Tooth transplantation with a β-tricalcium phosphate scaffold accelerates bone formation and periodontal tissue regeneration.
bone marrow mononuclear cells
bone regeneration
periodontal tissue regeneration
scaffold
tooth transplantation
β-tricalcium phosphate
Journal
Oral diseases
ISSN: 1601-0825
Titre abrégé: Oral Dis
Pays: Denmark
ID NLM: 9508565
Informations de publication
Date de publication:
Jul 2021
Jul 2021
Historique:
revised:
17
08
2020
received:
04
04
2020
accepted:
24
08
2020
pubmed:
4
9
2020
medline:
16
6
2021
entrez:
4
9
2020
Statut:
ppublish
Résumé
Although tooth transplantation is a useful treatment option as a substitute for a missing tooth, transplantation to a narrow alveolar ridge is not feasible. In this study, we tested a tissue engineering approach simultaneously with tooth transplantation using a scaffold or a combination with cells to accelerate bone formation and periodontal tissue regeneration. Bone marrow mononuclear cells (BM-MNCs) were harvested from C57BL/6J mice. The upper first or the second molar of 3-week-old C57BL/6J mice and a β-tricalcium phosphate (β-TCP) scaffold were transplanted with BM-MNCs (MNC group) or without BM-MNCs (β-TCP group) into the thigh muscle of syngeneic mice. The tooth alone was also transplanted (control group). After 4 weeks, the transplants were harvested and analyzed. Bone volume was significantly larger in the MNC and the β-TCP groups than that in the control group, and the newly formed bone was observed on the lateral wall of the root. Compared with the control group, the MNC group showed a larger trabecular thickness and fractal dimension. This study showed accelerated bone formation and periodontal tissue regeneration when tooth transplantation was performed with a β-TCP scaffold. BM-MNCs may accelerate bone maturation, while the effect on bone formation was limited.
Substances chimiques
Calcium Phosphates
0
beta-tricalcium phosphate
0
Types de publication
Journal Article
Langues
eng
Pagination
1226-1237Subventions
Organisme : Japan Society for the Promotion of Science
ID : 17K11923
Informations de copyright
© 2020 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd. All rights reserved.
Références
Al-Khaldi, A., Eliopoulos, N., Martineau, D., Lejeune, L., Lachapelle, K., & Galipeau, J. (2003). Postnatal bone marrow stromal cells elicit a potent VEGF-dependent neoangiogenic response in vivo. Gene Therapy, 10(8), 621-629. https://doi.org/10.1038/sj.gt.3301934
Andreasen, J. O. (1976). Histometric study of healing of periodontal tissues in rats after surgical injury. I. Design of a standardized surgical procedure. Odontol Revy, 27(2), 115-130.
Andreasen, J. O. (1992). Atlas of replantation and transplantation of teeth. Philadelphia, PAWB Saunders Co.
Assmus, B., Rolf, A., Erbs, S., Elsässer, A., Haberbosch, W., Hambrecht, R., … Schächinger, V. (2010). Clinical outcome 2 years after intracoronary administration of bone marrow-derived progenitor cells in acute myocardial infarction. Circulation: Heart Failure, 3(1), 89-96. https://doi.org/10.1161/CIRCHEARTFAILURE.108.843243
Atala-Acevedo, C., Abarca, J., Martínez-Zapata, M. J., Díaz, J., Olate, S., & Zaror, C. (2017). Success rate of autotransplantation of teeth with an open apex: Systematic review and meta-analysis. Journal of Oral and Maxillofacial Surgery, 75(1), 35-50. https://doi.org/10.1016/j.joms.2016.09.010
Bauss, O., Sadat-Khonsari, R., Engelkem, W., & Kahl-Nieke, B. (2002). Results of transplanting developing third molars as part of orthodontic space management. Part 1: Clinical and radiographic results. Journal of Orofacial Orthopedics, 63(6), 483-492. https://doi.org/10.1007/s00056-002-0131-4
