A machine learning-based multiscale model to predict bone formation in scaffolds.


Journal

Nature computational science
ISSN: 2662-8457
Titre abrégé: Nat Comput Sci
Pays: United States
ID NLM: 101775476

Informations de publication

Date de publication:
Aug 2021
Historique:
received: 01 02 2021
accepted: 19 07 2021
medline: 1 8 2021
pubmed: 1 8 2021
entrez: 13 1 2024
Statut: ppublish

Résumé

Computational modeling methods combined with non-invasive imaging technologies have exhibited great potential and unique opportunities to model new bone formation in scaffold tissue engineering, offering an effective alternate and viable complement to laborious and time-consuming in vivo studies. However, existing numerical approaches are still highly demanding computationally in such multiscale problems. To tackle this challenge, we propose a machine learning (ML)-based approach to predict bone ingrowth outcomes in bulk tissue scaffolds. The proposed in silico procedure is developed by correlating with a dedicated longitudinal (12-month) animal study on scaffold treatment of a major segmental defect in sheep tibia. Comparison of the ML-based time-dependent prediction of bone ingrowth with the conventional multilevel finite element (FE

Identifiants

pubmed: 38217252
doi: 10.1038/s43588-021-00115-x
pii: 10.1038/s43588-021-00115-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

532-541

Informations de copyright

© 2021. The Author(s), under exclusive licence to Springer Nature America, Inc.

