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Poroelastic modeling of the intervertebral disc: A path toward integrated studies of tissue biophysics and organ degeneration

Published online by Cambridge University Press:  01 April 2015

Andrea Malandrino
Affiliation:
Massachusetts Institute of Technology, USA; m_andrea@mit.edu
Alicia R. Jackson
Affiliation:
University of Miami, USA; a.jackson2@miami.edu
Jacques M. Huyghe
Affiliation:
University of Limerick, Ireland; jacques.huyghe@ul.ie and Eindhoven University of Technology, The Netherlands; j.m.r.huyghe@tue.nl
Jérôme Noailly
Affiliation:
Universitat Pompeu Fabra, Spain; jerome.noailly@upf.edu
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Abstract

Lumbar intervertebral disc (IVD) degeneration is the leading cause of lower back pain. While lumbar IVDs have low cellularity and limited capacity of regeneration, they bear high mechanical loads. Accelerated disc degeneration may happen because of undue cell stimulation, and cell nutrition also seems to be particularly influent in the disc. Cell nutrition depends on exchange of oxygen, glucose, and lactate between the periphery and the various regions of the IVD, which in turn depends on mechanical deformations. The mechanical regulation of disc cell nutrition, known as indirect mechanotransduction, is difficult to study in vivo or in vitro. This review reports on an important alternative in the form of numerical methods, which are based on the ability of poromechanical models to be coupled to solute transport-reaction models. Models need to address intricate nonlinear and time-dependent phenomena, but have allowed for important mechanisms to be proposed, complementing current knowledge gained from in vivo or in vitro observations.

Type
Research Article
Copyright
Copyright © Materials Research Society 2015 

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References

Livshits, G., Popham, M., Malkin, I., Sambrook, P.N., Macgregor, A.J., Spector, T., Williams, F.M.K., Ann. Rheum. Dis. 70, 1740 (2011).Google Scholar
Antoniou, J., Steffen, T., Nelson, F., Winterbottom, N., Hollander, A.P., Poole, R.A., Alini, M., J. Clin. Invest. 98, 996 (1996).Google Scholar
Vo, N.V., Hartman, R.A., Yurube, T., Jacobs, L.J., Sowa, G.A., Kang, J.D., Spine J. 13, 331 (2013).Google Scholar
Neidlinger-Wilke, C., Mietsch, A., Rinkler, C., Wilke, H.-J., Ignatius, A., Urban, J.P.G., J. Orthop. Res. 30, 112 (2012).Google Scholar
Rinkler, C., Heuer, F., Pedro, M.T., Mauer, U.M., Ignatius, A., Neidlinger-Wilke, C., J. Neurosurg. Spine 13, 535 (2010).CrossRefGoogle Scholar
Huang, Y.-C., Urban, J.P.G., Luk, K.D.K., Nat. Rev. Rheumatol. 10, 561 (2014).Google Scholar
Iatridis, J.C., MacLean, J.J., Roughley, P.J., Alini, M., J. Bone Joint Surg. Am. 88 (Suppl. 2), 41 (2006).Google Scholar
