UroPredict: Machine learning model on real-world data for prediction of kidney cancer recurrence (UroCCR-120).


Journal

NPJ precision oncology
ISSN: 2397-768X
Titre abrégé: NPJ Precis Oncol
Pays: England
ID NLM: 101708166

Informations de publication

Date de publication:
23 Feb 2024
Historique:
received: 01 09 2023
accepted: 30 01 2024
medline: 24 2 2024
pubmed: 24 2 2024
entrez: 23 2 2024
Statut: epublish

Résumé

Renal cell carcinoma (RCC) is most often diagnosed at a localized stage, where surgery is the standard of care. Existing prognostic scores provide moderate predictive performance, leading to challenges in establishing follow-up recommendations after surgery and in selecting patients who could benefit from adjuvant therapy. In this study, we developed a model for individual postoperative disease-free survival (DFS) prediction using machine learning (ML) on real-world prospective data. Using the French kidney cancer research network database, UroCCR, we analyzed a cohort of surgically treated RCC patients. Participating sites were randomly assigned to either the training or testing cohort, and several ML models were trained on the training dataset. The predictive performance of the best ML model was then evaluated on the test dataset and compared with the usual risk scores. In total, 3372 patients were included, with a median follow-up of 30 months. The best results in predicting DFS were achieved using Cox PH models that included 24 variables, resulting in an iAUC of 0.81 [IC95% 0.77-0.85]. The ML model surpassed the predictive performance of the most commonly used risk scores while handling incomplete data in predictors. Lastly, patients were stratified into four prognostic groups with good discrimination (iAUC = 0.79 [IC95% 0.74-0.83]). Our study suggests that applying ML to real-world prospective data from patients undergoing surgery for localized or locally advanced RCC can provide accurate individual DFS prediction, outperforming traditional prognostic scores.

Identifiants

pubmed: 38396089
doi: 10.1038/s41698-024-00532-x
pii: 10.1038/s41698-024-00532-x
doi:

Types de publication

Journal Article

Langues

eng

Pagination

45

Informations de copyright

© 2024. The Author(s).

