Abstract
The dynamic characteristic of bone is its ability to remodel itself through mechanobiological responses. Bone regeneration is triggered by mechanical cues from physiological activities that generate structural strain and cause bone marrow movement. This phenomenon is crucial for bone scaffold when implanted in the cancellous bone as host tissue. Often, the fluid movement of bone scaffold and cancellous bone is studied separately, which does not represent the actual environment once implanted. In the present study, the fluid flow analysis properties of bone scaffold integrated into the cancellous bone at different skeletal sites are investigated. Three types of porous bone scaffolds categorized based on pore size configurations: 1 mm, 0.8 mm and hybrid (0.8 mm interlaced with 0.5 mm) were used. Three different skeletal sites of femoral bone were selected: neck, lateral condyle and medial condyle. Computational fluid dynamics was utilized to analyze the fluid flow properties of bone scaffold integrated cancellous bone. The results of this study reveal that the localization and maximum value of shear stress in an independent bone scaffold are significantly different compared to the bone scaffold integrated with cancellous bone by about 160% to 448% percentage difference. Low shear stress and high permeability were found across models that have higher Tb.Sp (trabecular separation). Specimen C and femoral lateral condyle showed the highest permeability in their respective category.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ali, D., Sen, S.: Finite element analysis of mechanical behavior, permeability and fluid induced wall shear stress of high porosity scaffolds with gyroid and lattice-based architectures. J. Mech. Behav. Biomed. Mater. 75, 262–270 (2017). https://doi.org/10.1016/j.jmbbm.2017.07.035
Ali, D., Sen, S.: Permeability and fluid flow-induced wall shear stress of bone tissue scaffolds: computational fluid dynamic analysis using Newtonian and non-Newtonian blood flow models. Comput. Biol. Med. 99, 201–208 (2018). https://doi.org/10.1016/j.compbiomed.2018.06.017
Andreoli, A., Monteleone, M., Van Loan, M., Promenzio, L., Tarantino, U., De Lorenzo, A.: Effects of different sports on bone density and muscle mass in highly trained athletes. Med. Sci. Sports. Exerc. (2001). https://doi.org/10.1097/00005768-200104000-00001
Arnsdorf, E.J., Tummala, P., Kwon, R.Y., Jacobs, C.R.: Mechanically induced osteogenic differentiation—the role of RhoA, ROCKII and cytoskeletal dynamics. J. Cell Sci. 122, 546–553 (2009). https://doi.org/10.1242/jcs.036293
Baino, F., Yamaguchi, S.: The use of simulated body fluid (SBF) for assessing materials bioactivity in the context of tissue engineering: review and challenges. Biomimetics 5, 1–19 (2020). https://doi.org/10.3390/biomimetics5040057
Becquart, P., Cruel, M., Hoc, T., Sudre, L., Pernelle, K., Bizios, R., Logeart-Avramoglou, D., Petite, H., Bensidhoum, M.: Human mesenchymal stem cell responses to hydrostatic pressure and shear stress. Eur. Cell Mater. 31, 160–173 (2016). https://doi.org/10.22203/eCM.v031a11
Bidan, C.M., Kommareddy, K.P., Rumpler, M., Kollmannsberger, P., Fratzl, P., Dunlop, J.W.C.: geometry as a factor for tissue growth: towards shape optimization of tissue engineering scaffolds. Adv. Healthcare Mater. 2, 186–194 (2013). https://doi.org/10.1002/adhm.201200159
Birmingham, E., Grogan, J.A., Niebur, G.L., McNamara, L.M., McHugh, P.E.: Computational modelling of the mechanics of trabecular bone and marrow using fluid structure interaction techniques. Ann. Biomed. Eng. 41, 814–826 (2013). https://doi.org/10.1007/s10439-012-0714-1
