Abstract
Computational models of tumors have the potential to connect observations made on the cellular and the tissue scales. With cellular scale models, each cell can be treated as a discrete entity, while tissue scale models typically represent tumors as a continuum. Though the discrete approach often enables a more mechanistic and biologically driven description of cellular behavior, it is often computationally intractable on the tissue scale. Here, we adapt peridynamics, a theoretical and computational approach designed to unify the mechanics of discrete and continuous media, for the growth of biological materials. The result is a computational model for tumor growth that can represent either individual cells or the tissue as a whole. We take advantage of the flexibility provided by the peridynamic framework to implement a cell division mechanism, motivated by the fact that cell division is the mechanism driving tumor growth. This paper provides a general framework for implementing a new tumor growth modeling technique.
Similar content being viewed by others
References
Ambrosi D, Mollica F (2002) On the mechanics of a growing tumor. Int J Eng Sci 40:1297–1316
Ambrosi D, Preziosi L (2008) Cell adhesion mechanisms and stress relaxation in the mechanics of tumours. Biomech Model Mechanobiol 8(5):397–413
Ambrosi D, Ateshian G, Arruda E, Cowin S, Dumais J, Goriely A, Holzapfel G, Humphrey J, Kemkemer R, Kuhl E et al (2011) Perspectives on biological growth and remodeling. J Mech Phys Solids 59(4):863–883
Ambrosi D, Preziosi L, Vitale G (2012) The interplay between stress and growth in solid tumors. Mech Res Commun 42:87–91
Araujo RP, McElwain DLS (2004) A linear-elastic model of anisotropic tumour growth. Eur J Appl Math 15(3):365–384
Bellomo N, Li NK, Maini PK (2008) On the foundations of cancer modelling: selected topics, speculations, and perspectives. Math Models Methods Appl Sci 18(4):593–646
Bobaru F, Ha YD (2011) Adaptive refinement and multiscale modeling in 2D peridynamics. J Multiscale Comput Eng 9(6):635–659
Bobaru F, Yang M, Alves LF, Silling SA, Askari E, Xu J (2009) Convergence, adaptive refinement, and scaling in 1D peridynamics. Int J Numer Meth Eng 77(6):852–877
Byrne H (2003) Modelling solid tumour growth using the theory of mixtures. Math Med Biol 20(4):341–366
Byrne H, Drasdo D (2008) Individual-based and continuum models of growing cell populations: a comparison. J Math Biol 58(4–5):657–687
Clatz O, Sermesant M, Bondiau PY, Delingette H, Warfield SK, Malandain G, Ayache N (2005) Realistic simulation of the 3-D growth of brain tumors in MR images coupling diffusion with biomechanical deformation. IEEE Trans Med Imaging 24(10):1334–1346
Cristini V (2005) Morphologic instability and cancer invasion. Clin Cancer Res 11(19):6772–6779
Cristini V, Lowengrub J, Nie Q (2002) Nonlinear simulation of tumor growth. J Math Biol 46:191–224
Deisboeck TS, Wang Z, Macklin P, Cristini V (2011) Multiscale cancer modeling. Annu Rev Biomed Eng 13:127–155
Deng Q, Chen Y, Lee J (2008) An investigation of the microscopic mechanism of fracture and healing processes in cortical bone. Int J Damage Mech 18(5):491–502
Drasdo D, Höhme S (2005) A single-cell-based model of tumor growth in vitro: monolayers and spheroids. Phys Biol 2(3):133–147
Drasdo D, Höhme S, Block M (2007) On the role of physics in the growth and pattern formation of multi-cellular systems: What can we learn from individual-cell based models? J Stat Phys 128(1–2):287–345
Foster JT, Silling SA, Chen WW (2009) Viscoplasticity using peridynamics. Int J Numer Methods Eng 81:1242–1258
Frieboes HB, Lowengrub JS, Wise S, Zheng X, Macklin P, Bearer EL, Cristini V (2007) Computer simulation of glioma growth and morphology. Neuroimage 37:S59–S70
Gatenby R, Gawlinski E (1996) A reaction–diffusion model of cancer invasion. Cancer Res 56(24):5745–5753
Gillies TE, Cabernard C (2011) Cell division orientation in animals. Curr Biol 21(15):R599–R609
Helmlinger G, Netti PA, Lichtenbeld HC, Melder RJ, Jain RK (1997) Solid stress inhibits the growth of multicellular tumor spheroids. Nat Biotechnol 15:778–783