Battié, M.C., Videman, T., Kaprio, J., Gibbons, L.E., Gill, K., Manninen, H., Peltonen, L., Spine J. 9, 47 (2009).Google Scholar
O’Connell, G.D., Vresilovic, E.J., Elliott, D.M., J. Orthop. Res. 29, 547 (2011).Google Scholar
Mow, V.C., Kuei, S.C., Lai, W.M., Armstrong, C.G., J. Biomech. Eng. 102, 73 (1980).CrossRefGoogle Scholar
Biot, M.A., J. Appl. Phys. 12, 155 (1941).Google Scholar
Simon, B.R., Wu, J.S.S., Carlton, M.W., Evans, J.H., Kazarian, L.E., J. Biomech. Eng. 107, 327 (1985).Google Scholar
Huyghe, J.M., Janssen, J.D., Int. J. Eng. Sci. 35, 793 (1997).Google Scholar
Malandrino, A., Planell, J.A., Lacroix, D., J. Biomech. 42, 2780 (2009).Google Scholar
Wagner, D.R., Lotz, J.C., J. Orthop. Res. 22, 901 (2004).CrossRefGoogle Scholar
Hsieh, A.H., Wagner, D.R., Cheng, L.Y., Lotz, J.C., J. Biomech. Eng. 127, 1158 (2005).Google Scholar
Malandrino, A., Noailly, J., Lacroix, D., Comput. Methods Biomech. Biomed. Eng. 16, 923 (2013).Google Scholar
Simon, B.R., Kaufmann, M.V., McAfee, M.A., Baldwin, A.L., Wilson, L.M., J. Biomech. Eng. 120, 188 (1998).Google Scholar
Treloar, L., The Physics of Rubber Elasticity, (Oxford University Press, UK, 3rd ed. 2005).CrossRefGoogle Scholar
Jacobs, N.T., Cortes, D.H., Peloquin, J.M., Vresilovic, E.J., Elliott, D.M., J. Biomech. 47, 2540 (2014).CrossRefGoogle Scholar
Zhu, D., Gu, G., Wu, W., Gong, H., Zhu, W., Jiang, T., Cao, Z., Clin. Biomech. 23 (Suppl. 1), S74 (2008).Google Scholar
Holzapfel, G.A., Schulze-Bauer, C.A.J., Feigl, G., Regitnig, P., Biomech. Model. Mechanobiol. 3, 125 (2005).CrossRefGoogle Scholar
Ebara, S., Iatridis, J.C., Setton, L.A., Foster, R.J., Mow, V.C., Weidenbaum, M., Spine (Phila Pa 1976) 21, 452 (1996).Google Scholar
Noailly, J., Planell, J.A., Lacroix, D., Biomech. Model. Mechanobiol. 10, 203 (2011).Google Scholar
Caner, F.C., Guo, Z., Moran, B., Bazant, Z.P., Carol, I., J. Biomech. Eng. 129, 632 (2007).CrossRefGoogle Scholar
Reutlinger, C., Bürki, A., Brandejsky, V., Ebert, L., Büchler, P., J. Mech. Behav. Biomed. Mater. 30, 279 (2014).Google Scholar
Eberlein, R., Holzapfel, G.A., Schulze-Bauer, C., Comput. Methods Biomech. Biomed. Eng. 4, 209 (2001).Google Scholar
Eberlein, R., Holzapfel, G.A., Fröhlich, M., Comput. Mech. 34, 147 (2004).Google Scholar
Gasser, T.C., Ogden, R.W., Holzapfel, G.A., J. R. Soc. Interface 3, 15 (2006).Google Scholar
Holzapfel, G.A., Gasser, T.C., Ogden, R.W., J. Elast. 61, 1 (2000).Google Scholar
Schroeder, Y., Wilson, W., Huyghe, J.M., Baaijens, F.P.T., Eur. Spine J. 15 (Suppl. 3), S361 (2006).Google Scholar
Schroeder, Y., Huyghe, J.M., van Donkelaar, C.C., Ito, K., Biomech. Model. Mechanobiol. 9, 641 (2010).Google Scholar