Callens, S.J.P., Arns, C.H., Kuliesh, A., Zadpoor, A.A.: Decoupling minimal surface metamaterial properties through multi-material hyperbolic tilings. Adv. Func. Mater. 31, 2101373 (2021). https://doi.org/10.1002/adfm.202101373
Chen, Y., Zhang, S., Li, J., Song, Y., Zhao, C., Zhang, X.: Dynamic degradation behavior of MgZn alloy in circulating m-SBF. Mater. Lett. 64, 1996–1999 (2010). https://doi.org/10.1016/j.matlet.2010.06.011
Chen, X.T., Zhu, Y.J., Liu, Y.W., Chen, K., Xu, W.W., Zhang, L.L., Liang, D.W., Li, J., Ye, Y., Tian, K.W., Zhang, X.D., Li, H.J., Kang, Z.: Metal trabecular bone reconstruction system better improves clinical efficacy and biomechanical repair of osteonecrosis of the femoral head than free vascularized fibular graft: a case–control study. J. Cell Physiol. 234, 20957–20968 (2019). https://doi.org/10.1002/jcp.28700
Chen, H., Liu, Y., Wang, C., Zhang, A., Chen, B., Han, Q., Wang, J.: Design and properties of biomimetic irregular scaffolds for bone tissue engineering. Comput. Biol. Med. 130, 104241 (2021). https://doi.org/10.1016/j.compbiomed.2021.104241
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). https://doi.org/10.1007/s10439-019-02369-z
Cowin, S.C., Cardoso, L.: Blood and interstitial flow in the hierarchical pore space architecture of bone tissue. J. Biomech. 48, 842–854 (2015). https://doi.org/10.1016/j.jbiomech.2014.12.013
Delaine-Smith, R.M., MacNeil, S., Reilly, G.C.: Matrix production and collagen structure are enhanced in two types of osteogenic progenitor cells by a simple fluid shear stress stimulus. Eur. Cell Mater. 24, 162–174 (2012). https://doi.org/10.22203/eCM.v024a12
Deng, F., Liu, L., Li, Z., Liu, J.: 3D printed Ti6Al4V bone scaffolds with different pore structure effects on bone ingrowth. J. Biol. Eng. 15, 4 (2021). https://doi.org/10.1186/s13036-021-00255-8
Dias, M.R., Fernandes, P.R., Guedes, J.M., Hollister, S.J.: Permeability analysis of scaffolds for bone tissue engineering. J. Biomech. 45, 938–944 (2012). https://doi.org/10.1016/j.jbiomech.2012.01.019
Dogan, E., Bhusal, A., Cecen, B., Miri, A.K.: 3D Printing metamaterials towards tissue engineering. Appl. Mater. Today 20, 100752 (2020). https://doi.org/10.1016/j.apmt.2020.100752
Egger, D., Fischer, M., Clementi, A., Ribitsch, V., Hansmann, J., Kasper, C.: Development and characterization of a parallelizable perfusion bioreactor for 3D cell culture. Bioengineering 4, 51 (2017). https://doi.org/10.3390/bioengineering4020051
Fu, M., Wang, F., Lin, G.: Design and research of bone repair scaffold based on two-way fluid–structure interaction. Comput. Methods Progr. Biomed. 204, 106055 (2021). https://doi.org/10.1016/j.cmpb.2021.106055
Gomes, M.E., Sikavitsas, V.I., Behravesh, E., Reis, R.L., Mikos, A.G.: Effect of flow perfusion on the osteogenic differentiation of bone marrow stromal cells cultured on starch-based three-dimensional scaffolds. J. Biomed. Mater. Res. 67A, 87–95 (2003). https://doi.org/10.1002/jbm.a.10075
Hildebrand, T., Rüegsegger, P.: A new method for the model‐independent assessment of thickness in three‐dimensional images. J. Microsc. 185(1), 67–75 (1997). https://doi.org/10.1046/j.1365-2818.1997.1340694.x
Hill, P.A.: Bone remodelling. Br. J. Orthod. 25, 101–107 (1998). https://doi.org/10.1093/ortho/25.2.101
Jones, A.C., Arns, C.H., Hutmacher, D.W., Milthorpe, B.K., Sheppard, A.P., Knackstedt, M.A.: The correlation of pore morphology, interconnectivity and physical properties of 3D ceramic scaffolds with bone ingrowth. Biomaterials 30, 1440–1451 (2009). https://doi.org/10.1016/j.biomaterials.2008.10.056
