Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지
DOI QR코드

DOI QR Code

The impact of polydeoxyribonucleotide on early bone formation in lateral-window sinus floor elevation with simultaneous implant placement

  • Dongseob Lee (Department of Periodontology, School of Dentistry and Dental Research Institute, Seoul National University and Seoul National University Dental Hospital) ;
  • Jungwon Lee (Department of Periodontology, School of Dentistry and Dental Research Institute, Seoul National University and Seoul National University Dental Hospital) ;
  • Ki-Tae Koo (Department of Periodontology, School of Dentistry and Dental Research Institute, Seoul National University and Seoul National University Dental Hospital) ;
  • Yang-Jo Seol (Department of Periodontology, School of Dentistry and Dental Research Institute, Seoul National University and Seoul National University Dental Hospital) ;
  • Yong-Moo Lee (Department of Periodontology, School of Dentistry and Dental Research Institute, Seoul National University and Seoul National University Dental Hospital)
  • Received : 2022.06.12
  • Accepted : 2022.08.09
  • Published : 2023.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: The aim of this study was to evaluate the impact of polydeoxyribonucleotide (PDRN) on histologic outcomes when implant placement and lateral sinus floor elevation are performed simultaneously. Methods: Three bimaxillary premolars (P2, P3, and P4) were extracted from 4 beagle dogs 2 months before lateral sinus floor elevation. After lateral elevation of the sinus membrane, each sinus was allocated to either the test or control group. Sinuses underwent either 1) collagenated synthetic bone graft with PDRN following lateral sinus floor elevation (test group) or 2) collagenated synthetic bone graft without PDRN after lateral sinus floor elevation (control group). Eight weeks after the surgical procedure, all animals were euthanised for a histologic and histomorphometric assessment. Augmented height (AH), protruding height (PH), and bone-to-implant contact in pristine (BICp) and augmented (BICa) bone were measured. The composition of the augmented area, which was divided into 3 areas of interest located in coronal, middle and apical areas (AOI_C, AOI_M, and AOI_A), was calculated with 3 parameters: the area percentage of new bone (pNB), residual bone graft particle (pRBP), and fibrovascular connective tissue (pFVT). Results: AH, PH, BICp, BICa total, BICa coronal, and BICa middle values were not significantly different between sinuses in the control and test groups (all P>0.05). The BICa apical of sinuses in the test group (76.7%±9.3%) showed statistically higher values than those of sinuses in the control group (55.6%±22.1%) (P=0.038). pNB, pRBP, and pFVT showed statistically significant differences between the 2 groups in AOI_A (P=0.038, P=0.028, and P=0.007, respectively). pNB, pRBP, and pFVT in AOI_C and AOI_M were not significantly different between samples in the control and test groups (all P>0.05). Conclusions: The histologic findings revealed that lateral sinus floor elevation with PDRN might improve early new bone formation and enable higher bone-to-implant contact.

Keywords

Acknowledgement

The work was supported by Seoul National University Dental Hospital and Dental Research Institute, Seoul National University in Seoul, Republic of Korea. This funding source had no role in the design of this study and will not have any role during its execution, analyses, interpretation of the data, or decision to submit results.

