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Mathematical modelling of collagen fibres rearrangement during the tendon healing process. (English) Zbl 1502.35176

Summary: Tendon injuries present a clinical challenge to modern medicine as they heal slowly and rarely is there full restoration to healthy tendon structure and mechanical strength. Moreover, the process of healing is not fully elucidated. To improve understanding of tendon function and the healing process, we propose a new model of collagen fibres rearrangement during tendon healing. The model consists of an integro-differential equation describing the dynamics of collagen fibres distribution. We further reduce the model in a suitable asym-ptotic regime leading to a nonlinear non-local Fokker-Planck type equation for the spatial and orientation distribution of collagen fibre bundles. Due to its simplicity, the reduced model allows for possible parameter estimation based on data. We showcase some of the qualitative properties of this model simulating its long time asymptotic behaviour and the total time for tendon fibres to align in terms of the model parameters. A possible biological interpretation of the numerical experiments performed leads us to the working hypothesis of the importance of tendon cell size in patient recovery.

MSC:

35Q92 PDEs in connection with biology, chemistry and other natural sciences
35Q84 Fokker-Planck equations
35R09 Integro-partial differential equations
92-08 Computational methods for problems pertaining to biology
92-10 Mathematical modeling or simulation for problems pertaining to biology
92C10 Biomechanics
92C50 Medical applications (general)
92C37 Cell biology
35B40 Asymptotic behavior of solutions to PDEs
Full Text: DOI

References:

