The role of the angiogenic properties in bone augmentation materials

doi:10.12337/zgkqzzxzz.2024.04.010

Abstract

Abstract: Bone augmentation is a necessary method to solve the problem of insufficient bone in implant therapy. One of the keys to the success of bone augmentation is that the bone augmentation material should be capable of angiogenesis, forming a network for effective blood-oxygen exchange with the host tissue. In this paper, we review the progress and shortcomings of different bone grafting materials on the properties of angiogenesis, and provide suggestions and references for promoting research and development in bone augmentation materials and their clinical translation.

Key words: Bone augmentation materials, Angiogenesis, Tissue engineering

Liao Hongbing, Mai Yuying. The role of the angiogenic properties in bone augmentation materials[J]. Chinese Journal of Oral Implantology, 2024, 29(2): 150-158.

References

[1] Minabe M.A critical review of the biologic rationale for guided tissue regeneration[J]. J Periodontol, 1991,62(3):171-179. DOI: 10.1902/jop.1991.62.3.171.
[2] Wang HL, Boyapati L."PASS" principles for predictable bone regeneration[J]. Implant Dent, 2006,15(1):8-17. DOI: 10.1097/01.id.0000204762.39826.0f.
[3] Hu K, Olsen BR.Osteoblast-derived VEGF regulates osteoblast differentiation and bone formation during bone repair[J]. J Clin Invest, 2016,126(2):509-526. DOI: 10.1172/JCI82585.
[4] Duan X, Bradbury SR, Olsen BR, et al. VEGF stimulates intramembranous bone formation during craniofacial skeletal development[J]. Matrix Biol, 2016,52-54:127-140. DOI: 10.1016/j.matbio.2016.02.005.
[5] Liu Y, Berendsen AD, Jia S, et al.Intracellular VEGF regulates the balance between osteoblast and adipocyte differentiation[J]. J Clin Invest, 2012,122(9):3101-3113. DOI: 10.1172/JCI61209.
[6] Ozaki A, Tsunoda M, Kinoshita S, et al.Role of fracture hematoma and periosteum during fracture healing in rats: interaction of fracture hematoma and the periosteum in the initial step of the healing process[J]. J Orthop Sci, 2000,5(1):64-70. DOI: 10.1007/s007760050010.
[7] Kolar P, Schmidt-Bleek K, Schell H, et al.The early fracture hematoma and its potential role in fracture healing[J]. Tissue Eng Part B Rev, 2010,16(4):427-434. DOI: 10.1089/ten.TEB.2009.0687.
[8] Jamalpoor Z, Asgari A, Lashkari MH, et al.Modulation of macrophage polarization for bone tissue engineering applications[J]. Iran J Allergy Asthma Immunol, 2018,17(5):398-408.
[9] Spiller KL, Anfang RR, Spiller KJ, et al.The role of macrophage phenotype in vascularization of tissue engineering scaffolds[J]. Biomaterials, 2014,35(15):4477-4488. DOI: 10.1016/j.biomaterials.2014.02.012.
[10] Graney PL, Ben-Shaul S, Landau S, et al. Macrophages of diverse phenotypes drive vascularization of engineered tissues[J]. Sci Adv, 2020,6(18):eaay6391. DOI: 10.1126/sciadv.aay6391.
[11] Adams RH, Alitalo K.Molecular regulation of angiogenesis and lymphangiogenesis[J]. Nat Rev Mol Cell Biol, 2007,8(6):464-478. DOI: 10.1038/nrm2183.
[12] Jain RK.Molecular regulation of vessel maturation[J]. Nat Med, 2003,9(6):685-693. DOI: 10.1038/nm0603-685.
[13] Lurier EB, Dalton D, Dampier W, et al.Transcriptome analysis of IL-10-stimulated (M2c) macrophages by next-generation sequencing[J]. Immunobiology, 2017,222(7):847-856. DOI: 10.1016/j.imbio.2017.02.006.
