The latest study on biomimetic mineralized collagen-based bone materials for pediatric skull regeneration and repair_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LI Bo , WANG Shuo ^△ , ZHAO Yonggang ,  WANG Xiumei

State Key Laboratory of New Ceramics and Fine Processing, Key Laboratory of Advanced Materials, School of Materials Science and Engineering, Tsinghua University, Beijing, 100084, P.R.China;

Corresponding author：

WANG Xiumei, Email: wxm@mail.tsinghua.edu.cn

Keywords：

Mineralized collagen; pediatric cranioplasty; bone tissue engineering; skull defect

DOI：

10.7507/1002-1892.202009078

Video：

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Abstract Full text Figures/Tables Video References Cited by

As a worldwide challenge in the field of neurosurgery, there is no effective treatment method for pediatric skull defects repair in clinic. Currently clinical used cranioplasty materials couldn’t undergo adjustment in response to skull growth and deformation. An ideal material for pediatric cranioplasty should fulfill the requirements of achieving complete closure, good osseointegration, biodegradability and conformability, sufficient cerebral protection and optimal aesthetic, and functional restoration of calvaria. Biomimetic mineralized collagen-based bone material is a kind of material that simulates the microstructural unit of natural bone on the nanometer scale. Because of its high osteogenic activity, it is widely used in repair of all kinds of bone defects. Recently, the biomimetic mineralized collagen-based bone materials have successfully been applied for cranial regeneration and repair with satisfactory results. This review mainly introduces the characteristics of the biomimetic mineralized collagen-based bone materials, the advantages for the repair of pediatric skull defects, and the related progresses.

Citation： LI Bo, WANG Shuo, ZHAO Yonggang, WANG Xiumei. The latest study on biomimetic mineralized collagen-based bone materials for pediatric skull regeneration and repair. Chinese Journal of Reparative and Reconstructive Surgery, 2021, 35(3): 278-285. doi: 10.7507/1002-1892.202009078 Copy

