×

A framework for performing data-driven modeling of tumor growth with radiotherapy treatment. (English) Zbl 1460.92095

Segal, Rebecca (ed.) et al., Using mathematics to understand biological complexity. From cells to populations. Selected papers of the collaborative workshop for woman in mathematical biology, University of California, Los Angeles, CA, USA, June 17–21, 2019. Cham: Springer. Assoc. Women Math. Ser. 22, 179-216 (2021).
Summary: Recent technological advances make it possible to collect detailed information about tumors, and yet clinical assessments about treatment responses are typically based on sparse datasets. In this work, we propose a workflow for choosing an appropriate model, verifying parameter identifiability, and assessing the amount of data necessary to accurately calibrate model parameters. As a proof-of-concept, we compare tumor growth models of varying complexity in an effort to determine the level of model complexity needed to accurately predict tumor growth dynamics and response to radiotherapy. We consider a simple, one-compartment ordinary differential equation model which tracks tumor volume and a two-compartment model that accounts for tumor volume and the fraction of necrotic cells contained within the tumor. We investigate the structural and practical identifiability of these models, and the impact of noise on identifiability. We also generate synthetic data from a more complex, spatially-resolved, cellular automaton model (CA) that simulates tumor growth and response to radiotherapy. We investigate the fit of the ODE models to tumor volume data generated by the CA in various parameter regimes, and we use sequential model calibration to determine how many data points are required to accurately infer model parameters. Our results suggest that if data on tumor volumes alone is provided, then a tumor with a large necrotic volume is the most challenging case to fit. However, supplementing data on total tumor volume with additional information on the necrotic volume enables the two compartment ODE model to perform significantly better than the one compartment model in terms of parameter convergence and predictive power.
For the entire collection see [Zbl 1459.92003].

MSC:

92C50 Medical applications (general)
92C42 Systems biology, networks
68Q80 Cellular automata (computational aspects)
Full Text: DOI

References:

[1] E. Balsa-Canto, A. A. Alonso, J. R. Banga. An iterative identification procedure for dynamic modeling of biochemical networks. BMS Systems Biology. 4(11), (2010). doi:10.1186/1752-0509-4-11.
[2] Bellman, R.; Astrom, K. J., On structural Identifiability, Mathematical Biosciences, 7, 329-339 (1970) · doi:10.1016/0025-5564(70)90132-X
[3] Boemo, MA; Byrne, HM, Mathematical modelling of a hypoxia-regulated oncolytic virus delivered by tumour-associated macrophages, J Theor Biol, 461, 102-116 (2019) · Zbl 1406.92285 · doi:10.1016/j.jtbi.2018.10.044
[4] Byrne, H.; Preziosi, L., Modelling solid tumour growth using the theory of mixtures, Math Med Biol, 20, 341-366 (2003) · Zbl 1046.92023 · doi:10.1093/imammb/20.4.341
[5] Chappell, M. J.; Godfrey, K. R.; Vajda, S., Global identifiability of the parameters of nonlinear systems with specified inputs: a comparison of methods, Mathematical Biosciences, 102, 41-73 (1990) · Zbl 0789.93039 · doi:10.1016/0025-5564(90)90055-4
[6] Chis, OT; Banga, JR; Balsa-Canto, E., Structural identifiability of systems biology models: a critical comparison of methods, PLOS One., 6, 11, 1-16 (2011) · doi:10.1371/journal.pone.0027755
[7] Chis, OT; Banga, JR; Balsa-Canto, E., GenSSI: a software toolbox for structural identifiability analysis of biological models, Bioinformatics., 27, 18, 2610-2611 (2011)
[8] Collis, J.; Connor, AJ; Paczkowski, M.; Kannan, P.; Pitt-Francis, J.; Byrne, HM; Hubbard, ME, Bayesian calibration, validation and uncertainty quantification for predictive modeling of tumor growth: a tutorial, Bull. Math. Biol., 79, 4, 939-974 (2017) · Zbl 1372.92042 · doi:10.1007/s11538-017-0258-5
[9] da Costa, JMJ; Orlande, HRB; da Silaa, WB, Model selection and parameter estimation in tumor growth models using approximate Bayesian computation - ABC, Comp. Appl. Math., 37, 3, 2795-2815 (2018) · doi:10.1007/s40314-017-0479-0
[10] Enderling, H.; Chaplain, MAJ; Hahnfeldt, P., Quantitative modeling of tumor dynamics and radiotherapy, Acta Biotheoretica., 58, 4, 341-353 (2010) · doi:10.1007/s10441-010-9111-z
[11] Haario, H.; Laine, M.; Mira, A., Efficient adaptive MCMC, Stat. Comput., 26, 339-354 (2006) · doi:10.1007/s11222-006-9438-0
[12] E.J. Hall. Radiobiology for the radiologist. J.B. Lippincott, Philadelphia, 478-480 (1994).
[13] N. Harald. Random number generation and quasi-Monte Carlo method. SIAM (1992). · Zbl 0761.65002
[14] P. Kannan, M. Paczkowski, A. Miar, et al.: Radiation resistant cancer cells enhance the survival and resistance of sensitive cells in prostate spheroids. bioRxiv (2019). doi:10.1101/564724.
[15] Kursawe, J.; Baker, RE; Fletcher, AG, Approximate Bayesian computation reveals the importance of repeated measurements for parameterising cell-based models of growing tissues, J. Theor. Biol., 443, 66-81 (2018) · Zbl 1397.92165 · doi:10.1016/j.jtbi.2018.01.020
[16] Lambert, B.; MacLean, AL; Fletcher, AG; Combes, AN; Little, MH; Byrne, HM, Bayesian inference of agent-based models: a tool for studying kidney branching morphogenesis, J. Math. Biol., 76, 7, 1673-1697 (2018) · Zbl 1390.92022 · doi:10.1007/s00285-018-1208-z
[17] Lea, DE; Catcheside, DG, The mechanism of the induction by radiation of chromosome aberrations in tradescantia, Journal of Genetics., 44, 216-245 (1942) · doi:10.1007/BF02982830
[18] Lewin, TD, Modelling the impact of heterogeneity in tumor composition on the response to fractionated radiotherapy (2018), D. Phil: Thesis, University of Oxford, D. Phil
[19] T.D. Lewin, H.M. Byrne, P.K. Maini, J.J. Caudell, E.G. Moros, H. Enderling. The importance of dead material within a tumour on the dynamics in response to radiotherapy. Physics in Medicine and Biology. doi:10.1088/1361-6560/ab4c27 (2019).
[20] T.D. Lewin, P.K. Maini, E.G. Moros, H. Enderling, H.M. Byrne. A three-phase model to investigate the effects of dead material on the growth of avascular tumours. Mathematical Modelling of Natural Phenomena (in press) (2019). · Zbl 1467.92061
[21] Lima, E.; Oden, JT; Hormuth, DA 2nd; Yankeelov, TE; Almeida, RC, Selection, calibration, and validation of models of tumor growth, Mathematical Models and Methods in Applied Sciences, 26, 12, 2341-2368 (2016) · Zbl 1349.92075 · doi:10.1142/S021820251650055X
[22] Oden, JT; Hawkins, A.; Prudhomme, S., General diffuse-interface theories and an approach to predictive tumour growth modelling, Math. Models Meth. Appl. Sci., 20, 3, 477-517 (2010) · Zbl 1186.92024 · doi:10.1142/S0218202510004313
[23] Pohjanpalo, H., System identifiability based on the power series expansion of the solution, Mathematical Biosciences., 41, 21-33 (1978) · Zbl 0393.92008 · doi:10.1016/0025-5564(78)90063-9
[24] B. Ribba, N.H. Holford, P. Magni, I Troconiz, I Gueorguieva, P. Girard, C. Sarr, M. Elishmereni, C. Kloft, L.E. Friberg. A review of mixed-effects models of tumor growth and effects of anti-cancer treatment used in population analysis. CPT Pharmacometrics Syst. Pharmacol. 3, e113. (2014).
[25] R.C. Smith. Uncertainty Quantification: Theory, Implementation, and Applications. SIAM Computational Science and Engineering Series (CS12). (2014).
This reference list is based on information provided by the publisher or from digital mathematics libraries. Its items are heuristically matched to zbMATH identifiers and may contain data conversion errors. In some cases that data have been complemented/enhanced by data from zbMATH Open. This attempts to reflect the references listed in the original paper as accurately as possible without claiming completeness or a perfect matching.