journal article·2024-04-28

Quantifying pore characteristics in polymer glass–ceramics composite scaffolds using micro-tomography

Ashley Thomas, Ashish K. Agarwal, Y. S. Kashyap, I. Praveen Kumar, Japes Bera

Journal of Materials Research· Volume 39· Issue 8
Publisher page

Abstract

Biomaterials used in bone tissue engineering should mimic the pore characteristics and micro-architectural features of bone to facilitate successful regeneration and repair of damaged tissue in vivo. The complete qualitative and quantitative analysis of pore characteristics in tissue engineering scaffolds remains a challenge. Compared to the other traditional methods, micro-tomography is a reliable, efficient, and non-destructive technique to assess micro-architectural characteristics in scaffolds. In this study, composite scaffolds comprising natural polymers (alginate, gelatin and chitosan) reinforced with glass–ceramic powder was fabricated using the freeze-drying technique. The micro-architectural features were analyzed with quantification of different parameters—pore size, pore shape, pore orientation, pore interconnectivity and fractal analysis. The scaffolds exhibited macro-porosity with good pore architecture and connectivity. The quantification of different parameters yielded promising results and micro-tomography proves to be an efficient tool for analyzing and quantifying pore characteristics in bone tissue engineering scaffolds.Graphical abstract
Source: expertdata · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Innovations in Concrete and Construction Materials · Bone Tissue Engineering Materials · Innovative concrete reinforcement materials

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (77)

Show source-provided references
1. P.X. Ma, Scaffolds for tissue fabrication. Mater. Today 7, 30–40 (2004). https://doi.org/10.1016/S1369-7021(04)00233-010.1016/S1369-7021(04)00233-0 ↗
2. K.J.L. Burg, S. Porter, J.F. Kellam, Biomaterial developments for bone tissue engineering. Biomaterials 21, 2347–2359 (2000). https://doi.org/10.1016/S0142-9612(00)00102-210.1016/S0142-9612(00)00102-2 ↗
3. L.L. Hench, J.M. Polak, Third-generation biomedical materials. Science (80-) (2002). https://doi.org/10.1126/science.106740410.1126/science.1067404 ↗
4. A.I. Caplan, V.M. Goldberg, Principles of tissue engineered regeneration of skeletal tissues. Clin. Orthop. Relat. Res. (1999). https://doi.org/10.1097/00003086-199910001-0000310.1097/00003086-199910001-00003 ↗
5. V. Karageorgiou, D. Kaplan, Porosity of 3D biomaterial scaffolds and osteogenesis. Biomaterials 26, 5474–5491 (2005). https://doi.org/10.1016/j.biomaterials.2005.02.00210.1016/j.biomaterials.2005.02.002 ↗
6. T. Russo, A. Gloria, V. D’Antò, U. D’Amora, G. Ametrano, F. Bollino, R. De Santis, G. Ausanio, M. Catauro, S. Rengo, L. Ambrosio, Poly(ε-caprolactone) reinforced with sol-gel synthesized organic-inorganic hybrid fillers as composite substrates for tissue engineering. J. Appl. Biomater. Biomech. 8, 146–152 (2010). https://doi.org/10.5301/JABB.2010.609410.5301/JABB.2010.6094 ↗