Kilic B, Madenci E (2010a) An adaptive dynamic relaxation method for quasi-static simulations using the peridynamic theory. Theor Appl Fract Mech 53(3):194–204
Kilic B, Madenci E (2010b) Peridynamic theory for thermomechanical analysis. IEEE Trans Adv Packag 33(1):97–105
Kim Y, Stolarska MA, Othmer HG (2007) A hybrid model for tumor spheroid growth in vitro I: theoretical development and early results. Math Models Methods Appl Sci 17:1773–1798
Kuhl E, Maas R, Himpel G, Menzel A (2006) Computational modeling of arterial wall growth. Biomech Model Mechanobiol 6(5):321–331
Lejeune E, Javili A, Linder C (2016a) An algorithmic approach to multi-layer wrinkling. Extreme Mech Lett 7:10–17
Lejeune E, Javili A, Linder C (2016b) Understanding geometric instabilities in thin films via a multi-layer model. Soft Matter 12:806–816
Lejeune E, Javili A, Weickenmeier JE, Kuhl LC (2016c) Tri-layer wrinkling as a mechanism for anchoring center initiation in the developing cerebellum. Soft Matter 12:5613–5620
Linder C, Tkachuk M, Miehe C (2011) A micromechanically motivated diffusion-based transient network model and its incorporation into finite rubber viscoelasticity. J Mech Phys Solids 59(10):2134–2156
Littlewood D (2015) Roadmap for peridynamic software implementation. SAND Report, Aandia National Laboratories, Albuquerque, NM and Livermore, CA
Lowengrub JS, Frieboes HB, Jin F, Chuang YL, Li X, Macklin P, Wise SM, Cristini V (2010) Nonlinear modelling of cancer: bridging the gap between cells and tumours. Nonlinearity 23:R1–R91
Madenci E, Oterkus E (2014) Peridynamic theory and its applications. Springer, NewYork
Mitchell JA (2011) A nonlocal, ordinary, state-based plasticity model for peridynamics. SAND report 3166
Norton KA, Wininger M, Bhanot G, Ganesan S, Barnard N, Shinbrot T (2010) A 2d mechanistic model of breast ductal carcinoma in situ (DCIS) morphology and progression. J Theor Biol 263(4):393–406
Poste G, Fidler I (1980) The pathogenesis of cancer metastasis. Nature 283(5743):139–146
Preziosi L, Tosin A (2008) Multiphase modelling of tumour growth and extracellular matrix interaction: mathematical tools and applications. J Math Biol 58(4–5):625–656
Ren H, Zhuang X, Cai Y, Rabczuk T (2016) Dual-horizon peridynamics. Int J Numer Meth Eng 108(12):1451–1476
Sandersius SA, Newman TJ (2008) Modeling cell rheology with the subcellular element model. Phys Biol 5(1):015002
Silling S, Askari E (2005) A meshfree method based on the peridynamic model of solid mechanics. Comput Struct 83(17–18):1526–1535
Silling SA (2000) Reformulation of elasticity theory for discontinuities and long-range forces. J Mech Phys Solids 48:175–209
Silling SA, Lehoucq RB (2010) Peridynamic theory of solid mechanics. Adv Appl Mech 44:73–168
Silling SA, Epton M, Weckner O, Xu J, Askari E (2007) Peridynamic states and constitutive modeling. J Elast 88(2):151–184
Stolarska MA, Kim Y, Othmer HG (2009) Multi-scale models of cell and tissue dynamics. Philos Trans R Soc A Math Phys Eng Sci 367(1902):3525–3553
Timoshenko S (1925) Analysis of bi-metal thermostats. JOSA 11(3):233–255
Wang Z, Butner J, Kerketta R, Cristini V, Deisboeck TS (2015) Simulating cancer growth with multiscale agent-based modeling. Semin Cancer Biol 30:70–78
Warren TL, Silling SA, Askari A, Weckner O, Epton MA, Xu J (2009) A non-ordinary state-based peridynamic method to model solid material deformation and fracture. Int J Solids Struct 46(5):1186–1195
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Funding
This work was supported by the National Science Foundation Graduate Research Fellowship under Grant No. DGE-114747.
Conflict of interest
The authors declare that they have no conflict of interest.
Rights and permissions
About this article
Cite this article
Lejeune, E., Linder, C. Modeling tumor growth with peridynamics. Biomech Model Mechanobiol 16, 1141–1157 (2017). https://doi.org/10.1007/s10237-017-0876-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10237-017-0876-8