Predicting disease progression in high-grade glioma with neuropsychological parameters: the value of personalized longitudinal assessment

Elke Butterbrod, Jimme Bruijn, Meriam M Braaksma, Geert-Jan M Rutten, Cees C Tijssen, Monique C J Hanse, Margriet M Sitskoorn, Karin Gehring, Elke Butterbrod, Jimme Bruijn, Meriam M Braaksma, Geert-Jan M Rutten, Cees C Tijssen, Monique C J Hanse, Margriet M Sitskoorn, Karin Gehring

Abstract

Purpose: Progressive disease in patients with high-grade glioma may be reflected in cognitive decline. However, the cognitive functions most sensitive to progression may differ between patients. We investigated whether decline on a personalized selection of tests predicted progressive disease according to RANO criteria in high-grade glioma patients.

Methods: Starting one day before surgery, patients underwent neuropsychological assessment every three months during standard treatment and clinical follow-up. We first made a personalized selection of three tests that showed the highest Reliable Change Index (RCI) values, i.e., most positive change, at the first post-surgical assessment for each patient. In subsequent follow up, a decline of RCI ≤ - 1 on at least two of the three tests in the selection was considered cognitive decline. We performed a discrete Cox proportional hazards model including a time-dependent coefficient cognitive decline (vs. stability) and covariate age to predict progressive disease.

Results: Twenty five patients were included. Cognitive decline on the personalized test selection preceded or had occurred by the time progression was established in 9/15 patients with RANO confirmed progressive disease (60%). Decline was absent in 8/10 patients (80%) with stable disease during participation. The independent hazard ratio for progression in case of cognitive decline was 5.05 (p < 0.01) compared to stable performance.

Conclusions: Using only three patient-specific neuropsychological tests, we found a fivefold increased chance of disease progression in case of cognitive decline as compared to stable performance. Brief, patient-tailored cognitive assessment may be a noninvasive addition to disease monitoring without overburdening patients and clinical care.

Trial registration: ClinicalTrials.gov NCT02953756.

Keywords: Cognitive functioning; Disease progression; High-grade glioma; Neuropsychological assessment; RANO.

Conflict of interest statement

The authors declare that they have no conflict of interest.

Figures

Fig. 1
Fig. 1
Follow-up duration per patient and time of CD (filled circle) and PD. Lines stop at time of RANO PD (bold line) or end of participation (dotted line; censoring). Timing of CD differed between patients (one patient two intervals before PD, two patients one interval before PD, five patients at time of PD)

