Revascularization and angiogenesis for bone bioengineering in the craniofacial region: a review.
Bioengineering
Ischemia–reperfusion injuries
Mesenchymal stromal cells
Neovascularization
Reconstructive surgery
Revascularization
Journal
Journal of materials science. Materials in medicine
ISSN: 1573-4838
Titre abrégé: J Mater Sci Mater Med
Pays: United States
ID NLM: 9013087
Informations de publication
Date de publication:
30 May 2023
30 May 2023
Historique:
received:
12
12
2022
accepted:
17
04
2023
medline:
1
6
2023
pubmed:
30
5
2023
entrez:
30
5
2023
Statut:
epublish
Résumé
The revascularization of grafted tissues is a complicated and non-straightforward process, which makes it challenging to perform reconstructive surgery for critical-sized bone defects. This challenge is combined with the low vascularity that results from radiotherapy. This low vascularity could result from ischemia-reperfusion injuries, also known as ischemia which may happen upon grafting. Ischemia may affect the hard tissue during reconstruction, and this can often cause resorption, infections, disfigurement, and malunion. This paper therefore reviews the clinical and experimental application of procedures that were employed to improve the reconstructive surgery process, which would ensure that the vascularity of the tissue is maintained or enhanced. It also presents the key strategies that are implemented to perform tissue engineering within the grafted sites aiming to optimize the microenvironment and to enhance the overall process of neovascularization and angiogenesis. This review reveals that the current strategies, according to the literature, are the seeding of the mature and progenitor cells, use of extracellular matrix (ECM), co-culturing of osteoblasts with the ECM, growth factors and the use of microcapillaries incorporated into the scaffold design. However, due to the unstable and regression-prone capillary structures in bone constructs, further research focusing on creating long-lasting and stable blood vessels is required.
Identifiants
pubmed: 37249725
doi: 10.1007/s10856-023-06730-6
pii: 10.1007/s10856-023-06730-6
pmc: PMC10229479
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
30Subventions
Organisme : Deanship of Scientific Research, King Saud University
ID : RG-1439-062.
Informations de copyright
© 2023. The Author(s).
Références
Kang N, Hai Y, Liang F, Gao C-J, Liu X-H. Preconditioned hyper-baric oxygenation protects skin flap grafts in rats against ische-mia/reperfusion injury. Mol Med Rep. 2014;9:2124–30. https://doi.org/10.3892/mmr.2014.2064
doi: 10.3892/mmr.2014.2064
Hankenson KD, Dishowitz M, Gray C, Schenker M. Angiogenesis in bone regeneration. Injury. 2011;42:556–61. https://doi.org/10.1016/j.injury.2011.03.035
doi: 10.1016/j.injury.2011.03.035
Bauer SM, Bauer RJ, Velazquez OC. Angiogenesis, vasculogenesis, and induction of healing in chronic wounds. Vasc Endovasc Surg. 2005;39:293.
Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653–60.
Velazquez OC. Angiogenesis and vasculogenesis: Inducing the growth of new blood vessels and wound healing by stimulation of bone marrow-derived progenitor cell mobilization and homing. J Vasc Surg. 2007;45(Suppl. A):A39–A47.
Chung AS, Lee J, Ferrara N. Targeting the tumour vasculature: Insights from physiological angiogenesis. Nat Rev Cancer. 2010;10:505–14.
Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005;438:932–6.
Hirschi and Goodell. Common origins of blood and blood vessels in adults. Differentiation. 2001;68:186–92.
Barros JW, Barbieri CH, Fernandes CD. Scintigraphic evaluation of tibial shaft fracture healing. Injury. 2000;31:51–54.
Vunjak-Novakovic G, Kaplan DL. Tissue engineering: the next generation. Tissue Eng. 2005;12:3261–3.
Zura R, Xiong Z, Einhorn T, Watson JT, Ostrum RF, Prayson MJ, et al. Epidemiology of fracture nonunion in 18 human bones. JAMA Surg. 2016;151:e162775. https://doi.org/10.1001/jamasurg.2016.2775
doi: 10.1001/jamasurg.2016.2775
Jeffcoach DR, Sams VG, Lawson CM, Enderson BL, Smith ST, Kline H, et al. Nonsteroidal anti-inflammatory drugs’ impact on nonunion and infection rates in long-bone fractures. J Trauma Acute Care Surg. 2014;76:779–83. https://doi.org/10.1097/TA.0b013e3182aafe0d
doi: 10.1097/TA.0b013e3182aafe0d
Irwin TJ, Orgill D. Closed incision negative pressure wound therapy after resection of large, radiated, soft tissue sarcomas. Cureus. 2020;12:e8055. https://doi.org/10.7759/cureus.8055
doi: 10.7759/cureus.8055
Pak CS, Moon SY, Lee YE, Kang HJ. Therapeutic effects against tissue necrosis of remote ischemic preconditioning combined with human adipose-derived stem cells in random-pattern skin flap rat models. J Investig Surg. 2020;34:1304–11. https://doi.org/10.1080/08941939.2020.1795750
doi: 10.1080/08941939.2020.1795750
Warnke PH, Wiltfang J, Springer I, Acil Y, Bolte H, Kosmahl M, et al. Man as living bioreactor: fate of an exogenously prepared customized tissue-engineered mandible. Biomaterials. 2006;27:3163–7.