[14] Gordillo GM, Sen CK.Revisiting the essential role of oxygen in wound healing[J]. Am J Surg, 2003,186(3):259-263. DOI: 10.1016/s0002-9610(03)00211-3.
[15] Riddle RC, Khatri R, Schipani E, et al.Role of hypoxia-inducible factor-1alpha in angiogenic-osteogenic coupling[J]. J Mol Med (Berl), 2009,87(6):583-590. DOI: 10.1007/s00109-009-0477-9.
[16] Wang Y, Wan C, Deng L, et al.The hypoxia-inducible factor alpha pathway couples angiogenesis to osteogenesis during skeletal development[J]. J Clin Invest, 2007,117(6):1616-1626. DOI: 10.1172/JCI31581.
[17] Bai Y, Bai L, Zhou J, et al.Sequential delivery of VEGF, FGF-2 and PDGF from the polymeric system enhance HUVECs angiogenesis in vitro and CAM angiogenesis[J]. Cell Immunol, 2018,323:19-32. DOI: 10.1016/j.cellimm.2017.10.008.
[18] Wu Y, Wang M, Feng H, et al.Lactate induces osteoblast differentiation by stabilization of HIF1α[J]. Mol Cell Endocrinol, 2017,452:84-92. DOI: 10.1016/j.mce.2017.05.017.
[19] Castro AB, Andrade C, Li X, et al.Impact of g force and timing on the characteristics of platelet-rich fibrin matrices[J]. Sci Rep, 2021,11(1):6038. DOI: 10.1038/s41598-021-85736-y.
[20] Kawase T.Platelet-rich plasma and its derivatives as promising bioactive materials for regenerative medicine: basic principles and concepts underlying recent advances[J]. Odontology, 2015,103(2):126-135. DOI: 10.1007/s10266-015-0209-2.
[21] Diomede F, D'Aurora M, Gugliandolo A, et al. Biofunctionalized scaffold in bone tissue repair[J]. Int J Mol Sci, 2018,19(4):1022.DOI: 10.3390/ijms19041022.
[22] Masuki H, Okudera T, Watanebe T, et al.Growth factor and pro-inflammatory cytokine contents in platelet-rich plasma (PRP), plasma rich in growth factors (PRGF), advanced platelet-rich fibrin (A-PRF), and concentrated growth factors (CGF)[J]. Int J Implant Dent, 2016,2(1):19. DOI: 10.1186/s40729-016-0052-4.
[23] Calabriso N, Stanca E, Rochira A, et al.Angiogenic properties of concentrated growth factors (CGFs): the role of soluble factors and cellular components[J]. Pharmaceutics, 2021,13(5):635.DOI: 10.3390/pharmaceutics13050635.
[24] Ferrara N.Vascular endothelial growth factor: basic science and clinical progress[J]. Endocr Rev, 2004,25(4):581-611. DOI: 10.1210/er.2003-0027.
[25] De Falco E, Porcelli D, Torella AR, et al.SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells[J]. Blood, 2004,104(12):3472-3482. DOI: 10.1182/blood-2003-12-4423.
[26] Heissig B, Hattori K, Dias S, et al.Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand[J]. Cell, 2002,109(5):625-637. DOI: 10.1016/s0092-8674(02)00754-7.
[27] Hristov M, Weber C.Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance[J]. J Cell Mol Med, 2004,8(4):498-508. DOI: 10.1111/j.1582-4934.2004.tb00474.x.
[28] Martande SS, Kumari M, Pradeep AR, et al.Platelet-rich fibrin combined with 1.2% atorvastatin for treatment of intrabony defects in chronic periodontitis: a randomized controlled clinical trial[J]. J Periodontol, 2016,87(9):1039-1046. DOI: 10.1902/jop.2016.150306.
[29] Kassolis JD, Rosen PS, Reynolds MA.Alveolar ridge and sinus augmentation utilizing platelet-rich plasma in combination with freeze-dried bone allograft: case series[J]. J Periodontol, 2000,71(10):1654-1661. DOI: 10.1902/jop.2000.71.10.1654.
