The DOI matches its Crossref record; 38 of the 39 references it cites were found in a registry or an index.
Analysis of growth of multicellular tumour spheroids by mathematical models.
Abstract
We wished to determine the applicability of previously proposed deterministic mathematical models to description of growth of multicellular tumour spheroids. The models were placed into three general classes: empirical, functional and structural. From these classes, 17 models were applied systematically to growth curves of multicellular tumour spheroids used as paradigms of prevascular and microregional tumour growth. The spheroid growth curves were determined with uniquely high density of measurements and high precision. The theoretical growth curves obtained from the models were fitted by the weighted least-squares method to the 15 measured growth curves, each corresponding to a different cell line. The classical growth models such as von Bertalanffy, logistic and Gompertz were considered as nested within more general models. Our results demonstrate that most models fitted the data fairly well and that criteria other than statistical had to be used for final selection. The Gompertz, the autostimulation and the simple spheroid models were the most appropriate for spheroid growth in the empirical, functional and structural classes of models, respectively. We also showed that some models (e.g. logistic, von Bertalanffy) were clearly inadequate. Thus, contrary to the widely held belief, the sigmoid character of a three or more parameter growth function is not sufficient for adequate fits.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“The authors concluded that the standard Gompertz curve [29], defined as could not be distinguished from the actual growth curves within the margin of error of the experimental data.”
From When the Optimal Is Not the Best: Parameter Estimation in Complex Biological Models (2010) · cites this paper as [14]
Citations
Cites
Estimating the Dimension of a Model
Schwarz, G. (1978) · The Annals of Statistics · doi:10.1214/aos/1176344136 · Cited by 47,033
An introduction to probability theory and its applications
(1958) · Journal of the Franklin Institute · doi:10.1016/0016-0032(58)90688-4 · Cited by 29,621
An Introduction to Probability Theory and its Applications.
Kingmán, J. F. C., & Feller, W. (1972) · Journal of the Royal Statistical Society Series A (General) · doi:10.2307/2344620 · Cited by 5,297
Discrete Multivariate Analysis: Theory and Practice.
Beniger, J. R., Bishop, Y. M. M., Feinberg, S. E., Holland, P. W., Light, R. J., & Mosteller, F. C. (1975) · Contemporary Sociology A Journal of Reviews · doi:10.2307/2063625 · Cited by 5,119
Gompertz, B. (1825) · Philosophical Transactions of the Royal Society of London · doi:10.1098/rstl.1825.0026 · Cited by 3,816
TESTING FOR SERIAL CORRELATION IN LEAST SQUARES REGRESSION. II
Durbin, J., & Watson, G. S. (1951) · Biometrika · doi:10.1093/biomet/38.1-2.159 · Cited by 3,636
Quantitative Laws in Metabolism and Growth
von Bertalanffy, L. (1957) · The Quarterly Review of Biology · doi:10.1086/401873 · Cited by 2,068
Cell and environment interactions in tumor microregions: the multicell spheroid model.
Sutherland, R. M. (1988) · Science · doi:10.1126/science.2451290 · Cited by 1,803
TESTING FOR SERIAL CORRELATION IN LEAST SQUARES REGRESSION. I
Durbin, J., & Watson, G. S. (1950) · Biometrika · doi:10.1093/biomet/37.3-4.409 · Cited by 1,775
Discrete Multivariate Analysis: Theory and Practice.
Plackett, R. L., Bishop, Y. M. M., Fienberg, S. E., & Holland, P. W. (1976) · Journal of the Royal Statistical Society Series A (General) · doi:10.2307/2344845 · Cited by 1,727
Research works printed but not linked: 9
- Bajzer Ž, 1994, Proceedings of the First World Congress of Nonlinear Analists.