7. A.S.P. Lin, T.H. Barrows, S.H. Cartmell, R.E. Guldberg, Microarchitectural and mechanical characterization of oriented porous polymer scaffolds. Biomaterials 24, 481–489 (2003). https://doi.org/10.1016/S0142-9612(02)00361-710.1016/S0142-9612(02)00361-7 ↗
8. V. Guarino, F. Causa, L. Ambrosio, Porosity and mechanical properties relationship in PCL porous scaffolds. J. Appl. Biomater. Biomech. 5, 149–157 (2007). https://doi.org/10.1177/22808000070050030310.1177/228080000700500303 ↗
9. J. Wu, Q. Zhao, J. Sun, Q. Zhou, Preparation of poly(ethylene glycol) aligned porous cryogels using a unidirectional freezing technique. Soft Matter 8, 3620–3626 (2012). https://doi.org/10.1039/c2sm07411g10.1039/c2sm07411g ↗
10. M. Costantini, C. Colosi, P. Mozetic, J. Jaroszewicz, A. Tosato, A. Rainer, M. Trombetta, W. Więszkowski, M. Dentini, A. Barbetta, Correlation between porous texture and cell seeding efficiency of gas foaming and microfluidic foaming scaffolds. Mater. Sci. Eng. C 62, 668–677 (2016). https://doi.org/10.1016/j.msec.2016.02.01010.1016/j.msec.2016.02.010 ↗
11. J.S. Kaiser, M. Kamperman, E.J. de Souza, B. Schick, E. Arzt, Adhesion of biocompatible and biodegradable micropatterned surfaces. Int. J. Artif. Organs 34, 180–184 (2011). https://doi.org/10.5301/IJAO.2011.639310.5301/IJAO.2011.6393 ↗
12. S. Bertoldi, S. Farè, M.C. Tanzi, Assessment of scaffold porosity: The new route of micro-CT. J. Appl. Biomater. Biomech. 9, 165–175 (2011). https://doi.org/10.5301/JABB.2011.886310.5301/JABB.2011.8863 ↗
13. M. Bartoš, T. Suchý, R. Foltán, Note on the use of different approaches to determine the pore sizes of tissue engineering scaffolds: What do we measure? Biomed. Eng. (2018). https://doi.org/10.1186/s12938-018-0543-z10.1186/s12938-018-0543-z ↗
14. F. Peyrin, Evaluation of bone scaffolds by micro-CT, in: Osteoporos. Int., 2011: pp. 2043–2048. https://doi.org/10.1007/s00198-011-1609-y.10.1007/s00198-011-1609-y ↗
15. S.T. Ho, D.W. Hutmacher, A comparison of micro CT with other techniques used in the characterization of scaffolds. Biomaterials 27, 1362–1376 (2006). https://doi.org/10.1016/j.biomaterials.2005.08.03510.1016/j.biomaterials.2005.08.035 ↗
16. J.R. Jones, R.C. Atwood, G. Poologasundarampillai, S. Yue, P.D. Lee, Quantifying the 3D macrostructure of tissue scaffolds, in: J. Mater. Sci. Mater. Med., 2009: pp. 463–471. https://doi.org/10.1007/s10856-008-3597-9.10.1007/s10856-008-3597-9 ↗
17. F. Beltrame, R. Cancedda, B. Canesi, A. Crovace, M. Mastrogiacomo, R. Quarto, S. Scaglione, C. Valastro, F. Viti, A simple non invasive computerized method for the assessment of bone repair within osteoconductive porous bioceramic grafts. Biotechnol. Bioeng. 92, 189–198 (2005). https://doi.org/10.1002/bit.2059110.1002/bit.20591 ↗
18. N. Kotobuki, K. Ioku, D. Kawagoe, H. Fujimori, S. Goto, H. Ohgushi, Observation of osteogenic differentiation cascade of living mesenchymal stem cells on transparent hydroxyapatite ceramics. Biomaterials 26, 779–785 (2005). https://doi.org/10.1016/j.biomaterials.2004.03.02010.1016/j.biomaterials.2004.03.020 ↗
