020

01-12-2020 | Original Article

Sequential healing of the elevated sinus floor with different size of antrostomy: a histomorphometric study in rabbits

Authors: Alessandro Scala, Jose Viña-Almunia, Carmen Carda, José Javier Martín de Llano, David Soto-Peñaloza, Maria Peñarrocha-Diago, Miguel Peñarrocha-Diago, Daniele Botticelli

Published in: Oral and Maxillofacial Surgery | Issue 4/2020

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Abstract

Purpose

To study the influence of the access window dimensions on the healing at the antrostomy and within the augmented maxillary sinus.

Material and methods

A maxillary sinus augmentation was performed in twenty-four albino New Zealand rabbits. Antrostomies of 3 × 6 mm (small) or 5 × 6 mm (large) in dimensions were randomly prepared in each animal. A collagenated cortico-cancellous porcine bone was used to fill the elevated region, and an equine collagen membrane was placed on the antrostomies. Three different groups were formed, based on the time of euthanasia, i.e., 2, 4, and 8 weeks from surgery.

Results

No relevant changes of the height of the augmented sinus were detected over time. Mineralized bone increased between 2 and 4 weeks of healing while remained stable between 4 and 8 weeks. The highest amounts of new bone were found close to the sinus bone walls. No antrostomies were found healed with an even layer of corticalized bone, while large amounts of connective tissue were occupying the antrostomy in both groups.