Beltrán, V., Lazzarini, M., Figueroa, R., Sousa, V., & Engelke, W. (2019). In situ endoscopic analysis of vascular supply and regenerated alveolar bone in β-TCP grafted and ungrafted postextraction sites before implant placement: A prospective case control study. BioMed Research International, 6(2019), 2797210. https://doi.org/10.1155/2019/2797210
Bhatt, R. A., & Rozental, T. D. (2012). Bone graft substitutes. Hand Clinics, 28(4), 457-468. https://doi.org/10.1016/j.hcl.2012.08.001
Bouxsein, M. L., Boyd, S. K., Christiansen, B. A., Guldberg, R. E., Jepsen, K. J., & Müller, R. (2010). Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. Journal of Bone and Mineral Research, 25(7), 1468-1486. https://doi.org/10.1002/jbmr.141
Brenneman, M., Sharma, S., Harting, M., Strong, R., Cox, C. S., Aronowski, J., … Savitz, S. I. (2010). Autologous bone marrow mononuclear cells enhance recovery after acute ischemic stroke in young and middle-aged rats. Journal of Cerebral Blood Flow & Metabolism, 30(1), 140-149. https://doi.org/10.1038/jcbfm.2009.198
Chamberlain, G., Fox, J., Ashton, B., & Middleton, J. (2007). Concise review: Mesenchymal stem cells: Their phenotype, differentiation capacity, immunological features, and potential for homing. Stem Cells, 25(11), 2739-2749. https://doi.org/10.1634/stemcells.2007-0197
Chang, F., Ishii, T., Yanai, T., Mishima, H., Akaogi, H., Ogawa, T., & Ochiai, N. (2008). Repair of large full-thickness articular cartilage defects by transplantation of autologous uncultured bone-marrow-derived mononuclear cells. Journal of Orthopaedic Research, 26(1), 18-26. https://doi.org/10.1002/jor.20470
Chen, Y., Wang, J., Zhu, X. D., Tang, Z. R., Yang, X., Tan, Y. F., … Zhang, X. D. (2015). Enhanced effect of β-tricalcium phosphate phase on neovascularization of porous calcium phosphate ceramics: In vitro and in vivo evidence. Acta Biomaterialia, 11, 435-448. https://doi.org/10.1016/j.actbio.2014.09.028
Du, F., Wu, H., Li, H., Cai, L., Wang, Q., Liu, X., … Cao, Y. (2017). Bone marrow mononuclear cells combined with beta-tricalcium phosphate granules for alveolar cleft repair: A 12-month clinical study. Scientific Reports, 7(1), 13773. https://doi.org/10.1038/s41598-017-12602-1
Ghanaati, S., Udeabor, S. E., Barbeck, M., Willershausen, I., Kuenzel, O., Sader, R. A., & Kirkpatrick, C. J. (2013). Implantation of silicon dioxide-based nanocrystalline hydroxyapatite and pure phase beta-tricalcium phosphate bone substitute granules in caprine muscle tissue does not induce new bone formation. Head and Face Medicine, 9, 1. https://doi.org/10.1186/1746-160X-9-1
Glatt, V., Canalis, E., Stadmeyer, L., & Bouxsein, M. L. (2007). Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. Journal of Bone and Mineral Research, 22(8), 1197-1207. https://doi.org/10.1359/jbmr.070507
Hahn, M., Vogel, M., Pompesius-Kempa, M., & Delling, G. (1992). Trabecular bone pattern factor-a new parameter for simple quantification of bone microarchitecture. Bone, 13(4), 327-330. https://doi.org/10.1016/8756-3282(92)90078-b
Henrich, D., Seebach, C., Verboket, R., Schaible, A., Marzi, I., & Bonig, H. (2018). The osteo-inductive activity of bone-marrow-derived mononuclear cells resides within the CD14+ population and is independent of the CD34+ population. European Cells and Materials, 6(35), 165-177. https://doi.org/10.22203/eCM.v035a12
