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November 15, 2023 article Open access Aachen paper

Structural connectome-based predictive modeling of cognitive deficits in treated glioma patients

Neuro-Oncology Advances, vol. 6, pp. vdad151

DOI: 10.1093/noajnl/vdad151 Full text (OA) OpenAlex

Abstract

Abstract Background In glioma patients, tumor growth and subsequent treatments are associated with various types of brain lesions. We hypothesized that cognitive functioning in these patients critically depends on the maintained structural connectivity of multiple brain networks. Methods The study included 121 glioma patients (median age, 52 years; median Eastern Cooperative Oncology Group performance score 1; CNS-WHO Grade 3 or 4) after multimodal therapy. Cognitive performance was assessed by 10 tests in 5 cognitive domains at a median of 14 months after treatment initiation. Hybrid amino acid PET/MRI using the tracer O-(2-[18F]fluoroethyl)-L-tyrosine, a network-based cortical parcellation, and advanced tractography were used to generate whole-brain fiber count-weighted connectivity matrices. The matrices were applied to a cross-validated machine-learning model to identify predictive fiber connections (edges), critical cortical regions (nodes), and the networks underlying cognitive performance. Results Compared to healthy controls (n = 121), patients’ cognitive scores were significantly lower in 9 cognitive tests. The models predicted the scores of 7/10 tests (median correlation coefficient, 0.47; range, 0.39–0.57) from 0.6% to 5.4% of the matrix entries; 84% of the predictive edges were between nodes of different networks. Critically involved cortical regions (≥10 adjacent edges) included predominantly left-sided nodes of the visual, somatomotor, dorsal/ventral attention, and default mode networks. Highly critical nodes (≥15 edges) included the default mode network’s left temporal and bilateral posterior cingulate cortex. Conclusions These results suggest that the cognitive performance of pretreated glioma patients is strongly related to structural connectivity between multiple brain networks and depends on the integrity of known network hubs also involved in other neurological disorders.

Authors 13

  1. Michel Friedrich

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  2. Christian Filß

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  3. Philipp Lohmann

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  4. Felix Manuel Mottaghy Aachen Department of Nuclear Medicine

    Universitätsklinikum Aachen · RWTH Aachen University

    Affiliation as printed

    Department of Nuclear Medicine, RWTH University Hospital Aachen, RWTH University Aachen , Aachen , Germany

    Department of Nuclear Medicine, RWTH University Hospital Aachen, RWTH University Aachen , Aachen, Germany

  5. Gabriele Stoffels

    Forschungszentrum Jülich

    Affiliation as printed

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  6. Carolin Weiß Lucas

    University of Cologne · University Hospital Cologne

    Affiliation as printed

    Center of Integrated Oncology (CIO), Universities of Aachen , Bonn, Cologne, and Duesseldorf , Germany

    Department of General Neurosurgery, Center for Neurosurgery, Faculty of Medicine and University Hospital Cologne, University of Cologne , Cologne , Germany

    Center of Integrated Oncology (CIO), Universities of Aachen, Bonn , Cologne, and Duesseldorf, Germany

    Department of General Neurosurgery, Center for Neurosurgery, Faculty of Medicine and University Hospital Cologne , University of Cologne, Cologne, Germany

  7. Maximilian Ingolf Ruge

    University of Cologne · University Hospital Cologne

    Affiliation as printed

    Center of Integrated Oncology (CIO), Universities of Aachen , Bonn, Cologne, and Duesseldorf , Germany

    Department of Stereotaxy and Functional Neurosurgery, Center for Neurosurgery, Faculty of Medicine and University Hospital Cologne , Cologne , Germany

    Center of Integrated Oncology (CIO), Universities of Aachen, Bonn , Cologne, and Duesseldorf, Germany

    Department of Stereotaxy and Functional Neurosurgery, Center for Neurosurgery, Faculty of Medicine and University Hospital Cologne , Cologne, Germany

  8. Nadim Jon Shah Aachen Department of Neurology

    Forschungszentrum Jülich · Universitätsklinikum Aachen · Jülich Aachen Research Alliance · RWTH Aachen University

    Affiliation as printed

    Department of Neurology, RWTH University Hospital Aachen, RWTH University Aachen , Aachen , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Juelich-Aachen Research Alliance (JARA), Section JARA-Brain , Juelich , Germany

    Department of Neurology, RWTH University Hospital Aachen, RWTH University Aachen , Aachen, Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

    Juelich-Aachen Research Alliance (JARA), Section JARA-Brain , Juelich, Germany (NJS)

  9. Svenja Caspers

    Forschungszentrum Jülich · Düsseldorf University Hospital · Heinrich Heine University Düsseldorf

    Affiliation as printed

    Institute for Anatomy I, Medical Faculty and University Hospital Duesseldorf, Heinrich Heine University Duesseldorf , Duesseldorf , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Institute for Anatomy I, Medical Faculty and University Hospital Duesseldorf, Heinrich Heine University Duesseldorf , Duesseldorf, Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  10. Karl‐Josef Langen Aachen Department of Nuclear Medicine

    Forschungszentrum Jülich · Universitätsklinikum Aachen · RWTH Aachen University

    Affiliation as printed

    Center of Integrated Oncology (CIO), Universities of Aachen , Bonn, Cologne, and Duesseldorf , Germany

    Department of Nuclear Medicine, RWTH University Hospital Aachen, RWTH University Aachen , Aachen , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Center of Integrated Oncology (CIO), Universities of Aachen, Bonn , Cologne, and Duesseldorf, Germany

    Department of Nuclear Medicine, RWTH University Hospital Aachen, RWTH University Aachen , Aachen, Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  11. Gereon R. Fink

    Forschungszentrum Jülich · University of Cologne · University Hospital Cologne

    Affiliation as printed

    Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne , Cologne , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne , Cologne, Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  12. Norbert Galldiks

    Forschungszentrum Jülich · University of Cologne · University Hospital Cologne

    Affiliation as printed

    Center of Integrated Oncology (CIO), Universities of Aachen , Bonn, Cologne, and Duesseldorf , Germany

    Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne , Cologne , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Center of Integrated Oncology (CIO), Universities of Aachen, Bonn , Cologne, and Duesseldorf, Germany

    Department of Neurology, Faculty of Medicine and University Hospital Cologne, University of Cologne , Cologne, Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

  13. Martin Köcher corresponding

    Forschungszentrum Jülich · University of Cologne · University Hospital Cologne

    Affiliation as printed

    Center of Integrated Oncology (CIO), Universities of Aachen , Bonn, Cologne, and Duesseldorf , Germany

    Department of Stereotaxy and Functional Neurosurgery, Center for Neurosurgery, Faculty of Medicine and University Hospital Cologne , Cologne , Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4, INM-11), Forschungszentrum Juelich , Juelich , Germany

    Center of Integrated Oncology (CIO), Universities of Aachen, Bonn , Cologne, and Duesseldorf, Germany

    Department of Stereotaxy and Functional Neurosurgery, Center for Neurosurgery, Faculty of Medicine and University Hospital Cologne , Cologne, Germany

    Institute of Neuroscience and Medicine (INM-1, INM-3, INM-4 , INM-11), Forschungszentrum Juelich, Juelich, Germany

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References 51