A Two-Step Frailty Assessment Strategy in Older Patients With Solid Tumors: A Decision Curve Analysis

Adolfo González Serrano, Marie Laurent, Thomas Barnay, Claudia Martínez-Tapia, Etienne Audureau, Pascaline Boudou-Rouquette, Thomas Aparicio, Florence Rollot-Trad, Pierre Soubeyran, Carine Bellera, Philippe Caillet, Elena Paillaud, Florence Canouï-Poitrine, Adolfo González Serrano, Marie Laurent, Thomas Barnay, Claudia Martínez-Tapia, Etienne Audureau, Pascaline Boudou-Rouquette, Thomas Aparicio, Florence Rollot-Trad, Pierre Soubeyran, Carine Bellera, Philippe Caillet, Elena Paillaud, Florence Canouï-Poitrine

Abstract

Purpose: The intended clinical value of frailty screening is to identify unfit patients needing geriatric assessment (GA) and to prevent unnecessary GA in fit patients. These hypotheses rely on the sensitivity and specificity of screening tests, but they have not been verified.

Methods: We performed a cross-sectional analysis of outpatients age ≥ 70 years with prostate, breast, colorectal, or lung cancer included in the ELCAPA cohort study (ClinicalTrials.gov identifier: NCT02884375) between February 2007 and December 2019. The diagnostic accuracy of the G8 Geriatric Screening Tool (G8) and modified G8 scores for identifying unfit patients was determined on the basis of GA results. We used decision curve analysis to calculate the benefit of frailty screening for detecting unfit patients and avoiding unnecessary GA in fit patients across different threshold probabilities.

Results: We included 1,648 patients (median age, 81 years), and 1,428 (87%) were unfit. The sensitivity and specificity were, respectively, 85% (95% CI, 84 to 87) and 59% (95% CI, 57 to 61) for G8, and 86% (95% CI, 84 to 87) and 60% (95% CI, 58 to 63) for the modified G8 score. For decision curve analysis, the net benefit (NB) for identifying unfit patients were 0.72 for G8, 0.72 for the modified G8, and 0.82 for GA at a threshold probability of 0.25. At a threshold probability of 0.33, the NBs were 0.71, 0.72, and 0.80, respectively. At a threshold probability of 0.5, the NBs were 0.68, 0.69, and 0.73, respectively. No screening tool reduced unnecessary GA in fit patients at predefined threshold probabilities.

Conclusion: Although frailty screening tests showed good diagnostic accuracy, screening showed no clinical benefits over the GA-for-all strategy. NB approaches, in addition to diagnostic accuracy, are necessary to assess the clinical value of tests.

Conflict of interest statement

Elena Paillaud

Honoraria: GlaxoSmithKline, Pfizer, MSD, Novartis, LEO Pharma

Research Funding: Pfizer

No other potential conflicts of interest were reported.

Figures

FIG 1.
FIG 1.
Flow diagram of participants and available data.
FIG 2.
FIG 2.
Decision curve for the NB of three different strategies (relative to not doing GA for any patient), with different threshold probabilities. The odds of 1:3 and 1:2 mean that missing an unfit patient is, respectively, three and two times as bad as exposing a fit patient to an unnecessary GA. The odds of 1:1 mean missing an unfit patient is the same as exposing a fit patient to an unnecessary GA. The NB represents the number of patients (per 100) who will be found to be unfit using a given frailty screening tool. G8, G8 Geriatric Screening Tool; GA, geriatric assessment; NB, net benefit.

