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January 17, 2023; 100 (3) Research Article

Association of Regional Cortical Network Atrophy With Progression to Dementia in Patients With Primary Progressive Aphasia

View ORCID ProfileYuta Katsumi, Megan Quimby, Daisy Hochberg, Amelia Jones, Michael Brickhouse, Mark C. Eldaief, View ORCID ProfileBradford C. Dickerson, View ORCID ProfileAlexandra Touroutoglou
First published October 3, 2022, DOI: https://doi.org/10.1212/WNL.0000000000201403
Yuta Katsumi
*These authors contributed equally as co-first authors.
PhD
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Megan Quimby
MS, CCC-SLP
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Daisy Hochberg
MS, CCC-SLP
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Amelia Jones
MS
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Michael Brickhouse
BS
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Mark C. Eldaief
MD
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Bradford C. Dickerson
MD
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Alexandra Touroutoglou
PhD
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Association of Regional Cortical Network Atrophy With Progression to Dementia in Patients With Primary Progressive Aphasia
Yuta Katsumi, Megan Quimby, Daisy Hochberg, Amelia Jones, Michael Brickhouse, Mark C. Eldaief, Bradford C. Dickerson, Alexandra Touroutoglou
Neurology Jan 2023, 100 (3) e286-e296; DOI: 10.1212/WNL.0000000000201403

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Abstract

Background and Objectives Patients with primary progressive aphasia (PPA) have gradually progressive language deficits during the initial phase of the illness. As the underlying neurodegenerative disease progresses, patients with PPA start losing independent functioning due to the development of nonlanguage cognitive or behavioral symptoms. The timeline of this progression from the mild cognitive impairment stage to the dementia stage of PPA is variable across patients. In this study, in a sample of patients with PPA, we measured the magnitude of cortical atrophy within functional networks believed to subserve diverse cognitive and affective functions. The objective of the study was to evaluate the utility of this measure as a predictor of time to subsequent progression to dementia in PPA.

Methods Patients with PPA with largely independent daily function were recruited through the Massachusetts General Hospital Frontotemporal Disorders Unit. All patients underwent an MRI scan at baseline. Cortical atrophy was then estimated relative to a group of amyloid-negative cognitively normal control participants. For each patient, we measured the time between the baseline visit and the subsequent visit at which dementia progression was documented or last observation. Simple and multivariable Cox regression models were used to examine the relationship between cortical atrophy and the likelihood of progression to dementia.

Results Forty-nine patients with PPA (mean age = 66.39 ± 8.36 years, 59.2% females) and 25 controls (mean age = 67.43 ± 4.84 years, 48% females) were included in the data analysis. Greater baseline atrophy in not only the left language network (hazard ratio = 1.47, 95% CI = 1.17–1.84) but also in the frontoparietal control (1.75, 1.25–2.44), salience (1.63, 1.25–2.13), default mode (1.55, 1.19–2.01), and ventral frontotemporal (1.41, 1.16–1.71) networks was associated with a higher risk of progression to dementia. A multivariable model identified contributions of the left frontoparietal control (1.94, 1.09–3.48) and ventral frontotemporal (1.61, 1.09–2.39) networks in predicting dementia progression, with no additional variance explained by the language network (0.75, 0.43–1.31).

Discussion These results suggest that baseline atrophy in cortical networks subserving nonlanguage cognitive and affective functions is an important predictor of progression to dementia in PPA. This measure should be included in precision medicine models of prognosis in PPA.

Glossary

11C-PiB=
11C-Pittsburgh compound B;
DVR=
distribution volume ratio;
FLR=
frontal, lateral, and retrosplenial;
MCI=
mild cognitive impairment;
MGH=
Massachusetts General Hospital;
MMSE=
Mini-Mental State Examination;
PPA=
primary progressive aphasia

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Y. Katsumi, M. Quimby, and D. Hochberg contributed equally as cofirst authors. A. Touroutoglou and B.C. Dickerson contributed equally as cosenior authors.

  • Submitted and externally peer reviewed. The handling editor was Linda Hershey, MD, PhD, FAAN.

  • Editorial, page 111

  • Received June 3, 2022.
  • Accepted in final form August 30, 2022.
  • © 2022 American Academy of Neurology
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