Conclusion

Antrostomies of different dimensions resulted in similar outcome in bone formation both in the antrostomy regions and within the elevated sinus.
Literature
1.
go back to reference 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):216–240CrossRefPubMed 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):216–240CrossRefPubMed
2.
go back to reference 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 33:773–783CrossRefPubMed 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 33:773–783CrossRefPubMed
3.
go back to reference Corbella S, Taschieri S, Del Fabbro M (2015) Long-term outcomes for the treatment of atrophic posterior maxilla: a systematic review of literature. Clin Implant Dent Relat Res 17:120–132CrossRefPubMed Corbella S, Taschieri S, Del Fabbro M (2015) Long-term outcomes for the treatment of atrophic posterior maxilla: a systematic review of literature. Clin Implant Dent Relat Res 17:120–132CrossRefPubMed
4.
go back to reference Starch-Jensen T, Aludden H, Hallman M, Dahlin C, Christensen AE, Mordenfeld A (2018) A systematic review and meta-analysis of long-term studies (five or more years) assessing maxillary sinus floor augmentation. Int J Oral Maxillofac Surg 47:103–116CrossRefPubMed Starch-Jensen T, Aludden H, Hallman M, Dahlin C, Christensen AE, Mordenfeld A (2018) A systematic review and meta-analysis of long-term studies (five or more years) assessing maxillary sinus floor augmentation. Int J Oral Maxillofac Surg 47:103–116CrossRefPubMed
5.
go back to reference Starch-Jensen T, Mordenfeld A, Becktor JP, Jensen SS (2018) Maxillary sinus floor augmentation with synthetic bone substitutes compared with other grafting materials: a systematic review and meta-analysis. Implant Dent 27:363–374CrossRefPubMed Starch-Jensen T, Mordenfeld A, Becktor JP, Jensen SS (2018) Maxillary sinus floor augmentation with synthetic bone substitutes compared with other grafting materials: a systematic review and meta-analysis. Implant Dent 27:363–374CrossRefPubMed
6.
go back to reference Sbordone C, Toti P, Guidetti F, Califano L, Bufo P, Sbordone L (2013) Volume changes of autogenous bone after sinus lifting and grafting procedures: a 6-year computerized tomographic follow-up. J Craniomaxillofac Surg 41:235–241CrossRefPubMed Sbordone C, Toti P, Guidetti F, Califano L, Bufo P, Sbordone L (2013) Volume changes of autogenous bone after sinus lifting and grafting procedures: a 6-year computerized tomographic follow-up. J Craniomaxillofac Surg 41:235–241CrossRefPubMed
7.
go back to reference 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:e12362CrossRefPubMed 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:e12362CrossRefPubMed
8.
go back to reference 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 34:223–232CrossRefPubMed 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 34:223–232CrossRefPubMed
9.
go back to reference Barone A, Ricci M, Covani U, Nannmark U, Azarmehr I, Calvo-Guirado JL (2012) Maxillary sinus augmentation using prehydrated corticocancellous porcine bone: hystomorphometric evaluation after 6 months. Clin Implant Dent Relat Res 14:373–379CrossRefPubMed Barone A, Ricci M, Covani U, Nannmark U, Azarmehr I, Calvo-Guirado JL (2012) Maxillary sinus augmentation using prehydrated corticocancellous porcine bone: hystomorphometric evaluation after 6 months. Clin Implant Dent Relat Res 14:373–379CrossRefPubMed
10.
go back to reference 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 24:576–585CrossRefPubMed 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 24:576–585CrossRefPubMed
11.
go back to reference Tosta M, Cortes AR, Corrêa L, Pinto Ddos S Jr, Tumenas I, Katchburian E (2013) Histologic and histomorphometric evaluation of a synthetic bone substitute for maxillary sinus grafting in humans. Clin Oral Implants Res 24:866–870CrossRefPubMed Tosta M, Cortes AR, Corrêa L, Pinto Ddos S Jr, Tumenas I, Katchburian E (2013) Histologic and histomorphometric evaluation of a synthetic bone substitute for maxillary sinus grafting in humans. Clin Oral Implants Res 24:866–870CrossRefPubMed
12.
go back to reference 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 13:405–409CrossRefPubMed 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 13:405–409CrossRefPubMed
13.
go back to reference Xu H, Shimizu Y, Asai S, Ooya K (2003) Experimental sinus grafting with the use of deproteinized bone particles of different sizes. Clin Oral Implants Res 14:548–555CrossRefPubMed Xu H, Shimizu Y, Asai S, Ooya K (2003) Experimental sinus grafting with the use of deproteinized bone particles of different sizes. Clin Oral Implants Res 14:548–555CrossRefPubMed
