Comparison of the Bone Regenerative Capacity of Three-Dimensional Uncalcined and Unsintered Hydroxyapatite/Poly-d/l-Lactide and Beta-Tricalcium Phosphate Used as Bone Graft Substitutes

References

• Jazayeri M, Shokrgozar MA, Haghighipour N, et al. Evaluation of mechanical and chemical stimulations on osteocalcin and Runx2 expression in mesenchymal stem cells. Mol Cell Biomech. 2015;12(3):197–213. doi: 10.3970/mcb.2015.012.197.
   PubMed Web of Science ®Google Scholar
• Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: recent advances and challenges. Crit Rev Biomed Eng. 2012;40(5):363–408. doi: 10.1615/CritRevBiomedEng.v40.i5.10.
   PubMedGoogle Scholar
• Salgado AJ, Oliveira JT, Pedro AJ, Reis RL. Adult stem cells in bone and cartilage tissue engineering. Curr Stem Cell Res Ther. 2006;1(3):345–364. doi: 10.2174/157488806778226803.
   PubMedGoogle Scholar
• Kanno T, Sukegawa S, Furuki Y, et al. Overview of innovative advances in bioresorbable plate systems for oral and maxillofacial surgery. Jpn Dent Sci Rev. 2018;54(3):127–138. doi: 10.1016/j.jdsr.2018.03.003.
   PubMed Web of Science ®Google Scholar
• Kanno T, Tatsumi H, Karino M, et al. Applicability of an unsintered hydroxyapatite particles/poly-l-lactide composite sheet with tack fixation for orbital fracture reconstruction. J Hard Tissue Biol. 2016;25(3):329–334. doi: 10.2485/jhtb.25.329.
   Web of Science ®Google Scholar
• Sukegawa S, Kanno T, Koyama Y, et al. Precision of post-traumatic orbital reconstruction using unsintered hydroxyapatite particles/poly-l-lactide composite bioactive/resorbable mesh plate with and without navigation: a retrospective study. J Hard Tissue Biol. 2017;26(3):274–280. doi: 10.2485/jhtb.26.274.
   Web of Science ®Google Scholar
• Kanno T, Karino M, Yoshino A, et al. Feasibility of single folded unsintered hydroxyapatite particles/poly-l-lactide composite sheet in combined orbital floor and medial wall fracture reconstruction. J Hard Tissue Biol. 2017;26(2):237–244. doi: 10.2485/jhtb.26.237.
   Web of Science ®Google Scholar
• Sukegawa S, Kanno T, Kawai H, et al. Clinical report long-term bioresorption of bone fixation devices made from composites of unsintered hydroxyapatite particles and poly-l-lactide. J Hard Tissue Biol. 2015;24(2):219–224. doi: 10.2485/jhtb.24.219.
   Web of Science ®Google Scholar
• Sukegawa S, Kanno T, Manabe Y, et al. Biomechanical loading evaluation of unsintered hydroxyapatite/poly-l-lactide plate system in bilateral sagittal split ramus osteotomy. Materials (Basel). 2017;10(7):764. doi: 10.3390/ma10070764.
   Web of Science ®Google Scholar
• Sukegawa S, Kanno T, Shibata A, et al. Use of the bioactive resorbable plate system for zygoma and zygomatic arch replacement and fixation with modified crockett’s method for maxillectomy: a technical note. Mol Clin Oncol. 2017;7(1):47–50. doi: 10.3892/mco.2017.1269.
   PubMed Web of Science ®Google Scholar
• Sukegawa S, Kawai H, Nakano K, et al. Feasible advantage of bioactive/bioresorbable devices made of forged composites of hydroxyapatite particles and poly-L-lactide in alveolar bone augmentation: a preliminary study. Int J Med Sci. 2019;16(2):311–317. doi: 10.7150/ijms.27986.
   PubMed Web of Science ®Google Scholar
• Lewandrowski KU, Gresser JD, Wise DL, Trantolo DJ. Bioresorbable bone graft substitutes of different osteoconductivities: a histologic evaluation of osteointegration of poly (propylene glycol-co-fumaric acid)-based cement implants in rats. J Orthop Res. 2000;21:757–764. doi: 10.1016/S0142-9612(99)00179-9.
