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CC BY 4.0 · Eur J Dent 2023; 17(03): 871-880
DOI: 10.1055/s-0042-1756691
Original Article

The Osteogenesis Mechanisms of Dental Alveolar Bone Socket Post Induction with Hydroxyapatite Bovine Tooth Graft: An Animal Experimental in Rattus norvegicus Strain Wistar

Nanik Zubaidah
1   Doctoral Program of Medical Science, Faculty of Medicine, Universitas Airlangga, Indonesia
2   Department of Conservative Dentistry, Faculty of Dental Medicine, Universitas Airlangga, Surabaya, Indonesia
,
Dian Dwi Pratiwi
3   Post Graduate Program of Conservative Dentistry Specialist, Faculty of Dental Medicine, Universitas Airlangga, Surabaya, Indonesia
,
Maria Margaretha S. Nogo Masa
3   Post Graduate Program of Conservative Dentistry Specialist, Faculty of Dental Medicine, Universitas Airlangga, Surabaya, Indonesia
,
Ernie Maduratna Setiawatie
4   Department of Periodontics, Faculty of Dental Medicine, Universitas Airlangga, Surabaya, Indonesia
,
Sri Kunarti 
2   Department of Conservative Dentistry, Faculty of Dental Medicine, Universitas Airlangga, Surabaya, Indonesia
› Author Affiliations Funding This study was supported by a grant from the Ministry of Research and Technology, Republic of Indonesia, No. B/112/E3/RA.00/2021.
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Abstract

Objectives Surgical endodontics (hemisection) commonly involves the alveolar bone socket and the periradicular tissue. In today's era, optimizing the bone healing process is updated by using bone graft induction. This study explores the mechanisms of bone healing of the alveolar bone socket post-dental extraction of Wistar rats after administration of a bovine tooth graft (hydroxyapatite bovine tooth graft [HAp-BTG]).

Materials and Methods Fifty Wistar rats were randomly selected into two groups, control and treatment, and into five subgroups on days 3, 7, 14, 21, and 28. The postextraction socket was filled with polyethylene glycol (PEG) as the control and PEG + HAp-BTG as the treatment group. On days 3, 7, 14, 21, and 28, Wistar rats were sacrificed, mandibles were taken, paraffin blocks were made, cut 4 µm thick, and made into glass preparations for microscopic examination. The variable analysis was performed by staining hematoxylin-eosin for osteoblasts (OBs) and osteoclasts (OCs) and immunohistochemistry for runt-related transcription factor 2 (RUNX2), osterix (OSX), osteocalcin (OCN), bone morphogenic protein (BMP) 2. We analyzed the expressed cell count per microscope field.

Results In general, the number of cell expressions in the treatment group was significantly higher and faster, except for significantly lower OC. The high variables peak occurred on day 14 for RUNX2 and OCN, on day 7 for OSX, while OB significantly increased on day 21 and remained until day 28. The decrease of OC cells occurred on day 7 and remained low until 28 days. BMP2 was first dominantly induced by HAp-BTG, then the others.

Conclusion HAp-BTG can induce higher and faster bone healing biomarkers. BMP2 is the dominant first impacted. On the 28th day, it did not significantly express the suppression of OC by OB, which entered the bone formation and remodeling step.

Keywords

hydroxyapatite bovine tooth graft - osteogenesis - osteoblast - osteoclast - dental health

Authors' Contributions

Conceptualization: N.Z., S.K., E.M.S.; Data analysis: N.Z., S.K., E.M.S.; Data collection: N.Z.; Writing draft preparation: N.Z., S.K., E.M.S.; Draft editing and references: N.Z., S.K., E.M.S., D.D.P., M.M.S.N.M; Final writing and editing: N.Z., S.K., E.M.S., D.D.P., M.M.S.N.M.; Funding application: N.Z.; All authors agreed to the published final version.


Institutional Review Board Statement

The study was approved by the Ethical Committee, Faculty of Dental Medicine, Universitas Airlangga, No. 348/HRECC.FODM/VII/2020.


Informed Consent Statement

Not applicable.


Data Availability Statement

The data of this study are available from the corresponding author on request.