Références

Bukavina, L. et al. Epidemiology of renal cell carcinoma: 2022 update. Eur. Urol. 82, 529–542 (2022).
pubmed: 36100483 doi: 10.1016/j.eururo.2022.08.019
Sung, H. et al. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71, 209–249 (2021).
pubmed: 33538338 doi: 10.3322/caac.21660
Ferlay, J. et al. Cancer incidence and mortality patterns in Europe: Estimates for 40 countries and 25 major cancers in 2018. Eur. J. Cancer 103, 356–387 (2018).
pubmed: 30100160 doi: 10.1016/j.ejca.2018.07.005
Ljungberg, B. et al. European association of urology guidelines on renal cell carcinoma: the 2022 update. Eur. Urol. 82, 399–410 (2022).
pubmed: 35346519 doi: 10.1016/j.eururo.2022.03.006
Kane, C. J., Mallin, K., Ritchey, J., Cooperberg, M. R. & Carroll, P. R. Renal cell cancer stage migration: analysis of the National Cancer Data Base. Cancer 113, 78–83 (2008).
pubmed: 18491376 doi: 10.1002/cncr.23518
Turner, R. M., Morgan, T. M. & Jacobs, B. L. Epidemiology of the small renal mass and the treatment disconnect phenomenon. Urologic Clin. North Am. 44, 147–154 (2017).
doi: 10.1016/j.ucl.2016.12.001
Williamson, T. J., Pearson, J. R., Ischia, J., Bolton, D. M. & Lawrentschuk, N. Guideline of guidelines: follow-up after nephrectomy for renal cell carcinoma. BJU Int. 117, 555–562 (2016).
pubmed: 26617405 doi: 10.1111/bju.13384
Jamil, M. L. et al. Long-term risk of recurrence in surgically treated renal cell carcinoma: a Post Hoc Analysis of the Eastern Cooperative Oncology Group—American College of Radiology Imaging Network E2805 Trial Cohort. Eur. Urol. 77, 277–281 (2020).
pubmed: 31703971 doi: 10.1016/j.eururo.2019.10.028
Borregales, L. D. et al. Prognosticators and outcomes of patients with renal cell carcinoma and adjacent organ invasion treated with radical nephrectomy. Urol. Oncol. 34, 237.e19–26 (2016).
pubmed: 26707613 doi: 10.1016/j.urolonc.2015.11.020
Escudier, B. et al. Renal cell carcinoma: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann. Oncol. 30, 706–720 (2019).
pubmed: 30788497 doi: 10.1093/annonc/mdz056
Bora, A. et al. Predicting the risk of developing diabetic retinopathy using deep learning. Lancet Digital Health 3, e10–e19 (2021).
pubmed: 33735063 doi: 10.1016/S2589-7500(20)30250-8
Tran, K. A. et al. Deep learning in cancer diagnosis, prognosis and treatment selection. Genome Med. 13, 152 (2021).
pubmed: 34579788 pmcid: 8477474 doi: 10.1186/s13073-021-00968-x
Boulenger de Hauteclocque, A. et al. Machine-learning approach for prediction of pT3a upstaging and outcomes of localized renal cell carcinoma (UroCCR-15). BJU Int. https://doi.org/10.1111/bju.15959 (2023)
Compérat, E. et al. Comparison of UICC and AJCC 8th edition TNM classifications in uropathology. Ann. Pathol. 39, 158–166 (2019).
pubmed: 30711335 doi: 10.1016/j.annpat.2018.12.005
Fuhrman, S. A., Lasky, L. C. & Limas, C. Prognostic significance of morphologic parameters in renal cell carcinoma. Am. J. Surg. Pathol. 6, 655–663 (1982).
pubmed: 7180965 doi: 10.1097/00000478-198210000-00007
Cheville, J. C., Lohse, C. M., Zincke, H., Weaver, A. L. & Blute, M. L. Comparisons of outcome and prognostic features among histologic subtypes of renal cell carcinoma. Am. J. Surg. Pathol. 27, 612–624 (2003).
pubmed: 12717246 doi: 10.1097/00000478-200305000-00005
Patard, J.-J. et al. Prognostic value of histologic subtypes in renal cell carcinoma: a multicenter experience. J. Clin. Oncol. 23, 2763–2771 (2005).
pubmed: 15837991 doi: 10.1200/JCO.2005.07.055
Huang, H. et al. Microvascular invasion as a prognostic indicator in renal cell carcinoma: a systematic review and meta-analysis. Int. J. Clin. Exp. Med. 8, 10779–10792 (2015).
pubmed: 26379872 pmcid: 4565255
Grivennikov, S. I., Greten, F. R. & Karin, M. Immunity, inflammation, and cancer. Cell 140, 883–899 (2010).
pubmed: 20303878 pmcid: 2866629 doi: 10.1016/j.cell.2010.01.025
Templeton, A. J. et al. Prognostic role of neutrophil-to-lymphocyte ratio in solid tumors: a systematic review and meta-analysis. J. Natl Cancer Inst. 106, dju124 (2014).
pubmed: 24875653 doi: 10.1093/jnci/dju124
Nunno, V. D. et al. Prognostic impact of neutrophil-to-lymphocyte ratio in renal cell carcinoma: a systematic review and meta-analysis. Immunotherapy 11, 631–643 (2019).
pubmed: 30943858 doi: 10.2217/imt-2018-0175
Allenet, C. et al. Can pre-operative neutrophil-to-lymphocyte ratio (NLR) help predict non-metastatic renal carcinoma recurrence after nephrectomy? (UroCCR-61 Study). Cancers (Basel) 14, 5692 (2022).
pubmed: 36428784 doi: 10.3390/cancers14225692
Pichler, M. et al. Validation of the pre-treatment neutrophil–lymphocyte ratio as a prognostic factor in a large European cohort of renal cell carcinoma patients. Br. J. Cancer 108, 901–907 (2013).
pubmed: 23385728 pmcid: 3590665 doi: 10.1038/bjc.2013.28
Zisman, A. et al. Improved prognostication of renal cell carcinoma using an integrated staging system. JCO 19, 1649–1657 (2001).
doi: 10.1200/JCO.2001.19.6.1649
Khene, Z.-E. et al. Application of machine learning models to predict recurrence after surgical resection of nonmetastatic renal cell carcinoma. European Urol. Oncol. S2588931122001377 https://doi.org/10.1016/j.euo.2022.07.007 (2022)