Références

Hollister, S. J. Porous scaffold design for tissue engineering. Nat. Mater. 4, 518–524 (2005).
doi: 10.1038/nmat1421
Petite, H. et al. Tissue-engineered bone regeneration. Nat. Biotechnol. 18, 959–963 (2000).
doi: 10.1038/79449
Choi, N. W. et al. Microfluidic scaffolds for tissue engineering. Nat. Mater. 6, 908–915 (2007).
doi: 10.1038/nmat2022
Ringe, J. & Sittinger, M. Regenerative medicine: selecting the right biological scaffold for tissue engineering. Nat. Rev. Rheumatol. 10, 388–389 (2014).
doi: 10.1038/nrrheum.2014.79
Moutos, F. T., Freed, L. E. & Guilak, F. A biomimetic three-dimensional woven composite scaffold for functional tissue engineering of cartilage. Nat. Mater. 6, 162–167 (2007).
doi: 10.1038/nmat1822
Schouman, T., Schmitt, M., Adam, C., Dubois, G. & Rouch, P. Influence of the overall stiffness of a load-bearing porous titanium implant on bone ingrowth in critical-size mandibular bone defects in sheep. J. Mech. Behav. Biomed. Mater. 59, 484–496 (2016).
doi: 10.1016/j.jmbbm.2016.02.036
Pobloth, A. M. et al. Mechanobiologically optimized 3D titanium-mesh scaffolds enhance bone regeneration in critical segmental defects in sheep. Sci. Transl. Med. 10, 8828 (2018).
doi: 10.1126/scitranslmed.aam8828
Li, J. J. et al. A novel bone substitute with high bioactivity, strength, and porosity for repairing large and load‐bearing bone defects. Adv. Healthc. Mater. 8, 1801298 (2019).
doi: 10.1002/adhm.201801298
Sharma, U. et al. The development of bioresorbable composite polymeric implants with high mechanical strength. Nat. Mater. 17, 96–102 (2018).
doi: 10.1038/nmat5016
Entezari, A. et al. Architectural design of 3D printed scaffolds controls the volume and functionality of newly formed bone. Adv. Healthc. Mater. 8, 1801353 (2019).
doi: 10.1002/adhm.201801353
Chen, Y., Zhou, S. & Li, Q. Microstructure design of biodegradable scaffold and its effect on tissue regeneration. Biomaterials 32, 5003–5014 (2011).
doi: 10.1016/j.biomaterials.2011.03.064
Chen, Y., Zhou, S. & Li, Q. Mathematical modeling of degradation for bulk-erosive polymers: applications in tissue engineering scaffolds and drug delivery systems. Acta Biomater. 7, 1140–1149 (2011).
doi: 10.1016/j.actbio.2010.09.038
Sturm, S., Zhou, S., Mai, Y. W. & Li, Q. On stiffness of scaffolds for bone tissue engineering—a numerical study. J. Biomech. 43, 1738–1744 (2010).
doi: 10.1016/j.jbiomech.2010.02.020
Adachi, T., Osako, Y., Tanaka, M., Hojo, M. & Hollister, S. J. Framework for optimal design of porous scaffold microstructure by computational simulation of bone regeneration. Biomaterials 27, 3964–3972 (2006).
doi: 10.1016/j.biomaterials.2006.02.039
Sanz-Herrera, J. A., García-Aznar, J. M. & Doblaré, M. On scaffold designing for bone regeneration: a computational multiscale approach. Acta Biomater. 5, 219–229 (2009).
doi: 10.1016/j.actbio.2008.06.021
Zhao, F., Melke, J., Ito, K., van Rietbergen, B. & Hofmann, S. A multiscale computational fluid dynamics approach to simulate the micro-fluidic environment within a tissue engineering scaffold with highly irregular pore geometry. Biomech. Model. Mechanobiol. 18, 1965–1977 (2019).
doi: 10.1007/s10237-019-01188-4
Marin, A. C., Grossi, T., Bianchi, E., Dubini, G. & Lacroix, D. µ-Particle tracking velocimetry and computational fluid dynamics study of cell seeding within a 3D porous scaffold. J. Mech. Behav. Biomed. Mater. 75, 463–469 (2017).
doi: 10.1016/j.jmbbm.2017.08.003
Kelly, D. J. & Prendergast, P. J. Mechano-regulation of stem cell differentiation and tissue regeneration in osteochondral defects. J. Biomech. 38, 1413–1422 (2005).
doi: 10.1016/j.jbiomech.2004.06.026
Huiskes, R., Van Driel, W. D., Prendergast, P. J. & Soballe, K. A biomechanical regulatory model for periprosthetic fibrous-tissue differentiation. J. Mater. Sci. Mater. Med. 8, 785–788 (1997).
doi: 10.1023/A:1018520914512
Prendergast, P. J., Huiskes, R. & Søballe, K. Biophysical stimuli on cells during tissue differentiation at implant interfaces. J. Biomech. 30, 539–548 (1997).
doi: 10.1016/S0021-9290(96)00140-6
Maslov, L. B. Mathematical model of bone regeneration in a porous implant. Mech. Compos. Mater. 53, 399–414 (2017).
doi: 10.1007/s11029-017-9671-y
Shi, Q., Shui, H., Chen, Q. & Li, Z. Y. How does mechanical stimulus affect the coupling process of the scaffold degradation and bone formation: an in silico approach. Comput. Biol. Med. 117, 103588 (2020).
doi: 10.1016/j.compbiomed.2019.103588
Beaupré, G. S., Orr, T. E. & Carter, D. R. An approach for time‐dependent bone modeling and remodeling—theoretical development. J. Orthop. Res. 8, 651–661 (1990).
