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Histomorphometric evaluation of different graft associations for maxillary sinus elevation in wide antral cavities: a randomized controlled clinical trial

Clinical Oral Investigations volume 26, pages 1–9 (2022)Cite this article

Abstract

Objectives

Pneumatization of the maxillary sinus can make it difficult, if not impossible, to install osseointegrated implants, and undertake their eventual functional rehabilitation, which may ultimately require regenerative techniques to achieve. This randomized controlled study proposed conducting a histological evaluation of the behavior of different graft materials in wide maxillary sinuses, at a height of 8 to 10 mm from the alveolar ridge, combined with bone remnants less than 3mm.

Materials and methods

Thirty-six patients underwent a sinus elevation procedure through the lateral window. The sinuses were randomly filled with the following materials (n=12/group): group 1, xenogenic bone + autogenous bone (ratio 70:30, respectively); group 2, xenogenic bone + L-PRF; and group 3, xenogenic bone. At 8 months, bone biopsies of engrafted sites were harvested and analyzed histomorphometrically in order to quantify newly formed bone tissue.

Results

The results showed a greater area of newly formed bone for G1, averaging 2678.37 (1116.40) μm2, compared with G2 at 984.87 (784.27) μm2, and G3 at 480.66 (384.76) μm2 (p < 0.05). Additionally, fewer xenogenic bone particles and a large amount of connective tissue were observed in G2.

Conclusions

In maxillary sinuses with large antral cavities, autogenous bone combined with xenogenic bone seems to demonstrate better graft remodeling and improve bone formation, compared with the addition of L-PRF.

Clinical relevance

L-PRF produces few advantages regarding new bone formation in the wide maxillary sinuses.

Trial registration

Brazilian Clinical Trials Registry (REBEC) number RBR-2pbbrvg.

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References

  1. Sahlstrand-Johnson P, Jannert M, Strömbeck A, Abul-Kasim K (2011) Computed tomography measurements of different dimensions of maxillary and frontal sinuses. BMC Med Imaging 5(11:8). https://doi.org/10.1186/1471-2342-11-8

  2. Cruz AD, Peixoto GA, Aguiar MF, Camargo GACG, Homs N (2017) Surgeons' performance determining the amount of graft material for sinus floor augmentation using tomography. Braz Dent J 28(3):385–390. https://doi.org/10.1590/0103-6440201601442

    Article  PubMed  Google Scholar 

  3. Cara-Fuentes M, Machuca-Ariza J, Ruiz-Martos A, Ramos-Robles MC, Martínez-Lara I (2016) Long-term outcome of dental implants after maxillary augmentation with and without bone grafting. Med Oral Patol Oral Cir Bucal 1;21(2):e229-35. https://doi.org/10.4317/medoral.21055

  4. Zaniol T, Zaniol A (2017) A rational approach to sinus augmentation: the low window sinus lift. Case Rep Dent 2017:7610607. https://doi.org/10.1155/2017/7610607

    Article  PubMed  PubMed Central  Google Scholar 

  5. Molina A, Sanz-Sánchez I, Sanz-Martín I, Ortiz-Vigón A (2000) Sanz M (2022) Complications in sinus lifting procedures: classification and management. Periodontol 88(1):103–115. https://doi.org/10.1111/prd.12414

    Article  Google Scholar 

  6. Tomasi C, Derks J (2022) Etiology, occurrence, and consequences of implant loss. Periodontol 88(1):13–35. https://doi.org/10.1111/prd.12408

    Article  Google Scholar 

  7. Castagna L, Polido WD, Soares LG, Tinoco EM (2013) Tomographic evaluation of iliac crest bone grafting and the use of immediate temporary implants to the atrophic maxilla. Int J Oral Maxillofac Surg 42(9):1067–1072. https://doi.org/10.1016/j.ijom.2013.04.020