References

  1. Pietrokovski J, Starinsky R, Arensburg B, Kaffe I. Morphologic characteristics of bony edentulous jaws. J Prosthodont 2007;16:141-7.  https://doi.org/10.1111/j.1532-849X.2007.00165.x
  2. Boyne PJ, James RA. Grafting of the maxillary sinus floor with autogenous marrow and bone. J Oral Surg 1980;38:613-6. 
  3. Kim HJ, Yea S, Kim KH, Lee YM, Ku Y, Rhyu IC, et al. 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 2020;91:183-93.  https://doi.org/10.1002/JPER.19-0066
  4. Zhou Y, Shi Y, Si M, Wu M, Xie Z. The comparative evaluation of transcrestal and lateral sinus floor elevation in sites with residual bone height ≤6 mm: a two-year prospective randomized study. Clin Oral Implants Res 2021;32:180-91.  https://doi.org/10.1111/clr.13688
  5. Freitas RM, Spin-Neto R, Marcantonio Junior E, Pereira LA, Wikesjo UM, Susin C. Alveolar ridge and maxillary sinus augmentation using rhBMP-2: a systematic review. Clin Implant Dent Relat Res 2015;17 Suppl 1:e192-201.  https://doi.org/10.1111/cid.12156
  6. Boyne PJ, Lilly LC, Marx RE, Moy PK, Nevins M, Spagnoli DB, et al. De novo bone induction by recombinant human bone morphogenetic protein-2 (rhBMP-2) in maxillary sinus floor augmentation. J Oral Maxillofac Surg 2005;63:1693-707.  https://doi.org/10.1016/j.joms.2005.08.018
  7. Kim HJ, Chung JH, Shin SY, Shin SI, Kye SB, Kim NK, et al. Efficacy of rhBMP-2/hydroxyapatite on sinus floor augmentation: a multicenter, randomized controlled clinical trial. J Dent Res 2015;94:158S-165S.  https://doi.org/10.1177/0022034515594573
  8. Pichotano EC, de Molon RS, de Souza RV, Austin RS, Marcantonio E, Zandim-Barcelos DL. 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 2019;21:253-62.  https://doi.org/10.1111/cid.12713
  9. Kumar N, Prasad K, Ramanujam L, K R, Dexith J, Chauhan A. Evaluation of treatment outcome after impacted mandibular third molar surgery with the use of autologous platelet-rich fibrin: a randomized controlled clinical study. J Oral Maxillofac Surg 2015;73:1042-9.  https://doi.org/10.1016/j.joms.2014.11.013
  10. Liu R, Yan M, Chen S, Huang W, Wu D, Chen J. 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 2019;2019:7267062. 
  11. Thellung S, Florio T, Maragliano A, Cattarini G, Schettini G. Polydeoxyribonucleotides enhance the proliferation of human skin fibroblasts: involvement of A2 purinergic receptor subtypes. Life Sci 1999;64:1661-74.  https://doi.org/10.1016/S0024-3205(99)00104-6
  12. Koo Y, Yun Y. Effects of polydeoxyribonucleotides (PDRN) on wound healing: electric cell-substrate impedance sensing (ECIS). Mater Sci Eng C 2016;69:554-60.  https://doi.org/10.1016/j.msec.2016.06.094
  13. Bitto A, Polito F, Altavilla D, Minutoli L, Migliorato A, Squadrito F. Polydeoxyribonucleotide (PDRN) restores blood flow in an experimental model of peripheral artery occlusive disease. J Vasc Surg 2008;48:1292-300.  https://doi.org/10.1016/j.jvs.2008.06.041
  14. Minutoli L, Antonuccio P, Squadrito F, Bitto A, Nicotina PA, Fazzari C, et al. Effects of polydeoxyribonucleotide on the histological damage and the altered spermatogenesis induced by testicular ischaemia and reperfusion in rats. Int J Androl 2012;35:133-44.  https://doi.org/10.1111/j.1365-2605.2011.01194.x
  15. Lee DW, Hong HJ, Roh H, Lee WJ. The effect of polydeoxyribonucleotide on ischemic rat skin flap survival. Ann Plast Surg 2015;75:84-90.  https://doi.org/10.1097/SAP.0000000000000053
  16. Altavilla D, Bitto A, Polito F, Marini H, Minutoli L, Di Stefano V, et al. Polydeoxyribonucleotide (PDRN): a safe approach to induce therapeutic angiogenesis in peripheral artery occlusive disease and in diabetic foot ulcers. Cardiovasc Hematol Agents Med Chem 2009;7:313-21. https://doi.org/10.2174/187152509789541909
  17. Bowler WB, Buckley KA, Gartland A, Hipskind RA, Bilbe G, Gallagher JA. Extracellular nucleotide signaling: a mechanism for integrating local and systemic responses in the activation of bone remodeling. Bone 2001;28:507-12.  https://doi.org/10.1016/S8756-3282(01)00430-6
  18. Nakamura E, Uezono Y, Narusawa K, Shibuya I, Oishi Y, Tanaka M, et al. ATP activates DNA synthesis by acting on P2X receptors in human osteoblast-like MG-63 cells. Am J Physiol Cell Physiol 2000;279:C510-9.  https://doi.org/10.1152/ajpcell.2000.279.2.C510
  19. Guizzardi S, Galli C, Govoni P, Boratto R, Cattarini G, Martini D, et al. Polydeoxyribonucleotide (PDRN) promotes human osteoblast proliferation: a new proposal for bone tissue repair. Life Sci 2003;73:1973-83.  https://doi.org/10.1016/S0024-3205(03)00547-2
  20. Buffoli B, Favero G, Borsani E, Boninsegna R, Sancassani G, Labanca M, et al. Sodium-DNA for bone tissue regeneration: an experimental study in rat calvaria. BioMed Res Int 2017;2017:7320953. 
  21. Kim SK, Huh CK, Lee JH, Kim KW, Kim MY. Histologic study of bone-forming capacity on polydeoxyribonucleotide combined with demineralized dentin matrix. Maxillofac Plast Reconstr Surg 2016;38:7. 
  22. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol 2010;8:e1000412. 
  23. Liu N, Sun F, Xu C, Lin T, Lu E. A comparative study of dog models for osteotome sinus floor elevation and dental implants in posterior maxilla subjacent to the maxillary sinus. Oral Surg Oral Med Oral Pathol Oral Radiol 2013;115:e15-20.  https://doi.org/10.1016/j.oooo.2011.10.024
  24. Zhu L, Yang J, Gong J, Zhang C, Wang H. Optimized beagle model for maxillary sinus floor augmentation via a mini-lateral window with simultaneous implant placement. J Int Med Res 2018;46:4684-92.  https://doi.org/10.1177/0300060518796759
  25. Betsy J, Prasanth CS, Baiju KV, Prasanthila J, Subhash N. Efficacy of antimicrobial photodynamic therapy in the management of chronic periodontitis: a randomized controlled clinical trial. J Clin Periodontol 2014;41:573-81.  https://doi.org/10.1111/jcpe.12249
  26. Haas R, Baron M, Donath K, Zechner W, Watzek G. Porous hydroxyapatite for grafting the maxillary sinus: a comparative histomorphometric study in sheep. Int J Oral Maxillofac Implants 2002;17:337-46. 
  27. Srouji S, Kizhner T, Ben David D, Riminucci M, Bianco P, Livne E. The Schneiderian membrane contains osteoprogenitor cells: in vivo and in vitro study. Calcif Tissue Int 2009;84:138-45.  https://doi.org/10.1007/s00223-008-9202-x
  28. Guo J, Weng J, Rong Q, Zhang X, Zhu S, Huang D, et al. Investigation of multipotent postnatal stem cells from human maxillary sinus membrane. Sci Rep 2015;5:11660. 
  29. Scala A, Botticelli D, Faeda RS, Garcia Rangel I Jr, Americo 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 2012;23:175-81.  https://doi.org/10.1111/j.1600-0501.2011.02227.x
  30. Jungner M, Cricchio G, Salata LA, Sennerby L, Lundqvist C, Hultcrantz M, et al. On the early mechanisms of bone formation after maxillary sinus membrane elevation: an experimental histological and immunohistochemical study. Clin Implant Dent Relat Res 2015;17:1092-102.  https://doi.org/10.1111/cid.12218
  31. Kim JS, Cha JK, Cho AR, Kim MS, Lee JS, Hong JY, et al. Acceleration of bone regeneration by BMP2-loaded collagenated biphasic calcium phosphate in rabbit sinus. Clin Implant Dent Relat Res 2015;17:1103-13.  https://doi.org/10.1111/cid.12223
  32. Kim DS, Lee JK, Jung JW, Baek SW, Kim JH, Heo Y, et al. Promotion of bone regeneration using bioinspired PLGA/MH/ECM scaffold combined with bioactive PDRN. Materials (Basel) 2021;14:4149. 
  33. Mediero A, Wilder T, Perez-Aso M, Cronstein BN. Direct or indirect stimulation of adenosine A2A receptors enhances bone regeneration as well as bone morphogenetic protein-2. FASEB J 2015;29:1577-90. https://doi.org/10.1096/fj.14-265066
  34. Jhin MJ, Kim KH, Kim SH, Kim YS, Kim ST, Koo KT, et al. Ex vivo bone morphogenetic protein-2 gene delivery using bone marrow stem cells in rabbit maxillary sinus augmentation in conjunction with implant placement. J Periodontol 2013;84:985-94.  https://doi.org/10.1902/jop.2012.120221
  35. Kim DH, Ko MJ, Lee JH, Jeong SN. A radiographic evaluation of graft height changes after maxillary sinus augmentation. J Periodontal Implant Sci 2018;48:174-81.  https://doi.org/10.5051/jpis.2018.48.3.174
  36. James AW, LaChaud G, Shen J, Asatrian G, Nguyen V, Zhang X, et al. A review of the clinical side effects of bone morphogenetic protein-2. Tissue Eng Part B Rev 2016;22:284-97.  https://doi.org/10.1089/ten.teb.2015.0357
  37. Zara JN, Siu RK, Zhang X, Shen J, Ngo R, Lee M, et al. High doses of bone morphogenetic protein 2 induce structurally abnormal bone and inflammation in vivo. Tissue Eng Part A 2011;17:1389-99.  https://doi.org/10.1089/ten.tea.2010.0555
  38. Garrett MP, Kakarla UK, Porter RW, Sonntag VK. Formation of painful seroma and edema after the use of recombinant human bone morphogenetic protein-2 in posterolateral lumbar spine fusions. Neurosurgery 2010;66:1044-9.  https://doi.org/10.1227/01.NEU.0000369517.21018.F2
  39. Sul SH, Choi BH, Li J, Jeong SM, Xuan F. Histologic changes in the maxillary sinus membrane after sinus membrane elevation and the simultaneous insertion of dental implants without the use of grafting materials. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2008;105:e1-5.  https://doi.org/10.1016/j.tripleo.2007.11.019
  40. Zhu L, Yang J, Gong J, Zhang C, Ganss B, Wang H. Early bone formation in mini-lateral window sinus floor elevation with simultaneous implant placement: an in vivo experimental study. Clin Oral Implants Res 2021;32:448-59. https://doi.org/10.1111/clr.13714