Malandrino, A., Pozo, J.M., Castro-Mateos, I., Frangi, A.F., van Rijsbergen, M.M., Ito, K., Noailly, J., Front. Bioeng. Biotechnol. 3, 1 (2015).Google Scholar
Holmes, M.H., Mow, V.C., J. Biomech. 23, 1145 (1990).Google Scholar
Galbusera, F., van Rijsbergen, M., Ito, K., Huyghe, J.M., Brayda-Bruno, M., Wilke, H.-J., Eur. Spine J. 23 (Suppl. 3), S324 (2014).Google Scholar
Wognum, S., Huyghe, J.M., Baaijens, F.P.T., Spine (Phila Pa 1976) 31, 1783 (2006).Google Scholar
Galbusera, F., Schmidt, H., Noailly, J., Malandrino, A., Lacroix, D., Wilke, H.-J., Shirazi-Adl, A., J. Mech. Behav. Biomed. Mater. 4, 1234 (2011).Google Scholar
Argoubi, M., Shirazi-Adl, A., J. Biomech. 29, 1331 (1996).Google Scholar
Ferguson, S.J., Ito, K., Nolte, L.-P., J. Biomech. 37, 213 (2004).Google Scholar
Schmidt, H., Shirazi-Adl, A., Galbusera, F., Wilke, H.-J., J. Biomech. 43, 1849 (2010).Google Scholar
Malandrino, A., Noailly, J., Lacroix, D., PLoS Comput. Biol. 7, e1002112 (2011).CrossRefGoogle Scholar
Lai, W.M., Hou, J.S., Mow, V.C., J. Biomech. Eng. 113, 245 (1991).Google Scholar
Yao, H., Gu, W.Y., Biorheology 43, 323 (2006).Google Scholar
Yao, H., Gu, W.Y., J. Biomech. 40, 2071 (2007).Google Scholar
Jin, M., Grodzinsky, A.J., Macromolecules 34, 8330 (2001).Google Scholar
Roos, R.W., Petterson, R., Huyghe, J.M., Biomech. Model. Mechanobiol. 12, 617 (2013).CrossRefGoogle Scholar
Zhu, Q., Jackson, A.R., Gu, W.Y., J. Biomech. 45, 2769 (2012).Google Scholar
Ruiz, C., Malandrino, A., Lacroix, D., Ito, K., Noailly, J., paper presented at the 11th World Congress on Computational Mechanics (WCCM XI), Barcelona, Spain, July 20–25 2014.Google Scholar
Coventry, M.B., Ghormley, R.K., Kernohan, J.W., J. Bone Joint Surg. 27, 105 (1945).Google Scholar
Pokharna, H.K., Phillips, F.M., Spine (Phila Pa 1976) 23, 1645 (1998).Google Scholar
Iatridis, J.C., Setton, L.A., Foster, R.J., Rawlins, B.A., Weidenbaum, M., Mow, V.C., J. Biomech. 31, 535 (1998).Google Scholar
Malandrino, A., thesis, Technical University of Catalonia, Barcelona, Spain (2012).Google Scholar
Galbusera, F., Schmidt, H., Neidlinger-Wilke, C., Gottschalk, A., Wilke, H.-J., Eur. Spine J. 20, 563 (2011).CrossRefGoogle Scholar
Dormieux, L., Kondo, D., Rev. Eur. Génie Civ. 11, 945 (2007).Google Scholar
Antoniou, J., Epure, L.M., Michalek, A.J., Grant, M.P., Iatridis, J.C., Mwale, F., J. Magn. Reson. Imaging 38, 1402 (2013).Google Scholar
Sharma, A., Pilgram, T., Wippold, F.J., AJNR Am. J. Neuroradiol. 30, 500 (2009).Google Scholar
Hilton, R.C., Ball, J., Benn, R.T., Ann. Rheum. Dis. 39, 533 (1980).Google Scholar
Munter, F.M., Wasserman, B.A., Wu, H.-M., Yousem, D.M., AJNR Am. J. Neuroradiol. 23, 1105 (2002).Google Scholar
Gardner-Morse, M., J. Biomech. 37, 205 (2004).Google Scholar
Panjabi, M.M., Krag, M.H., Chung, T.Q., Spine (Phila Pa 1976) 9, 707 (1984).Google Scholar
