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
Computer solution of ordinary differential equations : the initial value problem
Shampine, L. F., & Gordon, M. K. (1975) · CERN Document Server (European Organization for Nuclear Research) · Cited by 1,308
Freyer, J. P., & Sutherland, R. M. (1986) · PubMed · Cited by 318
Self-citationRole of optimal control theory in cancer chemotherapy
Swan, G. W. (1990) · Mathematical Biosciences · doi:10.1016/0025-5564(90)90021-p · Cited by 310
Mathematical models in cancer research
Wheldon, T. E. (1988) · A. Hilger eBooks · Cited by 238
Turner, M. E., Bradley, E. L., Kirk, K. A., & Pruitt, K. M. (1976) · Mathematical Biosciences · doi:10.1016/0025-5564(76)90112-7 · Cited by 218
Mathematical modelling of microenvironment and growth in EMT6/Ro multicellular tumour spheroids
Casciari, J. J., Sotirchos, S. V., & Sutherland, R. M. (1992) · Cell Proliferation · doi:10.1111/j.1365-2184.1992.tb01433.x · Cited by 193
Evaluation of some mathematical models for tumor growth
Vaidya, V. G., & Alexandro, F. J. (1982) · International Journal of Bio-Medical Computing · doi:10.1016/0020-7101(82)90048-4 · Cited by 181
Role of necrosis in regulating the growth saturation of multicellular spheroids.
Freyer, J. P. (1988) · PubMed · Cited by 162
Self-citationOn the logistic law of growth and its empirical verifications in biology
Feller, W. (1940) · Acta Biotheoretica · doi:10.1007/bf01602862 · Cited by 137
Introductory Mathematical Statistics.
Nicholson, R. J., & Kreyszig, E. (1971) · Journal of the Royal Statistical Society Series A (General) · doi:10.2307/2343874 · Cited by 118
Quiescence as an explanation of Gompertzian tumor growth.
Gyllenberg, M., & Webb, G. F. (1989) · PubMed · Cited by 111
Spheroid Culture in Cancer Research (1991)
(2017) · CRC Press eBooks · doi:10.1201/9780203710241 · Cited by 105
Freyer, J. P., & Sutherland, R. M. (1986) · PubMed · Cited by 105
Self-citationAllometric morphogenesis of complex systems: Derivation of the basic equations from first principles
Savageau, M. A. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.12.6023 · Cited by 83
Growth of mammalian multicellular tumor spheroids.
Conger, A. D., & Ziskin, M. C. (1983) · PubMed · Cited by 82
A model for the growth of multicellular spheroids
Landry, J., Freyer, J. P., & Sutherland, R. M. (1982) · Cell Proliferation · doi:10.1111/j.1365-2184.1982.tb01065.x · Cited by 67
Self-citationMathematical model of prevascular growth of a spherical carcinoma
Maggelakis, S., & Adam, J. (1990) · Mathematical and Computer Modelling · doi:10.1016/0895-7177(90)90040-t · Cited by 56
Generalized Two-Parameter Equation of Growth
Marušić, M., & Bajzer, Ž. (1993) · Journal of Mathematical Analysis and Applications · doi:10.1006/jmaa.1993.1361 · Cited by 53
Self-citationMathematical model of prevascular growth of a spherical carcinoma—part II
Maggelakis, S. (1993) · Mathematical and Computer Modelling · doi:10.1016/0895-7177(93)90114-e · Cited by 47
Growth in solid heterogeneous human colon adenocarcinomas: comparison of simple logistical models
Michelson, S., Glicksman, A. S., & Leith, J. T. (1987) · Cell Proliferation · doi:10.1111/j.1365-2184.1987.tb01316.x · Cited by 40
Regrowth kinetics of cells from different regions of multicellular spheroids of four cell lines
Freyer, J. P., & Schor, P. L. (1989) · Journal of Cellular Physiology · doi:10.1002/jcp.1041380222 · Cited by 35
Self-citationA new model for tumor growth analysis based on a postulated inhibitory substance
Cox, E. B., Woodbury, M. A., & Myers, L. E. (1980) · Computers and Biomedical Research · doi:10.1016/0010-4809(80)90041-5 · Cited by 26
Mitotic autoregulation, growth control and neoplasia
Wheldon, T. E., Kirk, J., & Gray, W. M. (1973) · Journal of Theoretical Biology · doi:10.1016/0022-5193(73)90262-2 · Cited by 25
A model of growth with first-order birth and death rates
Piantadosi, S. (1985) · Computers and Biomedical Research · doi:10.1016/0010-4809(85)90047-3 · Cited by 24
Modeling autostimulation of growth in multicellular tumor spheroids
Marušić, M., Bajzer, Ž., Freyer, J. P., & Vuk‐Pavlović, S. (1991) · International Journal of Bio-Medical Computing · doi:10.1016/0020-7101(91)90005-y · Cited by 22
Self-citationPartial purification of a protein growth inhibitor from multicellular spheroids
Freyer, J. P., Schor, P. L., & Saponara, A. G. (1988) · Biochemical and Biophysical Research Communications · doi:10.1016/s0006-291x(88)80736-8 · Cited by 20
Self-citationQuantitative aspects of autocrine regulation in tumors.
Bajzer, Ž., & Vuk‐Pavlović, S. (1990) · PubMed · Cited by 13
Self-citationGeneralizing growth functions assuming parameter heterogeneity.
Piantadosi, S. T. (1987) · PubMed · Cited by 7
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
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