Cited by 271Breast Cancer Treatment StudiesStatistical Methods in EpidemiologyMeta-analysis and systematic reviews

The DOI matches its Crossref record; 62 of the 63 references it cites were found in a registry or an index.

Methodological challenges in the evaluation of prognostic factors in breast cancer.

Altman, Douglas G., Lyman, Gary H.·1998·Breast Cancer Research and Treatment

DOI 10.1023/a:1006193704132

Open this paper in CoChat — free account

Abstract

Many studies are carried out in an effort to find factors that help explain the large unexplained variation in prognosis of breast cancer patients. The principles of good study design and analysis are less well appreciated for prognostic factor studies than for therapeutic trials. The oncology literature is full of results from studies of varying quality, often with conflicting findings. As a consequence, despite the large number of studies, there is still uncertainty about the importance of most prognostic factors. Few recently proposed prognostic factors for breast cancer have become widely accepted. This paper reviews the important methodological issues underlying such research. These issues are illustrated with examples from published studies and recent reviews of papers published in cancer journals. Guidelines are proposed for conducting and evaluating prognostic factor studies which should improve the quality of research in this important area.

Integrity signals

Registry

Crossref · 10.1023/a:1006193704132

Cites

62 of 62 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT
Martin Bland, J., & Altman, D. (1986) · The Lancet · doi:10.1016/s0140-6736(86)90837-8 · Cited by 47,965
Self-citation
Regression Models and Life-Tables
Cox, D. R. (1972) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1972.tb00899.x · Cited by 39,793
Regression Models and Life-Tables
Cox, D. R. (1992) · Springer Series in Statistics · doi:10.1007/978-1-4612-4380-9_37 · Cited by 26,297
A Predictive Model for Aggressive Non-Hodgkin's Lymphoma
The International Non-Hodgkin's Lymphoma Prognostic Factors Project (1993) · New England Journal of Medicine · doi:10.1056/nejm199309303291402 · Cited by 4,950
Flexible regression models with cubic splines
Durrleman, S., & Simon, R. M. (1989) · Statistics in Medicine · doi:10.1002/sim.4780080504 · Cited by 2,722
Importance of events per independent variable in proportional hazards regression analysis. II. Accuracy and precision of regression estimates
Peduzzi, P., Concato, J., Feinstein, A. R., & Holford, T. R. (1995) · Journal of Clinical Epidemiology · doi:10.1016/0895-4356(95)00048-8 · Cited by 2,154
Regression Using Fractional Polynomials of Continuous Covariates: Parsimonious Parametric Modelling
Royston, P. J., & Altman, D. G. (1994) · Journal of the Royal Statistical Society Series C (Applied Statistics) · doi:10.2307/2986270 · Cited by 1,797
Self-citation
Sample Size Tables for Clinical Studies
Machin, D., Campbell, M. J., Tan, S. B., & Tan, S. H. (2008) · Wiley eBooks · doi:10.1002/9781444300710 · Cited by 1,336
Dangers of Using "Optimal" Cutpoints in the Evaluation of Prognostic Factors
Altman, D. G., Lausen, B., Sauerbrei, W., & Schumacher, M. (1994) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/86.11.829 · Cited by 1,143
Self-citation
Publication bias: evidence of delayed publication in a cohort study of clinical research projects
Stern, J. M., & Simes, R. J. (1997) · BMJ · doi:10.1136/bmj.315.7109.640 · Cited by 818
A prognostic index in primary breast cancer.