1.	Rocque BG, Agee BS, Thompson EM, et al. Complications following pediatric cranioplasty after decompressive craniectomy: a multicenter retrospective study. J Neurosurg Pediatr, 2018, 22(3): 225-232.
2.	Li G, Wen L, Zhan RY, et al. Cranioplasty for patients developing large cranial defects combined with post-traumatic hydrocephalus after head trauma. Brain Inj, 2008, 22(4): 333-337.
3.	Fu L, Tang T, Miao Y, et al. Stimulation of osteogenic differentiation and inhibition of adipogenic differentiation in bone marrow stromal cells by alendronate via ERK and JNK activation. Bone, 2008, 43(1): 40-47.
4.	Honeybul S. Complications of decompressive craniectomy for head injury. J Clin Neurosci, 2010, 17(4): 430-435.
5.	Kuo JR, Wang CC, Chio CC, et al. Neurological improvement after cranioplasty-analysis by transcranial doppler ultrasonography. J Clin Neurosci, 2004, 11(5): 486-489.
6.	Lee JC, Volpicelli EJ. Bioinspired collagen scaffolds in cranial bone regeneration: From bedside to bench. Adv Healthcare Mater, 2017, 6(17): 10.1002/adhm.201700232.
7.	Uysal T, Amasyali M, Enhos S, et al. Effect of periosteal stimulation therapy on bone formation in orthopedically expanded suture in rats. Orthod Craniofac Res, 2010, 13(2): 89-95.
8.	Spetzger U, Vougioukas V, Schipper J. Materials and techniques for osseous skull reconstruction. Minim Invasive Ther Allied Technol, 2010, 19(2): 110-121.
9.	Aydin S, Kucukyuruk B, Abuzayed B, et al. Cranioplasty: Review of materials and techniques. J Neurosci Rural Pract, 2011, 2(2): 162-167.
10.	Klieverik VM, Miller KJ, Singhal A, et al. Cranioplasty after craniectomy in pediatric patients-a systematic review. Childs Nerv Syst, 2019, 35(9): 1481-1490.
11.	Salam AA, Ibbett I, Thani N. Paediatric cranioplasty: A review. Interdiscipl Neurosurg, 2018, 13: 59-65.
12.	Ellis H, Logan BM, Dixon AK. Human Sectional Anatomy. Oxford: Oxford University Press, 2008: 56.
13.	Guihard-Costa AM, Ramirez-Rozzi F. Growth of the human brain and skull slows down at about 2.5 years old. Comptes Rendus Palevol, 2004, 3(5): 397-402.
14.	Purkait R. Growth of cranial volume: an anthropometric study. J Plast Reconstr Aesthet Surg, 2011, 64(5): e115-117.
15.	Martini M, Klausing A, Lüchters G, et al. Head circumference-a useful single parameter for skull volume development in cranial growth analysis. Head Face Med, 2018, 14(1): 3-11.
16.	Joseph L, Arsalan M, David J, et al. Modelling human skull growth: a validated computational model. J R Soc Interface, 2017, 14(130): 20170202.
17.	Gosain AK, Santoro TD, Song LS, et al. Osteogenesis in calvarial defects: contribution of the dura, the pericranium, and the surrounding bone in adult versus infant animals. Plast Reconstr Surg, 2003, 112(2): 515-527.
18.	Petrie Aronin CE, Cooper JA, Sefcik LS, et al. Osteogenic differentiation of dura mater stem cells cultured in vitro on three-dimensional porous scaffolds of poly (epsilon-caprolactone) fabricated via co-extrusion and gas foaming. Acta Biomater, 2008, 4(5): 1187-1197.
19.	Debnath S, Yallowitz AR, McCormick J, et al. Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature, 2018, 562(7725): 133-139.
20.	Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials, 2006, 27(15): 2907-2915.
21.	Zhang S, Wei Q, Cheng L, et al. Effects of scan line spacing on pore characteristics and mechanical properties of porous Ti6Al4V implants fabricated by selective laser melting. Mater Des, 2014, 63: 185-193.
22.	Li X, Wei J, Aifantis KE, et al. Current investigations into magnetic nanoparticles for biomedical applications. J Biomed Mater Res A, 2016, 104(5): 1285-1296.
23.	Chung RJ, Ou KL, Tseng WK, et al. Controlled release of BMP-2 by chitosan/γ-PGA polyelectrolyte multilayers coating on titanium alloy promotes osteogenic differentiation in rat bone-marrow mesenchymal stem cells. Surface and Coatings Technology, 2016, 303: 283-288.
24.	Liu J, Mao K, Liu Z, et al. Injectable biocomposites for bone healing in rabbit femoral condyle defects. PLoS One, 2013, 8(10): e75668.
25.	Doostmohammadi A, Monshi A, Salehi R, et al. Bioactive glass nanoparticles with negative zeta potential. Ceramics International, 2011, 37(7): 2311-2316.