Hisatome, T., Yasunaga, Y., Yanada, S., Tabata, Y., Ikada, Y., & Ochi, M. (2005). Neovascularization and bone regeneration by implantation of autologous bone marrow mononuclear cells. Biomaterials, 26(22), 4550-4556. https://doi.org/10.1016/j.biomaterials.2004.11.032
Hoggatt, J., Mohammad, K. S., Singh, P., Hoggatt, A. F., Chitteti, B. R., Speth, J. M., … Pelus, L. M. (2013). Differential stem- and progenitor-cell trafficking by prostaglandin E2. Nature, 495(7441), 365-369. https://doi.org/10.1038/nature11929
Horch, H. H., Sader, R., Pautke, C., Neff, A., Deppe, H., & Kolk, A. (2006). Synthetic, pure-phase beta-tricalcium phosphate ceramic granules (Cerasorb) for bone regeneration in the reconstructive surgery of the jaws. International Journal of Oral and Maxillofacial Surgery, 35(8), 708-713. https://doi.org/10.1016/j.ijom.2006.03.017
Hori, A., Agata, H., Takaoka, M., Tojo, A., & Kagami, H. (2016). Effect of cell seeding conditions on the efficiency of in vivo bone formation. International Journal of Oral and Maxillofacial Implants, 31, 232-239. https://doi.org/10.11607/jomi.4729
Hosoya, A., Yukita, A., Yoshiba, K., Yoshiba, N., Takahashi, M., & Nakamura, H. (2012). Two distinct processes of bone-like tissue formation by dental pulp cells after tooth transplantation. Journal of Histochemistry and Cytochemistry, 60(11), 861-873. https://doi.org/10.1369/0022155412459741
Jiang, J., Wu, X., Lin, M., Doan, N., Xiao, Y., & Yan, F. (2010). Application of autologous periosteal cells for the regeneration of class III furcation defects in beagle dogs. Cytotechnology, 62(3), 235-243. https://doi.org/10.1007/s10616-010-9284-y
Jurczyszyn, K., Kubasiewicz-Ross, P., Nawrot-Hadzik, I., Gedrange, T., Dominiak, M., & Hadzik, J. (2018). Fractal dimension analysis a supplementary mathematical method for bone defect regeneration measurement. Annals of Anatomy, 219, 83-88. https://doi.org/10.1016/j.aanat.2018.06.003
Kagami, H., Agata, H., & Tojo, A. (2011). Bone marrow stromal cells (bone marrow-derived multipotent mesenchymal stromal cells) for bone tissue engineering: Basic science to clinical translation. International Journal of Biochemistry & Cell Biology, 43(3), 286-289. https://doi.org/10.1016/j.biocel.2010.12.006
Kamihata, H., Matsubara, H., Nishiue, T., Fujiyama, S., Tsutsumi, Y., Ozono, R., … Iwasaka, T. (2001). Implantation of bone marrow mononuclear cells into ischemic myocardium enhances collateral perfusion and regional function via side supply of angioblasts, angiogenic ligands, and cytokines. Circulation, 104(9), 1046-1052. https://doi.org/10.1161/hc3501.093817
Kanda, Y. (2013). Investigation of the freely available easy-to-use software 'EZR' for medical statistics. Bone Marrow Transplantation, 48(3), 452-458. https://doi.org/10.1038/bmt.2012.244
Kang, Y., Kim, S., Bishop, J., Khademhosseini, A., & Yamg, Y. (2012). The osteogenic differentiation of human bone marrow MSCs on HUVEC-derived ECM and β-TCP scaffold. Biomaterials, 33(29), 6998-7007. https://doi.org/10.1016/j.biomaterials.2012.06.061
Kondo, N., Ogose, A., Tokunaga, K., Ito, T., Arai, K., Kudo, N., … Endo, N. (2005). Bone formation and resorption of highly purified beta-tricalcium phosphate in the rat femoral condyle. Biomaterials, 26(28), 5600-5608. https://doi.org/10.1016/j.biomaterials.2005.02.026
Kretlow, J. D., Spicer, P. P., Jansen, J. A., Vacanti, C. A., Kasper, F. K., & Mikos, A. G. (2010). Uncultured marrow mononuclear cells delivered within fibrin glue hydrogels to porous scaffolds enhance bone regeneration within critical-sized rat cranial defects. Tissue Engineering Part A, 16(23), 3555-3568. https://doi.org/10.1089/ten.TEA.2010.0471