[30] Wiltfang J, Schlegel KA, Schultze-Mosgau S, et al.Sinus floor augmentation with beta-tricalciumphosphate (beta-TCP): does platelet-rich plasma promote its osseous integration and degradation?[J]. Clin Oral Implants Res, 2003,14(2):213-218. DOI: 10.1034/j.1600-0501.2003.140212.x.
[31] Kim J.Utilization of autologous concentrated growth Factors (CGF) enriched bone graft matrix (sticky bone) and CGF-enriched fibrin membrane in implant dentistry[J]. J Implant Adv Clin Dent, 2015, 7(10): 11-8.
[32] Upadhayaya V, Arora A, Goyal A.Bioactive platelet aggregates: PRP, PRGF, PRF, CGF and sticky bone[J]. IOSR Journal of Dental and Medical Sciences, 2017, 16(05): 05-11.DOI:10.9790/0853-1605060511.
[33] Lourenço ES, Alves GG, de Lima Barbosa R, et al. Effects of rotor angle and time after centrifugation on the biological in vitro properties of platelet rich fibrin membranes[J]. J Biomed Mater Res B Appl Biomater, 2021,109(1):60-68. DOI: 10.1002/jbm.b.34680.
[34] Dimitriou R, Mataliotakis GI, Calori GM, et al.The role of barrier membranes for guided bone regeneration and restoration of large bone defects: current experimental and clinical evidence[J]. BMC Med, 2012,10(1):81. DOI: 10.1186/1741-7015-10-81.
[35] Caballé-Serrano J, Abdeslam-Mohamed Y, Munar-Frau A, et al.Adsorption and release kinetics of growth factors on barrier membranes for guided tissue/bone regeneration: a systematic review[J]. Arch Oral Biol, 2019,100:57-68. DOI: 10.1016/j.archoralbio.2019.02.006.
[36] Hämmerle CH, Jung RE.Bone augmentation by means of barrier membranes[J]. Periodontol 2000, 2003,33:36-53. DOI: 10.1046/j.0906-6713.2003.03304.x.
[37] Turri A, Omar O, Trobos M, et al.Modulation of gene expression and bone formation by expanded and dense polytetrafluoroethylene membranes during guided bone regeneration: an experimental study[J]. Clin Implant Dent Relat Res, 2024,26(2):266-280. DOI: 10.1111/cid.13241.
[38] Dimitriou R, Mataliotakis GI, Calori GM, et al.The role of barrier membranes for guided bone regeneration and restoration of large bone defects: current experimental and clinical evidence[J]. BMC Med, 2012,10(1):81. DOI: 10.1186/1741-7015-10-81.
[39] Liu J, Kerns DG.Mechanisms of guided bone regeneration: a review[J]. Open Dent J, 2014,8:56-65. DOI: 10.2174/1874210601408010056.
[40] Schwarz F, Rothamel D, Herten M, et al.Angiogenesis pattern of native and cross-linked collagen membranes: an immunohistochemical study in the rat[J]. Clin Oral Implants Res, 2006,17(4):403-409. DOI: 10.1111/j.1600-0501.2005.01225.x.
[41] Rothamel D, Schwarz F, Sager M, et al.Biodegradation of differently cross-linked collagen membranes: an experimental study in the rat[J]. Clin Oral Implants Res, 2005,16(3):369-378. DOI: 10.1111/j.1600-0501.2005.01108.x.
[42] Arrington ED, Smith WJ, Chambers HG, et al.Complications of iliac crest bone graft harvesting[J]. Clin Orthop Relat Res, 1996,(329):300-309. DOI: 10.1097/00003086-199608000-00037.
[43] Robertson PA, Wray AC.Natural history of posterior iliac crest bone graft donation for spinal surgery: a prospective analysis of morbidity[J]. Spine (Phila Pa 1976), 2001,26(13):1473-1476. DOI: 10.1097/00007632-200107010-00018.