- Bertalanffy L., 1941, Untersuchungen über dieGesetzlichkeit des Wachstums, VII, Stoffwechseltypen und Wachstumtypen, Biol. Zentralbl., 61, 510
- Cook RD, 1990, Statistical Methodology in the Pharmacological Sciences, 163
- Freyer JP, 1986, Regulation of growth saturation and development of necrosis by glucose and oxygen supply, Cancer Res., 46, 3504
- More JJ, 1977, Numerical Analysis
- Pearl R., 1924, Studies in Human Biology.
- Press WH, 1986, Numerical Recipes
- Steel GG, 1977, Growth kinetics of tumors., 21
- Verhulst PF, 1838, Notice sur la loi que la population suit dans son accroissement, Corr. Math. Phys., 10, 113
Cited by
Sorted by citations
Multicellular tumor spheroids: An underestimated tool is catching up again
Hirschhaeuser, F., Menne, H., Dittfeld, C., West, J., Mueller-Klieser, W., & Kunz-Schughart, L. A. (2010) · Journal of Biotechnology · doi:10.1016/j.jbiotec.2010.01.012 · Cited by 1,674
3D tumor spheroids: an overview on the tools and techniques used for their analysis
Costa, E. C., Moreira, A. F., de Melo-Diogo, D., Gaspar, V. M., Carvalho, M. P., & Correia, I. J. (2016) · Biotechnology Advances · doi:10.1016/j.biotechadv.2016.11.002 · Cited by 929
The use of 3-d cultures for high-throughput screening: the multicellular spheroid model.
Kunz-Schughart, L. A., Freyer, J. P., Hofstaedter, F., & Ebner, R. (2004) · SLAS DISCOVERY · doi:10.1177/1087057104265040 · Cited by 797
Self-citationClassical Mathematical Models for Description and Prediction of Experimental Tumor Growth
Benzekry, S., Lamont, C., Beheshti, A., Tracz, A., Ebos, J. M. L., Hlatky, L., & Hahnfeldt, P. (2014) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003800 · Cited by 586
A hybrid mathematical model of solid tumour invasion: the importance of cell adhesion
Anderson, A. R. A. (2005) · Mathematical Medicine and Biology A Journal of the IMA · doi:10.1093/imammb/dqi005 · Cited by 566
Growth of nonnecrotic tumors in the presence and absence of inhibitors
Byrne, H. M., & Chaplain, M. A. J. (1995) · Mathematical Biosciences · doi:10.1016/0025-5564(94)00117-3 · Cited by 475
Simulated Brain Tumor Growth Dynamics Using a Three-Dimensional Cellular Automaton
KANSAL, A. R., Salvatore Torquato, A., Harsh, G. R., Chiocca, E. A., & Deisboeck, T. S. (2000) · Journal of Theoretical Biology · doi:10.1006/jtbi.2000.2000 · Cited by 436
Challenges of applying multicellular tumor spheroids in preclinical phase
Han, S. J., Kwon, S., & Kim, K. S. (2021) · Cancer Cell International · doi:10.1186/s12935-021-01853-8 · Cited by 428
A single-cell-based model of tumor growth in vitro : monolayers and spheroids
Drasdo, D., & Hoehme, S. (2005) · Physical Biology · doi:10.1088/1478-3975/2/3/001 · Cited by 426
A Multiscale Model for Avascular Tumor Growth
Jiang, Y., Pješivac–Grbović, J., Cantrell, C., & Freyer, J. P. (2005) · Biophysical Journal · doi:10.1529/biophysj.105.060640 · Cited by 382
Self-citationMathematical Modelling of Tumour Invasion and Metastasis
Anderson, A. R. A., Chaplain, M. A. J., Newman, E. L., Steele, R. J., & Thompson, A. M. (1999) · Computational and Mathematical Methods in Medicine · doi:10.1080/10273660008833042 · Cited by 373
An Integrated Computational/Experimental Model of Tumor Invasion
