Skip to main content
PMC home page
British Journal of Cancer logoLink to British Journal of Cancer
. 1995 Aug;72(2):511–518. doi: 10.1038/bjc.1995.364

Review of survival analyses published in cancer journals.

D G Altman 1, B L De Stavola 1, S B Love 1, K A Stepniewska 1
PMCID: PMC2033978  PMID: 7640241

Abstract

Survival analysis has found widespread applications in medicine in the last 10-15 years. However, there has been no published review of the use and presentation of survival analyses. We have carried out a systematic review of the research papers published between October and December 1991 in five clinical oncology journals. A total of 132 papers were reviewed. We looked at several aspects of study design, data handling, analysis and presentation of the results. We found that almost half of the papers did not give any summary of length of follow-up; that in 62% of papers at least one end point was not clearly defined; and that both logrank and multivariate analyses were frequently reported at most only as P-values [63/84 (75%) and 22/47 (47%) respectively]. Furthermore, although many studies were small, uncertainty of the estimates was rarely indicated [in 13/84 (15%) logrank and 16/47 (34%) multivariate results]. The procedure for categorisation of continuous variables in logrank analyses was explained in only 8/49 (16%) papers. The quality of graphs was felt to be poor in 43/117 (37%) papers which included at least one survival curve. To address some of the presentational inadequacies found in this review we include new suggested guidelines for the presentation of survival analyses in medical journals. These would complement the statistical guidelines recommended by several clinical oncology journals.

Full text

PDF
511

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Altman D. G. Categorising continuous variables. Br J Cancer. 1991 Nov;64(5):975–975. doi: 10.1038/bjc.1991.441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Altman D. G., Lausen B., Sauerbrei W., Schumacher M. Dangers of using "optimal" cutpoints in the evaluation of prognostic factors. J Natl Cancer Inst. 1994 Jun 1;86(11):829–835. doi: 10.1093/jnci/86.11.829. [DOI] [PubMed] [Google Scholar]
  3. Altman D. G. Statistics in medical journals. Stat Med. 1982 Jan-Mar;1(1):59–71. doi: 10.1002/sim.4780010109. [DOI] [PubMed] [Google Scholar]
  4. Altman D. G. Statistics in medical journals: developments in the 1980s. Stat Med. 1991 Dec;10(12):1897–1913. doi: 10.1002/sim.4780101206. [DOI] [PubMed] [Google Scholar]
  5. Andersen P. K. Survival analysis 1982-1991: the second decade of the proportional hazards regression model. Stat Med. 1991 Dec;10(12):1931–1941. doi: 10.1002/sim.4780101208. [DOI] [PubMed] [Google Scholar]
  6. Anderson J. R., Cain K. C., Gelber R. D., Gelman R. S. Analysis and interpretation of the comparison of survival by treatment outcome variables in cancer clinical trials. Cancer Treat Rep. 1985 Oct;69(10):1139–1146. [PubMed] [Google Scholar]
  7. Basu A., Teicher B. A., Lazo J. S. Involvement of protein kinase C in phorbol ester-induced sensitization of HeLa cells to cis-diamminedichloroplatinum(II). J Biol Chem. 1990 May 25;265(15):8451–8457. [PubMed] [Google Scholar]
  8. Berkow R. L., Kraft A. S. Bryostatin, a non-phorbol macrocyclic lactone, activates intact human polymorphonuclear leukocytes and binds to the phorbol ester receptor. Biochem Biophys Res Commun. 1985 Sep 30;131(3):1109–1116. doi: 10.1016/0006-291x(85)90205-0. [DOI] [PubMed] [Google Scholar]
  9. Berkow R. L., Schlabach L., Dodson R., Benjamin W. H., Jr, Pettit G. R., Rustagi P., Kraft A. S. In vivo administration of the anticancer agent bryostatin 1 activates platelets and neutrophils and modulates protein kinase C activity. Cancer Res. 1993 Jun 15;53(12):2810–2815. [PubMed] [Google Scholar]
  10. Christensen E. Multivariate survival analysis using Cox's regression model. Hepatology. 1987 Nov-Dec;7(6):1346–1358. doi: 10.1002/hep.1840070628. [DOI] [PubMed] [Google Scholar]
  11. Dale I. L., Gescher A. Effects of activators of protein kinase C, including bryostatins 1 and 2, on the growth of A549 human lung carcinoma cells. Int J Cancer. 1989 Jan 15;43(1):158–163. doi: 10.1002/ijc.2910430129. [DOI] [PubMed] [Google Scholar]
  12. Dekker L. V., Parker P. J. Protein kinase C--a question of specificity. Trends Biochem Sci. 1994 Feb;19(2):73–77. doi: 10.1016/0968-0004(94)90038-8. [DOI] [PubMed] [Google Scholar]
  13. Dell'Aquila M. L., Nguyen H. T., Herald C. L., Pettit G. R., Blumberg P. M. Inhibition by bryostatin 1 of the phorbol ester-induced blockage of differentiation in hexamethylene bisacetamide-treated Friend erythroleukemia cells. Cancer Res. 1987 Nov 15;47(22):6006–6009. [PubMed] [Google Scholar]
  14. Elashoff J. D. Surviving proportional hazards. Hepatology. 1983 Nov-Dec;3(6):1031–1035. doi: 10.1002/hep.1840030623. [DOI] [PubMed] [Google Scholar]
  15. Fields A. P., Pettit G. R., May W. S. Phosphorylation of lamin B at the nuclear membrane by activated protein kinase C. J Biol Chem. 1988 Jun 15;263(17):8253–8260. [PubMed] [Google Scholar]
  16. Gebbia V., Citarrella P., Miserendino V., Valenza R., Borsellino N., Pesta A., Pettit R., May S. The effects of the macrocyclic lactone bryostatin-1 on leukemic cells in vitro. Tumori. 1992 Jun 30;78(3):167–171. doi: 10.1177/030089169207800304. [DOI] [PubMed] [Google Scholar]
  17. Gelber R. D., Goldhirsch A. Reporting and interpreting adjuvant therapy clinical trials. International Breast Cancer Study Group (formerly Ludwig Group). J Natl Cancer Inst Monogr. 1992;(11):59–69. [PubMed] [Google Scholar]
  18. Gescher A. Antiproliferative properties of phorbol ester tumour promoters. Biochem Pharmacol. 1985 Aug 1;34(15):2587–2592. doi: 10.1016/0006-2952(85)90552-0. [DOI] [PubMed] [Google Scholar]
  19. Gescher A. Towards selective pharmacological modulation of protein kinase C--opportunities for the development of novel antineoplastic agents. Br J Cancer. 1992 Jul;66(1):10–19. doi: 10.1038/bjc.1992.209. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Gignac S. M., Buschie M., Pettit G. R., Hoffbrand A. V., Drexler H. G. Expression of proto-oncogene c-jun during differentiation of B-chronic lymphocytic leukemia. Leukemia. 1990 Jun;4(6):441–444. [PubMed] [Google Scholar]
  21. Gøtzsche P. C. Methodology and overt and hidden bias in reports of 196 double-blind trials of nonsteroidal antiinflammatory drugs in rheumatoid arthritis. Control Clin Trials. 1989 Mar;10(1):31–56. doi: 10.1016/0197-2456(89)90017-2. [DOI] [PubMed] [Google Scholar]
  22. Haynes R. B., Mulrow C. D., Huth E. J., Altman D. G., Gardner M. J. More informative abstracts revisited. Ann Intern Med. 1990 Jul 1;113(1):69–76. doi: 10.7326/0003-4819-113-1-69. [DOI] [PubMed] [Google Scholar]
  23. Hennings H., Blumberg P. M., Pettit G. R., Herald C. L., Shores R., Yuspa S. H. Bryostatin 1, an activator of protein kinase C, inhibits tumor promotion by phorbol esters in SENCAR mouse skin. Carcinogenesis. 1987 Sep;8(9):1343–1346. doi: 10.1093/carcin/8.9.1343. [DOI] [PubMed] [Google Scholar]
  24. Hokanson J. A., Luttman D. J., Weiss G. B. Frequency and diversity of use of statistical techniques in oncology journals. Cancer Treat Rep. 1986 May;70(5):589–594. [PubMed] [Google Scholar]
  25. Hornung R. L., Pearson J. W., Beckwith M., Longo D. L. Preclinical evaluation of bryostatin as an anticancer agent against several murine tumor cell lines: in vitro versus in vivo activity. Cancer Res. 1992 Jan 1;52(1):101–107. [PubMed] [Google Scholar]
  26. Isakov N., Galron D., Mustelin T., Pettit G. R., Altman A. Inhibition of phorbol ester-induced T cell proliferation by bryostatin is associated with rapid degradation of protein kinase C. J Immunol. 1993 Feb 15;150(4):1195–1204. [PubMed] [Google Scholar]
  27. Jones R. J., Sharkis S. J., Miller C. B., Rowinsky E. K., Burke P. J., May W. S. Bryostatin 1, a unique biologic response modifier: anti-leukemic activity in vitro. Blood. 1990 Mar 15;75(6):1319–1323. [PubMed] [Google Scholar]
  28. Kennedy M. J., Prestigiacomo L. J., Tyler G., May W. S., Davidson N. E. Differential effects of bryostatin 1 and phorbol ester on human breast cancer cell lines. Cancer Res. 1992 Mar 1;52(5):1278–1283. [PubMed] [Google Scholar]
  29. Kiss Z., Deli E., Girard P. R., Pettit G. R., Kuo J. F. Comparative effects of polymyxin B, phorbol ester and bryostatin on protein phosphorylation, protein kinase C translocation, phospholipid metabolism and differentiation of HL60 cells. Biochem Biophys Res Commun. 1987 Jul 15;146(1):208–215. doi: 10.1016/0006-291x(87)90712-1. [DOI] [PubMed] [Google Scholar]
  30. Kraft A. S., Baker V. V., May W. S. Bryostatin induces changes in protein kinase C location and activity without altering c-myc gene expression in human promyelocytic leukemia cells (HL-60). Oncogene. 1987 May;1(2):111–118. [PubMed] [Google Scholar]
  31. Kraft A. S., Smith J. B., Berkow R. L. Bryostatin, an activator of the calcium phospholipid-dependent protein kinase, blocks phorbol ester-induced differentiation of human promyelocytic leukemia cells HL-60. Proc Natl Acad Sci U S A. 1986 Mar;83(5):1334–1338. doi: 10.1073/pnas.83.5.1334. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kraft A. S., William F., Pettit G. R., Lilly M. B. Varied differentiation responses of human leukemias to bryostatin 1. Cancer Res. 1989 Mar 1;49(5):1287–1293. [PubMed] [Google Scholar]
  33. Lamb W. R., Pumphrey R. S., Brenchley P. E. A peroxidase-linked enzyme immunoassay for tumour necrosis factor alpha utilising alternative colorimetric or chemilumimetric substrates. J Immunol Methods. 1992 Nov 5;155(2):215–223. doi: 10.1016/0022-1759(92)90288-5. [DOI] [PubMed] [Google Scholar]
  34. Leonard J. P., May W. S., Ihle J. N., Pettit G. R., Sharkis S. J. Regulation of hematopoiesis-IV: The role of interleukin-3 and bryostatin 1 in the growth of erythropoietic progenitors from normal and anemic W/Wv mice. Blood. 1988 Nov;72(5):1492–1496. [PubMed] [Google Scholar]
  35. May W. S., Sharkis S. J., Esa A. H., Gebbia V., Kraft A. S., Pettit G. R., Sensenbrenner L. L. Antineoplastic bryostatins are multipotential stimulators of human hematopoietic progenitor cells. Proc Natl Acad Sci U S A. 1987 Dec;84(23):8483–8487. doi: 10.1073/pnas.84.23.8483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. McCrady C. W., Staniswalis J., Pettit G. R., Howe C., Grant S. Effect of pharmacologic manipulation of protein kinase C by phorbol dibutyrate and bryostatin 1 on the clonogenic response of human granulocyte-macrophage progenitors to recombinant GM-CSF. Br J Haematol. 1991 Jan;77(1):5–15. doi: 10.1111/j.1365-2141.1991.tb07941.x. [DOI] [PubMed] [Google Scholar]
  37. Mohammad R. M., al-Katib A., Pettit G. R., Sensenbrenner L. L. Successful treatment of human Waldenström's macroglobulinemia with combination biological and chemotherapy agents. Cancer Res. 1994 Jan 1;54(1):165–168. [PubMed] [Google Scholar]
  38. Nutt J. E., Harris A. L., Lunec J. Phorbol ester and bryostatin effects on growth and the expression of oestrogen responsive and TGF-beta 1 genes in breast tumour cells. Br J Cancer. 1991 Oct;64(4):671–676. doi: 10.1038/bjc.1991.379. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Peto R., Pike M. C., Armitage P., Breslow N. E., Cox D. R., Howard S. V., Mantel N., McPherson K., Peto J., Smith P. G. Design and analysis of randomized clinical trials requiring prolonged observation of each patient. II. analysis and examples. Br J Cancer. 1977 Jan;35(1):1–39. doi: 10.1038/bjc.1977.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Philip P. A., Rea D., Thavasu P., Carmichael J., Stuart N. S., Rockett H., Talbot D. C., Ganesan T., Pettit G. R., Balkwill F. Phase I study of bryostatin 1: assessment of interleukin 6 and tumor necrosis factor alpha induction in vivo. The Cancer Research Campaign Phase I Committee. J Natl Cancer Inst. 1993 Nov 17;85(22):1812–1818. doi: 10.1093/jnci/85.22.1812. [DOI] [PubMed] [Google Scholar]
  41. Pocock S. J., Hughes M. D., Lee R. J. Statistical problems in the reporting of clinical trials. A survey of three medical journals. N Engl J Med. 1987 Aug 13;317(7):426–432. doi: 10.1056/NEJM198708133170706. [DOI] [PubMed] [Google Scholar]
  42. Prendiville J., Crowther D., Thatcher N., Woll P. J., Fox B. W., McGown A., Testa N., Stern P., McDermott R., Potter M. A phase I study of intravenous bryostatin 1 in patients with advanced cancer. Br J Cancer. 1993 Aug;68(2):418–424. doi: 10.1038/bjc.1993.352. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Rosenberg S. A., Lotze M. T., Muul L. M., Chang A. E., Avis F. P., Leitman S., Linehan W. M., Robertson C. N., Lee R. E., Rubin J. T. A progress report on the treatment of 157 patients with advanced cancer using lymphokine-activated killer cells and interleukin-2 or high-dose interleukin-2 alone. N Engl J Med. 1987 Apr 9;316(15):889–897. doi: 10.1056/NEJM198704093161501. [DOI] [PubMed] [Google Scholar]
  44. Schuchter L. M., Esa A. H., May S., Laulis M. K., Pettit G. R., Hess A. D. Successful treatment of murine melanoma with bryostatin 1. Cancer Res. 1991 Jan 15;51(2):682–687. [PubMed] [Google Scholar]
  45. Sharkis S. J., Jones R. J., Bellis M. L., Demetri G. D., Griffin J. D., Civin C., May W. S. The action of bryostatin on normal human hematopoietic progenitors is mediated by accessory cell release of growth factors. Blood. 1990 Aug 15;76(4):716–720. [PubMed] [Google Scholar]
  46. Shuster J. J. Median follow-up in clinical trials. J Clin Oncol. 1991 Jan;9(1):191–192. doi: 10.1200/JCO.1991.9.1.191. [DOI] [PubMed] [Google Scholar]
  47. Simon R., Altman D. G. Statistical aspects of prognostic factor studies in oncology. Br J Cancer. 1994 Jun;69(6):979–985. doi: 10.1038/bjc.1994.192. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Simon R. Confidence intervals for reporting results of clinical trials. Ann Intern Med. 1986 Sep;105(3):429–435. doi: 10.7326/0003-4819-105-3-429. [DOI] [PubMed] [Google Scholar]
  49. Simon R. Patient subsets and variation in therapeutic efficacy. Br J Clin Pharmacol. 1982 Oct;14(4):473–482. doi: 10.1111/j.1365-2125.1982.tb02015.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Stanwell C., Gescher A., Bradshaw T. D., Pettit G. R. The role of protein kinase C isoenzymes in the growth inhibition caused by bryostatin 1 in human A549 lung and MCF-7 breast carcinoma cells. Int J Cancer. 1994 Feb 15;56(4):585–592. doi: 10.1002/ijc.2910560420. [DOI] [PubMed] [Google Scholar]
  51. Stone R. M., Sariban E., Pettit G. R., Kufe D. W. Bryostatin 1 activates protein kinase C and induces monocytic differentiation of HL-60 cells. Blood. 1988 Jul;72(1):208–213. [PubMed] [Google Scholar]
  52. Szallasi Z., Smith C. B., Pettit G. R., Blumberg P. M. Differential regulation of protein kinase C isozymes by bryostatin 1 and phorbol 12-myristate 13-acetate in NIH 3T3 fibroblasts. J Biol Chem. 1994 Jan 21;269(3):2118–2124. [PubMed] [Google Scholar]
  53. Tibshirani R. A plain man's guide to the proportional hazards model. Clin Invest Med. 1982;5(1):63–68. [PubMed] [Google Scholar]
  54. Tuttle T. M., Inge T. H., Bethke K. P., McCrady C. W., Pettit G. R., Bear H. D. Activation and growth of murine tumor-specific T-cells which have in vivo activity with bryostatin 1. Cancer Res. 1992 Feb 1;52(3):548–553. [PubMed] [Google Scholar]
  55. Warren B. S., Kamano Y., Pettit G. R., Blumberg P. M. Mimicry of bryostatin 1 induced phosphorylation patterns in HL-60 cells by high-phorbol ester concentrations. Cancer Res. 1988 Nov 1;48(21):5984–5988. [PubMed] [Google Scholar]
  56. Whetton A. D., Heyworth C. M., Nicholls S. E., Evans C. A., Lord J. M., Dexter T. M., Owen-Lynch P. J. Cytokine-mediated protein kinase C activation is a signal for lineage determination in bipotential granulocyte macrophage colony-forming cells. J Cell Biol. 1994 May;125(3):651–659. doi: 10.1083/jcb.125.3.651. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. William F., Mroczkowski B., Cohen S., Kraft A. S. Differentiation of HL-60 cells is associated with an increase in the 35-kDa protein lipocortin I. J Cell Physiol. 1988 Dec;137(3):402–410. doi: 10.1002/jcp.1041370303. [DOI] [PubMed] [Google Scholar]
  58. Zelen M. Guidelines for publishing papers on cancer clinical trials: responsibilities of editors and authors. J Clin Oncol. 1983 Feb;1(2):164–169. doi: 10.1200/JCO.1983.1.2.164. [DOI] [PubMed] [Google Scholar]
  59. al-Katib A., Mohammad R. M., Dan M., Hussein M. E., Akhtar A., Pettit G. R., Sensenbrenner L. L. Bryostatin 1-induced hairy cell features on chronic lymphocytic leukemia cells in vitro. Exp Hematol. 1993 Jan;21(1):61–65. [PubMed] [Google Scholar]

Articles from British Journal of Cancer are provided here courtesy of Cancer Research UK

RESOURCES