26.	Janković A, Eraković S, Mitrić M, et al. Bioactive hydroxyapatite/graphene composite coating and its corrosion stability in simulated body fluid. Journal of Alloys and Compounds, 2015, 624: 148-157.
27.	Deng H, Wang XM, Du C, et al. Combined effect of ion concentration and functional groups on surface chemistry modulated CaCO₃ crystallization. Cryst Eng Comm, 2012, 14(20): 6647-6653.
28.	Grant GA, Jolley M, Ellenbogen RG, et al. Failure of autologous bone-assisted cranioplasty following decompressive craniectomy in children and adolescents. J Neurosurg, 2004, 100(2 Suppl Pediatrics): 163-168.
29.	Braem A, Chaudhari A, Vivan Cardoso M, et al. Peri- and intra-implant bone response to microporous Ti coatings with surface modification. Acta Biomater, 2014, 10(2): 986-995.
30.	Niinomi M. Mechanical biocompatibilities of titanium alloys for biomedical applications. J Mech Behav Biomed Mater, 2008, 1(1): 30-42.
31.	Wu J, Xu S, Qiu Z, et al. Comparison of human mesenchymal stem cells proliferation and differentiation on poly (methyl methacrylate) bone cements with and without mineralized collagen incorporation. J Biomater Appl, 2016, 30(6): 722-731.
32.	Bykowski MR, Goldstein JA, Losee JE. Pediatric cranioplasty. Clin Plast Surg, 2019, 46(2): 173-183.
33.	Liu Y, Ma J, Zhang S. Synthesis and thermal stability of selenium-doped hydroxyapatite with different substitutions. Front Mater Sci, 2015, 9(4): 392-396.
34.	Tilley JM, Chaudhury S, Hakimi O, et al. Tenocyte proliferation on collagen scaffolds protects against degradation and improves scaffold properties. J Mater Sci Mater Med, 2012, 23(3): 823-833.
35.	Suliman S, Sun Y, Pedersen TO, et al. In vivo host response and degradation of copolymer scaffolds functionalized with nanodiamonds and bone morphogenetic protein 2. Adv Healthc Mater, 2016, 5(6): 730-742.
36.	Park SH, Gil ES, Kim HJ, et al. Relationships between degradability of silk scaffolds and osteogenesis. Biomaterials, 2010, 31(24): 6162-6172.
37.	Gajjeraman S, Narayanan K, Hao J, et al. Matrix macromolecules in hard tissues control the nucleation and hierarchical assembly of hydroxyapatite. J Biol Chem, 2007, 282(2): 1193-1204.
38.	Brugmans MM, Soekhradj-Soechit RS, van Geemen D, et al. Superior tissue evolution in slow-degrading scaffolds for valvular tissue engineering. Tissue Eng Part A, 2016, 22(1-2): 123-132.
39.	Gower LB. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem Rev, 2008, 108(11): 4551-4627.
40.	Tavafoghi M, Cerruti M. The role of amino acids in hydroxyapatite mineralization. J R Soc Interface, 2016, 13(123): 20160462.
41.	Li X, Huang Y, Zheng L, et al. Effect of substrate stiffness on the functions of rat bone marrow and adipose tissue derived mesenchymal stem cells in vitro. J Biomed Mater Res A, 2014, 102(4): 1092-1101.
42.	Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol, 2014, 32(8): 773-785.
43.	Teoh SH, Goh BT, Lim J. Three-dimensional printed polycaprolactone scaffolds for bone regeneration success and future perspective. Tissue Eng Part A, 2019, 25(13-14): 931-935.
44.	Kang HW, Lee SJ, Ko IK, et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol, 2016, 34(3): 312-319.
45.	Kim JA, Lim J, Naren R, et al. Effect of the biodegradation rate controlled by pore structures in magnesium phosphate ceramic scaffolds on bone tissue regeneration in vivo. Acta Biomater, 2016, 44: 155-167.
46.	Yao Q, Cosme JG, Xu T, et al. Three dimensional electrospun PCL/PLA blend nanofibrous scaffolds with significantly improved stem cells osteogenic differentiation and cranial bone formation. Biomaterials, 2017, 115: 115-127.
47.	Prananingrum W, Naito Y, Galli S, et al. Bone ingrowth of various porous titanium scaffolds produced by a moldless and space holder technique: an in vivo study in rabbits. Biomed Mater, 2016, 11(1): 015012.
48.	Wang XM, Cui FZ, Ge J, et al. Hierarchical structural comparisons of bones from wild-type and liliput (dtc232) gene-mutated Zebrafish. J Struct Biol, 2004, 145(3): 236-245.
49.	Zhang M, Lin W, Li S, et al. Application and effectiveness evaluation of electrostatic spinning plga-silk fibroin-collagen nerve conduits for peripheral nerve regeneration. J Nanosci Nanotechnol, 2016, 16(9): 9413-9420.