   Web of Science ®Google Scholar
• Hasegawa S, Tamura J, Neo M, et al. In vivo evaluation of a porous hydroxyapatite/poly-DL-lactide composite for use as a bone substitute. J Biomed Mater Res. 2005;75(3):567–579. doi: 10.1002/jbm.a.30460.
   Web of Science ®Google Scholar
• Pina S, Ferreira JM. Bioresorbable plates and screws for clinical applications: a review. J Health Eng. 2012;3(2):243–260. doi: 10.1260/2040-2295.3.2.243.
   Web of Science ®Google Scholar
• Saeidlou S, Huneault MA, Li H, Park CB. Poly (lactic acid) crystallization. Prog Polym Sci. 2012;37(12):1657–1677. doi: 10.1016/j.progpolymsci.2012.07.005.
   Web of Science ®Google Scholar
• Hasegawa S, Neo M, Tamura J, et al. In vivo evaluation of a porous hydroxyapatite/poly-DL- lactide composite for bone tissue engineering. J Biomed Mater Res. 2007;81(4):930–938. doi: 10.1002/jbm.a.31109.
   Web of Science ®Google Scholar
• Bai YP, Kanno T, Tatsumi H, et al. Feasibility of a three-dimensional porous uncalcined and unsintered hydroxyapatite/poly-d/l-lactide composite as a regenerative biomaterial in maxillofacial surgery. Materials (Basel). 2018;11(10):2047. doi: 10.3390/ma11102047.
   Web of Science ®Google Scholar
• Müller P, Bulnheim U, Diener A, et al. Calcium phosphate surfaces promote osteogenic differentiation of mesenchymal stem cells. J Cell Mol Med. 2007;12(1):281–291. doi: 10.1111/j.1582-4934.2007.00103.x.
   Web of Science ®Google Scholar
• Seto S, Muramatsu K, Hashimoto T, et al. A new β-tricalcium phosphate with uniform triple superporous structure as a filling material after curettage of bone tumor. Anticancer Res. 2013;33(11):5075–5082. doi:http://ar.iiarjournals.org/content/33/11/5075.short.
   PubMed Web of Science ®Google Scholar
• Jensen SS, Broggini N, Hjørting‐Hansen E, Schenk R, Buser D. Bone healing and graft resorption of autograft, an organic bovine bone and β‐tricalcium phosphate. A histologic and histomorphometric study in the mandibles of minipigs. Clin Oral Implants Res. 2006;17(3):237–243. doi: 10.1111/j.1600-0501.2005.01257.x.
   PubMed Web of Science ®Google Scholar
• Horch HH, Sader R, Pautke C, et al. Synthetic, pure-phase beta-tricalcium phosphate ceramic granules (Cerasorb®) for bone regeneration in the reconstructive surgery of the jaws. Int J Oral Maxillofac Surg. 2006;35(8):708–713. doi: 10.1016/j.ijom.2006.03.017.
   PubMed Web of Science ®Google Scholar
• Shikinami Y, Okazaki K, Saito M, et al. Bioactive and bioresorbable cellular cubic-composite scaffolds for use in bone reconstruction. J R Soc Interface. 2006;3(11):805–821. doi: 10.1098/rsif.2006.0144.
   PubMed Web of Science ®Google Scholar
• Jafari S, Morteza S, Hunger R. IHC optical density score: a new practical method for quantitative immunohistochemistry image analysis. Appl Immunohistochem Mol Morphol. 2017;25(1):e12–e13. doi: 10.1097/PAI.0000000000000370.
   PubMedGoogle Scholar
• Ja ¨Hne B. Practical handbook on image processing for scientific applications. Boca Raton: CRC Press; 1997: 76–82.
   Google Scholar
• Ruifrok AC, Johnston DA. Quantification of histochemical staining by color deconvolution. Anal Quant Cytol Histol. 2001;23(4):291–299. PMID: 11531144.
   PubMed Web of Science ®Google Scholar
• Varghese F, Bukhari AB, Malhotra R, De A. IHC profiler: an open source plugin for the quantitative evaluation and automated scoring of immunohistochemistry images of human tissue samples. PLoS One. 2014;9(5):e96801. doi: 10.1371/journal.pone.0096801.
   PubMed Web of Science ®Google Scholar
• Doube M, Kłosowski MM, Arganda-Carreras I, et al. BoneJ: free and extensible bone image analysis in image. J Bone. 2010;47(6):1076–1079. doi: 10.1016/j.bone.2010.08.023.