Publication History

Article published online:
28 October 2022

© 2022. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Venkataraman N, Bansal S, Bansal P, Narayan S. Dynamics of bone graft healing around implants. J Int Clin Dent Res Organ 2015; 7 (03) 40
    CrossrefSearch in Google Scholar
  • 2 Kamadjaja MJ, Tumali BA, Laksono H. et al. Effect of socket preservation using crab shell-based hydroxyapatite in Wistar rats. Recent Adv Biol Med 2020; 6 (02) 1-9
    CrossrefSearch in Google Scholar
  • 3 Patel A. Updates and practical guide on antifungal agents Updates and Practical Guide on Antifungal Agents. Presented in MMTN, Vietnam Conference, Ho Chi Minh City , 1–3 Dec (2017)
  • 4 Titsinides S, Agrogiannis G, Karatzas T. Bone grafting materials in dentoalveolar reconstruction: a comprehensive review. Jpn Dent Sci Rev 2019; 55 (01) 26-32
    CrossrefPubMedSearch in Google Scholar
  • 5 Widhiartini IAA, Wirasuta IMAG, Sukrama DM, Rai IBN. Therapeutic drug monitoring of rifampicin, isoniazid, and pyrazinamide in newly-diagnosed pulmonary tuberculosis outpatients in Denpasar area. Bali Med J. 2019; 8 (01) 107-113
    CrossrefSearch in Google Scholar
  • 6 Sotto Maior BS, Senna PM, Aarestrup BJV, Ribeiro RA, De Souza Picorelli Assis NM, Del Bel Cury AA. Effect of bovine hydroxyapatite on early stages of bone formation. Rev Odonto Ciênc 2011; 26 (03) 198-202
    CrossrefSearch in Google Scholar
  • 7 Khanijou M, Seriwatanachai D, Boonsiriseth K. et al. Bone graft material derived from extracted tooth: a review literature. J Oral Maxillofac Surg Med Pathol 2019; 31 (01) 1-7
    CrossrefSearch in Google Scholar
  • 8 Kumar P, Vinitha B, Fathima G. Bone grafts in dentistry. J Pharm Bioallied Sci 2013; 5 (Suppl. 01) S125-S127
    CrossrefPubMedSearch in Google Scholar
  • 9 Sousa SB, Castro-Silva II, Da Rocha Coutinho LAC, Lenharo A, Granjeiro JM. Osteoconduction and bioresorption of bone allograft versus anorganic bovine bone xenograft: a histomorphometric study in humans. J Biomim Biomater Tissue Eng 2013; 18 (01) 85-95
    CrossrefSearch in Google Scholar
  • 10 Kim YK, Lee J, Um IW. et al. Tooth-derived bone graft material. J Korean Assoc Oral Maxillofac Surg 2013; 39 (03) 103-111
    CrossrefPubMedSearch in Google Scholar
  • 11 Takahashi I, Nishimura M, Onodera K. et al. Expression of MMP-8 and MMP-13 genes in the periodontal ligament during tooth movement in rats. J Dent Res 2003; 82 (08) 646-651
    CrossrefPubMedSearch in Google Scholar
  • 12 Murata M. Collagen biology for bone regenerative surgery. J Korean Assoc Oral Maxillofac Surg 2012; 38 (06) 321
    CrossrefSearch in Google Scholar
  • 13 Bae SE, Choi J, Joung YK, Park K, Han DK. Controlled release of bone morphogenetic protein (BMP)-2 from nanocomplex incorporated on hydroxyapatite-formed titanium surface. J Control Release 2012; 160 (03) 676-684
    CrossrefPubMedSearch in Google Scholar
  • 14 Wu S, Xiao Z, Song J, Li M, Li W. Evaluation of BMP-2 enhances the osteoblast differentiation of human amnion mesenchymal stem cells seeded on nano-hydroxyapatite/ collagen/poly(L-lactide). Int J Mol Sci 2018; 19 (08) E2171
    CrossrefPubMedSearch in Google Scholar
  • 15 Liu TM, Lee EH. Transcriptional regulatory cascades in Runx2-dependent bone development. Tissue Eng Part B Rev 2013; 19 (03) 254-263
    CrossrefPubMedSearch in Google Scholar
  • 16 Kamadjaja DB, Abidin ZZ, Diana R. et al. In vivo analyses of osteogenic activity and bone regeneration capacity of demineralized freeze-dried bovine bone xenograft: a potential candidate for alveolar bone fillers. Int J Dent 2021; 2021: 1724374
    CrossrefPubMedSearch in Google Scholar
  • 17 Nampo T, Watahiki J, Enomoto A. et al. A new method for alveolar bone repair using extracted teeth for the graft material. J Periodontol 2010; 81 (09) 1264-1272
    CrossrefPubMedSearch in Google Scholar
  • 18 Catros S, Molenberg A, Freilich M, Dard M. Evaluation of a polyethylene glycol-osteogenic protein-1 system on alveolar bone regeneration in the mini-pig. J Oral Implantol 2015; 41 (04) e96-e101
    CrossrefPubMedSearch in Google Scholar
  • 19 Thiele W, Kyjacova L, Köhler A, Sleeman JP. A cautionary note: toxicity of polyethylene glycol 200 injected intraperitoneally into mice. Lab Anim 2020; 54 (04) 391-396
    CrossrefPubMedSearch in Google Scholar