50.	Zhang W, Liao SS, Cui FZ. Hierarchical self-assembly of nano-fibrils in mineralized collagen. Chem Mater, 2003, 15(16): 3221-3226.
51.	Liao SS, Guan K, Cui FZ, et al. Lumbar spinal fusion with a mineralized collagen matrix and rhBMP-2 in a rabbit model. Spine (Phila Pa 1976), 2003, 28(17): 1954-1960.
52.	Qiu ZY, Cui Y, Tao CS, et al. Mineralized collagen: Rationale, current status, and clinical applications. Materials (Basel), 2015, 8(8): 4733-4750.
53.	Xu SJ, Qiu ZY, Wu JJ, et al. Osteogenic differentiation gene expression profiling of hMSCs on hydroxyapatite and mineralized collagen. Tissue Eng Part A, 2016, 22(1-2): 170-181.
54.	Koh JT, Zhao Z, Wang Z, et al. Combinatorial gene therapy with BMP2/7 enhances cranial bone regeneration. J Dent Res, 2008, 87(9): 845-849.
55.	Feng L, Zhang L, Cui Y, et al. Clinical evaluations of mineralized collagen in the extraction sites preservation. Regen Biomater, 2016, 3(1): 41-48.
56.	Zhu P, Masuda Y, Koumoto K. The effect of surface charge on hydroxyapatite nucleation. Biomaterials, 2004, 25(17): 3915-3921.
57.	Schilling K, Brown ST, Lammers LN. Mineralogical, nanostructural, and Ca isotopic evidence for non-classical calcium phosphate mineralization at circum-neutral pH. Geochim Cosmochim Acta, 2018, 241: 255-271.
58.	Liu X, Wang P, Chen W, et al. Human embryonic stem cells and macroporous calcium phosphate construct for bone regeneration in cranial defects in rats. Acta Biomater, 2014, 10(10): 4484-4493.
59.	Surmenev RA, Surmeneva MA, Ivanova AA. Significance of calcium phosphate coatings for the enhancement of new bone osteogenesis—a review. Acta Biomater, 2014, 10(2): 557-579.
60.	Alvares K. The role of acidic phosphoproteins in biomineralization. Connect Tissue Res, 2014, 55(1): 34-40.
61.	Viswanathan P, Ondeck MG, Chirasatitsin S, et al. 3D surface topology guides stem cell adhesion and differentiation. Biomaterials, 2015, 52: 140-147.
62.	Kilian KA, Bugarija B, Lahn BT, et al. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A, 2010, 107(11): 4872-4877.
63.	Bodhak S, Bose S, Bandyopadhyay A. Role of surface charge and wettability on early stage mineralization and bone cell-materials interactions of polarized hydroxyapatite. Acta Biomater, 2009, 5(6): 2178-2188.
64.	Chai Y, Maxson RE. Recent advances in craniofacial morphogenesis. Dev Dyn, 2006, 235(9): 2353-2375.
65.	Walters BD, Stegemann JP. Strategies for directing the structure and function of three-dimensional collagen biomaterials across length scales. Acta Biomater, 2014, 10(4): 1488-1501.
66.	Wieding J, Wolf A, Bader R. Numerical optimization of open-porous bone scaffold structures to match the elastic properties of human cortical bone. J Mech Behav Biomed Mater, 2014, 37: 56-68.
67.	Shao H, Ke X, Liu A, et al. Bone regeneration in 3D printing bioactive ceramic scaffolds with improved tissue/material interface pore architecture in thin-wall bone defect. Biofabrication, 2017, 9(2): 025003.
68.	Cui L, Liu B, Liu G, et al. Repair of cranial bone defects with adipose derived stem cells and coral scaffold in a canine model. Biomaterials, 2007, 28(36): 5477-5486.
69.	Tang D, Tare RS, Yang LY, et al. Biofabrication of bone tissue: approaches, challenges and translation for bone regeneration. Biomaterials, 2016, 83: 363-382.
70.	Kuemmerle JM, Oberle A, Oechslin C, et al. Assessment of the suitability of a new brushite calcium phosphate cement for cranioplasty—an experimental study in sheep. J Craniomaxillofac Surg, 2005, 33(1): 37-44.
71.	Wang S, Yang Y, Koons GL, et al. Tuning pore features of mineralized collagen/PCL scaffolds for cranial bone regeneration in a rat model. Mater Sci Eng C, 2020, 106: 110186.
72.	Wang S, Zhao Z, Yang Y, et al. A high-strength mineralized collagen bone scaffold for large-sized cranial bone defect repair in sheep. Regen Biomater, 2018, 5(5): 283-292.
73.	Wang S, Yang Y, Zhao Z, et al. Mineralized collagen-based composite bone materials for cranial bone regeneration in developing sheep. ACS Biomater Sci Eng, 2017, 3(6): 1092-1099.