Maroudas, A., Stockwell, R.A., Nachemson, A., Urban, J., J. Anat. 120, 113 (1975).Google Scholar
Urban, J.P.G., Smith, S., Fairbank, J.C.T., Spine (Phila Pa 1976) 29, 2700 (2004).Google Scholar
Holm, S., Maroudas, A., Urban, J.P.G., Selstam, G., Nachemson, A., Connect. Tissue Res. 8, 101 (1981).Google Scholar
Bibby, S.R.S., Jones, D.A., Lee, R.B., Yu, J., Urban, J.P.G., Joint Bone Spine 68, 537 (2001).Google Scholar
Bibby, S.R.S., Jones, D.A., Ripley, R.M., Urban, J.P.G., Spine 30, 487 (2005).CrossRefGoogle Scholar
Soukane, D.M., Shirazi-Adl, A., Urban, J.P.G., J. Biomech. 40, 2645 (2007).Google Scholar
Huang, C.-Y., Gu, W.Y., J. Biomech. 41, 1184 (2008).Google Scholar
Soukane, D.M., Shirazi-Adl, A., Urban, J.P.G., Eur. Spine J. 18, 254 (2009).Google Scholar
Soukane, D.M., Shirazi-Adl, A., Urban, J.P.G., J. Biomech. Eng. 127, 1121 (2005).Google Scholar
Magnier, C., Boiron, O., Wendling-Mansuy, S., Chabrand, P., Deplano, V., J. Biomech. 42, 100 (2009).Google Scholar
Jackson, A.R., Huang, C.-Y.C., Brown, M.D., Gu, W.Y., J. Biomech. Eng. 133, 091006 (2011).Google Scholar
Galbusera, F., Mietsch, A., Schmidt, H., Wilke, H.-J., Neidlinger-Wilke, C., Comput. Methods Biomech. Biomed. Eng. 16, 328 (2013).Google Scholar
Malandrino, A., Noailly, J., Lacroix, D., J. Biomech. 47, 1520 (2014).Google Scholar
Urban, J., Holm, S., Maroudas, A., Nachemson, A., Clin. Orthop. Relat. Res. 170, 296 (1982).Google Scholar
Katz, M.M., Hargens, A.R., Garfin, S.R., Clin. Orthop. Relat. Res. 210, 243 (1986).Google Scholar
Razaq, S., Wilkins, R.J., Urban, J.P.G., Eur. Spine J. 12, 341 (2003).CrossRefGoogle Scholar
Bibby, S.R.S., Fairbank, J.C.T., Urban, M.R., Urban, J.P.G., Spine (Phila Pa 1976) 27, 2220 (2002).Google Scholar
Horner, H.A., Urban, J.P., Spine (Phila Pa 1976) 26, 2543 (2001).Google Scholar
Johnson, W.E., Eisenstein, S.M., Roberts, S., Connect. Tissue Res. 42, 197 (2001).Google Scholar
Bibby, S.R.S., Urban, J.P.G., Eur. Spine J. 13, 695 (2004).Google Scholar
Guehring, T., Wilde, G., Sumner, M., Grünhagen, T., Karney, G.B., Tirlapur, U.K., Urban, J.P.G., Arthritis Rheum. 60, 1026 (2009).Google Scholar
Shirazi-Adl, A., Taheri, M., Urban, J., J. Biomech. 43, 1330 (2010).Google Scholar
Lin, J., Lee, S.-M., Lee, H.-J., Koo, Y.-M., Biotechnol. Bioprocess Eng. 5, 382 (2000).Google Scholar
Peloquin, J.M., Yoder, J.H., Jacobs, N.T., Moon, S.M., Wright, A.C., Vresilovic, E.J., Elliott, D.M., J. Biomech. 47, 2452 (2014).Google Scholar
Martinez, J.B., Oloyede, V.O., Broom, N.D., Med. Eng. Phys. 19, 145 (1997).Google Scholar
Williams, J.R., Natarajan, R.N., Andersson, G.B.J., J. Biomech. 40, 1981 (2007).Google Scholar
Castro, A.P.G., Paul, C.P.L., Detiger, S.E.L., Smit, T.H., van Royen, B.J., Pimenta Claro, J.C., Mullender, M.J., Alves, J.L., Front. Bioeng. Biotechnol. 2, 56 (2014).Google Scholar
