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Comparison of osteogenesis and osseointegration following implant placement with simultaneous maxillary sinus augmentation using particulate and collagenated block types of deproteinized porcine bone mineral: a radiographic and histomorphometric analysis

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Abstract

Objectives

This study aimed to compare osseointegration and osteogenesis after single-stage maxillary sinus augmentation with the lateral window using particulate deproteinized porcine bone mineral (PDPBM) and collagenated block deproteinized porcine bone mineral (BDPBM).

Materials and methods

Bi-maxillary premolars of six beagle dogs were extracted. Eight weeks later, an implant was placed into each augmented sinus with PDPBM or BDPBM according to a split-mouth design. Eight weeks later, all specimens were harvested. Each specimen was separated into the region of interest with the implant (ROI-I) and region of interest with sinus augmented area (ROI-S) 5 mm away from ROI-I. ROI-I and ROI-S were evaluated through micro-computed tomography and histomorphometry.

Results

Bone substitute insertion took longer for the PDPBM group than for the BDPBM group (P = 0.002). In ROI-I, three-dimensional bone-to-implant contact (BIC) did not show statistically significant differences between the groups. Two-dimensional BIC also showed comparable values for both groups. In ROI-S, the graft material volume/tissue volume, trabecular bone pattern factor, and structural model index were higher in the BDPBM group than in the PDPBM group (P < 0.05). The proportions of new bone, graft material, and connective tissue were not significantly statistically different between groups. Less new bone was found in the apical area than in the coronal or middle areas in the BCPBM group (P < 0.05).

Conclusions

BDPBM may save time in inserting bone substitutes and provide comparable osteogenesis and osseointegration to PDPBM.

Clinical relevance

When performing sinus augmentation, BDPBM might improve operator's convenience with comparable biological results compared to PDPBM.

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Data availability

The data that support the findings of this study are available from the corresponding authors upon reasonable request.

References

  1. Suzuki S, Sugihara N, Kamijo H, Morita M, Kawato T, Tsuneishi M et al (2022) Reasons for tooth extractions in Japan: the second nationwide survey. Int Dent J 72:366–372

    Article  PubMed  Google Scholar 

  2. Taiwo AO, Ibikunle AA, Braimah RO, Sulaiman OA, Gbotolorun OM (2017) Tooth extraction: pattern and etiology from extreme Northwestern Nigeria. Eur J Dent 11:335–339

    Article  PubMed  PubMed Central  Google Scholar 

  3. Sharan A, Madjar D (2008) Maxillary sinus pneumatization following extractions: a radiographic study. Int J Oral Maxillofac Implants 23:48–56

    PubMed  Google Scholar 

  4. Cavalcanti MC, Guirado TE, Sapata VM, Costa C, Pannuti CM, Jung RE et al (2018) Maxillary sinus floor pneumatization and alveolar ridge resorption after tooth loss: a cross-sectional study. Braz Oral Res 32:e64

    Article  PubMed  Google Scholar 

  5. Kim HJ, Yea S, Kim KH, Lee YM, Ku Y, Rhyu IC et al (2020) A retrospective study of implants placed following 1-stage or 2-stage maxillary sinus floor augmentation by the lateral window technique performed on residual bone of <4 mm: results up to 10 years of follow-up. J Periodontol 91:183–193

    Article  PubMed  Google Scholar 

  6. Rapone B, Inchingolo AD, Trasarti S, Ferrara E, Qorri E, Mancini A et al (2022) Long-term outcomes of implants placed in maxillary sinus floor augmentation with Porous Fluorohydroxyapatite (Algipore(®) FRIOS(®)) in comparison with anorganic bovine bone (Bio-Oss(®)) and Platelet Rich Plasma (PRP): a retrospective study. J Clin Med 11(9):2491

    Article  PubMed  PubMed Central  Google Scholar 

  7. Block MS, Kent JN (1997) Sinus augmentation for dental implants: the use of autogenous bone. J Oral Maxillofac Surg 55:1281–1286

    Article  PubMed  Google Scholar 

  8. Starch-Jensen T, Ahmad M, Bruun NH, Becktor JP (2021) Patient’s perception of recovery after maxillary sinus floor augmentation with autogenous bone graft compared with composite grafts: a single-blinded randomized controlled trial. Int J Implant Dent 7:99

    Article  PubMed  PubMed Central  Google Scholar 

  9. Peng W, Kim IK, Cho HY, Pae SP, Jung BS, Cho HW et al (2013) Assessment of the autogenous bone graft for sinus elevation. J Korean Assoc Oral Maxillofac Surg 39:274–282

    Article  PubMed  PubMed Central  Google Scholar 

  10. Al-Moraissi E, Alhajj WA, Al-Qadhi G, Christidis N (2022) Bone graft osseous changes after maxillary sinus floor augmentation: a systematic review. J Oral Implantol 48:464–471