Kapfer, S.C., Hyde, S.T., Mecke, K., Arns, C.H., Schröder-Turk, G.E.: Minimal surface scaffold designs for tissue engineering. Biomaterials 32, 6875–6882 (2011). https://doi.org/10.1016/j.biomaterials.2011.06.012
Karim, A.R., Cherian, J.J., Jauregui, J.J., Pierce, T., Mont, M.A.: Osteonecrosis of the knee: review. Ann. Transl. Med. 3, 1–11 (2015). https://doi.org/10.3978/j.issn.2305-5839.2014.11.13
Kokubo, T., Takadama, H.: How useful is SBF in predicting in vivo bone bioactivity? Biomaterials 27, 2907–2915 (2006). https://doi.org/10.1016/j.biomaterials.2006.01.017
Kou, S., Pan, L., van Noort, D., Meng, G., Wu, X., Sun, H., Xu, J., Lee, I.: A multishear microfluidic device for quantitative analysis of calcium dynamics in osteoblasts. Biochem. Biophys. Res. Commun. 408, 350–355 (2011). https://doi.org/10.1016/j.bbrc.2011.04.044
Li, Y., Jahr, H., Lietaert, K., Pavanram, P., Yilmaz, A., Fockaert, L.I., Leeflang, M.A., Pouran, B., Gonzalez-Garcia, Y., Weinans, H., Mol, J.M.C., Zhou, J., Zadpoor, A.A.: Additively manufactured biodegradable porous iron. Acta Biomater. 77, 380–393 (2018). https://doi.org/10.1016/j.actbio.2018.07.011
Li, Y., Jahr, H., Pavanram, P., Bobbert, F.S.L., Puggi, U., Zhang, X., Pouran, B., Leeflang, M.A., Weinans, H., Zhou, J., Zadpoor, A.A.: Additively manufactured functionally graded biodegradable porous iron. Acta Biomater. 96, 646–661 (2019a). https://doi.org/10.1016/j.actbio.2019.11.040
Li, Y., Jahr, H., Zhang, X.Y., Leeflang, M.A., Li, W., Pouran, B., Tichelaar, F.D., Weinans, H., Zhou, J., Zadpoor, A.A.: Biodegradation-affected fatigue behavior of additively manufactured porous magnesium. Addit. Manufac. 28, 299–311 (2019b). https://doi.org/10.1016/j.addma.2019.05.013
Loh, Q.L., Choong, C.: Three-Dimensional Scaffolds for Tissue Engineering Applications: Role of Porosity and Pore Size. Tissue Eng. Part B Rev. 19(6), 485–502 (2013). https://doi.org/10.1089/ten.teb.2012.0437
Mazumdar, J.: Models of Biofluid Flows. In: Biofluid Mechanics, pp. 41–78. World Scientific (1992). https://doi.org/10.1142/1623
Mccoy, R.J., Jungreuthmayer, C., O’Brien, F.J.: Influence of flow rate and scaffold pore size on cell behavior during mechanical stimulation in a flow perfusion bioreactor. Biotechnol. Bioeng. 109, 1583–1594 (2012). https://doi.org/10.1002/bit.24424
Md Saad, A.P., Abdul Rahim, R.A., Harun, M.N., Basri, H., Abdullah, J., Abdul Kadir, M.R., Syahrom, A.: The influence of flow rates on the dynamic degradation behaviour of porous magnesium under a simulated environment of human cancellous bone. Mater. Des. 122, 268–279 (2017). https://doi.org/10.1016/j.matdes.2017.03.029
Metzger, T.A., Kreipke, T.C., Vaughan, T.J., McNamara, L.M., Niebur, G.L.: The in situ mechanics of trabecular bone marrow: the potential for mechanobiological response. J. Biomech. Eng. 137, 1–7 (2015). https://doi.org/10.1115/1.4028985
Nauman, E.A., Fong, K.E., Keaveny, T.M.: Dependence of intertrabecular permeability on flow direction and anatomic site. Ann. Biomed. Eng. 27, 517–524 (1999). https://doi.org/10.1114/1.195
Niu, J., Choo, H.L., Sun, W., Mok, S.H.: Numerical study on load-bearing capabilities of beam-like lattice structures with three different unit cells. Int. J. Mech. Mater. Des. 14, 443–460 (2018). https://doi.org/10.1007/s10999-017-9384-3
Noordin, M.A., Rahim, R.A.A., Roslan, A.N.H., Ali, I.A., Syahrom, A., Saad, A.P.M.: Controllable macroscopic architecture of subtractive manufactured porous iron for cancellous bone analogue: computational to experimental validation. J. Bionic. Eng. 17, 357–369 (2020). https://doi.org/10.1007/s42235-020-0029-0