Haybittle, J., Blamey, R., Elston, C., Johnson, J., Doyle, P., Campbell, F., Nicholson, R. I., & Griffiths, K. (1982) · British Journal of Cancer · doi:10.1038/bjc.1982.62 · Cited by 758
A bootstrap resampling procedure for model building: Application to the cox regression model
Sauerbrei, W., & Schumacher, M. (1992) · Statistics in Medicine · doi:10.1002/sim.4780111607 · Cited by 601
Statistical aspects of prognostic factor studies in oncology
Simon, R. M., & Altman, D. G. (1994) · British Journal of Cancer · doi:10.1038/bjc.1994.192 · Cited by 586
Self-citation
Regression models for prognostic prediction: advantages, problems, and suggested solutions.
Fe, H., Kl, L., Matchar, D. B., & Ta, R. (1985) · PubMed · Cited by 559
Some Thoughts on Clinical Trials, Especially Problems of Multiplicity
Tukey, J. W. (1977) · Science · doi:10.1126/science.333584 · Cited by 480
Sensitivity of HER-2/neu antibodies in archival tissue samples: potential source of error in immunohistochemical studies of oncogene expression.
Press, M. F., Hung, G., Godolphin, W. J., & Slamon, D. (1994) · PubMed · Cited by 478
Review of survival analyses published in cancer journals
Altman, D., De Stavola, B., Love, S., & Stepniewska, K. (1995) · British Journal of Cancer · doi:10.1038/bjc.1995.364 · Cited by 438
Self-citation
Confidence Intervals for Reporting Results of Clinical Trials
Simon, R. M. (1986) · Annals of Internal Medicine · doi:10.7326/0003-4819-105-3-429 · Cited by 410
Commentary: Prognostic models: clinically useful or quickly forgotten?
Wyatt, J. C., & Altman, D. G. (1995) · BMJ · doi:10.1136/bmj.311.7019.1539 · Cited by 374
Self-citation
Urokinase (uPA) and its inhibitor PAI-1 are strong and independent prognostic factors in node-negative breast cancer
Jänicke, F., Schmitt, M., Pache, L., Ulm, K., Harbeck, N., Höfler, H., & Graeff, H. (1993) · Breast Cancer Research and Treatment · doi:10.1007/bf01833260 · Cited by 354
Bootstrap investigation of the stability of a cox regression model
Altman, D. G., & Andersen, P. K. (1989) · Statistics in Medicine · doi:10.1002/sim.4780080702 · Cited by 311
Self-citation
Confirmation of a prognostic index in primary breast cancer
Todd, J. H., Dowle, C. S., Williams, M., Elston, C., Ellis, I. O., Hinton, C. P., Blamey, R. W., & Haybittle, J. L. (1987) · British Journal of Cancer · doi:10.1038/bjc.1987.230 · Cited by 308
Breast Cancer Prognostic Factors: Evaluation Guidelines
McGuire, W. L. (1991) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/83.3.154 · Cited by 298
SINGLE SOLUTION FOR ORAL THERAPY OF DIARRHŒA
Hirschhorn, N. (1975) · The Lancet · doi:10.1016/s0140-6736(75)90351-7 · Cited by 281
Evaluating the Potential Usefulness of New Prognostic and Predictive Indicators on Node-Negative Breast Cancer Patients
Gasparini, G., Pozza, F., & Harris, A. L. (1993) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/85.15.1206 · Cited by 244
Tumor Angiogenesis as a Prognostic Assay for Invasive Ductal Breast Carcinoma
Axelsson, K., Ljung, B., Moore, D. H., Thor, A. D., Chew, K., Edgerton, S. M., Smith, H. S., & Mayall, B. H. (1995) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/87.13.997 · Cited by 218
An overview of prognostic factors in small cell lung cancer
Rawson, N. S. B., & Peto, J. (1990) · British Journal of Cancer · doi:10.1038/bjc.1990.133 · Cited by 204
The bootstrap and identification of prognostic factors via cox's proportional hazards regression model
Chen, C., & George, S. L. (1985) · Statistics in Medicine · doi:10.1002/sim.4780040107 · Cited by 202
The future of prognostic factors in outcome prediction for patients with cancer
