Hostname: page-component-cd9895bd7-dk4vv Total loading time: 0 Render date: 2024-12-23T16:37:25.778Z Has data issue: false hasContentIssue false

On the avascular ellipsoidal tumour growth model within a nutritive environment

Published online by Cambridge University Press:  18 September 2018

GEORGE FRAGOYIANNIS
Affiliation:
Department of Chemical Engineering, University of Patras, Patras, Greece email: [email protected]; [email protected]
FOTEINI KARIOTOU
Affiliation:
School of Science and Technology, Hellenic Open University, Patras, Greece email: [email protected]
PANAYIOTIS VAFEAS*
Affiliation:
Department of Chemical Engineering, University of Patras, Patras, Greece email: [email protected]; [email protected]

Abstract

The present work is part of a series of studies conducted by the authors on analytical models of avascular tumour growth that exhibit both geometrical anisotropy and physical inhomogeneity. In particular, we consider a tumour structure formed in distinct ellipsoidal regions occupied by cell populations at a certain stage of their biological cycle. The cancer cells receive nutrient by diffusion from an inhomogeneous supply and they are subject to also an inhomogeneous pressure field imposed by the tumour microenvironment. It is proved that the lack of symmetry is strongly connected to a special condition that should hold between the data imposed by the tumour’s surrounding medium, in order for the ellipsoidal growth to be realizable, a feature already present in other non-symmetrical yet more degenerate models. The nutrient and the inhibitor concentration, as well as the pressure field, are provided in analytical fashion via closed-form series solutions in terms of ellipsoidal eigenfunctions, while their behaviour is demonstrated by indicative plots. The evolution equation of all the tumour’s ellipsoidal interfaces is postulated in ellipsoidal terms and a numerical implementation is provided in view of its solution. From the mathematical point of view, the ellipsoidal system is the most general coordinate system that the Laplace operator, which dominates the mathematical models of avascular growth, enjoys spectral decomposition. Therefore, we consider the ellipsoidal model presented in this work, as the most general analytic model describing the avascular growth in inhomogeneous environment. Additionally, due to the intrinsic degrees of freedom inherited to the model by the ellipsoidal geometry, the ellipsoidal model presented can be adapted to a very populous class of avascular tumours, varying in figure and in orientation.