Frieboes, H. B., Zheng, X., Sun, C., Tromberg, B. J., Gatenby, R. A., & Vittorio Cristini, C. (2006) · Cancer Research · doi:10.1158/0008-5472.can-05-3166 · Cited by 299
A method for estimating the oxygen consumption rate in multicellular tumour spheroids
Grimes, D. R., Kelly, M., Bloch, K. M., & Partridge, M. (2014) · Journal of The Royal Society Interface · doi:10.1098/rsif.2013.1124 · Cited by 310
A mathematical model of glioma growth: the effect of chemotherapy on spatio‐temporal growth
Tracqui, P., Cruywagen, G. C., Woodward, D. E., Bartoo, G. T., Murray, J. D., & Alvord, E. C. (1995) · Cell Proliferation · doi:10.1111/j.1365-2184.1995.tb00036.x · Cited by 291
Simulation of anisotropic growth of low‐grade gliomas using diffusion tensor imaging
Jbabdi, S., Mandonnet, E., Duffau, H., Capelle, L., Swanson, K. R., Pélégrini‐Issac, M., Guillevin, R., & Benali, H. (2005) · Magnetic Resonance in Medicine · doi:10.1002/mrm.20625 · Cited by 291
d’Onofrio, A. (2005) · Physica D Nonlinear Phenomena · doi:10.1016/j.physd.2005.06.032 · Cited by 289
Patel, A. A., Gawlinski, E. T., Lemieux, S. K., & Gatenby, R. A. (2001) · Journal of Theoretical Biology · doi:10.1006/jtbi.2001.2385 · Cited by 268
Growth of necrotic tumors in the presence and absence of inhibitors
Byrne, H. M., & Chaplain, M. A. J. (1996) · Mathematical Biosciences · doi:10.1016/0025-5564(96)00023-5 · Cited by 259
Specific Growth Rate versus Doubling Time for Quantitative Characterization of Tumor Growth Rate
Mehrara, E., Forssell-Aronsson, E. B., Ahlman, H., & Bernhardt, P. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-3822 · Cited by 247
Stein, A. M., Demuth, T., Mobley, D. L., Berens, M. E., & Sander, L. M. (2006) · Biophysical Journal · doi:10.1529/biophysj.106.093468 · Cited by 237
Modelling the role of cell-cell adhesion in the growth and development of carcinomas
Byrne, H. M., & Chaplain, M. A. J. (1996) · Mathematical and Computer Modelling · doi:10.1016/s0895-7177(96)00174-4 · Cited by 233
Deisboeck, T. S., Berens, M. E., Kansal, A. R., Salvatore Torquato, A., Stemmer-Rachamimov, A. O., & Chiocca, E. A. (2001) · Cell Proliferation · doi:10.1046/j.1365-2184.2001.00202.x · Cited by 212
Biophysical models of tumour growth
Tracqui, P. (2009) · Reports on Progress in Physics · doi:10.1088/0034-4885/72/5/056701 · Cited by 191
CELLULAR AUTOMATON MODELS OF TUMOR DEVELOPMENT: A CRITICAL REVIEW
MOREIRA, J., & Deutsch, A. (2002) · Advances in Complex Systems · doi:10.1142/s0219525902000572 · Cited by 174
Vaghi, C., Rodallec, A., Fanciullino, R., Ciccolini, J., Mochel, J. P., Mastri, M., Poignard, C., Ebos, J. M. L., & Benzekry, S. (2020) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1007178 · Cited by 171
The effect of time delays on the dynamics of avascular tumor growth
Byrne, H. M. (1997) · Mathematical Biosciences · doi:10.1016/s0025-5564(97)00023-0 · Cited by 156
Mikhail, A. S., Eetezadi, S., & Allen, C. J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0062630 · Cited by 145
New dimensions in tumor immunology: what does 3D culture reveal?
Feder-Mengus, C., Ghosh, S., Reschner, A., Martin, I., & Spagnoli, G. C. (2008) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2008.06.001 · Cited by 139
In silico cancer modeling: is it ready for prime time?