References

    1. Wildiers H, Heeren P, Puts M, et al. : International Society of Geriatric Oncology consensus on geriatric assessment in older patients with cancer. J Clin Oncol 32:2595-2603, 2014
    1. Caillet P, Canoui-Poitrine F, Vouriot J, et al. : Comprehensive geriatric assessment in the decision-making process in elderly patients with cancer: ELCAPA study. J Clin Oncol 29:3636-3642, 2011
    1. Caillet P, Laurent M, Bastuji-Garin S, et al. : Optimal management of elderly cancer patients: Usefulness of the comprehensive geriatric assessment. Clin Interv Aging 9:1645-1660, 2014
    1. Corre R, Greillier L, Le Caër H, et al. : Use of a comprehensive geriatric assessment for the management of elderly patients with advanced non–small-cell lung cancer: The phase III randomized ESOGIA-GFPC-GECP 08-02 study. J Clin Oncol 34:1476-1483, 2016
    1. Li D, Sun CL, Kim H, et al. : Geriatric Assessment-Driven Intervention (GAIN) on chemotherapy-related toxic effects in older adults with cancer: A randomized clinical trial. JAMA Oncol 7:e214158, 2021
    1. Mohile SG, Mohamed MR, Xu H, et al. : Evaluation of geriatric assessment and management on the toxic effects of cancer treatment (GAP70+): A cluster-randomised study. Lancet 398:1894-1904, 2021
    1. Mohile SG, Dale W, Somerfield MR, et al. : Practical assessment and management of vulnerabilities in older patients receiving chemotherapy: ASCO guideline for geriatric oncology. J Clin Oncol 36:2326-2347, 2018
    1. Dotan E, Walter LC, Browner IS, et al. : NCCN Clinical Practice Guidelines in Oncology: Older Adult Oncology. Version 1.2021.
    1. Decoster L, Van Puyvelde K, Mohile S, et al. : Screening tools for multidimensional health problems warranting a geriatric assessment in older cancer patients: An update on SIOG recommendations. Ann Oncol 26:288-300, 2015
    1. Garcia MV, Agar MR, Soo WK, et al. : Screening tools for identifying older adults with cancer who may benefit from a geriatric assessment: A systematic review. JAMA Oncol 7:616-627, 2021
    1. Pallis AG, Gridelli C, Wedding U, et al. : Management of elderly patients with NSCLC; updated expert’s opinion paper: EORTC Elderly Task Force, Lung Cancer Group and International Society for Geriatric Oncology. Ann Oncol 25:1270-1283, 2014
    1. Biganzoli L, Wildiers H, Oakman C, et al. : Management of elderly patients with breast cancer: Updated recommendations of the International Society of Geriatric Oncology (SIOG) and European Society of Breast Cancer Specialists (EUSOMA). Lancet Oncol 13:e148-e160, 2012
    1. Mottet N, van den Bergh RCN, Briers E, et al. : EAU-EANM-ESTRO-ESUR-SIOG guidelines on prostate cancer—2020 update. Part 1: Screening, diagnosis, and local treatment with curative intent. Eur Urol 79:243-262, 2021
    1. Montroni I, Ugolini G, Saur NM, et al. : Personalized management of elderly patients with rectal cancer: Expert recommendations of the European Society of Surgical Oncology, European Society of Coloproctology, International Society of Geriatric Oncology, and American College of Surgeons Commission on Cancer. Eur J Surg Oncol 44:1685-1702, 2018
    1. Pallis AG, Fortpied C, Wedding U, et al. : EORTC elderly task force position paper: Approach to the older cancer patient. Eur J Cancer 46:1502-1513, 2010
    1. Vickers AJ, Elkin EB: Decision curve analysis: A novel method for evaluating prediction models. Med Decis Making 26:565-574, 2006
    1. Moons KGM, Harrell FE: Sensitivity and specificity should be de-emphasized in diagnostic accuracy studies. Acad Radiol 10:670-672, 2003
    1. Vickers AJ, Calster BV, Steyerberg EW: Net benefit approaches to the evaluation of prediction models, molecular markers, and diagnostic tests. BMJ 352:i6, 2016
    1. Fitzgerald M, Saville BR, Lewis RJ: Decision curve analysis. JAMA 313:409-410, 2015
    1. Bellera CA, Rainfray M, Mathoulin-Pélissier S, et al. : Screening older cancer patients: First evaluation of the G-8 geriatric screening tool. Ann Oncol 23:2166-2172, 2012
    1. Martinez-Tapia C, Canoui-Poitrine F, Bastuji-Garin S, et al. : Optimizing the G8 screening tool for older patients with cancer: Diagnostic performance and validation of a six-item version. Oncologist 21:188-195, 2016