[44] Silber JS, Anderson DG, Daffner SD, et al.Donor site morbidity after anterior iliac crest bone harvest for single-level anterior cervical discectomy and fusion[J]. Spine (Phila Pa 1976), 2003,28(2):134-139. DOI: 10.1097/00007632-200301150-00008.
[45] Dai Z, Shu Y, Wan C, et al.Effects of pH and thermally sensitive hybrid gels on osteogenic differentiation of mesenchymal stem cells[J]. J Biomater Appl, 2015,29(9):1272-1283. DOI: 10.1177/0885328214557904.
[46] Bexell D, Gunnarsson S, Tormin A, et al.Bone marrow multipotent mesenchymal stroma cells act as pericyte-like migratory vehicles in experimental gliomas[J]. Mol Ther, 2009,17(1):183-190. DOI: 10.1038/mt.2008.229.
[47] Davani S, Marandin A, Mersin N, et al. Mesenchymal progenitor cells differentiate into an endothelial phenotype, enhance vascular density,improve heart function in a rat cellular cardiomyoplasty model[J]. Circulation, 2003,108(Suppl 1):II253-II258. DOI: 10.1161/01.cir.0000089186.09692.fa.
[48] Kinnaird T, Stabile E, Burnett MS, et al.Local delivery of marrow-derived stromal cells augments collateral perfusion through paracrine mechanisms[J]. Circulation, 2004,109(12):1543-1549. DOI: 10.1161/01.CIR.0000124062.31102.57.
[49] Zhu W, Huang L, Li Y, et al.Exosomes derived from human bone marrow mesenchymal stem cells promote tumor growth in vivo[J]. Cancer Lett, 2012,315(1):28-37. DOI: 10.1016/j.canlet.2011.10.002.
[50] Hsiao ST, Asgari A, Lokmic Z, et al.Comparative analysis of paracrine factor expression in human adult mesenchymal stem cells derived from bone marrow, adipose, and dermal tissue[J]. Stem Cells Dev, 2012,21(12):2189-2203. DOI: 10.1089/scd.2011.0674.
[51] Chim SM, Tickner J, Chow ST, et al.Angiogenic factors in bone local environment[J]. Cytokine Growth Factor Rev, 2013,24(3):297-310. DOI: 10.1016/j.cytogfr.2013.03.008.
[52] Prasadam I, Zhou Y, Du Z, et al.Osteocyte-induced angiogenesis via VEGF-MAPK-dependent pathways in endothelial cells[J]. Mol Cell Biochem, 2014,386(1-2):15-25. DOI: 10.1007/s11010-013-1840-2.
[53] Gangopahyay A, Oran M, Bauer EM, et al.Bone morphogenetic protein receptor II is a novel mediator of endothelial nitric-oxide synthase activation[J]. J Biol Chem, 2011,286(38):33134-33140. DOI: 10.1074/jbc.M111.274100.
[54] Yang X, Liaw L, Prudovsky I, et al.Fibroblast growth factor signaling in the vasculature[J]. Curr Atheroscler Rep, 2015,17(6):509. DOI: 10.1007/s11883-015-0509-6.
[55] Phelps EA, García AJ.Engineering more than a cell: vascularization strategies in tissue engineering[J]. Curr Opin Biotechnol, 2010,21(5):704-709. DOI: 10.1016/j.copbio.2010.06.005.
[56] Kennedy OD, Herman BC, Laudier DM, et al.Activation of resorption in fatigue-loaded bone involves both apoptosis and active pro-osteoclastogenic signaling by distinct osteocyte populations[J]. Bone, 2012,50(5):1115-1122. DOI: 10.1016/j.bone.2012.01.025.
[57] Khoury F, Antoun H, Missika P.Bone augmenation in oral implantology[M]. London: Quintessence Publishing 2007.
[58] Sandino C, McErlain DD, Schipilow J, et al. The poro-viscoelastic properties of trabecular bone: a micro computed tomography-based finite element study[J]. J Mech Behav Biomed Mater, 2015,44:1-9. DOI: 10.1016/j.jmbbm.2014.12.018.