1. Rocque BG, Agee BS, Thompson EM, et al. Complications following pediatric cranioplasty after decompressive craniectomy: a multicenter retrospective study. J Neurosurg Pediatr, 2018, 22(3): 225-232.
2. Li G, Wen L, Zhan RY, et al. Cranioplasty for patients developing large cranial defects combined with post-traumatic hydrocephalus after head trauma. Brain Inj, 2008, 22(4): 333-337.
3. Fu L, Tang T, Miao Y, et al. Stimulation of osteogenic differentiation and inhibition of adipogenic differentiation in bone marrow stromal cells by alendronate via ERK and JNK activation. Bone, 2008, 43(1): 40-47.
4. Honeybul S. Complications of decompressive craniectomy for head injury. J Clin Neurosci, 2010, 17(4): 430-435.
5. Kuo JR, Wang CC, Chio CC, et al. Neurological improvement after cranioplasty-analysis by transcranial doppler ultrasonography. J Clin Neurosci, 2004, 11(5): 486-489.
6. Lee JC, Volpicelli EJ. Bioinspired collagen scaffolds in cranial bone regeneration: From bedside to bench. Adv Healthcare Mater, 2017, 6(17): 10.1002/adhm.201700232.
7. Uysal T, Amasyali M, Enhos S, et al. Effect of periosteal stimulation therapy on bone formation in orthopedically expanded suture in rats. Orthod Craniofac Res, 2010, 13(2): 89-95.
8. Spetzger U, Vougioukas V, Schipper J. Materials and techniques for osseous skull reconstruction. Minim Invasive Ther Allied Technol, 2010, 19(2): 110-121.
9. Aydin S, Kucukyuruk B, Abuzayed B, et al. Cranioplasty: Review of materials and techniques. J Neurosci Rural Pract, 2011, 2(2): 162-167.
10. Klieverik VM, Miller KJ, Singhal A, et al. Cranioplasty after craniectomy in pediatric patients-a systematic review. Childs Nerv Syst, 2019, 35(9): 1481-1490.
11. Salam AA, Ibbett I, Thani N. Paediatric cranioplasty: A review. Interdiscipl Neurosurg, 2018, 13: 59-65.
12. Ellis H, Logan BM, Dixon AK. Human Sectional Anatomy. Oxford: Oxford University Press, 2008: 56.
13. Guihard-Costa AM, Ramirez-Rozzi F. Growth of the human brain and skull slows down at about 2.5 years old. Comptes Rendus Palevol, 2004, 3(5): 397-402.
14. Purkait R. Growth of cranial volume: an anthropometric study. J Plast Reconstr Aesthet Surg, 2011, 64(5): e115-117.
15. Martini M, Klausing A, Lüchters G, et al. Head circumference-a useful single parameter for skull volume development in cranial growth analysis. Head Face Med, 2018, 14(1): 3-11.
16. Joseph L, Arsalan M, David J, et al. Modelling human skull growth: a validated computational model. J R Soc Interface, 2017, 14(130): 20170202.
17. Gosain AK, Santoro TD, Song LS, et al. Osteogenesis in calvarial defects: contribution of the dura, the pericranium, and the surrounding bone in adult versus infant animals. Plast Reconstr Surg, 2003, 112(2): 515-527.
18. Petrie Aronin CE, Cooper JA, Sefcik LS, et al. Osteogenic differentiation of dura mater stem cells cultured in vitro on three-dimensional porous scaffolds of poly (epsilon-caprolactone) fabricated via co-extrusion and gas foaming. Acta Biomater, 2008, 4(5): 1187-1197.
19. Debnath S, Yallowitz AR, McCormick J, et al. Discovery of a periosteal stem cell mediating intramembranous bone formation. Nature, 2018, 562(7725): 133-139.
20. Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials, 2006, 27(15): 2907-2915.