Ouyang, P., Dong, H., He, X., Cai, X., Wang, Y., Li, J., Li, H., Jin, Z.: Hydromechanical mechanism behind the effect of pore size of porous titanium scaffolds on osteoblast response and bone ingrowth. Mater. Des. 183, 108151 (2019). https://doi.org/10.1016/j.matdes.2019.108151
Pandithevan, P., Saravana Kumar, G.: Personalised bone tissue engineering scaffold with controlled architecture using fractal tool paths in layered manufacturing. Virtual Phys. Prototyp. 4, 165–180 (2009a). https://doi.org/10.1080/17452750903055512
Pandithevan, P., Saravana Kumar, G.: Reconstruction of subject-specific human femoral bone model with cortical porosity data using macro-CT. Virtual Phys. Prototyp. 4, 115–129 (2009b). https://doi.org/10.1080/17452750902823241
Qin, Y.X., Kaplan, T., Saldanha, A., Rubin, C.: Fluid pressure gradients, arising from oscillations in intramedullary pressure, is correlated with the formation of bone and inhibition of intracortical porosity. J. Biomech. 36, 1427–1437 (2003). https://doi.org/10.1016/S0021-9290(03)00127-1
Rabiatul, A.A.R., Fatihhi, S.J., Md Saad, A.P., Zakaria, Z., Harun, M.N., Kadir, M.R.A., Öchsner, A., Zaman, T.K., Syahrom, A.: Fluid–structure interaction (FSI) modeling of bone marrow through trabecular bone structure under compression. Biomech. Model Mechanobiol. 20, 957–968 (2021). https://doi.org/10.1007/s10237-021-01423-x
Renders, G.A.P., Mulder, L., van Ruijven, L.J., van Eijden, T.M.G.J.: Porosity of human mandibular condylar bone. J. Anat. 210, 239–248 (2007). https://doi.org/10.1111/j.1469-7580.2007.00693.x
Sandino, C., Lacroix, D.: A dynamical study of the mechanical stimuli and tissue differentiation within a CaP scaffold based on micro-CT finite element models. Biomech. Model. Mechanobiol. 10, 565–576 (2011). https://doi.org/10.1007/s10237-010-0256-0
Schemitsch, E.H.: Size matters: defining critical in bone defect size! J. Orthop. Trauma 31, S20–S22 (2017). https://doi.org/10.1097/BOT.0000000000000978
Schubert, T., Lafont, S., Beaurin, G., Grisay, G., Behets, C., Gianello, P., Dufrane, D.: Critical size bone defect reconstruction by an autologous 3D osteogenic-like tissue derived from differentiated adipose MSCs. Biomaterials 34, 4428–4438 (2013). https://doi.org/10.1016/j.biomaterials.2013.02.053
Sharma, P., Pandey, P.M.: Corrosion behaviour of the porous iron scaffold in simulated body fluid for biodegradable implant application. Mater. Sci. Eng. C 99, 838–852 (2019). https://doi.org/10.1016/j.msec.2019.01.114
Shimko, D.A., Shimko, V.F., Sander, E.A., Dickson, K.F., Nauman, E.A.: Effect of porosity on the fluid flow characteristics and mechanical properties of tantalum scaffolds. J. Biomed. Mater. Res. Part B Appl. Biomater. 73, 315–324 (2005). https://doi.org/10.1002/jbm.b.30229
Sladkova, M., de Peppo, G.: Bioreactor systems for human bone tissue engineering. Processes. 2, 494–525 (2014). https://doi.org/10.3390/pr2020494
Stavenschi, E., Labour, M.-N., Hoey, D.A.: Oscillatory fluid flow induces the osteogenic lineage commitment of mesenchymal stem cells: the effect of shear stress magnitude, frequency, and duration. J. Biomech. 55, 99–106 (2017). https://doi.org/10.1016/j.jbiomech.2017.02.002
Syahrom, A., Abdul Kadir, M.R., Abdullah, J., Öchsner, A.: Permeability studies of artificial and natural cancellous bone structures. Med. Eng. Phys. 35, 792–799 (2013). https://doi.org/10.1016/j.medengphy.2012.08.011