    Article  PubMed  Google Scholar 

  8. Danesh-Sani SA, Loomer PM, Wallace SS (2016) A comprehensive clinical review of maxillary sinus floor elevation: anatomy, techniques, biomaterials and complications. Br J Oral Maxillofac Surg 54(7):724–730. https://doi.org/10.1016/j.bjoms.2016.05.008

    Article  PubMed  Google Scholar 

  9. Taschieri S, Lolato A, Testori T, Francetti L, Del Fabbro M (2018) Short dental implants as compared to maxillary sinus augmentation procedure for the rehabilitation of edentulous posterior maxilla: three-year results of a randomized clinical study. Clin Implant Dent Relat Res 20(1):9–20. https://doi.org/10.1111/cid.12563

    Article  PubMed  Google Scholar 

  10. Zheng X, Teng M, Zhou F, Ye J, Li G, Mo A (2016) Influence of maxillary sinus width on transcrestal sinus augmentation outcomes: radiographic evaluation based on cone beam CT. Clin Implant Dent Relat Res 18(2):292–300. https://doi.org/10.1111/cid.12298

    Article  PubMed  Google Scholar 

  11. Jang HY, Kim HC, Lee SC, Lee JY (2010) Choice of graft material in relation to maxillary sinus width in internal sinus floor augmentation. J Oral Maxillofac Surg 68(8):1859–1868. https://doi.org/10.1016/j.joms.2009.09.093

    Article  PubMed  Google Scholar 

  12. Apuhan T, Yıldırım YS, Özaslan H (2011) The developmental relation between adenoid tissue and paranasal sinus volumes in 3-dimensional computed tomography assessment. Otolaryngol Head Neck Surg 144(6):964–971. https://doi.org/10.1177/0194599811399712

    Article  PubMed  Google Scholar 

  13. Poorey VK, Gupta N (2014) Endoscopic and computed tomographic evaluation of influence of nasal septal deviation on lateral wall of nose and its relation to sinus diseases. Indian J Otolaryngol Head Neck Surg 66(3):330–335. https://doi.org/10.1007/s12070-014-0726-2

    Article  PubMed  PubMed Central  Google Scholar 

  14. Likness MM, Pallanch JF, Sherris DA, Kita H, Mashtare TL Jr, Ponikau JU (2014) Computed tomography scans as an objective measure of disease severity in chronic rhinosinusitis. Otolaryngol Head Neck Surg 150(2):305–311. https://doi.org/10.1177/0194599813513881

    Article  PubMed  Google Scholar 

  15. Chan HL, Suarez F, Monje A, Benavides E, Wang HL (2014) Evaluation of maxillary sinus width on cone-beam computed tomography for sinus augmentation and new sinus classification based on sinus width. Clin Oral Implants Res 25(6):647–652. https://doi.org/10.1111/clr.12055

    Article  PubMed  Google Scholar 

  16. Duong HY, Roccuzzo A, Stähli A, Salvi GE, Lang NP, Sculean A (2000) Oral health-related quality of life of patients rehabilitated with fixed and removable implant-supported dental prostheses. Periodontol 88(1):201–237. https://doi.org/10.1111/prd.12419

    Article  Google Scholar 

  17. McGuire MK, Scheyer ET (2010) Xenogeneic collagen matrix with coronally advanced flap compared to connective tissue with coronally advanced flap for the treatment of dehiscence-type recession defects. J Periodontol 81(8):1108–1117. https://doi.org/10.1902/jop.2010.090698

    Article  PubMed  Google Scholar 

  18. Thoma DS, Zeltner M, Hüsler J, Hämmerle CH, Jung RE (2015) EAO Supplement Working Group 4 - EAO CC 2015 Short implants versus sinus lifting with longer implants to restore the posterior maxilla: a systematic review. Clin Oral Implants Res 26(Suppl 11):154–169. https://doi.org/10.1111/clr.12615