21. Zhang S, Wei Q, Cheng L, et al. Effects of scan line spacing on pore characteristics and mechanical properties of porous Ti6Al4V implants fabricated by selective laser melting. Mater Des, 2014, 63: 185-193.
22. Li X, Wei J, Aifantis KE, et al. Current investigations into magnetic nanoparticles for biomedical applications. J Biomed Mater Res A, 2016, 104(5): 1285-1296.
23. Chung RJ, Ou KL, Tseng WK, et al. Controlled release of BMP-2 by chitosan/γ-PGA polyelectrolyte multilayers coating on titanium alloy promotes osteogenic differentiation in rat bone-marrow mesenchymal stem cells. Surface and Coatings Technology, 2016, 303: 283-288.
24. Liu J, Mao K, Liu Z, et al. Injectable biocomposites for bone healing in rabbit femoral condyle defects. PLoS One, 2013, 8(10): e75668.
25. Doostmohammadi A, Monshi A, Salehi R, et al. Bioactive glass nanoparticles with negative zeta potential. Ceramics International, 2011, 37(7): 2311-2316.
26. Janković A, Eraković S, Mitrić M, et al. Bioactive hydroxyapatite/graphene composite coating and its corrosion stability in simulated body fluid. Journal of Alloys and Compounds, 2015, 624: 148-157.
27. Deng H, Wang XM, Du C, et al. Combined effect of ion concentration and functional groups on surface chemistry modulated CaCO₃ crystallization. Cryst Eng Comm, 2012, 14(20): 6647-6653.
28. Grant GA, Jolley M, Ellenbogen RG, et al. Failure of autologous bone-assisted cranioplasty following decompressive craniectomy in children and adolescents. J Neurosurg, 2004, 100(2 Suppl Pediatrics): 163-168.
29. Braem A, Chaudhari A, Vivan Cardoso M, et al. Peri- and intra-implant bone response to microporous Ti coatings with surface modification. Acta Biomater, 2014, 10(2): 986-995.
30. Niinomi M. Mechanical biocompatibilities of titanium alloys for biomedical applications. J Mech Behav Biomed Mater, 2008, 1(1): 30-42.
31. Wu J, Xu S, Qiu Z, et al. Comparison of human mesenchymal stem cells proliferation and differentiation on poly (methyl methacrylate) bone cements with and without mineralized collagen incorporation. J Biomater Appl, 2016, 30(6): 722-731.
32. Bykowski MR, Goldstein JA, Losee JE. Pediatric cranioplasty. Clin Plast Surg, 2019, 46(2): 173-183.
33. Liu Y, Ma J, Zhang S. Synthesis and thermal stability of selenium-doped hydroxyapatite with different substitutions. Front Mater Sci, 2015, 9(4): 392-396.
34. Tilley JM, Chaudhury S, Hakimi O, et al. Tenocyte proliferation on collagen scaffolds protects against degradation and improves scaffold properties. J Mater Sci Mater Med, 2012, 23(3): 823-833.
35. Suliman S, Sun Y, Pedersen TO, et al. In vivo host response and degradation of copolymer scaffolds functionalized with nanodiamonds and bone morphogenetic protein 2. Adv Healthc Mater, 2016, 5(6): 730-742.
36. Park SH, Gil ES, Kim HJ, et al. Relationships between degradability of silk scaffolds and osteogenesis. Biomaterials, 2010, 31(24): 6162-6172.
37. Gajjeraman S, Narayanan K, Hao J, et al. Matrix macromolecules in hard tissues control the nucleation and hierarchical assembly of hydroxyapatite. J Biol Chem, 2007, 282(2): 1193-1204.