Heliotis M, Lavery KM, Ripamonti U, Tsiridis E, di Silvio L. Transformation of a prefabricated hydroxyapatite/osteogenic protein-1 implant into a vascularised pedicled bone flap in the human chest. Int J Oral Maxillofac Surg. 2006;35:265–9.
Evans CH, Liu FJ, Glatt V, Hoyland JA, Kirker C-H, Walsh A, et al. Use of genetically modified muscle and fat grafts to repair defects in bone and cartilage. Eur Cell Mater. 2009;18:96.
Liu F, Porter RM, Wells J, Glatt V, Pilapil C, Evans CH. Evaluation of BMP-2 gene-activated muscle grafts for cranial defect repair. J Orthop Res. 2012;30:1095.
Alfotawi R, Alfayez M, Mahmood A. In situ tissue engineering using an induced muscle graft to reconstruct critical size bone defect. J Biomater Tissue Eng. 2017;7:1114–21.
Al-Fotawei R, Ayoub AF, Heath FN, Naudi KB, Tanner KE, Dalby MJ, et al. Radiological assessment of bio- engineered bone in a muscle flap for reconstruction of a critical-size mandibular defect. PLoS One. 2014;9:e107403.
Kolf CM, Cho E, Tuan RS. Mesenchymal stromal cells—Biology of adult mesenchymal stem cells: Regulation of niche, self-renewal and differentiation. Arthritis Res Ther. 2007;9:204.
Bauza-Mayol G, Quintela M, Brozovich A, Hopson M, Shaikh S, Cabrera F, et al. Biomimetic scaffolds modulate the post-traumatic inflammatory response in articular cartilage contributing to enhanced neoformation of cartilaginous tissue in vivo. Adv Healthc Mater. 2022;11:e2101127.
Alfotawi R, Ayoub AF, Tanner KE, Dalby M, Naudi KB, McMahon J. A novel surgical approach for the reconstruction of critical-size mandibular defects using calcium sulphate/hydroxyapatite cement, BMP-7 and Mesenchymal stem cells- Histological assessment. J Biomater Tissue Eng. 2016;6:1–6.
Porzionato A, Sfriso MM, Pontini A, Macchi V, Petrelli L, Pavan PG, et al. Decellularized human skeletal muscle as biologic scaffold for reconstructive surgery. Int J Mol Sci. 2015;16:14808–31.
Al-Fotawi R, Muthurangan M, Siyal A, Premnath S, Al-Fayez M, El-Ghannam A, et al. The use of muscle extracellular matrix (MEM) and SCPC bioceramic for bone augmentation. Biomed Mater. 2020;15:025005.
Goumans M-J, Zwijsen A, Dijke PT, Bailly S. Bone morphogenetic proteins in vascular homeostasis and disease. Cold Spring Harb Perspect Biol. 2018;10:a031989. https://doi.org/10.1101/cshperspect.a031989
doi: 10.1101/cshperspect.a031989
Zhai W, Lu H, Chen L, Lin X, Huang Y, Dai K, et al. Silicate bioceramics induce angiogenesis during bone regeneration. Acta Biomater. 2012;8:341.
Deng Y, Jiang C, Li C, Li T, Peng M, Wang J, et al. 3D printed scaffolds of calcium silicate-doped β-TCP synergize with co-cultured endothelial and stromal cells to promote vascularization and bone formation. Sci Rep. 2017;7:1–14.
Joshi A, Choudhury S, Gugulothu SB, Visweswariah SS, Chatterjee K. Strategies to promote vascularization in 3D printed tissue scaffolds: trends and challenges. Biomacromolecules. 2022;23:2730–2751.
Liu H, Du Y, Yang G, Hu X, Wang L, Liu B, et al. Delivering proangiogenic factors from 3D-printed polycaprolactone scaffolds for vascularized bone regeneration. Adv Healthc Mater. 2020;9:2000727.
Duan J, Lei D, Ling C, Wang Y, Cao Z, Zhang M, et al. Three-dimensional-printed polycaprolactone scafolds with interconnected hollow-pipe structures for enhanced bon regenertion. Regen Biomater. 2022;30:1–9.
Yan Y, Chen H, Zhang H, Guo C, Yang K, Chen K, et al. Vascularized 3D printed scaffolds for promoting bone regeneration. Biomaterials. 2019;190–191:97–110.
Wang C, Lai J, Li K, Zhu S, Lu B, Liu J, et al. Cryogenic 3D printing of dual-delivery scaffolds for improved bone regeneration with enhanced vascularization. Bioact Mater. 2020;6:137–45.
Lee S, Lee HS, Chung JJ, Kim SH, Park JW, Lee K, et al. Enhanced regeneration of vascularized adipose tissue with dual 3D-printed elastic polymer/DECM hydrogel complex. Int J Mol Sci. 2021;22:2886.
Makhoul N. Development of a microcapillary system for tissue engineering. J Oral Maxillofac Surg. 2008;66:45–46.