19. C. Vitale-Brovarone, S. Di Nunzio, O. Bretcanu, E. Verné, Macroporous glass-ceramic materials with bioactive properties. J. Mater. Sci. Mater. Med. 15, 209–217 (2004). https://doi.org/10.1023/B:JMSM.0000015480.49061.e110.1023/B:JMSM.0000015480.49061.e1 ↗
20. D.J. Mooney, D.F. Baldwin, N.P. Suh, J.P. Vacanti, R. Langer, Novel approach to fabricate porous sponges of poly(D, L-lactic-co-glycolic acid) without the use of organic solvents. Biomaterials (1996). https://doi.org/10.1016/0142-9612(96)87284-X10.1016/0142-9612(96)87284-X ↗
21. S.G. Kumbar, C. Laurencin, M. Deng, Natural and Synthetic Biomedical Polymers (Elsevier, Amsterdam, 2014)
22. J. Sun, H. Tan, Alginate-based biomaterials for regenerative medicine applications. Materials (Basel). 6, 1285–1309 (2013). https://doi.org/10.3390/ma604128510.3390/ma6041285 ↗
23. M.C. Echave, L.S. Burgo, J.L. Pedraz, G. Orive, Gelatin as biomaterial for tissue engineering. Curr. Pharm. Des. 23, 3567–3584 (2017). https://doi.org/10.2174/092986732466617051112310110.2174/0929867324666170511123101 ↗
24. I.Y. Kim, S.J. Seo, H.S. Moon, M.K. Yoo, I.Y. Park, B.C. Kim, C.S. Cho, Chitosan and its derivatives for tissue engineering applications. Biotechnol. Adv. 26, 1–21 (2008). https://doi.org/10.1016/j.biotechadv.2007.07.00910.1016/j.biotechadv.2007.07.009 ↗
25. A.R. Boccaccini, C. Fleck, D.W. Schubert, J.A. Roether, A. Philippart, A.R. Boccaccini, C. Fleck, D.W. Schubert, J.A. Roether, Toughening and functionalization of bioactive ceramic and glass bone scaffolds by biopolymer coatings and infiltration: A review of the last 5 years. Expert Rev. Med. Devices 12, 93–111 (2014). https://doi.org/10.1586/17434440.2015.95807510.1586/17434440.2015.958075 ↗
26. Q. Hou, D.W. Grijpma, J. Feijen, Preparation of interconnected highly porous polymeric structures by a replication and freeze-drying process. J. Biomed. Mater. Res. Part B (2003). https://doi.org/10.1002/jbm.b.1006610.1002/jbm.b.10066 ↗
27. M.K. Narbat, F. Orang, M.S. Hashtjin, A. Goudarzi, Fabrication of porous hydroxyapatite-gelatin composite scaffolds for bone tissue engineering. Iran. Biomed. J. 10, 215–223 (2006)
28. D.W. Hutmacher, Scaffolds in tissue engineering bone and cartilage. Biomaterials 21, 2529–2543 (2000). https://doi.org/10.1016/S0142-9612(00)00121-610.1016/S0142-9612(00)00121-6 ↗
29. S.J. Hollister, Porous scaffold design for tissue engineering. Nat. Mater. 4, 518–524 (2005). https://doi.org/10.1038/nmat142110.1038/nmat1421 ↗
30. Y. Kuboki, Q. Jin, H. Takita, Geometry of carriers controlling phenotypic expression in BMP-induced osteogenesis and chondrogenesis. J. Bone Jt. Surg. Am. 83 A Suppl, S101–S105 (2001)
31. E. Tsuruga, H. Takita, H. Itoh, Y. Wakisaka, Y. Kuboki, Pore size of porous hydroxyapatite as the cell-substratum controls BMP-induced osteogenesis. J. Biochem. 121, 317–324 (1997). https://doi.org/10.1093/oxfordjournals.jbchem.a02158910.1093/oxfordjournals.jbchem.a021589 ↗