FIELDING, L. P., Fenoglio‐Preiser, C. M., & Freedman, L. S. (1992) · Cancer · doi:10.1002/1097-0142(19921101)70:9 · Cited by 166
The epidermal growth factor receptor as a prognostic marker: Results of 370 patients and review of 3009 patients
Fox, S. B., Smith, K., Hollyer, J., Greenall, M. J., Hastrich, D. J., & Harris, A. L. (1994) · Breast Cancer Research and Treatment · doi:10.1007/bf00666180 · Cited by 160
Re: Tumor Angiogenesis as a Prognostic Assay for Invasive Ductal Breast Carcinoma
Vermeulen, P., Libura, J., Libura, M. A., Hellemans, P., Marck, E. V., OOSTEROM, A. T. V., & DIRIX, L. Y. (1995) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/87.23.1797 · Cited by 157
Stress Response Protein (srp-27) Determination in Primary Human Breast Carcinomas: Clinical, Histologic, and Prognostic Correlations
Thor, A. D., Benz, C. C., Moore, D. H., Goldman, E., Edgerton, S., Landry, J., Schwartz, L. H., Mayall, B. H., Hickey, E. D., & Weber, L. A. (1991) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/83.3.170 · Cited by 150
Small-cell carcinoma of the lung: derivation of a prognostic staging system.
Sagman, U., Maki, E., Evans, W. K., Warr, D. G., Shepherd, F. A., Sculier, J., Haddad, R., Payne, D. G., Pringle, J. F., & Yeoh, J. L. (1991) · Journal of Clinical Oncology · doi:10.1200/jco.1991.9.9.1639 · Cited by 145
Why do so many prognostic factors fail to pan out?
Hilsenbeck, S. G., Clark, G. M., & McGuire, W. L. (1992) · Breast Cancer Research and Treatment · doi:10.1007/bf01840833 · Cited by 138
UROKINASE-TYPE PLASMINOGEN ACTIVATOR ANTIGEN AND EARLY RELAPSE IN BREAST CANCER
Jänicke, F., Schmitt, M., Ulm, K., Gössner, W., & Graeff, H. (1989) · The Lancet · doi:10.1016/s0140-6736(89)91070-2 · Cited by 130
Patient subsets and variation in therapeutic efficacy.
Simon, R. M. (1982) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.1982.tb02015.x · Cited by 130
Evaluating black-boxes as medical decision aids: issues arising from a study of neural networks
Hart, A., & Wyatt, J. C. (1990) · Medical Informatics · doi:10.3109/14639239009025270 · Cited by 122
Relationship between cathepsin-D content and disease-free survival in node-negative breast cancer patients: a meta-analysis
Ferrandina, G., Scambia, G., Bardelli, F., Panici, P. B., Mancuso, S., & Messori, A. (1997) · British Journal of Cancer · doi:10.1038/bjc.1997.442 · Cited by 120
Processed meats and risk of childhood leukemia (California, USA)
Peters, J. M., Preston‐Martin, S., London, S. J., Bowthan, J. D., Buckley, J. D., & Thomas, D. C. (1994) · Cancer Causes & Control · doi:10.1007/bf01830266 · Cited by 107
Prognostic significance of urokinase-type plasminogen activator and plasminogen activator inhibitor-1 in primary breast cancer
Knoop, A. S., Andreasen, P. A., Andersen, J. A., Hansen, S., Lænkholm, A., Simonsen, A. H., Andersen, J., Overgaard, J., & Rose, C. (1998) · British Journal of Cancer · doi:10.1038/bjc.1998.154 · Cited by 101
Central nervous system involvement in adult T-cell leukemia/lymphoma
Teshima, T., Akashi, K., Shibuya, T., Taniguchi, S., Okamura, T., Harada, M., Sumida, I., Hanada, M., & Niho, Y. (1990) · Cancer · doi:10.1002/1097-0142(19900115)65:2 · Cited by 99
A comparison of prognostic covariates for uveal melanoma.
Gamel, J. W., McCurdy, J. B., & McLean, I. W. (1992) · PubMed · Cited by 92
Sample size: how many patients are necessary?
Fayers, P. M., & Machin, D. (1995) · British Journal of Cancer · doi:10.1038/bjc.1995.268 · Cited by 69
Prognostic significance of estrogen receptors in 405 primary breast cancers: a comparison of immunohistochemical and biochemical methods