14.
go back to reference 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 15:126–133CrossRefPubMed 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 15:126–133CrossRefPubMed
15.
go back to reference Moon YS, Sohn DS, Moon JW, Lee JH, Park IS, Lee JK (2014) Comparative histomorphometric analysis of maxillary sinus augmentation with absorbable collagen membrane and osteoinductive replaceable bony window in rabbits. Implant Dent 23:29–36CrossRefPubMed Moon YS, Sohn DS, Moon JW, Lee JH, Park IS, Lee JK (2014) Comparative histomorphometric analysis of maxillary sinus augmentation with absorbable collagen membrane and osteoinductive replaceable bony window in rabbits. Implant Dent 23:29–36CrossRefPubMed
16.
go back to reference 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 28:1567–1576CrossRefPubMed 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 28:1567–1576CrossRefPubMed
17.
go back to reference Omori Y, Ricardo Silva E, Botticelli D, Apaza Alccayhuaman KA, Lang NP, Xavier SP (2018) Reposition of the bone plate over the antrostomy in maxillary sinus augmentation: a histomorphometric study in rabbits. Clin Oral Implants Res 29:821–834CrossRefPubMed Omori Y, Ricardo Silva E, Botticelli D, Apaza Alccayhuaman KA, Lang NP, Xavier SP (2018) Reposition of the bone plate over the antrostomy in maxillary sinus augmentation: a histomorphometric study in rabbits. Clin Oral Implants Res 29:821–834CrossRefPubMed
18.
go back to reference Masuda K, Silva ER, Botticelli D, Apaza Alccayhuaman KA, Xavier SP (2019) Antrostomy preparation for maxillary sinus floor augmentation using drills or a sonic instrument: a microcomputed tomography and histomorphometric study in rabbits. Int J Oral Maxillofac Implants 34:819–827CrossRefPubMed Masuda K, Silva ER, Botticelli D, Apaza Alccayhuaman KA, Xavier SP (2019) Antrostomy preparation for maxillary sinus floor augmentation using drills or a sonic instrument: a microcomputed tomography and histomorphometric study in rabbits. Int J Oral Maxillofac Implants 34:819–827CrossRefPubMed
19.
go back to reference Hong JY, Kim MS, Lim HC, Lee JS, Choi SH, Jung UW (2016) A high concentration ofrecombinant human bone morphogenetic protein-2 induces low-efficacy bone regeneration in sinus augmentation: a histomorphometric analysis in rabbits. Clin Oral Implants Res 27:e199–e205CrossRefPubMed Hong JY, Kim MS, Lim HC, Lee JS, Choi SH, Jung UW (2016) A high concentration ofrecombinant human bone morphogenetic protein-2 induces low-efficacy bone regeneration in sinus augmentation: a histomorphometric analysis in rabbits. Clin Oral Implants Res 27:e199–e205CrossRefPubMed
20.
go back to reference Yoon SR, Cha JK, Lim HC, Lee JS, Choi SH, Jung UW (2017) De novo bone formation underneath the sinus membrane supported by a bone patch: a pilot experiment in rabbit sinus model. Clin Oral Implants Res 28:1175–1181CrossRefPubMed Yoon SR, Cha JK, Lim HC, Lee JS, Choi SH, Jung UW (2017) De novo bone formation underneath the sinus membrane supported by a bone patch: a pilot experiment in rabbit sinus model. Clin Oral Implants Res 28:1175–1181CrossRefPubMed
21.
go back to reference Iida T, Silva ER, Lang NP, Apaza Alccayhuaman KA, Botticelli D, Xavier SP (2018) Histological and micro-computed tomography evaluations of newly formed bone after maxillary sinus augmentation using a xenograft with similar density and mineral content of bone: an experimental study in rabbits. Clin Exp Dent Res 4:284–290CrossRefPubMedPubMedCentral Iida T, Silva ER, Lang NP, Apaza Alccayhuaman KA, Botticelli D, Xavier SP (2018) Histological and micro-computed tomography evaluations of newly formed bone after maxillary sinus augmentation using a xenograft with similar density and mineral content of bone: an experimental study in rabbits. Clin Exp Dent Res 4:284–290CrossRefPubMedPubMedCentral
22.
go back to reference Baldini N, D'Elia C, Bianco A, Goracci C, de Sanctis M, Ferrari M (2017) Lateral approach for sinus floor elevation: large versus small bone window – a split-mouth randomized clinical trial. Clin Oral Implants Res 28:974–981CrossRefPubMed Baldini N, D'Elia C, Bianco A, Goracci C, de Sanctis M, Ferrari M (2017) Lateral approach for sinus floor elevation: large versus small bone window – a split-mouth randomized clinical trial. Clin Oral Implants Res 28:974–981CrossRefPubMed
23.