[59] Bassetti MA, Bassetti RG, Bosshardt DD.The alveolar ridge splitting/expansion technique: a systematic review[J]. Clin Oral Implants Res, 2016,27(3):310-324. DOI: 10.1111/clr.12537.
[60] 李晓梅, 鲍济波, 谢志刚. 二次骨劈开技术在下颌狭窄牙槽嵴中的应用研究[J].华西口腔医学杂志,2020,38(3):338-342. DOI: 10.7518/hxkq.2020.03.019.
[61] Coatoam GW, Mariotti A.The segmental ridge-split procedure[J]. J Periodontol, 2003,74(5):757-770. DOI: 10.1902/jop.2003.74.5.757.
[62] Mounir M, Beheiri G, El-Beialy W.Assessment of marginal bone loss using full thickness versus partial thickness flaps for alveolar ridge splitting and immediate implant placement in the anterior maxilla[J]. Int J Oral Maxillofac Surg, 2014,43(11):1373-1380. DOI: 10.1016/j.ijom.2014.05.021.
[63] Blay A, Tunchel S, Sendyk WR.Viability of autogenous bone grafts obtained by using bone collectors: histological and microbiological study[J]. Pesqui Odontol Bras, 2003,17(3):234-240. DOI: 10.1590/s1517-74912003000300007.
[64] Sun YX, Sun CL, Tian Y, et al.A comparison of osteocyte bioactivity in fine particulate bone powder grafts vs larger bone grafts in a rat bone repair model[J]. Acta Histochem, 2014,116(6):1015-1021. DOI: 10.1016/j.acthis.2014.04.004.
[65] Pearson HB, Mason DE, Kegelman CD, et al.Effects of Bone Morphogenetic Protein-2 on neovascularization during large bone defect regeneration[J]. Tissue Eng Part A, 2019,25(23-24):1623-1634. DOI: 10.1089/ten.TEA.2018.0326.
[66] Ding A, Bian YY, Zhang ZH.SP1/TGF-β1/SMAD2 pathway is involved in angiogenesis during osteogenesis[J]. Mol Med Rep, 2020,21(3):1581-1589. DOI: 10.3892/mmr.2020.10965.
[67] Benic GI, Hämmerle CH.Horizontal bone augmentation by means of guided bone regeneration[J]. Periodontol 2000, 2014,66(1):13-40. DOI: 10.1111/prd.12039.
[68] Laino L, Iezzi G, Piattelli A, et al.Vertical ridge augmentation of the atrophic posterior mandible with sandwich technique: bone block from the chin area versus corticocancellous bone block allograft--clinical and histological prospective randomized controlled study[J]. Biomed Res Int, 2014,2014:982104. DOI: 10.1155/2014/982104.
[69] Chavda S, Levin L.Human studies of vertical and horizontal alveolar ridge augmentation vomparing different types of bone graft materials: a systematic review[J]. J Oral Implantol, 2018,44(1):74-84. DOI: 10.1563/aaid-joi-D-17-00053.
[70] Betz RR.Limitations of autograft and allograft: new synthetic solutions[J]. Orthopedics, 2002,25(5 Suppl):s561-570. DOI: 10.3928/0147-7447-20020502-04.
[71] Sandhu HS, Grewal HS, Parvataneni H.Bone grafting for spinal fusion[J]. Orthop Clin North Am, 1999,30(4):685-698. DOI: 10.1016/s0030-5898(05)70120-6.
[72] Pelker RR, Friedlaender GE.Biomechanical aspects of bone autografts and allografts[J]. Orthop Clin North Am, 1987,18(2):235-239.
[73] Moest T, Frabschka J, Kesting MR, et al.Osseous ingrowth in allogeneic bone blocks applied for vertical bone augmentation: a preclinical randomised controlled study[J]. Clin Oral Investig, 2020,24(8):2867-2879. DOI: 10.1007/s00784-019-03151-0.
[74] 高寰宇, 李彦林, 肖渝, 等. 五种松质骨理化性质的比较[J].中国组织工程研究,2016,20(42):6237-6243. DOI: 10.3969/j.issn.2095-4344.2016.42.001.