[1] A. R. Akintunde; K. S. Miller, Evaluation of microstructurally motivated constitutive models to describe age-dependent tendon healing, Biomech Model Mechanobiol., 17, 793-814 (2018) · doi:10.1007/s10237-017-0993-4
[2] A. R. Akintunde; K. S. Miller; D. E. Schiavazzi, Bayesian inference of constitutive model parameters from uncertain uniaxial experiments on murine tendons, J Mech Behav Biomed Mater., 96, 285-300 (2019) · doi:10.1016/j.jmbbm.2019.04.037
[3] A. R. Akintunde, D. E. Schiavazzi and K. S. Miller, Mathematical Model of Age-Specific Tendon Healing, Computer Methods, Imaging and Visualization in Biomechanics and Biomedical Engineering, Springer International Publishing, 36 (2020), 288-296.
[4] J. Banasiak and M. Lachowicz, Kinetic Model of Alignment, Methods of Small Parameter in Mathematical Biology, Modeling and Simulation in Science, Engineering and Technology, Birkhäuser, 2014. · Zbl 1277.92003
[5] P. K. Beredjiklian, Biologic Aspects of Flexor Tendon Laceration and Repair, J Bone Joint Surg Am., 85, 539-550 (2003) · doi:10.2106/00004623-200303000-00025
[6] R. B. Bird, Ch. F. Curtiss, R. C. Armstrong and O. Hassager, Dynamics of polymeric liquids, Volume 1: Fluid mechanics, Wiley, (1987).
[7] R. B. Bird, Ch. F. Curtiss, R. C. Armstrong and O. Hassager, Dynamics of polymeric liquids, Volume 2: Kinetic Theory, Wiley, (1987).
[8] J. A. Carrillo; S. Cordier; G. Toscani, Over-populated tails for conservative-in-the-mean inelastic Maxwell models, Discrete Contin. Dyn. Syst. A., 24, 59-81 (2009) · Zbl 1163.82008 · doi:10.3934/dcds.2009.24.59
[9] J. A. Carrillo; M. Fornasier; J. Rosado; G. Toscani, Asymptotic flocking dynamics for the kinetic Cucker-Smale model,, SIAM J. Math. Anal., 42, 218-236 (2010) · Zbl 1223.35058 · doi:10.1137/090757290
[10] J. A. Carrillo; B. Yan, An asymptotic preserving scheme for the diffusive limit of kinetic systems for chemotaxis, Multiscale Model. Simul., 11, 336-361 (2013) · Zbl 1274.92007 · doi:10.1137/110851687
[11] J. A. Carrillo; A. Chertock; Y. Huang, A finite-volume method for nonlinear nonlocal equations with a gradient flow structure, Commun Comput Phys., 17, 233-258 (2015) · Zbl 1388.65077 · doi:10.4208/cicp.160214.010814a
[12] J. A. Carrillo; R. Eftimie; F. Hoffmann, Non-local kinetic and macroscopic models for self-organised animal aggregations, Kinet. Relat. Models., 8, 413-441 (2015) · Zbl 1330.35465 · doi:10.3934/krm.2015.8.413
[13] C. Chainais-Hillairet; F. Filbet, Asymptotic behaviour of a finite-volume scheme for the transient drift-diffusion model, IMA J. Numer. Anal., 27, 689-716 (2007) · Zbl 1133.65060 · doi:10.1093/imanum/drl045
[14] A. Chauviere, L. Preziosi and T. Hillen, Modeling the motion of a cell population in the extracellular matrix, Discrete Contin. Dyn. Syst. A., (2007), 250-259. · Zbl 1163.92313
[15] S. Cordier; L. Pareschi; G. Toscani, On a kinetic model for a simple market economy, J Stat Phys., 120, 253-277 (2005) · Zbl 1133.91474 · doi:10.1007/s10955-005-5456-0
[16] S. L. Curwin, Rehabilitation after tendon injuries, Tendon Injuries, Springer-Verlag, 24 (2005), 242-266.
[17] L. E. Dahners, Growth and development of tendons, Tendon Injuries, Springer-Verlag, 3 (2005), 22-24.
[18] P. Degond; B. Lucquin-Desreux, The Fokker-Planck asymptotics of the Boltzmann collision operator in the Coulomb case, Math. Models Methods Appl. Sci., 2, 167-182 (1992) · Zbl 0755.35091 · doi:10.1142/S0218202592000119
[19] P. Degond; S. Motsch, Continuum limit of self-driven particles with orientation interaction, Math. Models Methods Appl. Sci., 18, 1193-1215 (2008) · Zbl 1157.35492 · doi:10.1142/S0218202508003005
[20] D. Docheva; S. A. Müller; M. Majewski; H. E. Evans, Biologics for tendon repair, Adv. Drug Deliv. Rev., 84, 222-239 (2015) · doi:10.1016/j.addr.2014.11.015
[21] M. Doumic, B. Perthame and J. P. Zubelli, Numerical solution of an inverse problem in size-structured population dynamics, Inverse Probl., 25 (2009), 045008, 25 pp. · Zbl 1161.92020
[22] M. Doumic; P. Maia; J. P. Zubelli, On the calibration of a size-structured population model from experimental data, Acta Biotheor., 58, 405-413 (2010) · doi:10.1007/s10441-010-9114-9
[23] M. Doumic; A. Marciniak-Czochra; B. Perthame; J. P. Zubelli, A structured population model of cell differentiation, SIAM J Appl Math., 71, 1918-1940 (2011) · Zbl 1235.35030 · doi:10.1137/100816584
[24] M. Doumic; M. Hoffmann; N. Krell; L. Robert, Statistical estimation of a growth-fragmentation model observed on a genealogical tree, BERNOULLI, 21, 1760-1799 (2015) · Zbl 1388.62318 · doi:10.3150/14-BEJ623
[25] G. Dudziuk; M. Lachowicz; H. Leszczyński; Z. Szymańska, A simple model of collagen remodeling, Discrete Contin. Dyn. Syst. Ser. B., 24, 2205-2217 (2019) · Zbl 1421.35380 · doi:10.3934/dcdsb.2019091
[26] R. Eftimie; G. de Vries; M. A. Lewis, Complex spatial group patterns result from different animal communication mechanisms, PNAS, 104, 6974-6979 (2007) · Zbl 1156.92334 · doi:10.1073/pnas.0611483104