Deisboeck, T. S., Zhang, L., Yoon, J., & Costa, J. C. (2008) · Nature Clinical Practice Oncology · doi:10.1038/ncponc1237 · Cited by 132
On Cellular Automaton Approaches to Modeling Biological Cells
Alber, M., Kiskowski, M. A., Glazier, J. A., & Jiang, Y. (2003) · The IMA volumes in mathematics and its applications · doi:10.1007/978-0-387-21696-6_1 · Cited by 132
MATHEMATICAL MODELLING OF GLIOBLASTOMA TUMOUR DEVELOPMENT: A REVIEW
Hatzikirou, H., Deutsch, A., Schaller, C., Simon, M., & Swanson, K. R. (2005) · Mathematical Models and Methods in Applied Sciences · doi:10.1142/s0218202505000960 · Cited by 125
Growth patterns of microscopic brain tumors
Sander, L. M., & Deisboeck, T. S. (2002) · Physical review. E, Statistical physics, plasmas, fluids, and related interdisciplinary topics · doi:10.1103/physreve.66.051901 · Cited by 117
Tumor growth dynamics: insights into evolutionary processes
Rodriguez-Brenes, I. A., Komarova, N. L., & Wodarz, D. (2013) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2013.05.020 · Cited by 116
Delay-induced oscillatory dynamics of tumour–immune system interaction
d’Onofrio, A., Gatti, F., Cerrai, P., & Freschi, L. (2009) · Mathematical and Computer Modelling · doi:10.1016/j.mcm.2009.11.005 · Cited by 111
Metamodeling tumor–immune system interaction, tumor evasion and immunotherapy
d’Onofrio, A. (2007) · Mathematical and Computer Modelling · doi:10.1016/j.mcm.2007.02.032 · Cited by 105
Tumor growthin vivo and as multicellular spheroids compared by mathematical models
Marušic, M., Bajzer, Ž., Vuk-Pavlovic, S., & Freyer, J. P. (1994) · Bulletin of Mathematical Biology · doi:10.1007/bf02460714 · Cited by 99
Self-citationHyperbolastic growth models: theory and application
Tabatabai, M., Williams, D. K., & Bursac, Z. (2005) · Theoretical Biology and Medical Modelling · doi:10.1186/1742-4682-2-14 · Cited by 97
From passive diffusion to active cellular migration in mathematical models of tumour invasion
Tracqui, P. (1995) · Acta Biotheoretica · doi:10.1007/bf00713564 · Cited by 97
Modelling and analysis of time-lags in some basic patterns of cell proliferation
Baker, C., Bocharov, G. A., Paul, C. A. H., & Rihan, F. A. (1998) · Journal of Mathematical Biology · doi:10.1007/s002850050133 · Cited by 93
Cellular automaton of idealized brain tumor growth dynamics
Kansal, A. R., Salvatore Torquato, A., Harsh, G. R., Chiocca, E. A., & Deisboeck, T. S. (2000) · Biosystems · doi:10.1016/s0303-2647(99)00089-1 · Cited by 92
A Patient-Specific Anisotropic Diffusion Model for Brain Tumour Spread
Swan, A., Hillen, T., Bowman, J. C., & Murtha, A. D. (2017) · Bulletin of Mathematical Biology · doi:10.1007/s11538-017-0271-8 · Cited by 89
Florczyk, S. J., Liu, G., Kievit, F. M., Lewis, A. M., Wu, J. D., & Zhang, M. (2012) · Advanced Healthcare Materials · doi:10.1002/adhm.201100054 · Cited by 85
Mathematical modeling of tumor-immune competitive system, considering the role of time delay
Khajanchi, S., & Nieto, J. J. (2018) · Applied Mathematics and Computation · doi:10.1016/j.amc.2018.08.018 · Cited by 84
Properties of Tumor Spheroid Growth Exhibited by Simple Mathematical Models
Wallace, D. I., & Guo, X. (2013) · Frontiers in Oncology · doi:10.3389/fonc.2013.00051 · Cited by 77
Cellular interactions constrain tumor growth