32. E.C. Shors, Coralline bone graft substitutes. Orthop. Clin. North Am. 30, 599–613 (1999). https://doi.org/10.1016/S0030-5898(05)70113-910.1016/S0030-5898(05)70113-9 ↗
33. B.N. Singh, V. Veeresh, S.P. Mallick, S. Sinha, A. Rastogi, P. Srivastava, Generation of scaffold incorporated with nanobioglass encapsulated in chitosan/chondroitin sulfate complex for bone tissue engineering. Int. J. Biol. Macromol. (2020). https://doi.org/10.1016/j.ijbiomac.2020.02.17310.1016/j.ijbiomac.2020.02.173 ↗
34. F. Polyak, G. Reich, Infrared spectroscopic study of the coil-helix transition of highly concentrated gelatin formulations. Eur. J. Pharm. Biopharm. (2019). https://doi.org/10.1016/j.ejpb.2019.04.01010.1016/j.ejpb.2019.04.010 ↗
35. F. Milano, A. Masi, M. Madaghiele, A. Sannino, L. Salvatore, N. Gallo, Current trends in gelatin-based drug delivery systems. Pharmaceutics (2023). https://doi.org/10.3390/pharmaceutics1505149910.3390/pharmaceutics15051499 ↗
36. C.S. Julie Chandra, S. Sasi, T.K. Bindu Sharmila, Material Applications of Gelatin, in: Handb. Biopolym., 2023. https://doi.org/10.1007/978-981-16-6603-2_28-1.10.1007/978-981-16-6603-2_28-1 ↗
37. S. Van Vlierberghe, G.J. Graulus, S.K. Samal, I. Van Nieuwenhove, P. Dubruel, Porous hydrogel biomedical foam scaffolds for tissue repair. Biomed. Foam. Tissue Eng. Appl. (2014). https://doi.org/10.1533/9780857097033.2.33510.1533/9780857097033.2.335 ↗
38. P. Rivero-Ramos, M.G. Unthank, T. Sanz, M.D. Rodrigo, M. Benlloch-Tinoco, Synergistic depolymerisation of alginate and chitosan by high hydrostatic pressure (HHP) and pulsed electric fields (PEF) treatment in the presence of H2O2. Carbohydr. Polym. (2023). https://doi.org/10.1016/j.carbpol.2023.12099910.1016/j.carbpol.2023.120999 ↗
39. M.I. Gariboldi, S.M. Best, Effect of ceramic scaffold architectural parameters on biological response. Front. Bioeng. Biotechnol. (2015). https://doi.org/10.3389/fbioe.2015.0015110.3389/fbioe.2015.00151 ↗
40. G. Hannink, J.J.C. Arts, Bioresorbability, porosity and mechanical strength of bone substitutes: What is optimal for bone regeneration? Injury 42, S22–S25 (2011). https://doi.org/10.1016/j.injury.2011.06.00810.1016/j.injury.2011.06.008 ↗
41. S.K. Lan Levengood, S.J. Polak, M.B. Wheeler, A.J. Maki, S.G. Clark, R.D. Jamison, A.J. Wagoner Johnson, Multiscale osteointegration as a new paradigm for the design of calcium phosphate scaffolds for bone regeneration. Biomaterials 31, 3552–3563 (2010). https://doi.org/10.1016/j.biomaterials.2010.01.05210.1016/j.biomaterials.2010.01.052 ↗
42. C.M. Murphy, M.G. Haugh, F.J. O’Brien, The effect of mean pore size on cell attachment, proliferation and migration in collagen-glycosaminoglycan scaffolds for bone tissue engineering. Biomaterials 31, 461–466 (2010). https://doi.org/10.1016/j.biomaterials.2009.09.06310.1016/j.biomaterials.2009.09.063 ↗
43. F.J. O’Brien, B.A. Harley, I.V. Yannas, L.J. Gibson, The effect of pore size on cell adhesion in collagen-GAG scaffolds. Biomaterials 26, 433–441 (2005). https://doi.org/10.1016/j.biomaterials.2004.02.05210.1016/j.biomaterials.2004.02.052 ↗