Type
Papers
Copyright
© Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adam, J. A. (1987) A mathematical model of tumour growth. II. Effects of geometry and spatial nonuniformity on stability. Math. Biosci. 86, 183211. doi: 10.1016/0025-5564(87)90010-1.CrossRefGoogle Scholar
Araujo, R. P. & McElwain, D. L. S. (2004) A history of the study of solid tumour growth: the contribution of mathematical modeling. Bull. Math. Biol. 66, 10391091. doi: 10.1016/j.bulm.2003.11.002.CrossRefGoogle Scholar
Burton, A. C. (1966) Rate of growth of solid tumors as a problem of diffusion. Growth 30, 157176.Google ScholarPubMed
Byrne, H. (1999) A weakly nonlinear analysis of a model of avascular solid tumour growth. J. Math. Biol. 39, 5989. doi: 10.1007/s002850050163.CrossRefGoogle Scholar
Byrne, H. M., Alarcon, T., Owen, M. R., Webb, S. D. & Maini, P. K. (2006) Modelling aspects of cancer dynamics: a review. Philos. Trans. R. Soc. 364, 15631578. doi: 10.1098/rsta.2006.1786.CrossRefGoogle ScholarPubMed
Byrne, H. M. & Chaplain, M. A. J. (1996) Growth of necrotic tumors in the presence and absence of inhibitors. Math. Biosci. 135, 187216. doi: 10.1016/0025-5564(96)00023-5.CrossRefGoogle ScholarPubMed
Chen, C. Y., Byrne, H. M. & King, J. R. (2001) The influence of growth induced stress from the surrounding medium on the development of multicell spheroids. J. Math. Biol. 43, 191220. doi: 10.1007/s002850100091.CrossRefGoogle ScholarPubMed
Dassios, G. (2012) Ellipsoidal Harmonics. Theory and Applications, Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Dassios, G., Kariotou, F., Sleeman, B. D. & Tsampas, M. N. (2012) Mathematical modeling of the avascular ellipsoidal tumour growth. Q. Appl. Math. 70, 124. doi: 10.1090/S0033-569X-2011-01240-2.CrossRefGoogle Scholar
Dassios, G., Kariotou, F. & Vafeas, P. (2013) Invariant vector harmonics. The ellipsoidal case. J. Math. Anal. Appl. 405, 652660. doi: 10.1016/j.jmaa.2013.03.015.CrossRefGoogle Scholar
Fasano, A., Bertuzzi, A. & Gandolfi, A. (2006) Mathematical modelling of tumour growth and treatment. In: Quarteroni, A., Formaggia, L., and Veneziani, A. (editors), Complex Systems in Biomedicine, Springer–Verlag, Milano, pp. 71108.CrossRefGoogle Scholar
Folkman, J. & Hochberg, M. (1973) Self-regulation of growth in three dimensions. J. Exp. Med. 138, 745753. doi: 10.1084/jem.138.4.745.CrossRefGoogle ScholarPubMed
Friedman, A. (2009) Free boundary problems associated with multiscale tumor models. Math. Model. Nat. Pheno. 4, 134155. doi: 10.1051/mmnp/20094306.CrossRefGoogle Scholar
Garcia, S. B., Park, H. S., Novelli, M. & Wright, N. A. (1999) Field cancerization, clonality and epithelial stem cells: the spread of mutated clones in epithelial sheets. J. Pathol. 187, 6181. doi: 10.1002/(ISSN)1096-9896.3.0.CO;2-I>CrossRefGoogle ScholarPubMed
Giverso, C. & Ciaretta, P. (2016) On the morphological stability of multicellular tumour spheroids growing in porous media. Eur. Phys. J. E. 39(10), 92.CrossRefGoogle ScholarPubMed
Greenspan, H. P. (1972) Models for the growth of a solid tumor by diffusion. Stud. Appl. Math. 51, 317340. doi: 10.1002/sapm.v51.4.CrossRefGoogle Scholar
Greenspan, H. P. (1976) On the growth and stability of cell cultures and solid tumors. J. Theor. Biol. 56, 229242. doi: 10.1016/S0022-5193(76)80054-9.CrossRefGoogle ScholarPubMed
Hadjinicolaou, M. & Kariotou, F. (2010) On the effect of 3D anisotropic tumour growth on modelling the nutrient distribution in the interior of the tumour. Bull. Greek Math. Soc. 57, 189197.Google Scholar
Helmlinger, G., Netti, P. A., Lichtenbeld, H. D., Melder, R. J. & Jain, R. K. (1997) Solid stress inhibits the growth of multicellular tumour spheroids. Nat. Biotechnol. 15, 778783. doi: 10.1038/nbt0897-778.CrossRefGoogle Scholar
Hobson, E. W. (1965) The Theory of Spherical and Ellipsoidal Harmonics, Chelsea Publishing Company, New York.Google Scholar
Jones, D. S. & Sleeman, B. D. (2008) Mathematical modeling of avascular and vascular tumor growth. Adv. Topics Scatter. Biomed. Eng. World Sci. 305331. doi: 10.1142/6865.CrossRefGoogle Scholar
Kariotou, F. & Vafeas, P. (2012) The avascular tumour growth in the presence of inhomogeneous physical parameters imposed from a finite spherical nutritive environment. Inter. J. Differ. Equ. 2012, 175434. doi: 10.1186/1687-1847-2012-1.Google Scholar
Kariotou, F. & Vafeas, P. (2014) On the transversally isotropic pressure effect on avascular tumour growth. Math. Methods Appl. Sci. 37, 277282. doi: 10.1002/mma.2789.CrossRefGoogle Scholar
Kariotou, F., Vafeas, P. & Papadopoulos, P. K. (2014) Mathematical modeling of tumour growth in inhomogeneous spheroidal environment. Inter. J. Biol. Biomed. Eng. 8, 132141.Google Scholar
Lowengrub, J. S., Frieboes, H. B., Jin, F., Chuang, Y.-L., Li, X., Macklin, P., Wise, S. M. & Christini, V. (2010) Nonlinear modelling of cancer: bridging the gap between cells and tumours. Nonlinearity 23, R1R9. doi: 10.1088/0951-7715/23/1/R01.CrossRefGoogle ScholarPubMed
Moon, P. & Spencer, D. E. (1988) Field Theory Handbook, Springer, Berlin.Google Scholar
Plank, M. J. & Sleeman, B. D. (2003) Tumour-induced angiogenesis: a review. J. Theor. Med. 5, 137153. doi: 10.1080/10273360410001700843.CrossRefGoogle Scholar
Preziosi, L. (2003) Cancer Modelling and Simulation, Chapman & Hall/CRC, London.CrossRefGoogle Scholar
Preziosi, L. & Tosin, A. (2009) Multiphase modelling of tumor growth and extra cellular matrix interaction: mathematical tools and applications. J. Math. Biol. 58, 625656. doi: 10.1007/s00285-008-0218-7.CrossRefGoogle Scholar
Roose, T., Chapman, S. J. & Maini, P. K. (2007) Mathematical models of avascular tumor growth. SIAM J. Appl. Math. 49, 179208. doi: 10.1137/S0036144504446291.Google Scholar
Sutherland, R. (1986) Importance of critical metabolites and cellular interactions in the biology of microregions of tumors. Cancer 58, 16681680. doi: 10.1002/(ISSN)1097-0142.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Sutherland, R. (1988) Cell and environment interactions in tumor microregions: the multicell spheroid model. Science 240, 177184. doi: 10.1126/science.2451290.CrossRefGoogle ScholarPubMed
Voutouri, C., Mpekris, F., Papageorgis, P., Odysseos, A. D., Stylianopoulos, T. (2014) Role of constitutive behavior and tumor-host mechanical interactions in the state of stress and growth of solid tumors. PLoS One 9(8), e104717. doi: 10.1371/journal.pone.0104717.CrossRefGoogle ScholarPubMed
Wright, N. A. (2002) Cell proliferation in carcinogenesis Chapter 18. In: Alison, M. R. (editor), The Cancer Handbook, Nature Publishing Group, MI, pp. 246255.Google Scholar