   PubMed Web of Science ®Google Scholar
• Dougherty R, Kunzelmann KH. Computing local thickness of 3D structures with ImageJ. Microsc Microanal. 2007;13(S02):1678–1679. doi: 10.1017/S1431927607074430.
   Google Scholar
• Hildebrand T, Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc. 1997;185(1):67–75. doi: 10.1046/j.1365-2818.1997.1340694.x.
   Web of Science ®Google Scholar
• Marsell R, Einhorn TA. The biology of fracture healing. Injury. 1984;33(6):60–82. doi: 10.1016/j.injury.2011.03.031.
   Web of Science ®Google Scholar
• Mackie EJ, Tatarczuch L, Mirams M. The skeleton: a multi-functional complex organ. The growth plate chondrocyte and endochondral ossification. J Endocrinol. 2011;211(2):109–121. doi: 10.1530/JOE-11-0048.
   PubMed Web of Science ®Google Scholar
• Nishimura R, Wakabayashi M, Hata K, et al. Osterix regulates calcification and degradation of chondrogenic matrices through matrix metalloproteinase 13 (MMP13) expression in association with transcription factor Runx2 during endochondral ossification. J Biol Chem. 2012;287(40):33179–33190. doi: 10.1074/jbc.M111.337063.
   PubMed Web of Science ®Google Scholar
• Inada M, Wang Y, Byrne MH, et al. Critical ROLES FOR COLLAGENASE-3 (MMP13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci. 2004;101(49):17192–17197. doi: 10.1073/pnas.0407788101.
   Web of Science ®Google Scholar
• 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(1):17–29. doi: 10.1016/S0092-8674(01)00622-5.
   PubMed Web of Science ®Google Scholar
• Mengshol JA, Vincenti MP, Brinckerhoff CE. IL-1 induces collagenase-3 (MMP-13) promoter activity in stably transfected chondrocytic cells: requirement for Runx-2 and activation by p38 MAPK and JNK pathways. Nucleic Acids Res. 2001;29(21):4361–4372. doi: 10.1093/nar/29.21.4361.
   PubMed Web of Science ®Google Scholar
• Kanno T, Takahashi T, Tsujisawa T, et al. Mechanical stress-mediated Runx2 activation is dependent on Ras/ERK1/2 MAPK signaling in osteoblasts. J Cell Biochem. 2007;101(5):1266–1277. doi: 10.1002/jcb.21249.
   PubMed Web of Science ®Google Scholar
• Xiao G, Jiang D, Thomas P, et al. MAPK pathways activate and phosphorylate the osteoblast-specific transcription factor, Cbfa1. J Biol Chem. 2000;275(6):4453–4459. doi: 10.1074/jbc.275.6.4453.
   PubMed Web of Science ®Google Scholar
• Deng Y, Wu S, Zhou H, et al. Effects of a miR-31, Runx2, and Satb2 regulatory loop on the osteogenic differentiation of bone mesenchymal stem cells. Stem Cells Dev. 2013;22(16):2278–2286. doi: 10.1089/scd.2012.0686.
   PubMed Web of Science ®Google Scholar
• Hauschka PV, Lian JB, Cole DE, Gundberg CM. Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiol Rev. 1989;69(3):990–1047. doi: 10.1152/physrev.1989.69.3.990.
   PubMed Web of Science ®Google Scholar
• Ketenjian AY, Arsenis C. Morphological and biochemical studies during differentiation and calcification of fracture callus cartilage. Clin Orthop Relat Res. 1975;107:266–273. doi: 10.1097/00003086-197503000-00031.
   PubMed Web of Science ®Google Scholar
• Gavaia PJ, Simes DC, Ortiz-Delgado JB, et al. Osteocalcin and matrix Gla protein in zebrafish (Danio Rerio) and senegal sole (Solea Senegalensis): comparative gene and protein expression during larval development through adulthood. Gene Expr Patterns. 2006;6(6):637–652. doi: 10.1016/j.modgep.2005.11.010.
   PubMed Web of Science ®Google Scholar
• Viegas CSB, Simes DC, Williamson MK, et al. Sturgeon osteocalcin shares structural features with matrix Gla protein: evolutionary relationship and functional implications. J Biol Chem. 2013;24:jbc–M113. doi: 10.1074/jbc.M113.450213.
