Abstract
Background:
Teeth can be used as a raw material for preparing bone substitutes due to their similar chemical composition to bone. The objective of our study was to evaluate the effect of odontogenic biphasic calcium phosphate (BCP) incorporating dentin noncollagenous proteins (DNCPs) on osteogenesis and stability in maxillary sinus augmentation.
Methods:
The composition, structure and morphology of the odontogenic BCP were tested by X-ray powder diffraction (XRD), Brunauer–Emmett–Teller, and scanning electron microscopy methods. The biocompatibility and osteoinduction of DNCPs and materials were examined in vitro and their bone regeneration capacity was verified in vivo.
Results:
The results showed that the cells adhered and proliferated well on the DNCP-loaded BCP scaffold. The odontogenic BCP and DNCPs promoted osteogenic differentiation of cells, The new bone formation in the BCP groups and DNCP subgroups was significantly higher than the new bone formation in the control, and the new bone quality was better. The bone regeneration effect of odontogenic BCP was similar to the effect of deproteinized bovine bone mineral, but β-TCP did not maintain the height and volume of bone reconstruction.
Conclusion:
In conclusion, the combined application of DNCPs and odontogenic BCP is an effective strategy for tissue engineering osteogenesis in the maxillary sinus region. The biomimetic strategy could provide a new approach for patients requiring maxillary sinus lifting.
Similar content being viewed by others
References
Stacchi C, Rapani A, Lombardi T, Bernardello F, Nicolin V, Berton F. Does new bone formation vary in different sites within the same maxillary sinus after lateral augmentation? A prospective histomorphometric study. Clin Oral Implants Res. 2022;33:322–32.
Soardi CM, Soardi B, Wang HL. Crestal window sinus lift and Its long-term clinical outcomes. Int J Periodontics Restorative Dent. 2020;40:757–64.
Guan X, Zhang J, Chen Y, Han J, Yu M, Zhou Y. Changes in bone graft height and influencing factors after sinus floor augmentation by using the lateral window approach: a clinical retrospective study of 1 to 2 years. J Prosthet Dent. 2021. https://doi.org/10.1016/j.prosdent.2021.10.010
Wu Z, Meng Z, Wu Q, Zeng D, Guo Z, Yao J, et al. Biomimetic and osteogenic 3D silk fibroin composite scaffolds with nano MgO and mineralized hydroxyapatite for bone regeneration. J Tissue Eng. 2020;11:2041731420967791.
Parisi C, Salvatore L, Veschini L, Serra MP, Hobbs C, Madaghiele M, et al. Biomimetic gradient scaffold of collagen–hydroxyapatite for osteochondral regeneration. J Tissue Eng. 2020;11:2041731419896068.
Fukuba S, Okada M, Nohara K, Iwata T. Alloplastic bone substitutes for periodontal and bone regeneration in dentistry: current status and prospects. Materials (Basel). 2021;14:1096.
Cheah CW, Al-Namnam NM, Lau MN, Lim GS, Raman R, Fairbairn P, et al. synthetic material for bone, periodontal, and dental tissue regeneration: where are we now, and where are we heading next? Materials (Basel). 2021;14:6123.
Gao C, Wei P, Feng P, Xiao T, Shuai C, Peng S. Nano SiO2 and MgO improve the properties of porous β-TCP scaffolds via advanced manufacturing technology. Int J Mol Sci. 2015;16:6818–30.
Wang C, Zhong D, Zhou X, Yin K, Liao Q, Kong L, et al. Preparation of a new composite combining strengthened β-tricalcium phosphate with platelet-rich plasma as a potential scaffold for the repair of bone defects. Exp Ther Med. 2014;8:1081–6.
Kato E, Lemler J, Sakurai K, Yamada M. Biodegradation property of beta-tricalcium phosphate-collagen composite in accordance with bone formation: a comparative study with Bio-Oss Collagen® in a rat critical-size defect model. Clin Implant Dent Relat Res. 2014;16:202–11.