Zhang W, Feng C, Yang G, Li G, Ding X, Wang S, et al. 3D-printed scaffolds with synergistic effect of hollow-pipe structure and bioactive ions for vascularized bone regeneration. Biomaterials. 2017;135:85–95.
Moghadam HG, Urist MR, Sandor GK, Clokie CM. Successful mandibular reconstruction using a BMP bioimplant. J Craniofacial Surg. 2001;12:119–27.
Ferretti C, Ripamonti U. Human segmental mandibular defects treated with naturally derived bone morphogenetic proteins. J Craniofacial Surg. 2002;13:434–44.
Marx RE, Armentano L, Olavarria A, Samaniego J. rhBMP-2/ACS grafts versus autogenous cancellous marrow grafts in large vertical defects of the maxilla: an unsponsored randomized open-label clinical trial. Int J Oral Maxillofac Implants. 2013;28:e243–e251.
Chao M, Donovan T, Sotelo C, Carstens MH. In situ osteogenesis of hemimandible with rhBMP-2 in a 9-year-old boy: osteoinduction via stem cell concentration. J Craniofacial Surg. 2006;17:405–12.
Herford AS, Boyne PJ, Rawson R, Williams RP. Bone morphogenetic protein- induced regeneration of the premaxillary cleft. J Oral Maxillofac Surg. 2007;65:2136–41.
Cicciù M, Herford AS, Stoffella E, Cervino G, Cicciù D. Protein-signaled guided bone regeneration using titanium mesh and Rh-BMP2 in oral surgery: a case report involving left mandibular reconstruction after tumor resection. Open Dent J. 2012;6:51–55.
Ayoub A, Gillgrass T. The clinical application of recombinant human bone morphogenetic protein 7 for reconstruction of alveolar cleft; 10 years follow up. J Oral Maxillofac Surg. 2019;77:571–81. https://doi.org/10.1016/j.joms.2018.08.031
doi: 10.1016/j.joms.2018.08.031
Meijer GJ, de Bruijn JD, Koole R, van Blitterswijk CA. Cell based bone tissue engineering in jaw defects. Biomaterials. 2008;29:3053–61.
Jin Q, Kim H, Na J, Jin C, Seon J. Anti-infammatory effects of mesenchymal stem cell-conditioned media inhibited macrophages activation in vitro. Sci Rep. 2022;12:4754.
Claes L, Recknagel S, Ignatius A. Fracture healing under healthy and inflammatory conditions. Nat Rev Rheumatol. 2012;8:133–43.
Kang T, Jones TM, Naddell C, Bacanamwo M, Calvert JW, Thompson WE, et al. Adipose-derived stem cells induce angiogenesis via microvesicle transport of miRNA-31. Stem Cells Transl Med. 2016;5:440–50.
Razban V, Lotfi AS, Soleimani M, Ahmadi H, Massumi M, Khajeh S, et al. HIF-1α overexpression induces angiogenesis in mesenchymal stem cells. BioRes Open Access. 2012;1:174–83. https://doi.org/10.1089/biores.2012.9905
doi: 10.1089/biores.2012.9905
Kinoshita Y, Kobayashi M, Hidaka T, Ikada Y. Reconstruction of mandibular continuity defects in dogs using poly (L-lactide) mesh and autogenic particulate cancellous bone and marrow: Preliminary report. J Oral Maxillofac Surg. 1997;55:718–23.
Lee T-J, Kang S-W, Bhang SH, Kang JM, Kim B-S. Apatite-coated porous poly (lactic-co-glycolic acid) microspheres as an injectable bone substitute. J Biomater Sci Polym Ed. 2010;21:635–45.
Hernandez-Alfaro F, Ruiz-Magaz V, Chatakun P, Guijarro-Martinez R. Mandibular reconstruction with tissue engineering in multiple recurrent ameloblastoma. Int J Periodontics Restor Dent. 2012;32:e82–e86.
Zamiri B, Shahidi S, Eslaminejad MB, Khoshzaban A, Gholami M, Bahramnejad E, et al. Reconstruction of human mandibular continuity defects with allogenic scaffold and autologous marrow mesenchymal stem cells. J Craniofacial Surg. 2013;24:1292–7.
Kim BC, Yoon J-H, Choi B, Lee J. Mandibular reconstructio with autologous human bone marrow stem cells and autogenous bone graft in a patient with plexiform ameloblastoma. J Craniofacial Surg. 2013;24:e409–e411.
Wolff J, Sandor GK, Miettinen A, Tuovinen VJ, Mannerstrom B, Patrikoski M. et al. GMP-level adipose stem cells combined with computer-aided manufacturing to reconstruct mandibular ameloblastoma resection defects: Experience with three cases. Ann Maxillofac Surg. 2013;3:114–25.
Sandor GK, Tuovinen VJ, Wolff J, Patrikoski M, Jokinen J, Nieminen E, et al. Adipose stem cell tissue-engineered construct used to treat large anterior mandibular defect: a case report and review of the clinical application of good manufacturing practice- level adipose stem cells for bone regeneration. J Oral Maxillofac Surg. 2013;71:938–50.