Molino, A., Micciolo, R., Turazza, M., Bonetti, F., Piubello, Q., Corgnati, A., Sperotto, L., Recaldin, E., Spagnolli, R., Manfrin, E., et al. (1997) · Breast Cancer Research and Treatment · doi:10.1023/a:1005769925670 · Cited by 66
A prospectively planned cumulative meta-analysis applied to a series of concurrent clinical trials
Whitehead, A. (1997) · Statistics in Medicine · doi:10.1002/(sici)1097-0258(19971230)16:24 · Cited by 66
Analysis of clinical trial outcomes: Some comments on subgroup analyses
Buyse, M. E. (1989) · Controlled Clinical Trials · doi:10.1016/0197-2456(89)90057-3 · Cited by 62
A comparison of Cox proportional hazards and artificial neural network models for medical prognosis
Ohno‐Machado, L. (1997) · Computers in Biology and Medicine · doi:10.1016/s0010-4825(96)00036-4 · Cited by 55
Problems in defining cutoff points of continuous prognostic factors: Example of tumor thickness in primary cutaneous melanoma
Buettner, P. G., Garbe, C., & Guggenmoos-Holzmann, I. (1997) · Journal of Clinical Epidemiology · doi:10.1016/s0895-4356(97)00155-8 · Cited by 54
CAUSALITY INFERENCE IN OBSERVATIONAL VS. EXPERIMENTAL STUDIES
Gray‐Donald, K., & Kramer, M. S. (1988) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a114891 · Cited by 52
Suboptimal analysis using 'optimal' cutpoints
Altman, D. (1998) · British Journal of Cancer · doi:10.1038/bjc.1998.537 · Cited by 46
Self-citation
Effect of Categorizing a Continuous Covariate on the Comparison of Survival Time
Morgan, T. M., & Elashoff, R. M. (1986) · Journal of the American Statistical Association · doi:10.1080/01621459.1986.10478350 · Cited by 42
Estrogen-replacement therapy after breast cancer risks versus benefits
Marchant, D. J. (1993) · Cancer · doi:10.1002/1097-0142(19930315)71:6+ · Cited by 36
Flexible covariate effects in the proportional hazards model
Hastie, T., Sleeper, L. A., & Tibshirani, R. J. (1992) · Breast Cancer Research and Treatment · doi:10.1007/bf01840837 · Cited by 35
Confirmation of a long-term prognostic index in breast cancer
Brown, J., Benson, E. A., & Jones, M. (1993) · The Breast · doi:10.1016/0960-9776(93)90057-m · Cited by 25
Prognostic value of total cathepsin B in invasive ductal carcinoma of the breast
Budihna, M., Skrk, J., Zakotnik, B., Gabrijelčič, D., & Lindtner, J. (1995) · European Journal of Cancer · doi:10.1016/0959-8049(94)00504-x · Cited by 15
Making the most of your prognostic factors: Presenting a more accurate survival model for breast cancer patients
Knorr, K. L., Hilsenbeck, S. G., Wenger, C. R., Pounds, G., Oldaker, T. A., Vendely, P., Pandian, M. R., Harrington, D. S., & Clark, G. M. (1992) · Breast Cancer Research and Treatment · doi:10.1007/bf01840838 · Cited by 11
Improved prognostication in small (pT1) breast cancers by image cytometry
Aubele, M. M., Auer, G., Falkmer, S., Voß, A., Rodenacker, K., Rutquist, L., & H�fler, H. (1995) · Breast Cancer Research and Treatment · doi:10.1007/bf00690188 · Cited by 10
Different detection rates of HER-2/NEU overexpression in ovarian carcinoma using two different commercially available detection kits
Romero, H., & Schneider, J. (1995) · European Journal of Cancer · doi:10.1016/0959-8049(95)00116-6 · Cited by 6
Razors and Refrigerators and Reindeer — Oh My!
Jenks, S., & Volkers, N. (1992) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/84.24.1863 · Cited by 4
Untitled work
(1997) · doi:10.1002/(sici)1097-0258(19970115)16:1
What do we mean by validating a prognostic model?
(2000) · doi:10.1002/(sici)1097-0258(20000229)19:4
Self-citation
Untitled work
Harrell, F., Jr. (1996) · doi:10.1002/(sici)1097-0258(19960229)15:4