Funayama T, Noguchi H, Kumagai H, Sato K, Yoshioka T, Yamazaki M. Unidirectional porous beta-tricalcium phosphate and hydroxyapatite artificial bone: a review of experimental evaluations and clinical applications. J Artif Organs. 2021;24:103–10.
Zhang B, Sun H, Wu L, Ma L, Xing F, Kong Q, et al. 3D printing of calcium phosphate bioceramic with tailored biodegradation rate for skull bone tissue reconstruction. Biodes Manuf. 2019;2:161–71.
Su J, Hua S, Chen A, Chen P, Yang L, Yuan X, et al. Three-dimensional printing of gyroid-structured composite bioceramic scaffolds with tuneable degradability. Biomater Adv. 2022;133:112595.
Ahn JH, Kim J, Han G, Kim D, Cheon KH, Lee H, et al. 3D-printed biodegradable composite scaffolds with significantly enhanced mechanical properties via the combination of binder jetting and capillary rise infiltration process. Addit Manuf. 2021;41:101988.
Frenken JW, Bouwman WF, Bravenboer N, Zijderveld SA, Schulten EA, ten Bruggenkate CM. The use of Straumann Bone Ceramic in a maxillary sinus floor elevation procedure: a clinical, radiological, histological and histomorphometric evaluation with a 6-month healing period. Clin Oral Implants Res. 2010;21:201–8.
Annibali S, Iezzi G, Sfasciotti GL, Cristalli MP, Vozza I, Mangano C, et al. Histological and histomorphometric human results of HA-Beta-TCP 30/70 compared to three different biomaterials in maxillary sinus augmentation at 6 months: a preliminary report. Biomed Res Int. 2015;2015:156850.
Bouwman WF, Bravenboer N, Ten Bruggenkate CM, Eijsackers FA, Stringa N, Schulten E. Tissue level changes after maxillary sinus floor elevation with three types of calcium phosphate ceramics: a radiological study with a 5-year follow-up. Materials (Basel). 2021;14:1471.
Lim HC, Hong JY, Lee JS, Jung UW, Choi SH. Late-term healing in an augmented sinus with different ratios of biphasic calcium phosphate: a pilot study using a rabbit sinus model. J Periodontal Implant Sci. 2016;46:57–69.
Chai YC, Carlier A, Bolander J, Roberts SJ, Geris L, Schrooten J, et al. Current views on calcium phosphate osteogenicity and the translation into effective bone regeneration strategies. Acta Biomater. 2012;8:3876–87.
Lim HC, Kim KT, Lee JS, Jung UW, Choi SH. In vivo comparative investigation of three synthetic graft materials with varying compositions processed using different methods. Int J Oral Maxillofac Implants. 2015;30:1280–6.
Karageorgiou V, Kaplan D. Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials. 2005;26:5474–91.
Dou W, Chen H, Chen T, Zhu Q, Jiang D, Xue Z, et al. Design and construction of a microporous CO32− -containing HA/β-TCP biphasic ceramic as a novel bone graft material. Mater Res Exp. 2020;7:025401.
Olszta MJ, Cheng X, Jee SS, Kumar R, Kim Y-Y, Kaufman MJ, et al. Bone structure and formation: a new perspective. Mater Sci Eng R Rep. 2007;58:77–116.
Morgan S, Poundarik AA, Vashishth D. Do Non-collagenous proteins affect skeletal mechanical properties? Calcif Tissue Int. 2015;97:281–91.
Stock SR. The mineral-collagen interface in bone. Calcif Tissue Int. 2015;97:262–80.
Gorski JP. Biomineralization of bone: a fresh view of the roles of non-collagenous proteins. Front Biosci (Landmark Ed). 2011;16:2598–621.
Bee SL, Bustami Y, Ul-Hamid A, Lim K, Abdul Hamid ZA. Synthesis of silver nanoparticle-decorated hydroxyapatite nanocomposite with combined bioactivity and antibacterial properties. J Mater Sci Mater Med. 2021;32:106.