West, J., & Newton, P. K. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1804150116 · Cited by 74
d’Onofrio, A. (2006) · Mathematical Models and Methods in Applied Sciences · doi:10.1142/s0218202506001571 · Cited by 72
Methods: Using Three-Dimensional Culture (Spheroids) as an In Vitro Model of Tumour Hypoxia
Leek, R., Grimes, D. R., Harris, A. L., & McIntyre, A. (2016) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-26666-4_10 · Cited by 74
Conceptual frameworks for mathematical modeling of tumor growth dynamics
Bajzer, Ž., Marušić, M., & Vuk‐Pavlović, S. (1996) · Mathematical and Computer Modelling · doi:10.1016/0895-7177(96)00018-0 · Cited by 71
Self-citationFreischel, A. R., Damaghi, M., Cunningham, J. J., Ibrahim‐Hashim, A., Gillies, R. J., Gatenby, R. A., & Brown, J. S. (2021) · Scientific Reports · doi:10.1038/s41598-021-84406-3 · Cited by 74
Front Instabilities and Invasiveness of Simulated 3D Avascular Tumors
Popławski, N. J., Shirinifard, A., Agero, U., Gens, J. S., Swat, M., & Glazier, J. A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010641 · Cited by 68
Can fractional calculus help improve tumor growth models?
Valentim, C. A., de Oliveira, N. A., Rabi, J. A., & David, S. A. (2020) · Journal of Computational and Applied Mathematics · doi:10.1016/j.cam.2020.112964 · Cited by 67
Time-dependent rheology of colloidal star glasses
Rogers, S. A., Callaghan, P. T., Petekidis, G., & Vlassopoulos, D. (2010) · Journal of Rheology · doi:10.1122/1.3270524 · Cited by 67
The impact of “search precision” in an agent-based tumor model
Mansury, Y. S., & Deisboeck, T. S. (2003) · Journal of Theoretical Biology · doi:10.1016/s0022-5193(03)00169-3 · Cited by 67
The Role of Oxygen in Avascular Tumor Growth
Grimes, D. R., Kannan, P., McIntyre, A., Kavanagh, A. P., Siddiky, A., Wigfield, S., Harris, A. L., & Partridge, M. (2016) · PLoS ONE · doi:10.1371/journal.pone.0153692 · Cited by 67
Prediction of traveling front behavior in a lattice-gas cellular automaton model for tumor invasion
Hatzikirou, H., Brusch, L., Schaller, C., Simon, M., & Deutsch, A. (2009) · Computers & Mathematics with Applications · doi:10.1016/j.camwa.2009.08.041 · Cited by 62
Digital Twins for Tissue Culture Techniques—Concepts, Expectations, and State of the Art
Möller, J., & Pörtner, R. (2021) · Processes · doi:10.3390/pr9030447 · Cited by 63
Improving cancer treatments via dynamical biophysical models
Kuznetsov, M. B., Clairambault, J., & Volpert, V. A. (2021) · Physics of Life Reviews · doi:10.1016/j.plrev.2021.10.001 · Cited by 64
Bi, P., & Ruan, S. (2013) · SIAM Journal on Applied Dynamical Systems · doi:10.1137/120887898 · Cited by 58
Modeling and Computer Simulations of Tumor Growth and Tumor Response to Radiotherapy
Borkenstein, K., Levegrün, S., & Peschke, P. (2004) · Radiation Research · doi:10.1667/rr3193 · Cited by 58
When the Optimal Is Not the Best: Parameter Estimation in Complex Biological Models
Fernández Slezak, D., Suárez, C., Cecchi, G. A., Marshall, G., & Stolovitzky, G. (2010) · PLoS ONE · doi:10.1371/journal.pone.0013283 · Cited by 57
“We generated synthetic growth data from a Gompertz model that was previously shown [13,14] to follow very closely experimental volume growth data with values of a ~ 7 : 6 , b ~{ 12 and c ~{ 0 : 121 .”