    1. Droz JP, Balducci L, Bolla M, et al. : Management of prostate cancer in older men: Recommendations of a working group of the International Society of Geriatric Oncology. BJU Int 106:462-469, 2010
    1. Van Calster B, Wynants L, Verbeek JFM, et al. : Reporting and interpreting decision curve analysis: A guide for investigators. Eur Urol 74:796-804, 2018
    1. Martinez-Tapia C, Laurent M, Paillaud E, et al. : Predicting frailty and geriatric interventions in older cancer patients: Performance of two screening tools for seven frailty definitions—ELCAPA cohort. Cancers (Basel) 14:244, 2022
    1. Soubeyran P, Bellera C, Goyard J, et al. : Screening for vulnerability in older cancer patients: The ONCODAGE prospective multicenter cohort study. PLoS One 9:e115060, 2014
    1. Luciani A, Ascione G, Bertuzzi C, et al. : Detecting disabilities in older patients with cancer: Comparison between comprehensive geriatric assessment and vulnerable elders survey-13. J Clin Oncol 28:2046-2050, 2010
    1. Biganzoli L, Boni L, Becheri D, et al. : Evaluation of the cardiovascular health study (CHS) instrument and the Vulnerable Elders Survey-13 (VES-13) in elderly cancer patients. Are we still missing the right screening tool? Ann Oncol 24:494-500, 2013
    1. Kenis C, Decoster L, Van Puyvelde K, et al. : Performance of two geriatric screening tools in older patients with cancer. J Clin Oncol 32:19-26, 2014
    1. Russo C, Giannotti C, Signori A, et al. : Predictive values of two frailty screening tools in older patients with solid cancer: A comparison of SAOP2 and G8. Oncotarget 9:35056-35068, 2018
    1. Bellera CA, Artaud F, Rainfray M, et al. : Modeling individual and relative accuracy of screening tools in geriatric oncology. Ann Oncol 28:1152-1157, 2017
    1. Liuu E, Canouï-Poitrine F, Tournigand C, et al. : Accuracy of the G-8 geriatric-oncology screening tool for identifying vulnerable elderly patients with cancer according to tumour site: The ELCAPA-02 study. J Geriatr Oncol 5:11-19, 2014
    1. Pamoukdjian F, Canoui-Poitrine F, Longelin-Lombard C, et al. : Diagnostic performance of gait speed, G8 and G8 modified indices to screen for vulnerability in older cancer patients: The prospective PF-EC cohort study. Oncotarget 8:50393-50402, 2017
    1. Velghe A, Petrovic M, De Buyser S, et al. : Validation of the G8 screening tool in older patients with aggressive haematological malignancies. Eur J Oncol Nurs 18:645-648, 2014
    1. O’Caoimh R, Sezgin D, O’Donovan MR, et al. : Prevalence of frailty in 62 countries across the world: A systematic review and meta-analysis of population-level studies. Age Ageing 50:96-104, 2021
    1. Wilson JMG, Jungner G: Principles and practice of screening for disease. Public Health Papers 34, 1968.
    1. Loh KP, Soto-Perez-de-Celis E, Hsu T, et al. : What every oncologist should know about geriatric assessment for older patients with cancer: Young International Society of Geriatric Oncology position paper. JCO Oncol Pract 14:85-94, 2018
    1. Ferrat E, Paillaud E, Caillet P, et al. : Performance of four frailty classifications in older patients with cancer: Prospective elderly cancer patients cohort study. J Clin Oncol 35:766-777, 2017
    1. Hurria A, Togawa K, Mohile SG, et al. : Predicting chemotherapy toxicity in older adults with cancer: A prospective multicenter study. J Clin Oncol 29:3457-3465, 2011
    1. Hurria A, Mohile S, Gajra A, et al. : Validation of a prediction tool for chemotherapy toxicity in older adults with cancer. J Clin Oncol 34:2366-2371, 2016
    1. Kerr KF, Brown MD, Zhu K, Janes H: Assessing the clinical impact of risk prediction models with decision curves: Guidance for correct interpretation and appropriate use. J Clin Oncol 34:2534-2540, 2016
    1. Vickers AJ: Prediction models: Revolutionary in principle, but do they do more good than harm? J Clin Oncol 29:2951-2952, 2011
    1. Canouï-Poitrine F, Martinez-Tapia C, Paillaud E, et al. : Geriatric impairments were directly and indirectly associated with mortality in older patients with cancer: A structural equation analysis. J Clin Epidemiol 148:17-26, 2022

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