[27] R. C. Fetecau, Collective behavior of biological aggregations in two dimensions: A nonlocal kinetic model, Math. Modelels Methods Appl. Sci., 21, 1539-1569 (2011) · Zbl 1219.92073 · doi:10.1142/S0218202511005489
[28] R. C. Fetecau; R. Eftimie, An investigation of a nonlocal hyperbolic model for self-organization of biological groups, J. Math. Biol., 61, 545-579 (2009) · Zbl 1204.92072 · doi:10.1007/s00285-009-0311-6
[29] G. Furioli; A. Pulvirenti; E. Terraneo; G. Toscani, Fokker-Planck equations in the modeling of socio-economic phenomena, Math. Models Methods Appl. Sci., 27, 115-158 (2017) · Zbl 1362.35305 · doi:10.1142/S0218202517400048
[30] Y. Hyon; J. A. Carrillo; Q. Du; Ch. Liu, A maximum entropy principle based closure method for macro-micro models of polymeric materials, Kinet. Relat. Models., 1, 171-184 (2008) · Zbl 1388.74005 · doi:10.3934/krm.2008.1.171
[31] G. Jull, A. Moore, D. Falla, J. Lewis, C. McCarthy and M. Sterling, Grieve’s Modern Musculoskeletal Physiotherapy, \(4^{th}\) ed., Elsevier, 2015.
[32] D. Kader, M. Mosconi, F. Benazzo and N. Maffulli, Achilles tendon rupture, Tendon Injuries, Springer-Verlag, 20 (2005), 187-200.
[33] M. Kjær, Role of extracellular matrix in adaptation of tendon and skeletal muscle to mechanical loading, Physiol. Rev, 84, 649-698 (2004)
[34] M. Lachowicz; H. Leszczyński; M. Parisot, Blow-up and global existence for a kinetic equation of swarm formation, Math. Models Methods Appl. Sci., 27, 1153-1175 (2017) · Zbl 1367.35046 · doi:10.1142/S0218202517400115
[35] H. Y. Li and Y. H. Hua, Achilles tendinopathy: Current concepts about the basic science and clinical treatments, Biomed Res Int., 2016 (2016), 6492597, 9 pp.
[36] T. W. Lin; L. Cardenas; L. J. Soslowsky, Biomechanics of tendon injury and repair, J Biomech., 37, 865-877 (2004) · doi:10.1016/j.jbiomech.2003.11.005
[37] N. Loy; L. Preziosi, Modelling physical limits of migration by a kinetic model with non-local sensing, J Math Biol., 80, 1759-1801 (2020) · Zbl 1434.92014 · doi:10.1007/s00285-020-01479-w
[38] G. Nourissat; X. Houard; J. Sellam; D. Duprez; F. Berenbaum, Use of autologous growth factors in aging tendon and chronic tendinopathy, Front. Biosci., E5, 911-921 (2013) · doi:10.2741/E670
[39] M. O’Brian, Anatomy of tendon, Tendon Injuries, Springer-Verlag, 1 (2005), 3-13.
[40] H. G. Othmer; S. R. Dunbar; W. Alt, Models of dispersal in biological systems, J Math Biol., 26, 263-298 (1988) · Zbl 0713.92018 · doi:10.1007/BF00277392
[41] H. G. Othmer; T. Hillen, The diffusion limit of transport equations. II. Chemotaxis equations, SIAM J. Appl. Math., 62, 1222-1250 (2002) · Zbl 1103.35098 · doi:10.1137/S0036139900382772
[42] M. Parisot; M. Lachowicz, A kinetic model for the formation of swarms with nonlinear interactions, Kinet. Relat. Models., 9, 131-164 (2016) · Zbl 1335.92114 · doi:10.3934/krm.2016.9.131
[43] P. Sharma; N. Maffulli, Biology of tendon injury: Healing, modeling and remodeling, J Musculoskelet Neuronal Interact., 6, 181-190 (2006)
[44] P. Sharma; N. Maffulli, Tendinopathy and tendon injury: The future, Disabil Rehabil., 30, 1733-1745 (2008) · doi:10.1080/09638280701788274
[45] J. G. Snedeker; J. Foolen, Tendon injury and repair - A perspective on the basic mechanisms of tendon disease and future clinical therapy, Acta Biomater., 63, 18-36 (2017) · doi:10.1016/j.actbio.2017.08.032
[46] B. Perthame; J. P. Zubelli, On the inverse problem for a size-structured population model, Inverse Probl., 23, 1037-1052 (2007) · Zbl 1118.35072 · doi:10.1088/0266-5611/23/3/012
[47] N. Takahashi; P. Tangkawattana; Y. Ootomo; T. Hirose; J. Minaguchi; H. Ueda; M. Yamada; K. Takehana, Morphometric analysis of growing tenocytes in the superficial digital flexor tendon of piglets, J Vet Med Sci., 79, 1960-1967 (2017) · doi:10.1292/jvms.17-0436
[48] C. T. Thorpe and H. R. C. Screen, Tendon structure and composition, Metabolic Influences on Risk for Tendon Disorders, Advances in Experimental Medicine and Biology, Springer, 920 (2016), 3-10.
[49] G. Toscani, The grazing collisions asymptotics of the non-cut-off Kac equation, Esaim Math Model Numer Anal., 32, 763-772 (1998) · Zbl 0912.76081 · doi:10.1051/m2an/1998320607631
[50] G. Toscani, One-dimensional kinetic models of granular flows, Esaim Math Model Numer Anal., 34, 1277-1291 (2000) · Zbl 0981.76098 · doi:10.1051/m2an:2000127
[51] G. Toscani, Kinetic models of opinion formation, Commun. Math. Sci., 4, 481-496 (2006) · Zbl 1195.91128 · doi:10.4310/CMS.2006.v4.n3.a1
[52] F. Wu; M. Nerlich; D. Docheva, Tendon injuries: Basic science and new repair proposals, EFORT Open Rev., 2, 332-342 (2017) · doi:10.1302/2058-5241.2.160075
[53] G. Yang; B. B. Rothrauff; R. S. Tuan, Tendon and ligament regeneration and repair: Clinical relevance and developmental paradigm, Birth Defects Res. C, Embryo Today., 99, 203-222 (2013) · doi:10.1002/bdrc.21041
[54] K. A. Young, J. A. Wise, P. DeSaix, D. H. Kruse, B. Poe, E. Johnson, J. E. Johnson, O. Korol, J. Gordon Betts and M. Womble, Anatomy & Physiology, OpenStax, 2013.
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