Kim SG. Bone grafting using particulate dentin. Key Eng Mater. 2007;342:29–32.
Ravindran S, George A. Multifunctional ECM proteins in bone and teeth. Exp Cell Res. 2014;325:148–54.
Butler WT, Ritchie H. The nature and functional significance of dentin extracellular matrix proteins. Int J Dev Biol. 1995;39:169–79.
Qin C, Baba O, Butler WT. Post-translational modifications of sibling proteins and their roles in osteogenesis and dentinogenesis. Crit Rev Oral Biol Med. 2004;15:126–36.
Han S, Paeng KW, Park S, Jung UW, Cha JK, Hong J. Programmed BMP-2 release from biphasic calcium phosphates for optimal bone regeneration. Biomaterials. 2021;272:120785.
Deng N, Sun J, Li Y, Chen L, Chen C, Wu Y, et al. Experimental study of rhBMP-2 chitosan nano-sustained release carrier-loaded PLGA/nHA scaffolds to construct mandibular tissue-engineered bone. Arch Oral Biol. 2019;102:16–25.
Sun Y, Jiang Y, Liu Q, Gao T, Feng JQ, Dechow P, et al. Biomimetic engineering of nanofibrous gelatin scaffolds with noncollagenous proteins for enhanced bone regeneration. Tissue Eng Part A. 2013;19:1754–63.
Huang B, Sun Y, Maciejewska I, Qin D, Peng T, McIntyre B, et al. Distribution of SIBLING proteins in the organic and inorganic phases of rat dentin and bone. Eur J Oral Sci. 2008;116:104–12.
Zyman ZZ, Tkachenko MV, Polevodin DV. Preparation and characterization of biphasic calcium phosphate ceramics of desired composition. J Mater Sci Mater Med. 2008;19:2819–25.
Brown O, McAfee M, Clarke S, Buchanan F. Sintering of biphasic calcium phosphates. J Mater Sci Mater Med. 2010;21:2271–9.
Collins MO, Yu L, Choudhary JS. Analysis of protein phosphorylation on a proteome-scale. Proteomics. 2007;7:2751–68.
Yang XJ. Multisite protein modification and intramolecular signaling. Oncogene. 2005;24:1653–62.
Kim JS, Cha JK, Lee JS, Choi SH, Cho KS. Increased osteoinductivity and mineralization by minimal concentration of bone morphogenetic protein-2 loaded onto biphasic calcium phosphate in a rabbit sinus. J Periodontal Implant Sci. 2016;46:350–9.
Zhang W, Wang X, Wang S, Zhao J, Xu L, Zhu C, et al. The use of injectable sonication-induced silk hydrogel for VEGF(165) and BMP-2 delivery for elevation of the maxillary sinus floor. Biomaterials. 2011;32:9415–24.
Del Fabbro M, Bortolin M, Taschieri S, Weinstein RL. Effect of autologous growth factors in maxillary sinus augmentation: a systematic review. Clin Implant Dent Relat Res. 2013;15:205–16.
Khouly I, Pardiñas López S, Aliaga I, Froum SJ. Long-term implant survival after 100 maxillary sinus augmentations using plasma rich in growth factors. Implant Dent. 2017;26:199–208.
Dimitriou R, Tsiridis E, Giannoudis PV. Current concepts of molecular aspects of bone healing. Injury. 2005;36:1392–404.
Lee CP, Colombo JS, Ayre WN, Sloan AJ, Waddington RJ. Elucidating the cellular actions of demineralised dentine matrix extract on a clonal dental pulp stem cell population in orchestrating dental tissue repair. J Tissue Eng. 2015;6:2041731415586318.
Walsh DP, Raftery RM, Chen G, Heise A, O’Brien FJ, Cryan SA. Rapid healing of a critical-sized bone defect using a collagen-hydroxyapatite scaffold to facilitate low dose, combinatorial growth factor delivery. J Tissue Eng Regen Med. 2019;13:1843–53.