44. S. Srinivasan, R. Jayasree, K.P.P. Chennazhi, S.V.V. Nair, R. Jayakumar, Biocompatible alginate/nano bioactive glass ceramic composite scaffolds for periodontal tissue regeneration. Carbohydr. Polym. 87, 274–283 (2012). https://doi.org/10.1016/j.carbpol.2011.07.05810.1016/j.carbpol.2011.07.058 ↗
45. H.W. Kim, J.C. Knowles, H.E. Kim, Hydroxyapatite and gelatin composite foams processed via novel freeze-drying and crosslinking for use as temporary hard tissue scaffolds. J. Biomed. Mater. Res. Part A 72, 136–145 (2005). https://doi.org/10.1002/jbm.a.3016810.1002/jbm.a.30168 ↗
46. K. Maji, S. Dasgupta, B. Kundu, A. Bissoyi, Development of gelatin-chitosan-hydroxyapatite based bioactive bone scaffold with controlled pore size and mechanical strength. J. Biomater. Sci. Polym. Ed. 26, 1190–1209 (2015). https://doi.org/10.1080/09205063.2015.108280910.1080/09205063.2015.1082809 ↗
47. K. Maji, S. Dasgupta, K. Pramanik, A. Bissoyi, Preparation and evaluation of gelatin-chitosan-nanobioglass 3D porous scaffold for bone tissue engineering. Int. J. Biomater. (2016). https://doi.org/10.1155/2016/982565910.1155/2016/9825659 ↗
48. Y. Xu, J. Guan, Interaction of Cells with Polyurethane Scaffolds, in: Adv. Polyurethane Biomater., 2016: pp. 523–542. https://doi.org/10.1016/B978-0-08-100614-6.00018-4.10.1016/B978-0-08-100614-6.00018-4 ↗
49. E.H. Macdonald, Sedimentation and detrital gold, in: Handb. Gold Explor. Eval., 2007: pp. 195–266. https://doi.org/10.1533/9781845692544.195.10.1533/9781845692544.195 ↗
50. C.M. Nelson, R.P. Jean, J.L. Tan, W.F. Liu, N.J. Sniadecki, A.A. Spector, C.S. Chen, Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. U.S.A. 102, 11594–11599 (2005). https://doi.org/10.1073/pnas.050257510210.1073/pnas.0502575102 ↗
51. D. Veljović, R. Jančić-Hajneman, I. Balać, B. Jokić, S. Putić, R. Petrović, D. Janaćković, The effect of the shape and size of the pores on the mechanical properties of porous HAP-based bioceramics. Ceram. Int. 37, 471–479 (2011). https://doi.org/10.1016/j.ceramint.2010.09.01410.1016/j.ceramint.2010.09.014 ↗
52. M. Nacucchi, F. De Pascalis, M. Scatto, L. Capodieci, R. Albertoni, Structural analysis of advanced polymeric foams by means of high resolution X-ray computed tomography. AIP Conf. Proc. (2016). https://doi.org/10.1063/1.495449210.1063/1.4954492 ↗
53. M.S. Rizvi, P. Kumar, D.S. Katti, A. Pal, Mathematical model of mechanical behavior of micro/nanofibrous materials designed for extracellular matrix substitutes. Acta Biomater. 8, 4111–4122 (2012). https://doi.org/10.1016/j.actbio.2012.07.02510.1016/j.actbio.2012.07.025 ↗
54. G.C. Engelmayr, G.D. Papworth, S.C. Watkins, J.E. Mayer, M.S. Sacks, Guidance of engineered tissue collagen orientation by large-scale scaffold microstructures. J. Biomech. 39, 1819–1831 (2006). https://doi.org/10.1016/j.jbiomech.2005.05.02010.1016/j.jbiomech.2005.05.020 ↗
55. B.B. Mandal, E.S. Gil, B. Panilaitis, D.L. Kaplan, Laminar silk scaffolds for aligned tissue fabrication. Macromol. Biosci. 13, 48–58 (2013). https://doi.org/10.1002/mabi.20120023010.1002/mabi.201200230 ↗