BackgroundMethodEvaluation of absolute quantitation by nonlinear regression in probe-based real-time PCR
Goll, R., Olsen, T., Cui, G., & Florholmen, J. R. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-107 · Cited by 56
Front Instabilities and Invasiveness of Simulated Avascular Tumors
Popławski, N. J., Agero, U., Gens, J. S., Swat, M., Glazier, J. A., & Anderson, A. R. A. (2009) · Bulletin of Mathematical Biology · doi:10.1007/s11538-009-9399-5 · Cited by 53
Mathematical Modeling of Tumor Growth Kinetics
Bajzer, Ž., Vuk‐Pavlović, S., & Huzak, M. (1997) · Modeling and simulation in science, engineering & technology · doi:10.1007/978-0-8176-8119-7_3 · Cited by 50
Self-citationGrowth modelling of non-functioning pituitary adenomas in patients referred for surgery
Honegger, J. B., Zimmermann, S., Psaras, T., Petrick, M., Mittelbronn, M. G. A., Ernemann, U., Reincke, M., & Dietz, K. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0502 · Cited by 49
A general bilinear model to describe growth or decline time profiles
Buchwald, P. (2006) · Mathematical Biosciences · doi:10.1016/j.mbs.2006.08.013 · Cited by 48
Growth model for multicellular tumor spheroids
Delsanto, P. P., Guiot, C., Degiorgis, P. G., Condat, C. A., Mansury, Y. S., & Deisboeck, T. S. (2004) · Applied Physics Letters · doi:10.1063/1.1812842 · Cited by 47
Habib, S., Molina-Parı́s, C., & Deisboeck, T. S. (2003) · Physica A Statistical Mechanics and its Applications · doi:10.1016/s0378-4371(03)00391-1 · Cited by 45
A dynamical model of tumour immunotherapy
Frascoli, F., Kim, P., Hughes, B. D., & Landman, K. A. (2014) · Mathematical Biosciences · doi:10.1016/j.mbs.2014.04.003 · Cited by 46
Nonlinear dynamics in tumor-immune system interaction models with delays
Ruan, S. (2020) · Discrete and Continuous Dynamical Systems - B · doi:10.3934/dcdsb.2020282 · Cited by 45
Tumor Volume Doubling Time as a Dynamic Prognostic Marker for Patients with Hepatocellular Carcinoma
Kim, J. K., Kim, H., Jun, M.-J., Yun, S., Shim, J. H., Lee, H. C., Lee, D., An, J., Lim, Y., Chung, Y.-H., et al. (2017) · Digestive Diseases and Sciences · doi:10.1007/s10620-017-4708-6 · Cited by 42
Cochran, D., Fukumura, D., Ancukiewicz, M., Carmeliet, P., & Jain, R. K. (2006) · Annals of Biomedical Engineering · doi:10.1007/s10439-006-9134-4 · Cited by 42
Mathematical modelling of avascular tumour growth based on diffusion of nutrients and its validation
Kiran, K. L., Devaraj, J., & Lakshminarayanan, S. (2009) · The Canadian Journal of Chemical Engineering · doi:10.1002/cjce.20204 · Cited by 41
Modeling Multi-drug Chemotherapy: Tailoring Treatment to Individuals
Gardner, S. N. (2002) · Journal of Theoretical Biology · doi:10.1006/jtbi.2001.2459 · Cited by 41
Diverse Ideas on the Growth Kinetics of Disseminated Cancer Cells
Afenya, E. (2000) · Bulletin of Mathematical Biology · doi:10.1006/bulm.1999.0165 · Cited by 40
Valentim, C. A., Rabi, J. A., & David, S. A. (2021) · Biosystems · doi:10.1016/j.biosystems.2021.104377 · Cited by 39
On multistep tumor growth models of fractional variable-order