References

    1. Johnson DR, Wefel JS. Relationship between cognitive function and prognosis in glioblastoma. CNS Oncol. 2013;2:195–201. doi: 10.2217/cns.13.5.
    1. Lamborn KR, Chang SM, Prados MD. Prognostic factors for survival of patients with glioblastoma: recursive partitioning analysis. Neuro Oncol. 2004;6:227–235. doi: 10.1215/S1152851703000620.
    1. Weller M, Felsberg J, Hartmann C, Berger H, Steinbach JP, Schramm J, et al. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J Clin Oncol. 2009;27:5743–5750. doi: 10.1200/JCO.2009.23.0805.
    1. Gately L, Collins A, Murphy M, Dowling A. Age alone is not a predictor for survival in glioblastoma. J Neuro-Oncol. 2016;129:479–485. doi: 10.1007/s11060-016-2194-x.
    1. Armstrong CL, Goldstein B, Shera D, Ledakis GE, Tallent EM. The predictive value of longitudinal neuropsychological assessment in the early detection of brain tumor recurrence. Cancer. 2003;97:649–656. doi: 10.1002/cncr.11099.
    1. Klein M, Postma T, Taphoorn M, Aaronson N, Vandertop W, Muller M, et al. The prognostic value of cognitive functioning in the survival of patients with high-grade glioma. Neurology. 2003;61:1796–1798. doi: 10.1212/01.WNL.0000098892.33018.4C.
    1. Lee S-T, Park C-K, Kim JW, Park M-J, Lee H, Lim J-A, et al. Early cognitive function tests predict early progression in glioblastoma. Neurooncol Pract. 2015;2:137–143.
    1. Meyers CA, Hess KR. Multifaceted end points in brain tumor clinical trials: Cognitive deterioration precedes MRI progression. Neuro-oncology. 2003;5:89–95. doi: 10.1093/neuonc/5.2.89.
    1. Meyers CA, Hess KR, Yung WA, Levin VA. Cognitive function as a predictor of survival in patients with recurrent malignant glioma. J Clin Oncol. 2000;18:646–650. doi: 10.1200/JCO.2000.18.3.646.
    1. Uhlhaas PJ, Singer W. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron. 2006;52:155–168. doi: 10.1016/j.neuron.2006.09.020.
    1. Habets EJ, Kloet A, Walchenbach R, Vecht CJ, Klein M, Taphoorn MJ. Tumour and surgery effects on cognitive functioning in high-grade glioma patients. Acta Neurochir. 2014;156:1451–1459. doi: 10.1007/s00701-014-2115-8.
    1. Johnson DR, Sawyer AM, Meyers CA, O’neill BP, Wefel JS. Early measures of cognitive function predict survival in patients with newly diagnosed glioblastoma. Neuro-oncology. 2012;14:808–816. doi: 10.1093/neuonc/nos082.
    1. Brown PD, Jensen AW, Felten SJ, Ballman KV, Schaefer PL, Jaeckle KA, et al. Detrimental effects of tumor progression on cognitive function of patients with high-grade glioma. J Clin Oncol. 2006;24:5427–5433. doi: 10.1200/JCO.2006.08.5605.
    1. Bosma I, Vos MJ, Heimans JJ, Taphoorn MJ, Aaronson NK, Postma TJ, et al. The course of neurocognitive functioning in high-grade glioma patients. Neuro-oncology. 2007;9:53–62. doi: 10.1215/15228517-2006-012.
    1. Anderson SW, Damasio H, Tranel D. Neuropsychological impairments associated with lesions caused by tumor or stroke. Archives Neurol-Chicago. 1990;47:397–405. doi: 10.1001/archneur.1990.00530040039017.
    1. Carrera E, Tononi G. Diaschisis: past, present, future. Brain. 2014;137:2408–2422. doi: 10.1093/brain/awu101.
    1. Heimans JJ, Reijneveld JC. Factors affecting the cerebral network in brain tumor patients. J Neuro-Oncol. 2012;108:231–237. doi: 10.1007/s11060-012-0814-7.
    1. Brainlab AG . Brainlab elements. Munich: BrainlabAG; 2018.
    1. Gualtieri CT, Johnson LG. Reliability and validity of a computerized neurocognitive test battery, CNS Vital Signs. Arch Clin Neuropsych. 2006;21:623–643. doi: 10.1016/j.acn.2006.05.007.
    1. Wechsler D. WAIS-III administration and scoring manual. San Antonio: The Psychological Corporation; 1997.
    1. Schmand B, Groenink S, van den Dungen M. Letter fluency: psychometric properties and Dutch normative data. Tijdschr Gerontol Geriat. 2008;39:64. doi: 10.1007/BF03078128.
    1. Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E, et al. Updated response assessment criteria for high-grade gliomas: Response assessment in neuro-oncology working group. J Clin Oncol. 2010;28:1963–1972. doi: 10.1200/JCO.2009.26.3541.
    1. Maassen GH, Bossema E, Brand N. Reliable change and practice effects: outcomes of various indices compared. J Clin Exp Neuropsych. 2009;31:339–352. doi: 10.1080/13803390802169059.
    1. Rijnen SJM, van der Linden SD, Emons WHM, Sitskoorn MM, Gehring K. Test-retest reliability and practice effects of a computerized neuropsychological battery: a solution-oriented approach. Psychol Assess. 2018;30:1652–1662. doi: 10.1037/pas0000618.
    1. Rijnen SJ, Meskal I, Emons WH, Campman CA, van der Linden SD, Gehring K, et al. Evaluation of normative data of a widely used computerized neuropsychological battery: applicability and effects of sociodemographic variables in a Dutch sample. Assessment. 2017 doi: 10.1177/1073191117727346.
    1. Stupp R, Hegi ME, Mason WP, van den Bent MJ, Taphoorn MJ, Janzer RC, et al. Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial. Lancet Oncol. 2009;10:459–466. doi: 10.1016/S1470-2045(09)70025-7.
    1. Hilverda K, Bosma I, Heimans JJ, Postma TJ, Peter Vandertop W, Slotman BJ, et al. Cognitive functioning in glioblastoma patients during radiotherapy and temozolomide treatment: initial findings. J Neuro-Oncol. 2010;97:89–94. doi: 10.1007/s11060-009-9993-2.
    1. Torres IJ, Mundt AJ, Sweeney PJ, Llanes-Macy S, Dunaway L, Castillo M, et al. A longitudinal neuropsychological study of partial brain radiation in adults with brain tumors. Neurology. 2003;60:1113–1118. doi: 10.1212/01.WNL.0000055862.20003.4A.
    1. Ismail MF, Lavelle C, Cassidy EM. Steroid-induced mental disorders in cancer patients: a systematic review. Future oncol. 2017;13:2719–2731. doi: 10.2217/fon-2017-0306.
    1. Rock PL, Roiser JP, Riedel WJ, Blackwell AD. Cognitive impairment in depression: a systematic review and meta-analysis. Psychol Med. 2013;44:2029–2040. doi: 10.1017/S0033291713002535.
    1. Verhage F (1983) Educational classification system for research purposes: revised version]. Academic Hospital Groningen, State University Groningen, Internal publication Groningen, the Netherlands

Source: PubMed

Sponsorer och medarbetare

Medicinska tillstånd

Läkemedelsinterventioner

3
Prenumerera