56. K.S. Halonen, M.E. Mononen, J.S. Jurvelin, J. Töyräs, R.K. Korhonen, Importance of depth-wise distribution of collagen and proteoglycans in articular cartilage-A 3D finite element study of stresses and strains in human knee joint. J. Biomech. 46, 1184–1192 (2013). https://doi.org/10.1016/j.jbiomech.2012.12.02510.1016/j.jbiomech.2012.12.025 ↗
57. A. Arora, A. Kothari, D.S. Katti, Pore orientation mediated control of mechanical behavior of scaffolds and its application in cartilage-mimetic scaffold design. J. Mech. Behav. Biomed. Mater. 51, 169–183 (2015). https://doi.org/10.1016/j.jmbbm.2015.06.03310.1016/j.jmbbm.2015.06.033 ↗
58. S. Blacher, V. Maquet, R. Jérôme, J.P. Pirard, A.R. Boccaccini, Study of the connectivity properties of Bioglass®-filled polylactide foam scaffolds by image analysis and impedance spectroscopy. Acta Biomater. 1, 565–574 (2005). https://doi.org/10.1016/j.actbio.2005.06.00310.1016/j.actbio.2005.06.003 ↗
59. K.F. Leong, C.M. Cheah, C.K. Chua, Solid freeform fabrication of three-dimensional scaffolds for engineering replacement tissues and organs. Biomaterials 24, 2363–2378 (2003). https://doi.org/10.1016/S0142-9612(03)00030-910.1016/S0142-9612(03)00030-9 ↗
60. S.L. Ishaug-Riley, G.M. Crane-Kruger, M.J. Yaszemski, A.G. Mikos, Three-dimensional culture of rat calvarial osteoblasts in porous biodegradable polymers. Biomaterials 19, 1405–1412 (1998). https://doi.org/10.1016/S0142-9612(98)00021-010.1016/S0142-9612(98)00021-0 ↗
61. A. Odgaard, H.J.G. Gundersen, Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 14, 173–182 (1993). https://doi.org/10.1016/8756-3282(93)90245-610.1016/8756-3282(93)90245-6 ↗
62. L. Brabant, J. Vlassenbroeck, Y. De Witte, V. Cnudde, M.N. Boone, J. Dewanckele, L. Van Hoorebeke, Three-dimensional analysis of high-resolution X-ray computed tomography data with morpho+. Microsc. Microanal. 17, 252–263 (2011). https://doi.org/10.1017/S143192761009438910.1017/S1431927610094389 ↗
63. C.H. Arns, M.A. Knackstedt, W.V. Pinczewski, K.R. Mecke, Euler-Poincaré characteristics of classes of disordered media. Phys. Rev. E 63, 311121–3111213 (2001). https://doi.org/10.1103/PhysRevE.63.03111210.1103/PhysRevE.63.031112 ↗
64. S. Anuradha, K. Uma Maheswari, S. Swaminathan, Fabrication of uniaxially aligned 3D electrospun scaffolds for neural regeneration. Biomed. Mater. 6, 25004 (2011)10.1088/1748-6041/6/2/025004 ↗
65. K. Stuckensen, A. Schwab, M. Knauer, E. Muiños-López, F. Ehlicke, J. Reboredo, F. Granero-Moltó, U. Gbureck, F. Prósper, H. Walles, J. Groll, Tissue mimicry in morphology and composition promotes hierarchical matrix remodeling of invading stem cells in osteochondral and meniscus scaffolds. Adv. Mater. (2018). https://doi.org/10.1002/adma.20170675410.1002/adma.201706754 ↗
66. P. Tayalia, C.R. Mendonca, T. Baldacchini, D.J. Mooney, E. Mazur, 3D cell-migration studies using two-photon engineered polymer scaffolds. Adv. Mater. 20, 4494–4498 (2008). https://doi.org/10.1002/adma.20080131910.1002/adma.200801319 ↗