Valentim, C. A., Rabi, J. A., David, S. A., & Machado, J. A. T. (2020) · Biosystems · doi:10.1016/j.biosystems.2020.104294 · Cited by 38
d’Onofrio, A. (2008) · Chaos Solitons & Fractals · doi:10.1016/j.chaos.2008.04.014 · Cited by 36
General Aspects of Modeling Tumor Growth and Immune Response
Adam, J. (1997) · Birkhäuser Boston eBooks · doi:10.1007/978-0-8176-8119-7_2 · Cited by 34
Using Physics-Informed Neural Networks (PINNs) for Tumor Cell Growth Modeling
Rodrigues, J. A. (2024) · Mathematics · doi:10.3390/math12081195 · Cited by 34
Eetezadi, S., Evans, J. C., Shen, Y.-T., Souza, R. D., Piquette‐Miller, M., & Allen, C. J. (2017) · Molecular Pharmaceutics · doi:10.1021/acs.molpharmaceut.7b00843 · Cited by 34
A Mathematical Model of Integrin-mediated Haptotactic Cell Migration
Mallet, D. G., & Pettet, G. J. (2006) · Bulletin of Mathematical Biology · doi:10.1007/s11538-005-9032-1 · Cited by 33
Roniotis, A., Manikis, G. C., Sakkalis, V., Zervakis, M. E., Karatzanis, I., & Kostas Marias, A. (2011) · IEEE Transactions on Information Technology in Biomedicine · doi:10.1109/titb.2011.2171190 · Cited by 33
Tumor Growth Instability and Its Implications for Chemotherapy
Castorina, P., Carcò, D., Guiot, C., & Deisboeck, T. S. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-0653 · Cited by 32
New Dimensions in Gompertzian Growth
Bajzer, Ž., & Vuk‐Pavlović, S. (1999) · Computational and Mathematical Methods in Medicine · doi:10.1080/10273660008833057 · Cited by 31
Self-citationHarko, T., & Mak, M. K. (2014) · Mathematical Biosciences & Engineering · doi:10.3934/mbe.2015.12.41 · Cited by 30
Intelligent solution predictive networks for non-linear tumor-immune delayed model
Anwar, N., Ahmad, I., Kiani, A. K., Shoaib, M., & Raja, M. A. Z. (2023) · Computer Methods in Biomechanics & Biomedical Engineering · doi:10.1080/10255842.2023.2227751 · Cited by 28
Duan, G., Tang, Q.-Y., Yan, H., Xie, L., Wang, Y., Zheng, X. E., Zhuge, Y., Shen, S., Zhang, B., Zhang, X., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-00422-2 · Cited by 26
Diffusive modelling of glioma evolution: a review
Roniotis, A., Kostas Marias, A., Sakkalis, V., & Zervakis, M. E. (2010) · Journal of Biomedical Science and Engineering · doi:10.4236/jbise.2010.35070 · Cited by 24
Tumor Gompertzian growth by cellular energetic balance
Castorina, P., & Zappalà, D. (2005) · Physica A Statistical Mechanics and its Applications · doi:10.1016/j.physa.2005.09.063 · Cited by 25
The nature of Hopf bifurcation for the Gompertz model with delays
Piotrowska, M. J., & Foryś, U. (2011) · Mathematical and Computer Modelling · doi:10.1016/j.mcm.2011.05.027 · Cited by 23
Yan, F., Gunay, G., Valerio, T. I., Wang, C., Wilson, J. A., Haddad, M., Watson, M., Connell, M. O., Davidson, N., Fung, K.-M. A., et al. (2021) · Biomedical Optics Express · doi:10.1364/boe.425512 · Cited by 23
Modeling tumor growth using fractal calculus: Insights into tumor dynamics
Golmankhaneh, A. K., Tunç, S., Schlichtinger, A. M., Asanza, D. M., & Golmankhaneh, A. K. (2023) · Biosystems · doi:10.1016/j.biosystems.2023.105071 · Cited by 23