    Article  PubMed  Google Scholar 

  11. 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 35:216–240

    Article  PubMed  Google Scholar 

  12. Lambert F, Lecloux G, Rompen E (2010) One-step approach for implant placement and subantral bone regeneration using bovine hydroxyapatite: a 2- to 6-year follow-up study. Int J Oral Maxillofac Implants 25:598–606

    PubMed  Google Scholar 

  13. Peleg M, Garg AK, Mazor Z (2006) Predictability of simultaneous implant placement in the severely atrophic posterior maxilla: a 9-year longitudinal experience study of 2132 implants placed into 731 human sinus grafts. Int J Oral Maxillofac Implants 21:94–102

    PubMed  Google Scholar 

  14. Song YW, Rafikov K, Paeng KW, Kim MJ, Cha JK, Thoma DS et al (2020) Dimensional changes of the maxillary sinus augmented with a collagenated synthetic bone block or synthetic bone particulates: a pre-clinical study in rabbits. J Clin Periodontol 47:1416–1426

    Article  PubMed  Google Scholar 

  15. Paik JW, Cha JK, Paeng KW, Kim MJ, Thoma DS, Jung RE et al (2020) Volume stability of the augmented sinus using a collagenated bovine bone mineral grafted in case of a perforated Schneiderian membrane: an experimental study in rabbits. J Clin Periodontol 47:649–656

    Article  PubMed  Google Scholar 

  16. Kim S, Chung JH, Shin SY, Shin SI, Hong JY, Lim HC (2020) Collagenated synthetic bone substitute material for sinus floor elevation at sites with a perforated Schneiderian membrane. J Clin Med 9(11):3764

    Article  PubMed  PubMed Central  Google Scholar 

  17. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 8:e1000412

    Article  PubMed  PubMed Central  Google Scholar 

  18. Lee D, Lee J, Koo KT, Seol YJ, Lee YM (2023) The impact of polydeoxyribonucleotide on early bone formation in lateral-window sinus floor elevation with simultaneous implant placement. J Periodontal Implant Sci 53:157–169

    Article  PubMed  Google Scholar 

  19. Hong JM, Kim UG, Yeo IL (2022) Comparison of three-dimensional digital analyses and two-dimensional histomorphometric analyses of the bone-implant interface. PLoS ONE 17:e0276269

    Article  PubMed  PubMed Central  Google Scholar 

  20. Araújo MG, Liljenberg B, Lindhe J (2010) Dynamics of Bio-Oss Collagen incorporation in fresh extraction wounds: an experimental study in the dog. Clin Oral Implants Res 21:55–64

    Article  PubMed  Google Scholar 

  21. Lim HC, Paeng KW, Jung UW, Benic GI (2023) Vertical bone augmentation using collagenated or non-collagenated bone substitute materials with or without recombinant human bone morphogenetic protein-2 in a rabbit calvarial model. J Periodontal Implant Sci 53:e7

  22. Bissinger O, Probst FA, Wolff KD, Jeschke A, Weitz J, Deppe H et al (2017) Comparative 3D micro-CT and 2D histomorphometry analysis of dental implant osseointegration in the maxilla of minipigs. J Clin Periodontol 44:418–427

    Article  PubMed  Google Scholar 

  23. Choi JY, Park JI, Chae JS, Yeo IL (2019) Comparison of micro-computed tomography and histomorphometry in the measurement of bone-implant contact ratios. Oral Surg Oral Med Oral Pathol Oral Radiol 128:87–95

    Article  PubMed  Google Scholar 

  24. Rozé J, Babu S, Saffarzadeh A, Gayet-Delacroix M, Hoornaert A, Layrolle P (2009) Correlating implant stability to bone structure. Clin Oral Implants Res 20:1140–1145

    Article  PubMed  Google Scholar 

  25. Sugisaki M, Agematsu H, Matsunaga S, Saka H, Sakiyama K, Ide Y (2009) Three-dimensional analysis of the internal structure of the mandibular condyle in dentulous and edentulous jaws using micro-CT. Cranio 27:78–87

    Article  PubMed  Google Scholar 

  26. Kim JJ, Schwarz F, Song HY, Choi Y, Kang KR, Koo KT (2017) Ridge preservation of extraction sockets with chronic pathology using Bio-Oss(®) Collagen with or without collagen membrane: an experimental study in dogs. Clin Oral Implants Res 28:727–733

    Article  PubMed  Google Scholar 

  27. Scala A, Viña-Almunia J, Carda C, Martín de Llano JJ, Soto-Peñaloza D, Peñarrocha-Diago M et al (2020) Sequential healing of the elevated sinus floor with different size of antrostomy: a histomorphometric study in rabbits. Oral Maxillofac Surg 24:403–410

  28. Sim JE, Kim S, Hong JY, Shin SI, Chung JH, Lim HC (2022) Effect of the size of the bony access window and the collagen barrier over the window in sinus floor elevation: a preclinical investigation in a rabbit sinus model. J Periodontal Implant Sci 52:325–337