Van Bael, S., Chai, Y.C., Truscello, S., Moesen, M., Kerckhofs, G., Van Oosterwyck, H., Kruth, J.P., Schrooten, J.: The effect of pore geometry on the in vitro biological behavior of human periosteum-derived cells seeded on selective laser-melted Ti6Al4V bone scaffolds. Acta Biomater. 8, 2824–2834 (2012). https://doi.org/10.1016/j.actbio.2012.04.001
van Gemert, J.T.M., Abbink, J.H., van Es, R.J.J., Rosenberg, A.J.W.P., Koole, R., Van Cann, E.M.: Early and late complications in the reconstructed mandible with free fibula flaps. J. Surg. Oncol. 117, 773–780 (2018). https://doi.org/10.1002/jso.24976
van Lenthe, G.H., Stauber, M., Müller, R.: Specimen-specific beam models for fast and accurate prediction of human trabecular bone mechanical properties. Bone 39, 1182–1189 (2006). https://doi.org/10.1016/j.bone.2006.06.033
Vaughan, T.J., Voisin, M., Niebur, G.L., McNamara, L.M.: Multiscale modeling of trabecular bone marrow: understanding the micromechanical environment of mesenchymal stem cells during osteoporosis. J. Biomech. Eng. 137, 011003 (2015). https://doi.org/10.1115/1.4028986
Vossenberg, P., Straten, G.A.H.G.V., Boxtel, C.A.V.B.A.J.B.V.: Darcian permeability constant as indicator for shear stresses in regular scaffold systems for tissue engineering. Biomech. Model. Mechanobiol. 8(6), 499–507 (2009). https://doi.org/10.1007/s10237-009-0153-6
Wang, S., Zhong, S., Lim, C.T., Nie, H.: Effects of fiber alignment on stem cells–fibrous scaffold interactions. J. Mater. Chem. B3(16), 3358–3366 (2015). https://doi.org/10.1039/C5TB00026B
Xu, B., Lee, K.W., Li, W., Yaszemski, M.J., Lu, L., Yang, Y., Wang, S.: A comparative study on cylindrical and spherical models in fabrication of bone tissue engineering scaffolds: finite element simulation and experiments. Mater. Des. 211, 110150 (2021). https://doi.org/10.1016/j.matdes.2021.110150
Yu, W., Qu, H., Hu, G., Zhang, Q., Song, K., Guan, H., Liu, T., Qin, J.: A microfluidic-based multi-shear device for investigating the effects of low fluid–induced stresses on osteoblasts. PLoS ONE 9, 1–7 (2014). https://doi.org/10.1371/journal.pone.0089966
Zhang, Y., Zhang, L., Sun, R., Jia, Y., Chen, X., Liu, Y., Oyang, H., Feng, L.: A new 3D printed titanium metal trabecular bone reconstruction system for early osteonecrosis of the femoral head. Medicine (united States). 97, 1–9 (2018). https://doi.org/10.1097/MD.0000000000011088
Zhao, F., Vaughan, T.J., Mcnamara, L.M.: Multiscale fluid–structure interaction modelling to determine the mechanical stimulation of bone cells in a tissue engineered scaffold. Biomech. Model. Mechanobiol. 14, 231–243 (2015). https://doi.org/10.1007/s10237-014-0599-z
Acknowledgements
This work was funded by the Ministry of Higher Education, Malaysia under the Fundamental Research Grant Scheme (FRGS/1/2018/TK03/UTM/02/8). The authors would like to thank the Research Management Centre (RMC), Universiti Teknologi Malaysia (UTM) for managing the project and the Center for Information and Communication Technology (CICT), Universiti Teknologi Malaysia (UTM) for supporting and providing high-performance computing facilities and services.
Funding
Funding is provided by Ministry of Higher Education, Malaysia (Grant No. FRGS/1/2018/TK03/UTM/02/8).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declared they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Noordin, M.A., Kori, M.I., Abdul Wahab, A.H. et al. Fluid Flow Analysis of Integrated Porous Bone Scaffold and Cancellous Bone at Different Skeletal Sites: In Silico Study. Transp Porous Med 145, 271–290 (2022). https://doi.org/10.1007/s11242-022-01849-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11242-022-01849-6