38. Brugmans MM, Soekhradj-Soechit RS, van Geemen D, et al. Superior tissue evolution in slow-degrading scaffolds for valvular tissue engineering. Tissue Eng Part A, 2016, 22(1-2): 123-132.
39. Gower LB. Biomimetic model systems for investigating the amorphous precursor pathway and its role in biomineralization. Chem Rev, 2008, 108(11): 4551-4627.
40. Tavafoghi M, Cerruti M. The role of amino acids in hydroxyapatite mineralization. J R Soc Interface, 2016, 13(123): 20160462.
41. Li X, Huang Y, Zheng L, et al. Effect of substrate stiffness on the functions of rat bone marrow and adipose tissue derived mesenchymal stem cells in vitro. J Biomed Mater Res A, 2014, 102(4): 1092-1101.
42. Murphy SV, Atala A. 3D bioprinting of tissues and organs. Nat Biotechnol, 2014, 32(8): 773-785.
43. Teoh SH, Goh BT, Lim J. Three-dimensional printed polycaprolactone scaffolds for bone regeneration success and future perspective. Tissue Eng Part A, 2019, 25(13-14): 931-935.
44. Kang HW, Lee SJ, Ko IK, et al. A 3D bioprinting system to produce human-scale tissue constructs with structural integrity. Nat Biotechnol, 2016, 34(3): 312-319.
45. Kim JA, Lim J, Naren R, et al. Effect of the biodegradation rate controlled by pore structures in magnesium phosphate ceramic scaffolds on bone tissue regeneration in vivo. Acta Biomater, 2016, 44: 155-167.
46. Yao Q, Cosme JG, Xu T, et al. Three dimensional electrospun PCL/PLA blend nanofibrous scaffolds with significantly improved stem cells osteogenic differentiation and cranial bone formation. Biomaterials, 2017, 115: 115-127.
47. Prananingrum W, Naito Y, Galli S, et al. Bone ingrowth of various porous titanium scaffolds produced by a moldless and space holder technique: an in vivo study in rabbits. Biomed Mater, 2016, 11(1): 015012.
48. Wang XM, Cui FZ, Ge J, et al. Hierarchical structural comparisons of bones from wild-type and liliput (dtc232) gene-mutated Zebrafish. J Struct Biol, 2004, 145(3): 236-245.
49. Zhang M, Lin W, Li S, et al. Application and effectiveness evaluation of electrostatic spinning plga-silk fibroin-collagen nerve conduits for peripheral nerve regeneration. J Nanosci Nanotechnol, 2016, 16(9): 9413-9420.
50. Zhang W, Liao SS, Cui FZ. Hierarchical self-assembly of nano-fibrils in mineralized collagen. Chem Mater, 2003, 15(16): 3221-3226.
51. Liao SS, Guan K, Cui FZ, et al. Lumbar spinal fusion with a mineralized collagen matrix and rhBMP-2 in a rabbit model. Spine (Phila Pa 1976), 2003, 28(17): 1954-1960.
52. Qiu ZY, Cui Y, Tao CS, et al. Mineralized collagen: Rationale, current status, and clinical applications. Materials (Basel), 2015, 8(8): 4733-4750.
53. Xu SJ, Qiu ZY, Wu JJ, et al. Osteogenic differentiation gene expression profiling of hMSCs on hydroxyapatite and mineralized collagen. Tissue Eng Part A, 2016, 22(1-2): 170-181.
54. Koh JT, Zhao Z, Wang Z, et al. Combinatorial gene therapy with BMP2/7 enhances cranial bone regeneration. J Dent Res, 2008, 87(9): 845-849.
55. Feng L, Zhang L, Cui Y, et al. Clinical evaluations of mineralized collagen in the extraction sites preservation. Regen Biomater, 2016, 3(1): 41-48.
56. Zhu P, Masuda Y, Koumoto K. The effect of surface charge on hydroxyapatite nucleation. Biomaterials, 2004, 25(17): 3915-3921.