    Article  PubMed  PubMed Central  Google Scholar 

  29. Cordaro L, Bosshardt DD, Palattella P, Rao W, Serino G, Chiapasco M (2008) Maxillary sinus grafting with Bio-Oss or Straumann bone ceramic: histomorphometric results from a randomized controlled multicenter clinical trial. Clin Oral Implants Res 19:796–803

    Article  PubMed  Google Scholar 

  30. Raghoebar GM, Onclin P, Boven GC, Vissink A, Meijer HJA (2019) Long-term effectiveness of maxillary sinus floor augmentation: a systematic review and meta-analysis. J Clin Periodontol 46(Suppl 21):307–318

    Article  PubMed  Google Scholar 

  31. Botticelli D, Lang NP (2017) Dynamics of osseointegration in various human and animal models-a comparative analysis. Clin Oral Implant Res 28:742–748

    Article  Google Scholar 

  32. Masuda K, Ricardo Silva E, Alccayhuaman KAA, Botticelli D, Porfirio Xavier S (2020) Histologic and Micro-CT Analyses at Implants Placed Immediately After Maxillary Sinus Elevation Using Large or Small Xenograft Granules: An Experimental Study in Rabbits. Int J Oral Maxillofac Implants 35(4):739–748

    Article  PubMed  Google Scholar 

  33. Scarano A, Piattelli A, Perrotti V, Manzon L, Iezzi G (2011) Maxillary sinus augmentation in humans using cortical porcine bone: a histological and histomorphometrical evaluation after 4 and 6 months. Clin Implant Dent Relat Res 13:13–18

    Article  PubMed  Google Scholar 

  34. Tanaka K, Iezzi G, Piattelli A, Ferri M, Mesa NF, Alccayhuaman KAA et al (2019) Sinus floor elevation and antrostomy healing: a histomorphometric clinical study in humans. Implant Dent 28:537–542

    PubMed  Google Scholar 

  35. Lee JH, Han JH, Jeong SN (2023) Porcine-derived soft block bone substitutes for the treatment of severe class II furcation-involved mandibular molars: a prospective controlled follow-up study. J Periodontal Implant Sci 53:e11

  36. Sim J-E, Kim S, Hong J-Y, Shin S-I, Chung J-H, Lim H-C (2021) Effect of the size of the bony access window and the collagen barrier over the window in sinus floor elevation: a preclinical investigation in a rabbit sinus model. J Periodontal Implant Sci 52(4):325–337

    Article  Google Scholar 

  37. Miyauchi Y, Izutani T, Teranishi Y, Iida T, Nakajima Y, Xavier SP et al (2022) Healing patterns of non-collagenated bovine and collagenated porcine xenografts used for sinus floor elevation: a histological study in rabbits. J Funct Biomater 13:276

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kamolratanakul P, Mattheos N, Yodsanga S, Jansisyanont P (2022) The impact of deproteinized bovine bone particle size on histological and clinical bone healing outcomes in the augmented sinus: a randomized controlled clinical trial. Clin Implant Dent Relat Res 24:361–371

    Article  PubMed  Google Scholar 

Download references

Funding

This research was supported by a grant from the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health & Welfare, Republic of Korea (grant number HI20C2114).

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Authors and Affiliations

  1. Department of Periodontology, School of Dentistry and Dental Research Institute, Seoul National University, 101, Daehak-Ro, Jongno-Gu, Seoul, 03080, Republic of Korea

    Dongseob Lee, Ki-Tae Koo, Yang-Jo Seol, Yong-Moo Lee & Jungwon Lee

  2. National Dental Care Center for Persons With Special Needs, Seoul National University Dental Hospital, Seoul, Republic of Korea

    Dongseob Lee

  3. One-Stop Specialty Center, Seoul National University Dental Hospital, Seoul, Republic of Korea

    Jungwon Lee

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  1. Dongseob Lee
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Contributions

Dongseob Lee: data curation, formal analysis, investigation, software, validation, and visualization, as well as drafting the manuscript.

Ki-Tae Koo: formal analysis, methodology, and critical revision of the manuscript.

Yang-Jo Seol: formal analysis, methodology, and critical revision of the manuscript.

Yong-Moo Lee: formal analysis, methodology, and critical revision of the manuscript.

Jungwon Lee: conceptualization, funding acquisition, investigation, project administration, supervision, and critical revision of the manuscript.

All authors read and approved the final manuscript.

Corresponding author

Correspondence to Jungwon Lee.

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Lee, D., Koo, KT., Seol, YJ. et al. Comparison of osteogenesis and osseointegration following implant placement with simultaneous maxillary sinus augmentation using particulate and collagenated block types of deproteinized porcine bone mineral: a radiographic and histomorphometric analysis. Clin Oral Invest 27, 5865–5874 (2023). https://doi.org/10.1007/s00784-023-05197-7

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  • DOI: https://doi.org/10.1007/s00784-023-05197-7

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