Usher-Smith, J. A. et al. Risk models for recurrence and survival after kidney cancer: a systematic review. BJU Int. 130, 562–579 (2022).
pubmed: 34914159 doi: 10.1111/bju.15673
Correa, A. F. et al. Predicting disease recurrence, early progression, and overall survival following surgical resection for high-risk localized and locally advanced renal cell carcinoma. Eur. Urol. 80, 20–31 (2021).
pubmed: 33707112 pmcid: 8627688 doi: 10.1016/j.eururo.2021.02.025
Lee, H. J., Lee, A., Huang, H. H. & Lau, W. K. O. External validation of the updated Leibovich prognostic models for clear cell and papillary renal cell carcinoma in an Asian population. Urol. Oncol. 37, 356.e9–356.e18 (2019).
pubmed: 30905510 doi: 10.1016/j.urolonc.2019.02.014
Khene, Z.-E. et al. External validation of the ASSURE model for predicting oncological outcomes after resection of high-risk renal cell carcinoma (RESCUE Study: UroCCR 88). Eur. Urol. Open Sci. 33, 89–93 (2021).
pubmed: 34661173 pmcid: 8502703 doi: 10.1016/j.euros.2021.09.004
Byun, S.-S. et al. Deep learning based prediction of prognosis in nonmetastatic clear cell renal cell carcinoma. Sci. Rep. 11, 1242 (2021).
pubmed: 33441830 pmcid: 7806580 doi: 10.1038/s41598-020-80262-9
Kim, H., Lee, S. J., Park, S. J., Choi, I. Y. & Hong, S.-H. Machine learning approach to predict the probability of recurrence of renal cell carcinoma after surgery: prediction model development study. JMIR Med Inf. 9, e25635 (2021).
doi: 10.2196/25635
Gui, C.-P. et al. Multimodal recurrence scoring system for prediction of clear cell renal cell carcinoma outcome: a discovery and validation study. Lancet Digit Health 5, e515–e524 (2023).
pubmed: 37393162 doi: 10.1016/S2589-7500(23)00095-X
Leibovich, B. C. et al. Prediction of progression after radical nephrectomy for patients with clear cell renal cell carcinoma: a stratification tool for prospective clinical trials. Cancer 97, 1663–1671 (2003).
pubmed: 12655523 doi: 10.1002/cncr.11234
Choueiri, T. K. et al. Adjuvant pembrolizumab after nephrectomy in renal-cell carcinoma. N. Engl. J. Med. 385, 683–694 (2021).
pubmed: 34407342 doi: 10.1056/NEJMoa2106391
Pal, S. K. et al. Adjuvant atezolizumab versus placebo for patients with renal cell carcinoma at increased risk of recurrence following resection (IMmotion010): a multicentre, randomised, double-blind, phase 3 trial. Lancet 400, 1103–1116 (2022).
pubmed: 36099926 doi: 10.1016/S0140-6736(22)01658-0
Motzer, R. J. et al. Adjuvant nivolumab plus ipilimumab versus placebo for localised renal cell carcinoma after nephrectomy (CheckMate 914): a double-blind, randomised, phase 3 trial. Lancet 401, 821–832 (2023).
pubmed: 36774933 doi: 10.1016/S0140-6736(22)02574-0
Bigot, P. et al. French AFU Cancer Committee Guidelines—Update 2022-2024: management of kidney cancer. Progrès. Urologie 32, 1195–1274 (2022).
doi: 10.1016/j.purol.2022.07.146
Raghunathan, T., Lepkowski, J., Hoewyk, J. & Solenberger, P. A multivariate technique for multiply imputing missing values using a sequence of regression models. Surv. Methodol. 27 (2000).
Azur, M. J., Stuart, E. A., Frangakis, C. & Leaf, P. J. Multiple imputation by chained equations: what is it and how does it work? Int. J. Methods Psychiatr. Res. 20, 40–49 (2011).
pubmed: 21499542 pmcid: 3074241 doi: 10.1002/mpr.329
Cox, D. R. Regression models and life-tables. J. R. Stat. Soc.: Ser. B (Methodol.) 34, 187–202 (1972).
Blanche, P., Kattan, M. W. & Gerds, T. A. The c-index is not proper for the evaluation of t-year predicted risks. Biostatistics 20, 347–357 (2019).
pubmed: 29462286 doi: 10.1093/biostatistics/kxy006
Uno, H., Cai, T., Pencina, M. J., D’Agostino, R. B. & Wei, L. J. On the C-statistics for evaluating overall adequacy of risk prediction procedures with censored survival data. Stat. Med. 30, 1105–1117 (2011).
pubmed: 21484848 pmcid: 3079915 doi: 10.1002/sim.4154
Nadeau, C. & Bengio, Y. Inference for the generalization error. Mach. Learn. 52, 239–281 (2003).
doi: 10.1023/A:1024068626366
Lundberg, S. M. et al. From local explanations to global understanding with explainable AI for trees. Nat. Mach. Intell. 2, 56–67 (2020).
pubmed: 32607472 pmcid: 7326367 doi: 10.1038/s42256-019-0138-9
Frank, I. et al. An outcome prediction model for patients with clear cell renal cell carcinoma treated with radical nephrectomy based on tumor stage, size, grade and necrosis: the Ssign Score. J. Urol. 168, 2395–2400 (2002).
pubmed: 12441925 doi: 10.1016/S0022-5347(05)64153-5
Buti, S. et al. Validation of a new prognostic model to easily predict outcome in renal cell carcinoma: the GRANT score applied to the ASSURE trial population. Ann. Oncol. 28, 2747–2753 (2017).
pubmed: 28945839 pmcid: 5815563 doi: 10.1093/annonc/mdx492
Leibovich, B. C. et al. Predicting oncologic outcomes in renal cell carcinoma after surgery. Eur. Urol. 73, 772–780 (2018).
pubmed: 29398265 doi: 10.1016/j.eururo.2018.01.005
Rivera, S. C. et al. Guidelines for clinical trial protocols for interventions involving artificial intelligence: the SPIRIT-AI extension. Lancet Digital Health 2, e549–e560 (2020).
doi: 10.1016/S2589-7500(20)30219-3