doi: 10.1002/jor.1100080506
Sanz-Herrera, J. A., García-Aznar, J. M. & Doblaré, M. Micro-macro numerical modelling of bone regeneration in tissue engineering. Comput. Methods Appl. Mech. Eng. 197, 3092–3107 (2008).
doi: 10.1016/j.cma.2008.02.010
Cheong, V. S., Fromme, P., Mumith, A., Coathup, M. J. & Blunn, G. W. Novel adaptive finite element algorithms to predict bone ingrowth in additive manufactured porous implants. J. Mech. Behav. Biomed. Mater. 87, 230–239 (2018).
doi: 10.1016/j.jmbbm.2018.07.019
Cheong, V. S., Fromme, P., Coathup, M. J., Mumith, A. & Blunn, G. W. Partial bone formation in additive manufactured porous implants reduces predicted stress and danger of fatigue failure. Ann. Biomed. Eng. 48, 502–514 (2020).
doi: 10.1007/s10439-019-02369-z
Taylor, M. & Prendergast, P. J. Four decades of finite element analysis of orthopaedic devices: where are we now and what are the opportunities? J. Biomech. 48, 767–778 (2015).
doi: 10.1016/j.jbiomech.2014.12.019
Checa, S. & Prendergast, P. J. A mechanobiological model for tissue differentiation that includes angiogenesis: a lattice-based modeling approach. Ann. Biomed. Eng. 37, 129–145 (2009).
doi: 10.1007/s10439-008-9594-9
Lecun, Y., Bengio, Y. & Hinton, G. Deep learning. Nature 521, 436–444 (2015).
doi: 10.1038/nature14539
Nguyen, A. H. et al. Cardiac tissue engineering: state-of-the-art methods and outlook. J. Biol. Eng. 13, 57 (2019).
doi: 10.1186/s13036-019-0185-0
Kavakiotis, I. et al. Machine learning and data mining methods in diabetes research. Comput. Struct. Biotechnol. J. 15, 104–116 (2017).
doi: 10.1016/j.csbj.2016.12.005
Zhang, Y. & Ye, W. Deep learning–based inverse method for layout design. Struct. Multidiscip. Optim. 60, 527–536 (2019).
doi: 10.1007/s00158-019-02222-w
Alber, M. et al. Integrating machine learning and multiscale modeling—perspectives, challenges, and opportunities in the biological, biomedical, and behavioral sciences. npj Digit. Med. 2, 115 (2019).
doi: 10.1038/s41746-019-0193-y
Huang, D., Fuhg, J. N., Weißenfels, C. & Wriggers, P. A machine learning based plasticity model using proper orthogonal decomposition. Comput. Methods Appl. Mech. Eng. 365, 1–33 (2020).
doi: 10.1016/j.cma.2020.113008
Mozaffar, M. et al. Deep learning predicts path-dependent plasticity. Proc. Natl Acad. Sci. USA 116, 26414–26420 (2019).
doi: 10.1073/pnas.1911815116
Freiberg, A. H. Wolff’s law and the functional pathogenesis of deformity. Am. J. Med. Sci. 124, 956–971 (1902).
doi: 10.1097/00000441-190212000-00003
Lin, D., Li, Q., Li, W., Duckmanton, N. & Swain, M. Mandibular bone remodeling induced by dental implant. J. Biomech. 43, 287–293 (2010).
doi: 10.1016/j.jbiomech.2009.08.024
Lin, D., Li, Q., Li, W. & Swain, M. Dental implant induced bone remodeling and associated algorithms. J. Mech. Behav. Biomed. Mater. 2, 410–432 (2009).
doi: 10.1016/j.jmbbm.2008.11.007
Rungsiyakull, C. et al. Bone’s responses to different designs of implant-supported fixed partial dentures. Biomech. Model. Mechanobiol. 14, 403–411 (2015).
doi: 10.1007/s10237-014-0612-6
Weinans, H., Huiskes, R. & Grootenboer, H. J. Effects of material properties of femoral hip components on bone remodeling. J. Orthop. Res. 10, 845–853 (1992).
doi: 10.1002/jor.1100100614
Liu, L., Shi, Q., Chen, Q. & Li, Z. Mathematical modeling of bone in-growth into undegradable porous periodic scaffolds under mechanical stimulus. J. Tissue Eng. 10, 204173141982716 (2019).
doi: 10.1177/2041731419827167
Feurer, M. et al. Efficient and robust automated machine learning. in Advances in Neural Information Processing Systems 28 (eds Ghahramani, Z. et al.) 2962–2970 (NIPS, 2015).
Snoek, J., Larochelle, H. & Adams, R. P. Practical Bayesian optimization of machine learning algorithms. Adv. Neural Inf. Process. Syst. 4, 2951–2959 (2012).
Perier-Metz, C., Duda, G. N. & Checa, S. Initial mechanical conditions within an optimized bone scaffold do not ensure bone regeneration – an in silico analysis. Biomech. Model. Mechanobiol. https://doi.org/10.1007/s10237-021-01472-2 (2021).
Cohen, D. O., Aboutaleb, S. M. G., Johnson, A. W. & Norato, J. A. Bone adaptation-driven design of periodic scaffolds. J. Mech. Des. Trans. ASME 143, 121701 (2021).
doi: 10.1115/1.4050928
Göpferich, A. Polymer bulk erosion. Macromolecules 30, 2598–2604 (1997).
doi: 10.1021/ma961627y
Shi, Q., Chen, Q., Pugno, N. & Li, Z. Y. Effect of rehabilitation exercise durations on the dynamic bone repair process by coupling polymer scaffold degradation and bone formation. Biomech. Model. Mechanobiol. 17, 763–775 (2018).