57. Schilling K, Brown ST, Lammers LN. Mineralogical, nanostructural, and Ca isotopic evidence for non-classical calcium phosphate mineralization at circum-neutral pH. Geochim Cosmochim Acta, 2018, 241: 255-271.
58. Liu X, Wang P, Chen W, et al. Human embryonic stem cells and macroporous calcium phosphate construct for bone regeneration in cranial defects in rats. Acta Biomater, 2014, 10(10): 4484-4493.
59. Surmenev RA, Surmeneva MA, Ivanova AA. Significance of calcium phosphate coatings for the enhancement of new bone osteogenesis—a review. Acta Biomater, 2014, 10(2): 557-579.
60. Alvares K. The role of acidic phosphoproteins in biomineralization. Connect Tissue Res, 2014, 55(1): 34-40.
61. Viswanathan P, Ondeck MG, Chirasatitsin S, et al. 3D surface topology guides stem cell adhesion and differentiation. Biomaterials, 2015, 52: 140-147.
62. Kilian KA, Bugarija B, Lahn BT, et al. Geometric cues for directing the differentiation of mesenchymal stem cells. Proc Natl Acad Sci U S A, 2010, 107(11): 4872-4877.
63. Bodhak S, Bose S, Bandyopadhyay A. Role of surface charge and wettability on early stage mineralization and bone cell-materials interactions of polarized hydroxyapatite. Acta Biomater, 2009, 5(6): 2178-2188.
64. Chai Y, Maxson RE. Recent advances in craniofacial morphogenesis. Dev Dyn, 2006, 235(9): 2353-2375.
65. Walters BD, Stegemann JP. Strategies for directing the structure and function of three-dimensional collagen biomaterials across length scales. Acta Biomater, 2014, 10(4): 1488-1501.
66. Wieding J, Wolf A, Bader R. Numerical optimization of open-porous bone scaffold structures to match the elastic properties of human cortical bone. J Mech Behav Biomed Mater, 2014, 37: 56-68.
67. Shao H, Ke X, Liu A, et al. Bone regeneration in 3D printing bioactive ceramic scaffolds with improved tissue/material interface pore architecture in thin-wall bone defect. Biofabrication, 2017, 9(2): 025003.
68. Cui L, Liu B, Liu G, et al. Repair of cranial bone defects with adipose derived stem cells and coral scaffold in a canine model. Biomaterials, 2007, 28(36): 5477-5486.
69. Tang D, Tare RS, Yang LY, et al. Biofabrication of bone tissue: approaches, challenges and translation for bone regeneration. Biomaterials, 2016, 83: 363-382.
70. Kuemmerle JM, Oberle A, Oechslin C, et al. Assessment of the suitability of a new brushite calcium phosphate cement for cranioplasty—an experimental study in sheep. J Craniomaxillofac Surg, 2005, 33(1): 37-44.
71. Wang S, Yang Y, Koons GL, et al. Tuning pore features of mineralized collagen/PCL scaffolds for cranial bone regeneration in a rat model. Mater Sci Eng C, 2020, 106: 110186.
72. Wang S, Zhao Z, Yang Y, et al. A high-strength mineralized collagen bone scaffold for large-sized cranial bone defect repair in sheep. Regen Biomater, 2018, 5(5): 283-292.
73. Wang S, Yang Y, Zhao Z, et al. Mineralized collagen-based composite bone materials for cranial bone regeneration in developing sheep. ACS Biomater Sci Eng, 2017, 3(6): 1092-1099.

Chinese Journal of Reparative and Reconstructive Surgery

The latest study on biomimetic mineralized collagen-based bone materials for pediatric skull regeneration and repair

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