    Article  PubMed  Google Scholar 

  19. Park WB, Kang KL, Han JY (2019) Factors influencing long-term survival rates of implants placed simultaneously with lateral maxillary sinus floor augmentation: a 6- to 20-year retrospective study. Clin Oral Implants Res 30(10):977–988. https://doi.org/10.1111/clr.13505

    Article  PubMed  Google Scholar 

  20. Esposito M, Felice P, Worthington HV (2014) Interventions for replacing missing teeth: augmentation procedures of the maxillary sinus. Cochrane Database Syst Rev 13(5):CD008397. https://doi.org/10.1002/14651858.CD008397.pub2

    Article  Google Scholar 

  21. Ferreira CE, Novaes AB, Haraszthy VI, Bittencourt M, Martinelli CB, Luczyszyn SM (2009) A clinical study of 406 sinus augmentations with 100% anorganic bovine bone. J Periodontol 80(12):1920–1927. https://doi.org/10.1902/jop.2009.090263

    Article  PubMed  Google Scholar 

  22. Lee DZ, Chen ST, Darby IB (2012) Maxillary sinus floor elevation and grafting with deproteinized bovine bone mineral: a clinical and histomorphometric study. Clin Oral Implants Res 23(8):918–924. https://doi.org/10.1111/j.1600-0501.2011.02239.x-

    Article  PubMed  Google Scholar 

  23. Bertl K, Mick RB, Heimel P, Gahleitner A, Stavropoulos A, Ulm C (2018) Variation in bucco-palatal maxillary sinus width does not permit a meaningful sinus classification. Clin Oral Implants Res 29(12):1220–1229. https://doi.org/10.1111/clr.13387

    Article  PubMed  Google Scholar 

  24. Artzi Z, Kozlovsky A, Nemcovsky CE, Weinreb M (2005) The amount of newly formed bone in sinus grafting procedures depends on tissue depth as well as the type and residual amount of the grafted material. J Clin Periodontol 32(2):193–199. https://doi.org/10.1111/j.1600-051X.2005.00656.x

    Article  PubMed  Google Scholar 

  25. 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 

  26. Pignaton TB, Wenzel A, Ferreira CEA, Borges Martinelli C, Oliveira GJPL, Marcantonio E Jr, Spin-Neto (2019). Influence of residual bone height and sinus width on the outcome of maxillary sinus bone augmentation using anorganic bovine bone. Clin Oral Implants Res 30(4):315-323. https://doi.org/10.1111/clr.13417

  27. Avila G, Wang HL, Galindo-Moreno P, Misch CE, Bagramian RA, Rudek I, Benavides E, Moreno-Riestra I, Braun T, Neiva R (2010) The influence of the bucco-palatal distance on sinus augmentation outcomes. J Periodontol 81(7):1041–1050. https://doi.org/10.1902/jop.2010.090686

    Article  PubMed  Google Scholar 

  28. Stumbras A, Krukis MM, Januzis G, Juodzbalys G (2019) Regenerative bone potential after sinus floor elevation using various bone graft materials: a systematic review. Quintessence Int 50(7):548–558. https://doi.org/10.3290/j.qi.a42482

    Article  PubMed  Google Scholar 

  29. Öncü E, Kaymaz E (2017) Assessment of the effectiveness of platelet rich fibrin in the treatment of Schneiderian membrane perforation. Clin Implant Dent Relat Res 19(6):1009–1014. https://doi.org/10.1111/cid.12528

    Article  PubMed  Google Scholar 

  30. Pichotano EC, de Molon RS, de Souza RV, Austin RS, Marcantonio E, Zandim-Barcelos DL (2019) Evaluation of L-PRF combined with deproteinized bovine bone mineral for early implant placement after maxillary sinus augmentation: a randomized clinical trial. Clin Implant Dent Relat Res 21(2):253–262. https://doi.org/10.1111/cid.12713