67. C.H. Lee, H.J. Shin, I.H. Cho, Y.M. Kang, I.A. Kim, K.D. Park, J.W. Shin, Nanofiber alignment and direction of mechanical strain affect the ECM production of human ACL fibroblast. Biomaterials 26, 1261–1270 (2005). https://doi.org/10.1016/j.biomaterials.2004.04.03710.1016/j.biomaterials.2004.04.037 ↗
68. K. Stuckensen, J.M. Lamo-Espinosa, E. Muiños-López, P. Ripalda-Cemboráin, T. López-Martínez, E. Iglesias, G. Abizanda, I. Andreu, M. Flandes-Iparraguirre, J. Pons-Villanueva, R. Elizalde, J. Nickel, A. Ewald, U. Gbureck, F. Prósper, J. Groll, F. Granero-Moltó, Anisotropic cryostructured collagen scaffolds for efficient delivery of RhBMP-2 and enhanced bone regeneration. Materials (Basel) (2019). https://doi.org/10.3390/ma1219310510.3390/ma12193105 ↗
69. I. Sánchez, G. Uzcátegui, Fractals in dentistry. J. Dent. 39, 273–292 (2011). https://doi.org/10.1016/j.jdent.2011.01.01010.1016/j.jdent.2011.01.010 ↗
70. J. Guédon, F. Autrusseau, Y. Amouriq, P. Bléry, J.-M. Bouler, P. Weiss, F.-X. Barbarin, T. Dallet, V. Dallerit, Exploring relationships between fractal dimension and trabecular bone characteristics, in: Med. Imaging 2012 Biomed. Appl. Mol. Struct. Funct. Imaging 2012: p. 831717. https://doi.org/10.1117/12.911164.10.1117/12.911164 ↗
71. D. Ulrich, B. van Rietbergen, A. Laib, P. R̈uegsegger, The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone 25, 55–60 (1999). https://doi.org/10.1016/S8756-3282(99)00098-810.1016/S8756-3282(99)00098-8 ↗
72. J.L. Drummond, M. Thompson, B.J. Super, Fracture surface examination of dental ceramics using fractal analysis. Dent. Mater. 21, 586–589 (2005). https://doi.org/10.1016/j.dental.2004.12.00210.1016/j.dental.2004.12.002 ↗
73. J.J. Mecholsky, D.E. Passoja, K.S. Feinberg-Ringel, Quantitative analysis of brittle fracture surfaces using fractal geometry. J. Am. Ceram. Soc. 72, 60–65 (1989). https://doi.org/10.1111/j.1151-2916.1989.tb05954.x10.1111/j.1151-2916.1989.tb05954.x ↗
74. T. Uchiyama, T. Tanizawa, H. Muramatsu, N. Endo, H.E. Takahashi, T. Hara, Three-dimensional microstructural analysis of human trabecular bone in relation to its mechanical properties. Bone 25, 487–491 (1999). https://doi.org/10.1016/S8756-3282(99)00188-X10.1016/S8756-3282(99)00188-X ↗
75. A. Thomas, J. Bera, Sol–gel synthesis and in vitro bioactivity of glass–ceramics in SiO2–CaO–Na2O–P2O5 system. J. Sol-Gel Sci. Technol. 80, 411–416 (2016). https://doi.org/10.1007/s10971-016-4110-410.1007/s10971-016-4110-4 ↗
76. A. Thomas, J. Bera, Preparation and characterization of gelatin-bioactive glass ceramic scaffolds for bone tissue engineering. J. Biomater. Sci. Polym. Ed. 30, 1–19 (2019). https://doi.org/10.1080/09205063.2019.158769710.1080/09205063.2019.1587697 ↗
77. A. Thomas, E. Johnson, A.K. Agrawal, J. Bera, Preparation and characterization of glass-ceramic reinforced alginate scaffolds for bone tissue engineering. J. Mater. Res. 34, 3798–3809 (2019). https://doi.org/10.1557/jmr.2019.34310.1557/jmr.2019.343 ↗