[75] Lee JS, Shin HK, Yun JH, et al.Randomized clinical trial of maxillary sinus grafting using deproteinized porcine and bovine bone mineral[J]. Clin Implant Dent Relat Res, 2017,19(1):140-150. DOI: 10.1111/cid.12430.
[76] Zhao Q, Ni Y, Wei H, et al.Ion incorporation into bone grafting materials[J]. Periodontol 2000, 2023,DOI: 10.1111/prd.12533.
[77] Pezzatini S, Morbidelli L, Solito R, et al.Nanostructured HA crystals up-regulate FGF-2 expression and activity in microvascular endothelium promoting angiogenesis[J]. Bone, 2007,41(4):523-534. DOI: 10.1016/j.bone.2007.06.016.
[78] Nakamura M, Soya T, Hiratai R, et al.Endothelial cell migration and morphogenesis on silk fibroin scaffolds containing hydroxyapatite electret[J]. J Biomed Mater Res A, 2012,100(4):969-977. DOI: 10.1002/jbm.a.34046.
[79] Canuto RA, Pol R, Martinasso G, et al.Hydroxyapatite paste Ostim, without elevation of full-thickness flaps, improves alveolar healing stimulating BMP- and VEGF-mediated signal pathways: an experimental study in humans[J]. Clin Oral Implants Res, 2013,24(Suppl A100):42-48. DOI: 10.1111/j.1600-0501.2011.02363.x.
[80] Laschke MW, Witt K, Pohlemann T, et al.Injectable nanocrystalline hydroxyapatite paste for bone substitution: in vivo analysis of biocompatibility and vascularization[J]. J Biomed Mater Res B Appl Biomater, 2007,82(2):494-505. DOI: 10.1002/jbm.b.30755.
[81] Chen Y, Wang J, Zhu XD, et al.Enhanced effect of β-tricalcium phosphate phase on neovascularization of porous calcium phosphate ceramics: in vitro and in vivo evidence[J]. Acta Biomater, 2015,11:435-448. DOI: 10.1016/j.actbio.2014.09.028.
[82] Castaño O, Sachot N, Xuriguera E, et al.Angiogenesis in bone regeneration: tailored calcium release in hybrid fibrous scaffolds[J]. ACS Appl Mater Interfaces, 2014,6(10):7512-7522. DOI: 10.1021/am500885v.
[83] Yang Z, Yang Z, Ding L, et al.Self-Adhesive Hydrogel biomimetic periosteum to promote critical-size bone defect repair via synergistic osteogenesis and angiogenesis[J]. ACS Appl Mater Interfaces, 2022,14(32):36395-36410. DOI: 10.1021/acsami.2c08400.
[84] Xu C, Chang Y, Xu Y, et al.Silicon-phosphorus-nanosheets-integrated 3D-printable hydrogel as a bioactive and biodegradable scaffold for vascularized bone regeneration[J]. Adv Healthc Mater, 2022,11(6):e2101911. DOI: 10.1002/adhm.202101911.
[85] Yang B, Yin J, Chen Y, et al.2D-black-phosphorus-reinforced 3D-printed scaffolds:a stepwise countermeasure for osteosarcoma[J]. Adv Mater, 2018,30(10):1705611.DOI: 10.1002/adma.201705611.
[86] Seo JJ, Mandakhbayar N, Kang MS, et al.Antibacterial, proangiogenic, and osteopromotive nanoglass paste coordinates regenerative process following bacterial infection in hard tissue[J]. Biomaterials, 2021,268:120593. DOI: 10.1016/j.biomaterials.2020.120593.
[87] Lin Y, Xiao W, Bal BS, et al.Effect of copper-doped silicate 13-93 bioactive glass scaffolds on the response of MC3T3-E1 cells in vitro and on bone regeneration and angiogenesis in rat calvarial defects in vivo[J]. Mater Sci Eng C Mater Biol Appl, 2016,67:440-452. DOI: 10.1016/j.msec.2016.05.073.