Kuçi, Z., Kuçi, S., Zircher, S., Koller, S., Schubert, R., Bönig, H., … Bader, P. (2011). Mesenchymal stromal cells derived from CD271(+) bone marrow mononuclear cells exert potent allosuppressive properties. Cytotherapy, 13(10), 1193-1204. https://doi.org/10.3109/14653249.2011.605118
Langer, R., & Vacanti, J. P. (1993). Tissue engineering. Science, 260(5110), 920-926. https://doi.org/10.1126/science.8493529
Lee, T.-J., Jang, J., Kang, S., Bhang, S. H., Jeong, G.-J., Shin, H., … Kim, B.-S. (2014). Mesenchymal stem cell-conditioned medium enhances osteogenic and chondrogenic differentiation of human embryonic stem cells and human induced pluripotent stem cells by mesodermal lineage induction. Tissue Engineering Part A, 20(7-8), 1306-1313. https://doi.org/10.1089/ten.TEA.2013.0265
Mejàre, I., Stenlund, H., & Zelezny-Holmlund, C. (2004). Caries incidence and lesion progression from adolescence to young adulthood: A prospective 15-year cohort study in Sweden. Caries Research, 38(2), 130-141. https://doi.org/10.1159/000075937
Moorrees, C. F., Fanning, E. A., & Hunt, E. E. Jr (1963). Age variation of formation stages for ten permanent teeth. Journal of Dental Research, 42, 1490-1502. https://doi.org/10.1177/00220345630420062701
Nagori, S. A., Bhutia, O., Roychoudhury, A., & Pandey, R. M. (2014). Immediate autotransplantation of third molars: An experience of 57 cases. Oral Surgery, Oral Medicine, Oral Pathology and Oral Radiology, 118(4), 400-407. https://doi.org/10.1016/j.oooo.2014.05.011
Nasjleti, C. E., Caffesse, R. G., Castelli, W. A., & Hoke, J. A. (1975). Healing after tooth reimplantation in monkeys. A radioautographic study. Oral Surgery, Oral Medicine, Oral Pathology, 39(3), 361-375. https://doi.org/10.1016/0030-4220(75)90079-1
Ogose, A., Kondo, N., Umezu, H., Hotta, T., Kawashima, H., Tokunaga, K., … Endo, N. (2006). Biomaterials, 27(8), 1542-1549. https://doi.org/10.1016/j.biomaterials.2005.08.034
Petters, O., Schmidt, C., Thuemmler, C., Peinemann, F., Zscharnack, M., Somerson, J. S., & Schulz, R. M. (2018). Point-of-care treatment of focal cartilage defects with selected chondrogenic mesenchymal stromal cells-An in vitro proof-of-concept study. Journal of Tissue Engineering and Regenerative Medicine, 12(7), 1717-1727. https://doi.org/10.1002/term.2699
Rakhshan, V. (2015). Congenitally missing teeth (hypodontia): A review of the literature concerning the etiology, prevalence, risk factors, patterns and treatment. Dental Research Journal, 12(1), 1-13. https://doi.org/10.4103/1735-3327.150286
RATOC System Engineering Co., Ltd. 3D medical image analysis application. Retrieved from https://www.ratoc.co.jp/ENG/3diryo.html
Rohof, E. C. M., Kerdijk, W., Jansma, J., Livas, C., & Ren, Y. (2018). Autotransplantation of teeth with incomplete root formation: A systematic review and meta-analysis. Clinical Oral Investigations, 22(4), 1613-1624. https://doi.org/10.1007/s00784-018-2408-z
Ross, G. D., & Vĕtvicka, V. (1993). CR3 (CD11b, CD18): A phagocyte and NK cell membrane receptor with multiple ligand specificities and functions. Clinical and Experimental Immunology, 92, 181-184. https://doi.org/10.1111/j.1365-2249.1993.tb03377.x
Saito, M., Shimizu, H., Beppu, M., & Takagi, M. (2000). The role of beta-tricalcium phosphate in vascularized periosteum. Journal of Orthopaedic Science, 5(3), 275-282. https://doi.org/10.1007/s007760050163
Schendel, K. U., Schwartz, O., Andreasen, J. O., & Hoffmeister, B. (1990). Reinnervation of autotransplanted teeth. A histological investigation in monkeys. International Journal of Oral and Maxillofacial Surgery, 19(4), 247-249. https://doi.org/10.1016/s0901-5027(05)80403-5