   Web of Science ®Google Scholar
• Hartmann C. Transcriptional networks controlling skeletal development. Curr Opin Genet Dev. 2009;19(5):437–443. doi: 10.1016/j.gde.2009.09.001.
   PubMed Web of Science ®Google Scholar
• Long F. Building strong bones: molecular regulation of the osteoblast lineage. Nat Rev Mol Cell Biol. 2012;13(1):27–38. doi: 10.1038/nrm3254.
   Web of Science ®Google Scholar
• Santo VE, Gomes ME, Mano JF, Reis RL. Controlled release strategies for bone, cartilage, and osteochondral engineering — part I: recapitulation of native tissue healing and variables for the design of delivery systems. Tissue Eng Part B Rev. 2013;19(4):308–326. doi: 10.1089/ten.teb.2012.0138.
   PubMed Web of Science ®Google Scholar
• Thompson EM, Matsiko A, Farrell E, Kelly DJ, O'Brien FJ. Recapitulating endochondral ossification: a promising route to in vivo bone regeneration. J Tissue Eng Regen Med. 2015;9(8):889–902. doi: 10.1002/term.1918.
   PubMed Web of Science ®Google Scholar
• Akagi H, Ochi H, Soeta S, et al. A comparison of the process of remodeling of hydroxyapatite/poly-d/l-lactide and beta-tricalcium phosphate in a loading site. Biomed Res Int. 2015;2015:1. doi: 10.1155/2015/730105.
   Web of Science ®Google Scholar
• Kondo N, Ogose A, Tokunaga K, et al. Osteoinduction with highly purified b -tricalcium phosphate in dog dorsal muscles and the proliferation of osteoclasts before heterotopic bone formation. Biomaterials. 2006;27(25):4419–4427. doi: 10.1016/j.biomaterials.2006.04.016.
   PubMed Web of Science ®Google Scholar
• Xiao X, Wang W, Liu D, et al. The promotion of angiogenesis induced by three-dimensional porous beta-tricalcium phosphate scaffold with different interconnection sizes via activation of PI3K/Akt pathways. Sci Rep. 2015;5:9409. doi: 10.1038/srep09409.
   PubMed Web of Science ®Google Scholar
• Tsuruga E, Takita H, Itoh H, Wakisaka Y, Kuboki Y. Pore size of porous hydroxyapatite as the controls EMP-induced osteogenesis. J Biochem. 1997;121(2):317–324. doi: 10.1093/oxfordjournals.jbchem.a021589.
   PubMed Web of Science ®Google Scholar
• Engler AJ, Sen S, Sweeney HL, Discher DE. Matrix elasticity directs stem cell lineage specification. Cell. 2006;12(4):677–689. doi: 10.1016/j.cell.2006.06.044.
   Web of Science ®Google Scholar
• Kelly DJ, Jacobs CR. The role of mechanical signals in regulating chondrogenesis and osteogenesis of mesenchymal stem cells. Birth Defect Res C. 2010;90(1):75–85. doi: 10.1002/bdrc.20173.
   PubMed Web of Science ®Google Scholar
• Bian L, Hou C, Tous E, Rai R, Mauck RL, Burdick JA. The influence of hyaluronic acid hydrogel crosslinking density and macromolecular diffusivity on human MSC chondrogenesis and hypertrophy. Biomaterials. 2013;34(2):413–421. doi: 10.1016/j.biomaterials.2012.09.052.
   PubMed Web of Science ®Google Scholar
• Maquet V, Boccaccini AR, Pravata L, Notingher I, JérôMe R, Preparation, characterization, and in vitro degradation of bioresorbable and bioactive composites based on Bioglass®-filled polylactide foams. J Biomed Mater Res. 2003;66(2):335–346. doi: 10.1002/jbm.a.10587.
   Web of Science ®Google Scholar
• Sha J, Kanno T, Miyamoto K, Bai Y, Hideshima K, Matsuzaki Y. Application of a bioactive/bioresorbable three-dimensional porous uncalcined and unsintered hydroxyapatite/poly-d/l-lactide composite with human mesenchymal stem cells for bone regeneration in maxillofacial surgery: a pilot animal study. Materials. 2019;12(5):705. doi: 10.3390/ma12050705.
   Web of Science ®Google Scholar