    Article  PubMed  Google Scholar 

  31. Liu R, Yan M, Chen S, Huang W, Wu D, Chen J (2019) Effectiveness of platelet-rich fibrin as an adjunctive material to bone graft in maxillary sinus augmentation: a meta-analysis of randomized controlled trails. Biomed Res Int 17(2019):7267062. https://doi.org/10.1155/2019/7267062

    Article  Google Scholar 

  32. Aludden HC, Mordenfeld A, Hallman M, Dahlin C, Jensen T (2017) Lateral ridge augmentation with Bio-Oss alone or Bio-Oss mixed with particulate autogenous bone graft: a systematic review. Int J Oral Maxillofac Surg 46(8):1030–1038. https://doi.org/10.1016/j.ijom.2017.03.008

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors would like to acknowledge NCristina Martorana for promptly volunteering to review this manuscript regarding its English language content, and Dr. Rafael Bovi Ambrosano for helping with the statistical analysis of the data.

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Authors and Affiliations

  1. Division of Implantology, Faculdade São Leopoldo Mandic (SLMandic), R. Dr. José Rocha Junqueira, 13, Campinas, São Paulo, Brazil

    Mauricio Marcelo Harlos, Thiago Bezerra da Silva, Pedro Giorgetti Montagner & Adriana Vanderley Gomes

  2. Division of Cell Biology, Faculdade São Leopoldo Mandic (SLMandic), Campinas, São Paulo, Brazil

    Lucas Novaes Teixeira & Elizabeth Ferreira Martinez

Authors
  1. Mauricio Marcelo Harlos
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  2. Thiago Bezerra da Silva
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  3. Pedro Giorgetti Montagner
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  4. Lucas Novaes Teixeira
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  5. Adriana Vanderley Gomes
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  6. Elizabeth Ferreira Martinez
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Contributions

M.M.H., T.B.S., and E.F.M. conceived the ideas; M.M.H. performed all the surgical procedures and collected the data; M.M.H, T.B.S., P.G.M., L.N.T., A.V., and E.F.M. analyzed the data; and M.M.H. and E.F.M. managed the writing of the manuscript. All the authors revised the article critically.

Corresponding author

Correspondence to Elizabeth Ferreira Martinez.

Ethics declarations

Ethical approval

All procedures performed in the studies involving human participants complied with the ethical standards of the institutional and/or national research committee, and with the 1964 Helsinki declaration, and its later amendments or comparable ethical standards. This study was approved by the Research Ethics Committee of the Faculdade São Leopoldo Mandic (Campinas, São Paulo, Brazil), under protocol number 3.575.313.

Informed consent

Informed consent was obtained individually from all the participants in the study.

Conflict of interest

The authors declare no competing interests.

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Supplementary information

s

784_2022_4515_Fig6_ESM.png

S1 Images from the clinical case of the different groups studied. Group 1: autogenous bone + Bio-Oss; Group 2: Bio-Oss combined with L-PRF; Group 3: Bio-Oss. A= initial CBCT, B= osteotomy, C= maxillary sinus filling, D= final CBCT, E= open flap, F= implant installation. (PNG 4927 kb)

High resolution (TIF 17849 kb)

S1_G2 (PNG 5886 kb)

High resolution (TIF 18009 kb)

S1_G3 (PNG 6118 kb)

High resolution (TIF 18008 kb)

784_2022_4515_Fig9_ESM.png

S2. Photomicrographs of the redefined samples of the maxillary sinus trephine of all the patients included in the study. Caption: Group 1: autogenous bone + Bio-Oss; Group 2: Bio-Oss combined with L-PRF; Group 3: Bio-Oss. Bar = 1000μm. (PNG 25425 kb)

High resolution image (TIF 60617 kb)

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Harlos, M.M., da Silva, T.B., Montagner, P.G. et al. Histomorphometric evaluation of different graft associations for maxillary sinus elevation in wide antral cavities: a randomized controlled clinical trial. Clin Oral Invest 26, 1–9 (2022). https://doi.org/10.1007/s00784-022-04515-9

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