Su, F., Liu, S. S., Ma, J. L., Wang, D. S., E, L. L., & Liu, H. C. (2015). Enhancement of periodontal tissue regeneration by transplantation of osteoprotegerin-engineered periodontal ligament stem cells. Stem Cell Research & Therapy, 6(1), 22. https://doi.org/10.1186/s13287-015-0023-3
Suda, S., Yang, B., Schaar, K., Xi, X., Pido, J., Parsha, K., … Savitz, S. I. (2015). Autologous bone marrow mononuclear cells exert broad effects on short- and long-term biological and functional outcomes in rodents with intracerebral hemorrhage. Stem Cells and Development, 24(23), 2756-2766. https://doi.org/10.1089/scd.2015.0107
Sun, Y., Feng, Y., & Zhang, C. (2009). The effect of bone marrow mononuclear cells on vascularization and bone regeneration in steroid-induced osteonecrosis of the femoral head. Joint Bone Spine, 76(6), 685-690. https://doi.org/10.1016/j.jbspin.2009.04.002
Tsukamoto-Tanaka, H., Ikegame, M., Takagi, R., Harada, H., & Ohshima, H. (2006). Histochemical and immunocytochemical study of hard tissue formation in dental pulp during the healing process in rat molars after tooth replantation. Cell and Tissue Research, 325(2), 219-229. https://doi.org/10.1007/s00441-005-0138-4
Uejima, S., Okada, K., Kagami, H., Taguchi, A., & Ueda, M. (2008). Bone marrow stromal cell therapy improves femoral bone mineral density and mechanical strength in ovariectomized rats. Cytotherapy, 10(5), 479-489. https://doi.org/10.1080/14653240802071616
Veronesi, F., Borsari, V., Sartori, M., Orciani, M., Mattioli-Belmonte, M., & Fini, M. (2018). The use of cell conditioned medium for musculoskeletal tissue regeneration. Journal of Cellular Physiology, 233(6), 4423-4442. https://doi.org/10.1002/jcp.26291
Vieira, A. E., Repeke, C. E., Ferreira Junior, S. D. B., Colavite, P. M., Biguetti, C. C., Oliveira, R. C., … Garlet, G. P. (2015). Intramembranous bone healing process subsequent to tooth extraction in mice: Micro-computed tomography, histomorphometric and molecular characterization. PLoS One, 10(5), e0128021. https://doi.org/10.1371/journal.pone.0128021
Wang, Y., Zhou, L., Li, C., Xie, H., Lu, Y., Wu, Y., & Liu, H. (2015). Bone marrow-derived cells homing for self-repair of periodontal tissues: a histological characterization and expression analysis. International Journal of Clinical and Experimental Pathology, 8(10), 12379-12389.
Weijs, W. L., Siebers, T. J., Kuijpers-Jagtman, A. M., Bergé, S. J., Meijer, G. J., & Borstlap, W. A. (2010). Early secondary closure of alveolar clefts with mandibular symphyseal bone grafts and beta-tri calcium phosphate (beta-TCP). International Journal of Oral and Maxillofacial Surgery, 39(5), 424-429. https://doi.org/10.1016/j.ijom.2010.02.004
Wise, J. K., Alford, A. I., Goldstein, S. A., & Stegemann, J. P. (2014). Comparison of uncultured marrow mononuclear cells and culture-expanded mesenchymal stem cells in 3D collagen-chitosan microbeads for orthopedic tissue engineering. Tissue Engineering Part A, 20(1-2), 210-224. https://doi.org/10.1089/ten.TEA.2013.0151
Yang, F., Wang, J., Hou, J., Guo, H., & Liu, C. (2012). Bone regeneration using cell-mediated responsive degradable PEG-based scaffolds incorporating with rhBMP-2. Biomaterials, 34(5), 1514-1528. https://doi.org/10.1016/j.biomaterials.2012.10.058
Yang, Y., Rossi, F. M., & Putnins, E. E. (2010). Periodontal regeneration using engineered bone marrow mesenchymal stromal cells. Biomaterials, 31(33), 8574-8582. https://doi.org/10.1016/j.biomaterials.2010.06.026