A Hybrid Cellular Automaton Model of Solid Tumor Growth and Bioreductive Drug Transport
Kazmi, N., Hossain, M. A., & Phillips, R. M. (2012) · IEEE Transactions on Computational Biology and Bioinformatics · doi:10.1109/tcbb.2012.118 · Cited by 23
The role of growth factors in avascular tumour growth
Byrne, H. M., & Gourley, S. A. (1997) · Mathematical and Computer Modelling · doi:10.1016/s0895-7177(97)00143-x · Cited by 22
A generalization of Gompertz law compatible with the Gyllenberg–Webb theory for tumour growth
d’Onofrio, A., Fasano, A., & Monechi, B. (2011) · Mathematical Biosciences · doi:10.1016/j.mbs.2011.01.001 · Cited by 22
A complete mathematical study of a 3D model of heterogeneous and anisotropic glioma evolution
Roniotis, A., Kostas Marias, A., Sakkalis, V., Tsibidis, G. D., & Zervakis, M. E. (2009) · Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) · doi:10.1109/iembs.2009.5333776 · Cited by 22
d’Onofrio, A., Gandolfi, A., & Gattoni, S. (2012) · Physica A Statistical Mechanics and its Applications · doi:10.1016/j.physa.2012.07.025 · Cited by 21
Cancer dissemination: A consequence of limited carrying capacity?
Deisboeck, T. S., & Wang, Z. (2006) · Medical Hypotheses · doi:10.1016/j.mehy.2006.11.007 · Cited by 20
In-Depth Analysis and Evaluation of Diffusive Glioma Models
Roniotis, A., Sakkalis, V., Karatzanis, I., Zervakis, M. E., & Kostas Marias, A. (2012) · IEEE Transactions on Information Technology in Biomedicine · doi:10.1109/titb.2012.2185704 · Cited by 19
Choice of optimal strategy of tumor chemotherapy in Gompertz model
Chumerina, E. S. (2009) · Journal of Computer and Systems Sciences International · doi:10.1134/s1064230709020154 · Cited by 18
Metadata
- Authors
- Marušić, M., Bajzer, Ž., Freyer, J. P., & Vuk‐Pavlović, S.
- Affiliations
- Mayo Clinic (US)
- Los Alamos National Laboratory (US)
- Corresponding author
- Vuk‐Pavlović, S.
- ORCID
- Marušić, M.
- Venue
- Cell Proliferation
- Publisher
- Wiley
- Published
- 1994-02
- Volume
- 27
- Issue
- 2
- Pages
- 73-94
- ISSN
- 0960-7722 (ISSN-L)
- 1365-2184
- OpenAlex
- W2099998237
- Cited by
- 203
- References
- 39
- Citations by year
- 2026: 6 · 2025: 5 · 2024: 3 · 2023: 8 · 2022: 4 · 2021: 8 · 2020: 11 · 2019: 4 · 2018: 4 · 2017: 9 · 2016: 8 · 2015: 4 · 2014: 8 · 2013: 10 · 2012: 8
- FWCI
- 4.12
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Cell Proliferation (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r29ca045312-04, 5r01ca051150-04)
- National Cancer Institute (CA45312, CA51150)
- Topics
- Physical Sciences › Mathematics › Modeling and Simulation › Mathematical Biology Tumor Growth
- Health Sciences › Medicine › Oncology › Cancer Cells and Metastasis
- Physical Sciences › Mathematics › Applied Mathematics › Mathematical and Theoretical Epidemiology and Ecology Models
- Keywords
- tumor spheroids, tumor growth modeling, Gompertz model, von Bertalanffy model, logistic model, model selection, cell lines
- MeSH terms
- Cell Division, Humans, Models, Biological, Spheroids, Cellular
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review