Auteurs

Gaëlle Margue (G)

Bordeaux University Hospital, Urology department, Bordeaux, France. gaelle.margue@chu-bordeaux.fr.
Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France. gaelle.margue@chu-bordeaux.fr.

Loïc Ferrer (L)

SOPHiA GENETICS, Multimodal R&D team, Pessac, France.

Guillaume Etchepare (G)

SOPHiA GENETICS, Multimodal R&D team, Pessac, France.

Pierre Bigot (P)

Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France.
Angers University hospital, Urology department, Angers, France.

Karim Bensalah (K)

Rennes university hospital, Urology department, Rennes, France.

Arnaud Mejean (A)

HEGP-APHP, Urology department, Paris, France.

Morgan Roupret (M)

Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France.
La Pitié APHP, Urology department, Paris, France.

Nicolas Doumerc (N)

Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France.
Toulouse university hospital, Urology department, Toulouse, France.

Alexandre Ingels (A)

Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France.
Mondor-APHP, Urology department, Paris, France.

Romain Boissier (R)

Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France.
APHM, Urology department, Marseille, France.

Géraldine Pignot (G)

IPC, Urology department, Marseille, France.

Bastien Parier (B)

Kremlin-Bicêtre -APHP, Urology department, Paris, France.

Philippe Paparel (P)

HCL, Urology department, Lyon, France.

Thibaut Waeckel (T)

Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France.
Caen University Hospital, Urology department, Caen, France.

Thierry Colin (T)

SOPHiA GENETICS, Multimodal R&D team, Pessac, France.

Jean-Christophe Bernhard (JC)

Bordeaux University Hospital, Urology department, Bordeaux, France.
Kidney Cancer group of the French Association of Urology Cancer Committee, Paris, France.

Classifications MeSH