Malandrino, A., Lacroix, D., Noailly, J., Poromechanics V (American Society of Civil Engineers, Reston, VA, 2013), pp. 21932201.Google Scholar
Jackson, A.R., Huang, C.-Y., Gu, W.Y., Comput. Methods Biomech. Biomed. Eng. 14, 195 (2011).Google Scholar
Illien-Jünger, S., Gantenbein-Ritter, B., Grad, S., Lezuo, P., Ferguson, S.J., Alini, M., Ito, K., Spine (Phila Pa 1976) 35, 1744 (2010).Google Scholar
Lee, C.R., Iatridis, J.C., Poveda, L., Alini, M., Spine (Phila Pa 1976) 31, 515 (2006).Google Scholar
Malandrino, A., Lacroix, D., Hellmich, C., Ito, K., Ferguson, S.J., Noailly, J., Osteoarthr. Cartil. 22, 1053 (2014).Google Scholar
Noailly, J., Malandrino, A., Galbusera, F., in Computational Modelling of Biomechanics and Biotribology in the Musculoskeletal System (Woodhead Publishing, Cambridge, UK, 2014), pp. 447484.Google Scholar
Rodriguez, A.G., Slichter, C.K., Acosta, F.L., Rodriguez-Soto, A.E., Burghardt, A.J., Majumdar, S., Lotz, J.C., Spine (Phila Pa 1976) 36, 512 (2011).Google Scholar
Lories, R.J., Luyten, F.P., Nat. Rev. Rheumatol. 7, 43 (2010).Google Scholar
Wuertz, K., Godburn, K., MacLean, J.J., Barbir, A., Donnelly, J.S., Roughley, P.J., Iatridis, J.C., J. Orthop. Res. 27, 1235 (2009).Google Scholar
Wang, D.-L., Jiang, S.-D., Dai, L.-Y., Spine (Phila Pa 1976) 32, 2521 (2007).Google Scholar
Kroeber, M., Unglaub, F., Guehring, T., Nerlich, A., Hadi, T., Carstens, C., Spine (Phila Pa 1976) 30, 181 (2005).Google Scholar
Kasra, M., Goel, V., Martin, J., Wang, S.-T., Choi, W., Buckwalter, J., J. Orthop. Res. 21, 597 (2003).Google Scholar
Iatridis, J.C., Michalek, A.J., Purmessur, D., Korecki, C.L., Cell. Mol. Bioeng. 2, 437 (2009).Google Scholar
Motaghinasab, S., Shirazi-Adl, A., Parnianpour, M., Urban, J.P.G., Eur. Spine J. 23, 715 (2014).Google Scholar
Stokes, I.A., Chegini, S., Ferguson, S.J., Gardner-Morse, M.G., Iatridis, J.C., Laible, J.P., Ann. Biomed. Eng. 38, 1780 (2010).Google Scholar
Ruiz, C., Noailly, J., Lacroix, D., J. Mech. Behav. Biomed. Mater. 26, 1 (2013).Google Scholar
Bartels, E.M., Fairbank, J.C.T., Winlove, C.P., Urban, J.P.G., Spine (Phila Pa 1976) 23, 1 (1998).Google Scholar
Salvatierra, J.C., Yuan, T.Y., Fernando, H., Castillo, A., Gu, W.Y., Cheung, H.S., Huant, C.-Y.C., Cell. Mol. Bioeng. 4, 302 (2011).Google Scholar
Fernando, H.N., Czamanski, J., Yuan, T.-Y., Gu, W., Salahadin, A., Huang, C.-Y.C., J. Orthop. Res. 29, 1634 (2011).Google Scholar
Gu, W., Zhu, Q., Gao, X., Brown, M.D., Spine (Phila Pa 1976) 39, E1411 (2014).Google Scholar
Handa, T., Ishihara, H., Ohshima, H., Osada, R., Tsuji, H., Obata, K., Spine (Phila Pa 1976) 22, 1085 (1997).Google Scholar
Iatridis, J.C., MacLean, J.J., O’Brien, M., Stokes, I.A.F., Spine (Phila Pa 1976) 32, 1493 (2007).Google Scholar