  • 20 Saskianti T, Nugraha AP, Prahasanti C, Ernawati DS, Suardita K, Riawan W. Immunohistochemical analysis of stem cells from human exfoliated deciduous teeth seeded in carbonate apatite scaffold for the alveolar bone defect in Wistar rats ( Rattus novergicus). F1000 Res 2020; 9: 1164
    CrossrefPubMedSearch in Google Scholar
  • 21 Kresnoadi U, Widjaja J, Laksono H. Ethanol extract of propolis-bovine bone graft combination as a prospective candidate for socket preservation: enhancing BMP7 and decreasing NFATc1. Saudi Dent J 2021; 33 (08) 1055-1062
    CrossrefPubMedSearch in Google Scholar
  • 22 Thahir H, Oktawati S, Gani A. et al. The effectiveness bone graft of snakehead fish bones (Channa striata) in the gelatin form on the osteocalcin (ocn) expressions. Int J Pharm Res 2020; 12 (02) 4365-4369
    Search in Google Scholar
  • 23 Mohammadi M, Mousavi Shaegh SA, Alibolandi M. et al. Micro and nanotechnologies for bone regeneration: recent advances and emerging designs. J Control Release 2018; 274 (January): 35-55
    CrossrefPubMedSearch in Google Scholar
  • 24 Listari KM, Ruhadi I, Ulfa N. Ekspresi rankl pada defek tulang dengan pemberian xenograft dibandingkan dengan xenograft dan PRF. E-Prodenta J Dent 2019; 3 (01) 216-224
    CrossrefSearch in Google Scholar
  • 25 Nosho S, Tosa I, Ono M. et al. Distinct osteogenic potentials of BMP-2 and FGF-2 in extramedullary and medullary microenvironments. Int J Mol Sci 2020; 21 (21) 1-14
    CrossrefPubMedSearch in Google Scholar
  • 26 James AW. Review of signaling pathways governing MSC osteogenic and adipogenic differentiation. Scientifica (Cairo) 2013; 2013: 684736
    PubMedSearch in Google Scholar
  • 27 Komori T. Regulation of proliferation, differentiation and functions of osteoblasts by runx2. Int J Mol Sci 2019; 20 (07) E1694
    CrossrefPubMedSearch in Google Scholar
  • 28 Nakashima K, Zhou X, Kunkel G. et al. The novel zinc finger-containing transcription factor osterix is required for osteoblast differentiation and bone formation. Cell 2002; 108 (01) 17-29
    CrossrefPubMedSearch in Google Scholar
  • 29 Tsai MT, Lin YS, Chen WC, Ho CH, Huang HL, Hsu JT. Runx2 and osterix gene expression in human bone marrow stromal cells are mediated by far-infrared radiation. Proc World Congr Eng 2011, WCE 2011 2011; 3: 2690-2694
    Search in Google Scholar
  • 30 Liu Q, Li M, Wang S, Xiao Z, Xiong Y, Wang G. Recent advances of osterix transcription factor in osteoblast differentiation and bone formation. Front Cell Dev Biol 2020; 8 (December): 601224
    CrossrefPubMedSearch in Google Scholar
  • 31 Rupani A, Balint R, Cartmell SH. Osteoblasts and their applications in bone tissue engineering. Cell Health Cytoskelet 2012; 4: 49-61
    Search in Google Scholar
  • 32 Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 2006; 8: 455-498
    CrossrefPubMedSearch in Google Scholar
  • 33 Salazar VS, Gamer LW, Rosen V. BMP signalling in skeletal development, disease and repair. Nat Rev Endocrinol 2016; 12 (04) 203-221
    CrossrefPubMedSearch in Google Scholar
  • 34 Komori T. Regulation of osteoblast and odontoblast differentiation by RUNX2. J Oral Biosci 2010; 52 (01) 22-25
    CrossrefSearch in Google Scholar
  • 35 Gomathi K, Akshaya N, Srinaath N, Moorthi A, Selvamurugan N. Regulation of Runx2 by post-translational modifications in osteoblast differentiation. Life Sci 2020; 245 (January): 117389
    CrossrefPubMedSearch in Google Scholar
  • 36 Piao M, Lee SH, Kim MJ, Kim HS, Lee KY. YY2 promotes osteoblast differentiation by upregulating osterix transcriptional activity. Int J Mol Sci 2022; 23 (08) 2-13
    CrossrefPubMedSearch in Google Scholar
  • 37 Glowacki J, Rey C, Glimcher MJ, Cox KA, Lian J. A role for osteocalcin in osteoclast differentiation. J Cell Biochem 1991; 45 (03) 292-302
    CrossrefPubMedSearch in Google Scholar
  • 38 Teitelbaum SL. Bone remodeling and the osteoclast. J Bone Miner Res 1993; 8 (Suppl. 02) S523-S525
    PubMedSearch in Google Scholar
  • 39 Schell H, Lienau J, Epari DR. et al. Osteoclastic activity begins early and increases over the course of bone healing. Bone 2006; 38 (04) 547-554
    CrossrefPubMedSearch in Google Scholar
  • 40 Komori T. Functions of osteocalcin in bone, pancreas, testis, and muscle. Int J Mol Sci 2020; 21 (20) 1-15
    CrossrefPubMedSearch in Google Scholar