go back to reference Lu W, Xu J, Wang HM, He FM (2018) Influence of lateral windows with decreased vertical height following maxillary sinus floor augmentation: a 1-year clinical and radiographic study. Int J Oral Maxillofac Implants 33:661–670CrossRefPubMed Lu W, Xu J, Wang HM, He FM (2018) Influence of lateral windows with decreased vertical height following maxillary sinus floor augmentation: a 1-year clinical and radiographic study. Int J Oral Maxillofac Implants 33:661–670CrossRefPubMed
24.
go back to reference Scala A, Botticelli D, Faeda RS, Garcia Rangel I Jr, Américo de Oliveira J, Lang NP (2012) 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 23:175–181CrossRefPubMed Scala A, Botticelli D, Faeda RS, Garcia Rangel I Jr, Américo de Oliveira J, Lang NP (2012) 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 23:175–181CrossRefPubMed
25.
go back to reference Scala A, Lang NP, de Carvalho Cardoso L, Pantani F, Schweikert M, Botticelli D (2015) Sequential healing of the elevated sinus floor after applying autologous bone grafting: an experimental study in minipigs. Clin Oral Implants Res 26:419–425CrossRefPubMed Scala A, Lang NP, de Carvalho Cardoso L, Pantani F, Schweikert M, Botticelli D (2015) Sequential healing of the elevated sinus floor after applying autologous bone grafting: an experimental study in minipigs. Clin Oral Implants Res 26:419–425CrossRefPubMed
26.
go back to reference Scala A, Lang NP, Velez JU, Favero R, Bengazi F, Botticelli D (2016) Effects of a collagen membrane positioned between augmentation material and the sinus mucosa in the elevation of the maxillary sinus floor. An experimental study in sheep. Clin Oral Implants Res 27:1454–1461CrossRefPubMed Scala A, Lang NP, Velez JU, Favero R, Bengazi F, Botticelli D (2016) Effects of a collagen membrane positioned between augmentation material and the sinus mucosa in the elevation of the maxillary sinus floor. An experimental study in sheep. Clin Oral Implants Res 27:1454–1461CrossRefPubMed
27.
go back to reference Favero V, Lang NP, Canullo L, Urbizo Velez J, Bengazi F, Botticelli D (2016) Sinus floor elevation outcomes following perforation of the Schneiderian membrane. An experimental study in sheep. Clin Oral Implants Res 27:233–240CrossRefPubMed Favero V, Lang NP, Canullo L, Urbizo Velez J, Bengazi F, Botticelli D (2016) Sinus floor elevation outcomes following perforation of the Schneiderian membrane. An experimental study in sheep. Clin Oral Implants Res 27:233–240CrossRefPubMed
28.
go back to reference Gruber R, Kandler B, Fuerst G, Fischer MB, Watzek G (2004) Porcine sinus mucosa holds cells that respond to bone morphogenetic protein (BMP)-6 and BMP-7 with increased osteogenic differentiation in vitro. Clin Oral Implants Res 15:575–580CrossRefPubMed Gruber R, Kandler B, Fuerst G, Fischer MB, Watzek G (2004) Porcine sinus mucosa holds cells that respond to bone morphogenetic protein (BMP)-6 and BMP-7 with increased osteogenic differentiation in vitro. Clin Oral Implants Res 15:575–580CrossRefPubMed
29.
go back to reference Srouji S, Kizhner T, Ben David D, Riminucci M, Bianco P, Livne E (2009) The Schneiderian membrane contains osteoprogenitor cells: in vivo and in vitro study. Calcif Tissue Int 84:138–145CrossRefPubMed Srouji S, Kizhner T, Ben David D, Riminucci M, Bianco P, Livne E (2009) The Schneiderian membrane contains osteoprogenitor cells: in vivo and in vitro study. Calcif Tissue Int 84:138–145CrossRefPubMed
30.
go back to reference Srouji S, Ben-David D, Funari A, Riminucci M, Bianco P (2013) Evaluation of the osteoconductive potential of bone substitutes embedded with Schneiderian membrane- or maxillary bone marrow-derived osteoprogenitor cells. Clin Oral Implants Res 24:1288–1294CrossRefPubMed Srouji S, Ben-David D, Funari A, Riminucci M, Bianco P (2013) Evaluation of the osteoconductive potential of bone substitutes embedded with Schneiderian membrane- or maxillary bone marrow-derived osteoprogenitor cells. Clin Oral Implants Res 24:1288–1294CrossRefPubMed
Metadata
Title
Sequential healing of the elevated sinus floor with different size of antrostomy: a histomorphometric study in rabbits
Authors
Alessandro Scala
Jose Viña-Almunia
Carmen Carda
José Javier Martín de Llano
David Soto-Peñaloza
Maria Peñarrocha-Diago
Miguel Peñarrocha-Diago
Daniele Botticelli
Publication date
01-12-2020
Publisher
Springer Berlin Heidelberg
Published in
Oral and Maxillofacial Surgery / Issue 4/2020
Print ISSN: 1865-1550
Electronic ISSN: 1865-1569
DOI
https://doi.org/10.1007/s10006-020-00859-2

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