Flagged first, then by citations

1 of the 63 references couldn’t be matched to a known paper.

Research works printed but not linked: 1

Gardner MJ, Altman DG (eds) Statistics with Confidence. British Medical Journal, London, 1989

Sorted by citations

Reporting Recommendations for Tumor Marker Prognostic Studies (REMARK)
McShane, L. M., Altman, D. G., Sauerbrei, W., Taube, S. E., Gion, M., & Clark, G. M. (2005) · JNCI: Journal of the National Cancer Institute · doi:10.1093/jnci/dji237 · Cited by 2,162
Self-citation
Critical appraisal and data extraction for systematic reviews of prediction modelling studies: the CHARMS checklist
Moons, K. G. M., de Groot, J. A. H., Bouwmeester, W., Vergouwe, Y., Mallett, S., Altman, D. G., Reitsma, J. B., & Collins, G. S. (2014) · PLoS Medicine · doi:10.1371/journal.pmed.1001744 · Cited by 2,018
Self-citation
Incidence, risk factors and prevention of mild traumatic brain injury: results of the who collaborating centre task force on mild traumatic brain injury
Cassidy, J. D., Carroll, L., Peloso, P. M. J., Borg, J., von Holst, H., Holm, L. W., Kraus, J. F., & Coronado, V. G. (2004) · Journal of Rehabilitation Medicine · doi:10.1080/16501960410023732 · Cited by 1,612
Evaluation of the Quality of Prognosis Studies in Systematic Reviews
Hayden, J. A., Côté, P., & Bombardier, C. (2006) · Annals of Internal Medicine · doi:10.7326/0003-4819-144-6-200603210-00010 · Cited by 1,452
REporting recommendations for tumour MARKer prognostic studies (REMARK).
for the Statistics Subcommittee of the NCI-EORTC Working Group on Cancer Diagnostics, McShane, L. M., Altman, D. G., Sauerbrei, W., Taube, S. E., Gion, M., & Clark, G. M. (2005) · British Journal of Cancer · doi:10.1038/sj.bjc.6602678 · Cited by 1,394
Self-citation

See all 271

Authors: Altman, D. G., & Lyman, G. H.
Affiliations: University of Oxford (GB)
University of South Florida (US)
ORCID: Altman, Douglas G.
Lyman, Gary H.
Venue: Breast Cancer Research and Treatment
Publisher: Springer Science and Business Media LLC
Published: 1998-11
Volume: 52
Issue: 1-3
Pages: 289-303
ISSN: 0167-6806 (ISSN-L)
1573-7217
DOI: 10.1023/a:1006193704132
OpenAlex: W2092931112
Cited by: 271
References: 63
Citations by year: 2026: 4 · 2025: 4 · 2024: 7 · 2023: 6 · 2022: 6 · 2021: 6 · 2020: 9 · 2019: 2 · 2018: 5 · 2017: 4 · 2016: 2 · 2015: 4 · 2014: 9 · 2013: 11 · 2012: 17
FWCI: 0.47
Type: journal article
Language: en
Open access: closed
Licence: www.springernature.com/gp/researchers/text-and-data-mining (tdm)
www.springernature.com/gp/researchers/text-and-data-mining (vor)
Locations: Breast Cancer Research and Treatment (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
Physical Sciences › Mathematics › Statistics and Probability › Statistical Methods in Epidemiology
Social Sciences › Decision Sciences › Statistics, Probability and Uncertainty › Meta-analysis and systematic reviews
Keywords: breast cancer, prognostic factors, research design, statistical analysis, research quality, methodological issues, research guidelines
MeSH terms: Breast Neoplasms, Female, Humans, Prognosis, Regression Analysis, Research Design, Meta-Analysis as Topic, Sample Size

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

Methodological challenges in the evaluation of prognostic factors in breast cancer.

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks