Reporting of prognostic studies of tumour markers: a review of published articles in relation to REMARK guidelines.
Open accessAbstract
BACKGROUND: Poor reporting compromises the reliability and clinical value of prognostic tumour marker studies. We review articles to assess the reporting of patients and events using REMARK guidelines, at the time of guideline publication. METHODS: We sampled 50 prognostic tumour marker studies from higher impact cancer journals between 2006 and 2007. The inclusion criteria were cancer; focus on single biological tumour marker; survival analysis; multivariable analysis; and not gene array or proteomic data. Articles were assessed for the REMARK profile and other REMARK guideline items. We propose a reporting aid, the REMARK profile, motivated by the CONSORT flowchart. RESULTS: In 50 studies assessed for the REMARK profile, the number of eligible patients (56% of articles), excluded patients (54%) and patients in analyses (98%) was reported. Only 50% of articles reported the number of outcome events. In multivariable analyses, 54% and 30% of articles reported patient and event numbers for all variables. Of the studies, 66% used archival samples, indicating a potentially biased patient selection. Only 36% of studies reported clearly defined outcomes. CONCLUSIONS: Good reporting is critical for the interpretability and clinical applicability of prognostic studies. Current reporting of key information, such as the number of outcome events in all patients and subgroups, is poor. Use of the REMARK profile would greatly improve reporting and enhance prognostic research.
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The REMARK guidelines for prognostic tumour marker studies recommend using a REMARK profile table instead of a flow diagram.
“The REMARK guidelines for prognostic tumour marker studies recommend using a REMARK profile table instead of a flow diagram [69].”
From Reporting and Methods in Clinical Prediction Research: A Systematic Review (2012) · cites this paper as [69]
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Moher, D., Schulz, K. F., & Altman, D. G. (2001) · The Lancet · doi:10.1016/s0140-6736(00)04337-3 · Cited by 5,373 · see citing works
Self-citationMoher, D., Schulz, K. F., & Altman, D. G. (2001) · BMC Medical Research Methodology · doi:10.1186/1471-2288-1-2 · Cited by 2,755 · see citing works
Self-citationA note on quantifying follow-up in studies of failure time
SCHEMPER, M., & Smith, T. L. (1996) · Controlled Clinical Trials · doi:10.1016/0197-2456(96)00075-x · Cited by 2,592 · see citing works
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 · see citing works
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 · see citing works
Self-citationDepression as a risk factor for mortality in patients with coronary heart disease: a meta-analysis
Barth, J., Schumacher, M., & Herrmann-Lingen, C. (2004) · Psychosomatic Medicine · doi:10.1097/01.psy.0000146332.53619.b2 · Cited by 1,358 · see citing works
de Azambuja, E., Cardoso, F., de Castro, G., Colozza, M., Mano, M. S., Durbecq, V., Sotiriou, C. P., Larsimont, D., Piccart, M. J., & Paesmans, M. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6603756 · Cited by 954 · see citing works
Hudis, C. A., Barlow, W. E., Costantino, J. P., Gray, R. J., Pritchard, K. I., Chapman, J. W., Sparano, J. A., Hunsberger, S., Enos, R. A., Gelber, R. D., et al. (2007) · Journal of Clinical Oncology · doi:10.1200/jco.2006.10.3523 · Cited by 864 · see citing works
Prognostic Factors in Non-small Cell Lung Cancer
Brundage, M., Davies, D. L., & Mackillop, W. J. (2002) · CHEST Journal · doi:10.1378/chest.122.3.1037 · Cited by 572 · see citing works
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 · see citing works
Self-citationScholten-Peeters, G. G. M., Verhagen, A. P., Bekkering, G. E., van der Windt, D., Barnsley, L., Oostendorp, R. A. B., & Hendriks, E. (2003) · Pain · doi:10.1016/s0304-3959(03)00050-2 · Cited by 431 · see citing works
Quantification of the completeness of follow-up
Clark, T. G., Altman, D. G., & Stavola, B. L. D. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08272-7 · Cited by 406 · see citing works
Self-citationSystematic review of prognostic cohort studies on shoulder disorders
Kuijpers, T., van der Windt, D., van der Heijden, G. J. M. G., & Bouter, L. M. (2004) · Pain · doi:10.1016/j.pain.2004.02.017 · Cited by 333 · see citing works
P53 as a prognostic marker for bladder cancer: a meta-analysis and review
Malats, N., Bustos, A., Murta‐Nascimento, C., Fernandez, F., Rivas, M., Puente, D., Kogevinas, M., & Real, F. X. (2005) · The Lancet Oncology · doi:10.1016/s1470-2045(05)70315-6 · Cited by 316 · see citing works
Blood Markers for the Prognosis of Ischemic Stroke
Whiteley, W. N., Chong, W. L., Sengupta, A., & Sandercock, P. A. (2009) · Stroke · doi:10.1161/strokeaha.108.528752 · Cited by 290 · see citing works
Methodological challenges in the evaluation of prognostic factors in breast cancer.
Altman, D. G., & Lyman, G. H. (1998) · Breast Cancer Research and Treatment · doi:10.1023/a:1006193704132 · Cited by 271 · see citing works
Self-citationPain and depression in patients with cancer
Spiegel, D., Sands, S. H., & Koopman, C. (1994) · Cancer · doi:10.1002/1097-0142(19941101)74:9 · Cited by 270 · see citing works
Self-citationKyzas, P., Cunha, I. W., & Ioannidis, J. P. A. (2005) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-04-1870 · Cited by 250 · see citing works
Sutcliffe, P., Hummel, S., Simpson, E., Young, T., Rees, A., Wilkinson, A., Hamdy, F. C., Clarke, N. W., & Staffurth, J. (2009) · Health Technology Assessment · doi:10.3310/hta13050 · Cited by 237 · see citing works
Almost all articles on cancer prognostic markers report statistically significant results
Kyzas, P., Denaxa-Kyza, D., & Ioannidis, J. P. A. (2007) · European Journal of Cancer · doi:10.1016/j.ejca.2007.08.030 · Cited by 231 · see citing works
Selective Reporting Biases in Cancer Prognostic Factor Studies
Kyzas, P., Loizou, K. T., & Ioannidis, J. P. A. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji184 · Cited by 231 · see citing works
Burton, A., & Altman, D. G. (2004) · British Journal of Cancer · doi:10.1038/sj.bjc.6601907 · Cited by 219 · see citing works
Self-citationRiley, R. D., Abrams, K. R., Sutton, A. J., Lambert, P. C., Jones, D. R., Heney, D., & Burchill, S. A. (2003) · British Journal of Cancer · doi:10.1038/sj.bjc.6600886 · Cited by 165 · see citing works
Riley, R. D., Sauerbrei, W., & Altman, D. G. (2009) · British Journal of Cancer · doi:10.1038/sj.bjc.6604999 · Cited by 161 · see citing works
Self-citationExpression of Carbonic Anhydrase IX in Astrocytic Tumors Predicts Poor Prognosis
Haapasalo, J. A., Nordfors, K., Hilvo, M., Rantala, I., Soini, Y., Parkkila, A., Pastoreková, S., Pastorek, J., Parkkila, S., & Haapasalo, H. (2006) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-05-0848 · Cited by 134 · see citing works
Prognostic Models: A Methodological Framework and Review of Models for Breast Cancer
Altman, D. G. (2009) · Cancer Investigation · doi:10.1080/07357900802572110 · Cited by 129 · see citing works
Self-citationSelenium binding protein 1 in ovarian cancer
Huang, K., Park, D. C., Ng, S., Lee, J. Y., Ni, X., Ng, N., Bandera, C. A., Welch, W. R., Berkowitz, R. S., Mok, S. C., et al. (2005) · International Journal of Cancer · doi:10.1002/ijc.21671 · Cited by 95 · see citing works
Kyzas, P., Denaxa-Kyza, D., & Ioannidis, J. P. A. (2007) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djk032 · Cited by 94 · see citing works
Identification of Clinically Useful Cancer Prognostic Factors: What Are We Missing?
McShane, L. M., Altman, D. G., & Sauerbrei, W. (2005) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/dji193 · Cited by 78 · see citing works
Self-citationPrimer: an evidence-based approach to prognostic markers
Altman, D. G., & Riley, R. D. (2005) · Nature Clinical Practice Oncology · doi:10.1038/ncponc0287 · Cited by 76 · see citing works
Self-citationSurvival Prediction in Patients With Glioblastoma Multiforme by Human Telomerase Genetic Variation
Wang, L., Wei, Q., Wang, L., Aldape, K., Cao, Y., Okcu, M. F., Hess, K. R., El‐Zein, R. A., Gilbert, M. R., Woo, S. Y., et al. (2006) · Journal of Clinical Oncology · doi:10.1200/jco.2005.04.0402 · Cited by 72 · see citing works
Potential for Selection Bias with Tumor Tissue Retrieval in Molecular Epidemiology Studies
Hoppin, J. A. (2002) · Annals of Epidemiology · doi:10.1016/s1047-2797(01)00250-2 · Cited by 65 · see citing works
Advances in Statistical Methods for the Health Sciences
(2007) · Birkhäuser Boston eBooks · doi:10.1007/978-0-8176-4542-7 · Cited by 62 · see citing works
Methodological issues associated with tumor marker development
Faraggi, D., & Kramar, A. (2000) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/s1078-1439(00)00075-2 · Cited by 59 · see citing works
Oberman, H. A. (1996) · The American Journal of Surgical Pathology · doi:10.1097/00000478-199607000-00022 · Cited by 54 · see citing works
Wadehra, M., Natarajan, S., Seligson, D. B., Williams, C. J., Hummer, A., Hedvat, C. V., Braun, J. G., & Soslow, R. A. (2006) · Cancer · doi:10.1002/cncr.21957 · Cited by 53 · see citing works
Prognosis of idiopathic membranous nephropathy: A methodologic meta-analysis
Marx, B. E., & Marx, M. (1997) · Kidney International · doi:10.1038/ki.1997.123 · Cited by 35 · see citing works
Sauerbrei, W., Holländer, N., Riley, R. D., & Altman, D. G. (2006) · Communication in Statistics- Theory and Methods · doi:10.1080/03610920600629666 · Cited by 31 · see citing works
Self-citationPrognostic factor studies in oncology: osteosarcoma as a clinical example
Bentzen, S. M. (2001) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/s0360-3016(00)01507-8 · Cited by 31 · see citing works
Sauerbrei, W. (2004) · KARGER eBooks · doi:10.1159/000082508 · Cited by 29 · see citing works
Self-citationPrognostic variables in node-negative and node-positive breast cancer - editorial
Gasparini, G. (1998) · Breast Cancer Research and Treatment · doi:10.1023/a:1006102021879 · Cited by 27 · see citing works
Infante‐Rivard, C., Villeneuve, J., & Esnaola, S. (1989) · Journal of Clinical Epidemiology · doi:10.1016/0895-4356(89)90077-2 · Cited by 22 · see citing works
Prognostic variables in node-negative and node-positive breast cancer — editorial
Gasparini, G. (1998) · Springer eBooks · doi:10.1007/978-1-4615-5195-9_30 · Cited by 12 · see citing works
Riley, R. D., Abrams, K. R., Lambert, P. C., Sutton, A. J., & Altman, D. G. (2007) · Birkhäuser Boston eBooks · doi:10.1007/978-0-8176-4542-7_3 · Cited by 12 · see citing works
Self-citationPrognostic Models: A Methodological Framework and Review of Models for Breast Cancer
Altman, D. G. (2007) · Translational medicine series · doi:10.3109/9781420019940.002 · Cited by 11 · see citing works
Self-citationStudies Investigating Prognostic Factors: Conduct and Evaluation
Altman, D. G. (2006) · TNM Online · doi:10.1002/0471463736.tnmp04.pub2 · Cited by 8 · see citing works
Self-citationCurrent Research in Head and Neck Cancer
Bier, H. (2004) · Advances in oto-rhino-laryngology · doi:10.1159/isbn.978-3-318-01119-7 · Cited by 5 · see citing works
Flagged first, then by citations
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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 · see citing works
Self-citationReporting Recommendations for Tumor Marker Prognostic Studies (REMARK): Explanation and Elaboration
Altman, D. G., McShane, L. M., Sauerbrei, W., & Taube, S. E. (2012) · PLoS Medicine · doi:10.1371/journal.pmed.1001216 · Cited by 1,019 · see citing works
Self-citationReporting and Methods in Clinical Prediction Research: A Systematic Review
Bouwmeester, W., Zuithoff, N. P. A., Mallett, S., Geerlings, M. I., Vergouwe, Y., Steyerberg, E. W., Altman, D. G., & Moons, K. G. M. (2012) · PLoS Medicine · doi:10.1371/journal.pmed.1001221 · Cited by 600 · see citing works
Self-citationMenyhárt, O., Nagy, Á., & Győrffy, B. (2018) · Royal Society Open Science · doi:10.1098/rsos.181006 · Cited by 507 · see citing works
Sauerbrei, W., Taube, S. E., McShane, L. M., Cavenagh, M. M., & Altman, D. G. (2018) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djy088 · Cited by 489 · see citing works
Self-citationReporting recommendations for tumor marker prognostic studies (REMARK): explanation and elaboration
Altman, D. G., McShane, L. M., Sauerbrei, W., & Taube, S. E. (2012) · BMC Medicine · doi:10.1186/1741-7015-10-51 · Cited by 374 · see citing works
Self-citationLuporsi, É., André, F., Spyratos, F., Martin, P., Jacquemier, J. D., Penault-Llorca, F. M., Tubiana-Mathieu, N., Sigal‐Zafrani, B., Arnould, L., Gompel, A., et al. (2011) · Breast Cancer Research and Treatment · doi:10.1007/s10549-011-1837-z · Cited by 320 · see citing works
Prognostic factors and prognostic models for renal cell carcinoma: a literature review
Klatte, T., Rossi, S. H., & Stewart, G. D. (2018) · World Journal of Urology · doi:10.1007/s00345-018-2309-4 · Cited by 274 · see citing works
Prognostic biomarkers in oral squamous cell carcinoma: A systematic review
Rivera, C., Oliveira, A. K., Costa, R. A. P. E., Rossi, T. D., & Leme, A. F. P. (2017) · Oral Oncology · doi:10.1016/j.oraloncology.2017.07.003 · Cited by 213 · see citing works
A conceptual framework for prognostic research
Kent, P., Cancelliere, C., Boyle, E., Cassidy, J., & Kongsted, A. (2020) · BMC Medical Research Methodology · doi:10.1186/s12874-020-01050-7 · Cited by 138 · see citing works
Goede, V., Coutelle, O., Neuneier, J., Reinacher-Schick, A. C., Schnell, R., Koslowsky, T. C., Weihrauch, M. R., Cremer, B., Kashkar, H., Odenthal, M., et al. (2010) · British Journal of Cancer · doi:10.1038/sj.bjc.6605925 · Cited by 186 · see citing works
Publication of Tumor Marker Research Results: The Necessity for Complete and Transparent Reporting
McShane, L. M., & Hayes, D. F. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2012.42.6858 · Cited by 185 · see citing works
Waste, Leaks, and Failures in the Biomarker Pipeline
Ioannidis, J. P. A., & Bossuyt, P. M. (2017) · Clinical Chemistry · doi:10.1373/clinchem.2016.254649 · Cited by 172 · see citing works
Graziano, F., Galluccio, N., Lorenzini, P., Ruzzo, A., Canestrari, E., D'Emidio, S., Catalano, V., Sisti, V., Ligorio, C., Andreoni, F., et al. (2011) · Journal of Clinical Oncology · doi:10.1200/jco.2011.36.7706 · Cited by 161 · see citing works
Heus, P., Damen, J. A., Pajouheshnia, R., Scholten, R. J. P. M., Reitsma, J. B., Collins, P. G. S., Altman, D. G., Moons, K. G. M., & Hooft, L. (2018) · BMC Medicine · doi:10.1186/s12916-018-1099-2 · Cited by 145 · see citing works
Self-citationPrognostic significance of immunohistochemical biomarkers in oral squamous cell carcinoma
Oliveira, L. R., & Ribeiro‐Silva, A. (2011) · International Journal of Oral and Maxillofacial Surgery · doi:10.1016/j.ijom.2010.12.003 · Cited by 136 · see citing works
STRengthening Analytical Thinking for Observational Studies: the STRATOS initiative
Sauerbrei, W., Abrahamowicz, M., Altman, D. G., le Cessie, S., Carpenter, J. R., & initiative, O. B. O. T. S. (2014) · Statistics in Medicine · doi:10.1002/sim.6265 · Cited by 135 · see citing works
Self-citationHayes, D. F., Allen, J. D., Compton, C. C., Gustavsen, G. G., Leonard, D. G. B., Mccormack, R. T., Newcomer, L. N., Pothier, K. C., Ransohoff, D. F., Schilsky, R. L., et al. (2013) · Science Translational Medicine · doi:10.1126/scitranslmed.3005950 · Cited by 123 · see citing works
Improving the reporting of randomised trials: the CONSORT Statement and beyond
Altman, D. G., Moher, D., & Schulz, K. F. (2012) · Statistics in Medicine · doi:10.1002/sim.5402 · Cited by 117 · see citing works
Self-citationPredicting Clinical Outcomes Using Molecular Biomarkers
BURKE, H. B. (2016) · Biomarkers in Cancer · doi:10.4137/bic.s33380 · Cited by 108 · see citing works
C-reactive protein and long-term ischemic stroke prognosis
VanGilder, R. L., Davidov, D. M., Stinehart, K. R., Huber, J. D., Turner, R. C., Wilson, K., Haney, E., Davis, S. M., Chantler, P. D., Theeke, L. A., et al. (2013) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2013.06.015 · Cited by 105 · see citing works
Agha, R. A., Fowler, A. J., Limb, C., Whitehurst, K., Coe, R., Sagoo, H., Jafree, D. J., Chandrakumar, C., & Gundogan, B. (2016) · International Journal of Surgery · doi:10.1016/j.ijsu.2016.04.032 · Cited by 99 · see citing works
Noordhuis, M. G., Eijsink, J. J. H., Roossink, F., de Graeff, P., Pras, E., Schuuring, E. M. D., Wisman, G. B. A., de Bock, G. H., & van der Zee, A. G. J. (2011) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2010.09.043 · Cited by 89 · see citing works
Lea, D., Håland, S., Hagland, H. R., & Søreide, K. (2014) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521.2014.950692 · Cited by 84 · see citing works
Khoja, L., Atenafu, E. G., Templeton, A. J., Qye, Y., Chappell, M. A., Saibil, S. D., Hogg, D., Butler, M. O., & Joshua, A. M. (2016) · Cancer Medicine · doi:10.1002/cam4.878 · Cited by 82 · see citing works
Circulating tumor cells in prostate cancer: A potential surrogate marker of survival
Doyen, J., Alix‐Panabières, C., Hofman, P. M., Parks, S. K., Chamorey, E., Naman, H. L., & Hannoun‐Lévi, J. (2011) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2011.05.004 · Cited by 80 · see citing works
Four Proposals to Help Improve the Medical Research Literature
Moher, D., & Altman, D. G. (2015) · PLoS Medicine · doi:10.1371/journal.pmed.1001864 · Cited by 78 · see citing works
Self-citationRuzzo, A., Graziano, F., Vincenzi, B., Canestrari, E., Perrone, G., Galluccio, N., Catalano, V., Loupakis, F., Rabitti, C., Santini, D., et al. (2012) · The Oncologist · doi:10.1634/theoncologist.2012-0081 · Cited by 76 · see citing works
Bone marrow WT1 levels at diagnosis, post-induction and post-intensification in adult de novo AML
Nomdedeu, J. F., Hoyos, M., Carricondo, M., Bussaglia, E., Estivill, C., Esteve, J., Tormo, M., Duarte, R. F., Salamero, O., Llano, M. P. Q. D., et al. (2013) · Leukemia · doi:10.1038/leu.2013.111 · Cited by 74 · see citing works
Sturgeon, C. M., Hill, R. G., Hortin, G. L., & Thompson, D. (2010) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201000073 · Cited by 73 · see citing works
Britten, C. M., Janetzki, S., van der Burg, S. H., Huber, C. H., Kalos, M. D., Levitsky, H. I., Maecker, H. T., Melief, C. J. M., O’Donnell-Tormey, J., Odunsi, K. O., et al. (2010) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-010-0940-z · Cited by 69 · see citing works
Intergroup, O. B. O. T. I. M., Massi, D., Rulli, E., Cossa, M., Valeri, B., Rodolfo, M., Merelli, B., Logu, F. D., Nassini, R., Vecchio, M. D., et al. (2019) · Journal for ImmunoTherapy of Cancer · doi:10.1186/s40425-019-0797-4 · Cited by 69 · see citing works
New biomarkers for diagnosis and prognosis of localized prostate cancer
Chistiakov, D. A., Myasoedova, V. A., Grechko, A. V., Melnichenko, A. А., & Orekhov, A. N. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.01.012 · Cited by 67 · see citing works
Anastasi, E., Granato, T., Marchei, G. G., Viggiani, V., Colaprisca, B., Comploj, S., Reale, M. G., Frati, L., & Midulla, C. (2010) · Tumor Biology · doi:10.1007/s13277-010-0049-1 · Cited by 62 · see citing works
Countering imprecision in precision medicine
Hey, S. P., & Kesselheim, A. S. (2016) · Science · doi:10.1126/science.aaf5101 · Cited by 59 · see citing works
Impact of adding breast density to breast cancer risk models: A systematic review
Vilmun, B. M., Vejborg, I., Lynge, E., Lillholm, M., Nielsen, M., Nielsen, M. B., & Carlsen, J. F. (2020) · European Journal of Radiology · doi:10.1016/j.ejrad.2020.109019 · Cited by 59 · see citing works
Halligan, S., Menu, Y., & Mallett, S. (2021) · European Radiology · doi:10.1007/s00330-021-07971-1 · Cited by 50 · see citing works
Self-citationGene signatures of breast cancer progression and metastasis
Rodenhiser, D. I., Andrews, J. D., Vandenberg, T. A., & Chambers, A. F. (2011) · Breast Cancer Research · doi:10.1186/bcr2791 · Cited by 58 · see citing works
Zlobec, I., Karamitopoulou, E., Terracciano, L., Piscuoglio, S., Iezzi, G., Muraro, M. G., Spagnoli, G. C., Baker, K., Tzankov, A., & Lugli, A. (2010) · PLoS ONE · doi:10.1371/journal.pone.0014282 · Cited by 58 · see citing works
p53 immunohistochemistry in bladder cancer—a new approach to an old question
Goebell, P. J., Groshen, S. G., & Schmitz‐Dräger, B. J. (2010) · Urologic Oncology Seminars and Original Investigations · doi:10.1016/j.urolonc.2010.03.021 · Cited by 57 · see citing works
Lee, H.-J., Kang, Y., Lee, J.-S., Byun, J., Kim, U., Jang, S., Rho, G., & Park, B.-W. (2015) · BMC Oral Health · doi:10.1186/s12903-015-0120-9 · Cited by 57 · see citing works
Jacot, W., Thézenas, S., Senal, R., Viglianti, C., Laberenne, A.-C., Lopez‐Crapez, E., Bibeau, F., Bleuse, J., Romieu, G., & Lamy, P. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-523 · Cited by 56 · see citing works
Schumacher, M. C., Holländer, N., Schwarzer, G., Binder, H., & Sauerbrei, W. (2012) · Chapman & Hall/CRC eBooks · doi:10.1201/b11800-30 · Cited by 57 · see citing works
Self-citationHuber, F., Montani, M., Sulser, T., Jaggi, R. B., Wild, P. J., Moch, H., Gevensleben, H., Schmid, M. C., Wyder, S., & Kristiansen, G. (2014) · British Journal of Cancer · doi:10.1038/bjc.2014.588 · Cited by 52 · see citing works
Aldin, A., Umlauff, L., Estcourt, L. J., Collins, P. G. S., Moons, K. G. M., Engert, A., Kobe, C., von Tresckow, B., Haque, M., Foroutan, F., et al. (2020) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012643.pub3 · Cited by 51 · see citing works
Hoyos, M., Nomdedeu, J. F., Esteve, J., Duarte, R. F., Ribera, J., Llorente, A., Escoda, L., Bueno, J., Tormo, M., Gallardo, D., et al. (2013) · European Journal Of Haematology · doi:10.1111/ejh.12130 · Cited by 48 · see citing works
New Prognostic Markers for Outcome of Acute Pancreatitis
Sigounas, D., Tatsioni, A., Christodoulou, D. K., Tsianos, E. V., & Ioannidis, J. P. A. (2011) · Pancreas · doi:10.1097/mpa.0b013e31820bf8ac · Cited by 44 · see citing works
Importance of Transparent Reporting of Health Research
Altman, D. G., & Moher, D. (2014) · Wiley eBooks · doi:10.1002/9781118715598.ch1 · Cited by 44 · see citing works
Self-citationPrognostic DNA methylation markers for sporadic colorectal cancer: a systematic review
Draht, M. X. G., Goudkade, D., Koch, A., Grabsch, H. I., Weijenberg, M. P., van Engeland, M., Melotte, V., & Smits, K. M. (2018) · Clinical Epigenetics · doi:10.1186/s13148-018-0461-8 · Cited by 42 · see citing works
Prognostic molecular markers in cancer – quo vadis?
Søland, T. M., & Brusevold, I. J. (2013) · Histopathology · doi:10.1111/his.12184 · Cited by 39 · see citing works
Sekula, P., Mallett, S., Altman, D. G., & Sauerbrei, W. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178531 · Cited by 38 · see citing works
Self-citationNomdedeu, J. F., Esquirol, A., Carricondo, M., Pratcorona, M., Hoyos, M., Garrido, A., Rubio, M., Bussaglia, E., García‐Cadenas, I., Estivill, C., et al. (2017) · Transplantation and Cellular Therapy · doi:10.1016/j.bbmt.2017.09.001 · Cited by 36 · see citing works
Overinterpretation and misreporting of prognostic factor studies in oncology: a systematic review
Kempf, E., de Beyer, J. A., Cook, J. A., Holmes, J., Mohammed, S. B., Nguyen, T., Simera, I., Trivella, M., Altman, D. G., Hopewell, S., et al. (2018) · British Journal of Cancer · doi:10.1038/s41416-018-0305-5 · Cited by 36 · see citing works
Self-citationBergot, E., Levallet, G., Campbell, K., Dubois, F., Lechapt, E., & Zalcman, G. (2013) · European Respiratory Review · doi:10.1183/09059180.00007113 · Cited by 32 · see citing works
Kaijser, J., Belle, V. V., Gorp, T. V., Sayasneh, A., Vergote, I. B., Bourne, T., CALSTER, B. V., & Timmerman, D. (2014) · International Journal of Gynecological Cancer · doi:10.1097/igc.0000000000000181 · Cited by 30 · see citing works
Making research articles fit for purpose: structured reporting of key methods and findings
Altman, D. G. (2015) · Trials · doi:10.1186/s13063-015-0575-7 · Cited by 28 · see citing works
Self-citationAldin, A., Umlauff, L., Estcourt, L. J., Collins, P. G. S., Moons, K. G. M., Engert, A., Kobe, C., von Tresckow, B., Haque, M., Foroutan, F., et al. (2019) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012643.pub2 · Cited by 28 · see citing works
collaborators, A., Søreide, K., Watson, M. M., Lea, D., Nordgård, O., Søreide, J. A., & Hagland, H. R. (2016) · Journal of Translational Medicine · doi:10.1186/s12967-016-0951-4 · Cited by 28 · see citing works
Estimation of prognosis by circulating biomarkers in patients with non-small cell lung cancer
Holdenrieder, S., Nagel, D., & Stieber, P. (2010) · Cancer Biomarkers · doi:10.3233/cbm-2009-0128 · Cited by 28 · see citing works
Structured reporting to improve transparency of analyses in prognostic marker studies
Sauerbrei, W., Haeussler, T., Balmford, J., & Huebner, M. (2022) · BMC Medicine · doi:10.1186/s12916-022-02304-5 · Cited by 27 · see citing works
Self-citationThe role of tissue microarray in the era of target-based agents
Franco, R., Caraglia, M., Facchini, G., Abbruzzese, A., & Botti, G. (2011) · Expert Review of Anticancer Therapy · doi:10.1586/era.11.65 · Cited by 26 · see citing works
Overview of data-synthesis in systematic reviews of studies on outcome prediction models
van den Berg, T., Heymans, M. W., Leone, S. S., Vergouw, D., Hayden, J. A., Verhagen, A. P., & de Vet, H. C. W. (2013) · BMC Medical Research Methodology · doi:10.1186/1471-2288-13-42 · Cited by 26 · see citing works
Yoneda, Y., Kunisada, T., Naka, N., Nishida, Y., Kawai, A., Morii, T., Takeda, K., Hasei, J., Yamakawa, Y., & Ozaki, T. (2013) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2013.09.004 · Cited by 24 · see citing works
Meisner, A., Kerr, K. F., Thiessen‐Philbrook, H., Coca, S. G., & Parikh, C. R. (2015) · Kidney International · doi:10.1038/ki.2015.283 · Cited by 22 · see citing works
Monitoring the AML1/ETO fusion transcript to predict outcome in childhood acute myeloid leukemia
Zhang, L., Cao, Z., Ruan, M., Zeng, Q., Zhao, L., Li, Q., Zou, Y., Wang, J., & Zhu, X. (2014) · Pediatric Blood & Cancer · doi:10.1002/pbc.25109 · Cited by 22 · see citing works
Kim, H., Kang, Y., Byun, J., Jang, S., Rho, G., Lee, J.-S., & Park, B.-W. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18112339 · Cited by 21 · see citing works
Determinants of recurrence after intended curative resection for colorectal cancer
Wilhelmsen, M., Kring, T. C., Jørgensen, L. N., Madsen, M. R., Jess, P., Bulut, O., Nielsen, K. T., Andersen, C. L., & Nielsen, H. J. (2014) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521.2014.926981 · Cited by 21 · see citing works
Wen, S. W. C., Andersen, R. F., Hansen, T. F., Nyhus, C. H., Hager, H., Hilberg, O., & Jakobsen, A. K. M. (2021) · Translational Lung Cancer Research · doi:10.21037/tlcr-20-826 · Cited by 20 · see citing works
Winzer, K., Buchholz, A., Schumacher, M. C., & Sauerbrei, W. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149977 · Cited by 20 · see citing works
Self-citationPrognostic Significance of Dickkopf-1 in Gastric Cancer Survival: A Meta-Analysis
Liu, Q.-R., Li, Y., Deng, Z., & Cao, J. (2016) · Genetic Testing and Molecular Biomarkers · doi:10.1089/gtmb.2015.0154 · Cited by 20 · see citing works
Reporting of Rehabilitation Intervention for Low Back Pain in Randomized Controlled Trials
Gianola, S., Castellini, G., Agostini, M., Bolotta, R., Corbetta, D., Frigerio, P., Gasparini, M., Gozzer, P., Guariento, E., LI, L. C., et al. (2015) · Spine · doi:10.1097/brs.0000000000001290 · Cited by 19 · see citing works
KLK15 is a prognostic marker for progression‐free survival in patients with radical prostatectomy
Rabien, A., Fritzsche, F. R., Jung, M., Tölle, A., Diamandis, E. P., Miller, K., Jung, K., Kristiansen, G., & Stephan, C. (2010) · International Journal of Cancer · doi:10.1002/ijc.25435 · Cited by 19 · see citing works
Knowledge Integration in Cancer: Current Landscape and Future Prospects
Ioannidis, J. P. A., Schully, S. D., Lam, T. K., & Khoury, M. J. (2012) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-12-1144 · Cited by 18 · see citing works
Timms, J. F., Hale, O. J., & Cramer, R. (2016) · Expert Review of Proteomics · doi:10.1080/14789450.2016.1182431 · Cited by 18 · see citing works
Sauerbrei, W., Bland, M., Evans, S. J. W., Riley, R. D., Royston, P. J., Schumacher, M. C., & Collins, P. G. S. (2020) · Biometrical Journal · doi:10.1002/bimj.202000053 · Cited by 16 · see citing works
Self-citationde Morais, É. F., Pinheiro, J. C., Sena, D. A. C., Galvão, H. C., de Souza, L. B., & Freitas, R. D. A. (2019) · Journal of Oral Pathology and Medicine · doi:10.1111/jop.12841 · Cited by 17 · see citing works
Biomarkers of progression to oral cancer in patients with dysplasia: A systematic review
Rivera, C., Gallegos, R., & Figueroa, C. (2020) · Molecular and Clinical Oncology · doi:10.3892/mco.2020.2112 · Cited by 17 · see citing works
An Online Tool for Improving Biospecimen Data Element Reporting
Cheah, S., Dee, S., Cole, A., Matzke, L. A. M., O’Donoghue, S., & Watson, P. H. (2012) · Biopreservation and Biobanking · doi:10.1089/bio.2012.0033 · Cited by 16 · see citing works
García‐Dabrio, M. C., Hoyos, M., Brunet, S., Tormo, M., Ribera, J., Esteve, J., Gallardo, D., Duarte, R. F., Llano, M. P. Q. D., Bargay, J., et al. (2015) · American Journal of Clinical Pathology · doi:10.1309/ajcprl6xsvfmlh9v · Cited by 15 · see citing works
An Attempt at a Molecular Prediction of Metastasis in Patients with Primary Cutaneous Melanoma
Gschaider, M., Neumann, F., Peters, B., Lenz, F., Cibena, M., Goiser, M., Wolf, I. H., Wenzel, J., Mauch, C., Schreiner, W., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0049865 · Cited by 15 · see citing works
Lung cancer biomarkers – Where we are and what we need
Stieber, P., & Holdenrieder, S. (2010) · Cancer Biomarkers · doi:10.3233/cbm-2009-0132 · Cited by 15 · see citing works
AlHammadi, S. A., Nagshabandi, L. N., Muhammad, H., Sukkarieh, H. H., & Aljada, A. (2025) · Clinical Proteomics · doi:10.1186/s12014-025-09567-z · Cited by 14 · see citing works
A Survey of the Prevalence and Impact of Reporting Guideline Endorsement in Pathology Journals
Caron, J. E., March, J. K., Cohen, M. B., & Schmidt, R. L. (2017) · American Journal of Clinical Pathology · doi:10.1093/ajcp/aqx080 · Cited by 13 · see citing works
Graziano, F., Catalano, V., Lorenzini, P., Giacomini, E., Sarti, D., Fiorentini, G., Nictolis, M. D., Magnani, M., & Ruzzo, A. (2014) · The Pharmacogenomics Journal · doi:10.1038/tpj.2014.11 · Cited by 13 · see citing works
Zalcman, G., Bergot, E., Créveuil, C., Levallet, G., & Lechapt, E. (2010) · Current Opinion in Oncology · doi:10.1097/cco.0b013e3283412eca · Cited by 13 · see citing works
O’Mahony, F. C., Nanda, J., Laird, A., Mullen, P., Caldwell, H., Overton, I. M., Eöry, L., O’Donnell, M., Faratian, D., Powles, T. B., et al. (2013) · Journal of Visualized Experiments · doi:10.3791/50221 · Cited by 11 · see citing works
Special considerations in prognostic research in cancer involving genetic polymorphisms
Savas, S., Liu, G., & Xu, W. (2013) · BMC Medicine · doi:10.1186/1741-7015-11-149 · Cited by 11 · see citing works
Report on a pilot project to introduce a publications officer
Cobey, K. D., Galipeau, J., Shamseer, L., & Moher, D. (2016) · Canadian Medical Association Journal · doi:10.1503/cmaj.151340 · Cited by 10 · see citing works
de Morais, É. F., Pinheiro, J. C., Lira, J., Mafra, R. P., Barboza, C. A. G., Souza, L., & Freitas, R. A. (2020) · Medicina oral, patología oral y cirugía bucal · doi:10.4317/medoral.23305 · Cited by 10 · see citing works
Emerging trends in biomarker discovery: Ease of prognosis and prediction in cancer
Sharma, A. K. (2018) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2018.05.008 · Cited by 10 · see citing works
Bussaglia, E., Pratcorona, M., Carricondo, M., San‐Segundo, L., Rubio, M. A., Monter‐Rovira, A., Brell, A., Badell, I., Esteve, J., Arnán, M., et al. (2020) · Annals of Hematology · doi:10.1007/s00277-020-03910-0 · Cited by 9 · see citing works
Iafolla, M. A. J., Picardo, S. L., Aung, K. L., & Hansen, A. R. (2019) · PLoS ONE · doi:10.1371/journal.pone.0222359 · Cited by 9 · see citing works
Iglesias, A. I., Mihăescu, R., Ioannidis, J. P. A., Khoury, M. J., Little, J., van Duijn, C. M., & Janssens, A. C. J. W. (2014) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2013.10.006 · Cited by 8 · see citing works
Pallarès, V., Hoyos, M., Chillón, C., Barragán, E., Conde, M. I. P., Llop, M., Falgàs, A., Céspedes, M. V., Montesinos, P., Nomdedeu, J. F., et al. (2018) · Cancers · doi:10.3390/cancers10110436 · Cited by 8 · see citing works
Epistemology, Ethics, and Progress in Precision Medicine
Hey, S. P., & Barsanti-Innes, B. (2016) · Perspectives in biology and medicine · doi:10.1353/pbm.2016.0026 · Cited by 8 · see citing works
Altman, D. G., Hrynaszkiewicz, I., Furberg, C. D., Grimshaw, J., & Rothwell, P. M. (2011) · Trials · doi:10.1186/1745-6215-12-248 · Cited by 8 · see citing works
Self-citationPGK1 is a potential biomarker for early diagnosis and prognosis of hepatocellular carcinoma
Yi, J., Luo, X.-H., Huang, W., Yang, W., Qi, Y., He, J., & Xie, H. (2024) · Oncology Letters · doi:10.3892/ol.2024.14242 · Cited by 7 · see citing works
Complex Underdetermination and the Units of Clinical Translation
Hey, S. P. (2015) · THEORIA An International Journal for Theory History and Foundations of Science · doi:10.1387/theoria.12697 · Cited by 6 · see citing works
Jankova, L., Dent, O. F., Molloy, M. P., Chan, C., Chapuis, P. H., Howell, V. M., & Clarke, S. J. (2015) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201400177 · Cited by 7 · see citing works
Misiak, M., & Kurpas, D. (2022) · Advances in Clinical and Experimental Medicine · doi:10.17219/acem/155921 · Cited by 7 · see citing works
- Authors
- Mallett, S., Timmer, A., Sauerbrei, W., & Altman, D. G.
- Affiliations
- University of Oxford (GB)
- University Medical Center Freiburg (DE)
- Corresponding author
- Mallett, S
- Venue
- British Journal of Cancer
- Published
- 2009-12-08
- Volume
- 102
- Issue
- 1
- Pages
- 173-180
- ISSN
- 0007-0920 (ISSN-L)
- 1532-1827
- PMC
- PMC2795163
- OpenAlex
- W2124593264
- Cited by
- 122
- References
- 48
- Citations by year
- 2025: 3 · 2024: 1 · 2023: 1 · 2022: 2 · 2021: 2 · 2020: 10 · 2019: 5 · 2018: 9 · 2017: 10 · 2016: 10 · 2015: 8 · 2014: 13 · 2013: 12 · 2012: 13
- FWCI
- 0.91
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-sa
- www.springer.com/tdm (unspecified)
- Locations
- British Journal of Cancer (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion, cc-by-nc-sa)
- PubMed (publishedVersion)
- Oxford University Research Archive (ORA) (University of Oxford) (acceptedVersion)
- Site cant be reached (submittedVersion)
- University of Birmingham Research Portal (University of Birmingham) (submittedVersion)
- Funders
- Cancer Research UK
- Bundesministerium für Gesundheit
- Topics
- Social Sciences › Decision Sciences › Statistics, Probability and Uncertainty › Meta-analysis and systematic reviews
- Physical Sciences › Mathematics › Statistics and Probability › Statistical Methods in Epidemiology
- Social Sciences › Decision Sciences › Information Systems and Management › Academic Publishing and Open Access
- Keywords
- tumor markers, reporting quality, patient selection bias, multivariable analysis, survival analysis
- MeSH terms
- Humans, Neoplasms, Prognosis, Publishing, Research Design, Biomarkers, Tumor, Writing, Selection Bias, Multivariate Analysis, Survival Analysis, Treatment Outcome, Guidelines as Topic, Patient Selection
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