[88] Qin H, Weng J, Zhou B, et al.Magnesium ions promote in vitro rat bone marrow stromal cell angiogenesis through notch signaling[J]. Biol Trace Elem Res, 2023,201(6):2823-2842. DOI: 10.1007/s12011-022-03364-7.
[89] Liu W, Guo S, Tang Z, et al.Magnesium promotes bone formation and angiogenesis by enhancing MC3T3-E1 secretion of PDGF-BB[J]. Biochem Biophys Res Commun, 2020,528(4):664-670. DOI: 10.1016/j.bbrc.2020.05.113.
[90] Hang R, Tian X, Qu G, et al.Exosomes derived from magnesium ion-stimulated macrophages inhibit angiogenesis[J]. Biomed Mater, 2022,17(4):045008.DOI: 10.1088/1748-605X/ac6b03.
[91] Tan Z, Zhou B, Zheng J, et al.Lithium and copper induce the osteogenesis-angiogenesis coupling of bone marrow mesenchymal stem cells via crosstalk between canonical wnt and HIF-1α signaling pathways[J]. Stem Cells Int, 2021,2021:6662164. DOI: 10.1155/2021/6662164.
[92] Liu K, Li L, Chen J, et al.Bone ECM-like 3D printing scaffold with liquid crystalline and viscoelastic microenvironment for bone regeneration[J]. ACS Nano, 2022,16(12):21020-21035. DOI: 10.1021/acsnano.2c08699.
[93] Bobbert F, Zadpoor AA.Effects of bone substitute architecture and surface properties on cell response, angiogenesis, and structure of new bone[J]. J Mater Chem B, 2017,5(31):6175-6192. DOI: 10.1039/c7tb00741h.
[94] Choi SW, Zhang Y, Macewan MR, et al.Neovascularization in biodegradable inverse opal scaffolds with uniform and precisely controlled pore sizes[J]. Adv Healthc Mater, 2013,2(1):145-154. DOI: 10.1002/adhm.201200106.
[95] Feng B, Jinkang Z, Zhen W, et al.The effect of pore size on tissue ingrowth and neovascularization in porous bioceramics of controlled architecture in vivo[J]. Biomed Mater, 2011,6(1):015007. DOI: 10.1088/1748-6041/6/1/015007.
[96] Bai F, Wang Z, Lu J, et al.The correlation between the internal structure and vascularization of controllable porous bioceramic materials in vivo: a quantitative study[J]. Tissue Eng Part A, 2010,16(12):3791-3803. DOI: 10.1089/ten.TEA.2010.0148.
[97] Wang WY, Kent RN 3rd, Huang SA, et al. Direct comparison of angiogenesis in natural and synthetic biomaterials reveals that matrix porosity regulates endothelial cell invasion speed and sprout diameter[J]. Acta Biomater, 2021,135:260-273. DOI: 10.1016/j.actbio.2021.08.038.
[98] Polo-Corrales L, Latorre-Esteves M, Ramirez-Vick JE.Scaffold design for bone regeneration[J]. J Nanosci Nanotechnol, 2014,14(1):15-56. DOI: 10.1166/jnn.2014.9127.
[99] Velasco MA, Narváez-Tovar CA, Garzón-Alvarado DA.Design, materials, and mechanobiology of biodegradable scaffolds for bone tissue engineering[J]. Biomed Res Int, 2015,2015:729076. DOI: 10.1155/2015/729076.
[100] Chung TW, Liu DZ, Wang SY, et al.Enhancement of the growth of human endothelial cells by surface roughness at nanometer scale[J]. Biomaterials, 2003,24(25):4655-4661. DOI: 10.1016/s0142-9612(03)00361-2.
[101] Wang G, Lv Z, Wang T, et al.Surface functionalization of hydroxyapatite scaffolds with MgAlEu-LDH nanosheets for high-performance bone regeneration[J]. Adv Sci (Weinh), 2022,10(1):e2204234. DOI: 10.1002/advs.202204234.