doi: 10.1007/s10237-017-0991-6
Wang, L. et al. Mechanical–chemical coupled modeling of bone regeneration within a biodegradable polymer scaffold loaded with VEGF. Biomech. Model. Mechanobiol. 19, 2285–2306 (2020).
doi: 10.1007/s10237-020-01339-y
Roohani-Esfahani, S.-I. I., Newman, P. & Zreiqat, H. Design and fabrication of 3D printed scaffolds with a mechanical strength comparable to cortical bone to repair large bone defects. Sci. Rep. 6, 19468 (2016).
doi: 10.1038/srep19468
Duda, G. N. et al. Analysis of inter-fragmentary movement as a function of musculoskeletal loading conditions in sheep. J. Biomech. 31, 201–210 (1997).
doi: 10.1016/S0021-9290(97)00127-9
Guedes, J. & Kikuchi, N. Preprocessing and postprocessing for materials based on the homogenization method with adaptive finite element methods. Comput. Methods Appl. Mech. Eng. 83, 143–198 (1990).
doi: 10.1016/0045-7825(90)90148-F
Numerical experiments of the homogenization method. in Computing methods in applied sciences and engineering, 1977, I 330–356 (Springer, 1979).
Bendsøe, M. P. & Kikuchi, N. Generating optimal topologies in structural design using a homogenization method. Comput. Methods Appl. Mech. Eng. 71, 197–224 (1988).
doi: 10.1016/0045-7825(88)90086-2
Wu, C., Zheng, K., Fang, J., Steven, G. P. & Li, Q. Time-dependent topology optimization of bone plates considering bone remodeling. Comput. Methods Appl. Mech. Eng. 359, 112702 (2020).
doi: 10.1016/j.cma.2019.112702
Turner, C. H., Anne, V. & Pidaparti, R. M. V. A uniform strain criterion for trabecular bone adaptation: do continuum-level strain gradients drive adaptation? J. Biomech. 30, 555–563 (1997).
doi: 10.1016/S0021-9290(97)84505-8
Checa, S., Prendergast, P. J. & Duda, G. N. Inter-species investigation of the mechano-regulation of bone healing: comparison of secondary bone healing in sheep and rat. J. Biomech. 44, 1237–1245 (2011).
doi: 10.1016/j.jbiomech.2011.02.074
Perier-Metz, C., Duda, G. N. & Checa, S. Mechano-Biological Computer Model of Scaffold-Supported Bone Regeneration: Effect of Bone Graft and Scaffold Structure on Large Bone Defect Tissue Patterning. Front. Bioeng. Biotechnol. 8, 585799 (2020).
doi: 10.3389/fbioe.2020.585799
Chen, G. et al. A new approach for assigning bone material properties from CT images into finite element models. J. Biomech. 43, 1011–1015 (2010).
doi: 10.1016/j.jbiomech.2009.10.040
Suquet, P. M. Elements of homogenization for inelastic solid mechanics, homogenization techniques for composite media. Lect. Notes Phys. 272, 193 (1985).
doi: 10.1007/3-540-17616-0_15
White, D. A., Arrighi, W. J., Kudo, J. & Watts, S. E. Multiscale topology optimization using neural network surrogate models. Comput. Methods Appl. Mech. Eng. 346, 1118–1135 (2019).
doi: 10.1016/j.cma.2018.09.007
Funahashi, K. I. On the approximate realization of continuous mappings by neural networks. Neural Netw. 2, 183–192 (1989).
doi: 10.1016/0893-6080(89)90003-8
Hassoun, M. H. Fundamentals of artificial neural networks (MIT press, 1995).
Hogg, M. mhogg/pyvxray: an ABAQUS plug-in for the creation of virtual X-rays from 3D finite element bone/implant models (GitHub, 2013); https://github.com/mhogg/pyvxray
Pearson, K. Notes on regression and inheritance in the case of two parents. Proc. R. Soc. Lond. 58, 240–42 (1895).
doi: 10.1098/rspl.1895.0041
Wu, C. Machine learning based multi-scale remodelling code (Zenodo, 2021); https://doi.org/10.5281/ZENODO.5017032

Auteurs

Chi Wu (C)

School of Aerospace, Mechanical and Mechatronic Engineering, The University of Sydney, Sydney, New South Wales, Australia.

Ali Entezari (A)

School of Biomedical Engineering, The University of Sydney, Sydney, New South Wales, Australia.

Keke Zheng (K)

School of Aerospace, Mechanical and Mechatronic Engineering, The University of Sydney, Sydney, New South Wales, Australia.

Jianguang Fang (J)

School of Civil and Environmental Engineering, University of Technology Sydney, Sydney, New South Wales, Australia.

Hala Zreiqat (H)

School of Biomedical Engineering, The University of Sydney, Sydney, New South Wales, Australia.

Grant P Steven (GP)

School of Aerospace, Mechanical and Mechatronic Engineering, The University of Sydney, Sydney, New South Wales, Australia.

Michael V Swain (MV)

School of Aerospace, Mechanical and Mechatronic Engineering, The University of Sydney, Sydney, New South Wales, Australia.

Qing Li (Q)

School of Aerospace, Mechanical and Mechatronic Engineering, The University of Sydney, Sydney, New South Wales, Australia. qing.li@sydney.edu.au.

Classifications MeSH