Chen FM, Zhang M, Wu ZF. Toward delivery of multiple growth factors in tissue engineering. Biomaterials. 2010;31:6279–308.
Kavukcuoglu NB, Denhardt DT, Guzelsu N, Mann AB. Osteopontin deficiency and aging on nanomechanics of mouse bone. J Biomed Mater Res A. 2007;83:136–44.
Hansma PK, Fantner GE, Kindt JH, Thurner PJ, Schitter G, Turner PJ, et al. Sacrificial bonds in the interfibrillar matrix of bone. J Musculoskelet Neuronal Interact. 2005;5:313–5.
Nikel O, Laurencin D, McCallum SA, Gundberg CM, Vashishth D. NMR investigation of the role of osteocalcin and osteopontin at the organic-inorganic interface in bone. Langmuir. 2013;29:13873–82.
Poundarik AA, Diab T, Sroga GE, Ural A, Boskey AL, Gundberg CM, et al. Dilatational band formation in bone. Proc Natl Acad Sci U S A. 2012;109:19178–83.
Wang K, Leng Y, Lu X, Ren F. Calcium phosphate bioceramics induce mineralization modulated by proteins. Mater Sci Eng C Mater Biol Appl. 2013;33:3245–55.
Wang J, Chen Y, Zhu X, Yuan T, Tan Y, Fan Y, et al. Effect of phase composition on protein adsorption and osteoinduction of porous calcium phosphate ceramics in mice. J Biomed Mater Res A. 2014;102:4234–43.
LeGeros RZ, Lin S, Rohanizadeh R, Mijares D, LeGeros JP. Biphasic calcium phosphate (BCP) Bioceramics: preparation, properties and applications. J Mater Sci Mater Med. 2003;14:201–9.
Rh Owen G, Dard M, Larjava H. Hydoxyapatite/beta-tricalcium phosphate biphasic ceramics as regenerative material for the repair of complex bone defects. J Biomed Mater Res B Appl Biomater. 2018;106:2493–512.
Jones AC, Arns CH, Hutmacher DW, Milthorpe BK, Sheppard AP, Knackstedt MA. The correlation of pore morphology, interconnectivity and physical properties of 3D ceramic scaffolds with bone ingrowth. Biomaterials. 2009;30:1440–51.
Zhu XD, Fan HS, Xiao YM, Li DX, Zhang HJ, Luxbacher T, et al. Effect of surface structure on protein adsorption to biphasic calcium-phosphate ceramics in vitro and in vivo. Acta Biomater. 2009;5:1311–8.
Khan MUA, Abd Razak SI, Mehboob H, Abdul Kadir MR, Anand TJS, Inam F, et al. Synthesis and characterization of silver-coated polymeric scaffolds for bone tissue engineering: antibacterial and in vitro evaluation of cytotoxicity and biocompatibility. ACS Omega. 2021;6:4335–46.
Acknowledgements
The authors are thankful to Center for Scientific Research and Key Lab. of Oral Diseases Research of Anhui Medical University for supporting the research. This work was supported by the Anhui Provincial Key Research and Development Plan (201904a07020062). Anhui Provincial Key Research and Development Plan, 201904a07020062, Yuanyin Wang. 2021Disciplinary Construction Project in School of Dentistry, Anhui Medical University 2021kqxkFY10.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors have no financial conflicts of interest.
Ethical statement
The animal studies were performed after receiving approval of the Animal Research Committee of Anhui Medical University (LLSC 20210681).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Yang, G., Liu, X., Huang, T. et al. Combined Application of Dentin Noncollagenous Proteins and Odontogenic Biphasic Calcium Phosphate in Rabbit Maxillary Sinus Lifting. Tissue Eng Regen Med 20, 93–109 (2023). https://doi.org/10.1007/s13770-022-00502-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13770-022-00502-z