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November 01, 2022; 99 (18) Research Article

Enhanced Imaging and Language Assessments for Primary Progressive Aphasia

Kristina Ruch, Melissa Dawn Stockbridge, Alexandra Walker, Emilia Vitti, View ORCID ProfileJennifer Shea, Shannon Sheppard, Alex Pacl, Hana Kim, View ORCID ProfileAndreia Vasconcellos Faria, Argye Elizabeth Hillis
First published August 17, 2022, DOI: https://doi.org/10.1212/WNL.0000000000201040
Kristina Ruch
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Melissa Dawn Stockbridge
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Alexandra Walker
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Emilia Vitti
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Jennifer Shea
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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  • ORCID record for Jennifer Shea
Shannon Sheppard
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Alex Pacl
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Hana Kim
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Andreia Vasconcellos Faria
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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  • ORCID record for Andreia Vasconcellos Faria
Argye Elizabeth Hillis
From the Department of Neurology (K.R., M.D.S., A.W., E.V., A.P., H.K., A.E.H.), Johns Hopkins School of Medicine, Baltimore, MD; Department of Cognitive Science (J.S., A.E.H.), Johns Hopkins University, Baltimore, MD; Department of Communication Disorders (S.S.), Chapman University, Orange, CA; Department of Radiology (A.V.F.), Johns Hopkins School of Medicine; and Department of Physical Medicine and Rehabilitation (A.E.H.), Johns Hopkins University School of Medicine.
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Enhanced Imaging and Language Assessments for Primary Progressive Aphasia
Kristina Ruch, Melissa Dawn Stockbridge, Alexandra Walker, Emilia Vitti, Jennifer Shea, Shannon Sheppard, Alex Pacl, Hana Kim, Andreia Vasconcellos Faria, Argye Elizabeth Hillis
Neurology Nov 2022, 99 (18) e2044-e2051; DOI: 10.1212/WNL.0000000000201040

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Abstract

Background and Objectives It is widely agreed that primary progressive aphasia (PPA) is a clinical syndrome with at least 3 distinct variants that differ in phenotype, areas of atrophy, and most common underlying neurodegenerative disease. The distinction between logopenic variant PPA (lvPPA) and other variants is important for prognosis and medical management. However, differentiating logopenic from nonfluent agrammatic variant can be difficult. We aimed to identify a novel behavioral assessment that (1) distinguishes logopenic from the other variants with a high degree of accuracy and (2) correlates with left superior temporal-inferior parietal atrophy (previously shown to be associated with this variant). The location of atrophy was measured using a novel, clinically useful imaging analysis.

Methods In this observational cohort study of 227 individuals with PPA, participants were administered sentence reading and repetition subtests from a standard battery. A subset of 41 participants were administered enhanced reading and repetition subtests with 5 longer sentences, of which 13 had brain imaging. Ratios of word-level and sentence-level accuracy in reading:repetition were calculated. We used one-way analysis of variance (ANOVA) to determine whether either or both ratios of reading:repetition independently discriminated between variants and t test to determine whether the ratios distinguished between nonfluent and logopenic variants. We identified receiver operating characteristics and Pearson correlations between the reading:repetition ratios and ratio of left:right superior temporal-inferior parietal volume.

Results The sentence reading:repetition ratio using the new stimuli significantly differed across the 3 variants (p < 0.00001) and differed between nonfluent and logopenic variants (t(27) = 4.1; p = 0.0003). The area under the curve for distinguishing logopenic from other variants was 0.85 (0.71–0.99), and the diagnostic accuracy was 87.5%. The sentence reading:repetition ratio correlated with left:right superior temporal-inferior parietal volume (r = 0.69; p = 0.0087), but not with left:right volume of regions of interest associated with other variants.

Discussion Results provide an efficient and reliable clinical assessment, and a novel imaging analysis, to distinguish the clinical syndrome of logopenic variant from other variants of PPA. Results also support the proposal that lvPPA reflects a defect in phonological short-term memory caused by atrophy in the superior temporal-inferior parietal cortex.

Classification of Evidence This study provides Class III evidence that the sentence reading:repetition ratio distinguished logopenic PPA from other PPA variants.

Glossary

AG=
angular gyrus;
ANOVA=
analysis of variance;
AUC=
area under the curve;
FTLD-MOD=
Frontotemporal Lobar Degeneration Module;
IFG=
inferior frontal gyrus;
ITG=
inferior temporal gyrus;
INS=
insular gyrus;
lvPPA=
logopenic variant PPA;
NACC=
National Alzheimer's Coordinating Centers;
nfaPPA=
nonfluent agrammatic variant PPA;
PPA=
primary progressive aphasia;
ROC=
receiver operating characteristics;
ROI=
region of interest;
SMG=
superior marginal gyrus;
STG=
superior temporal gyrus;
svPPA=
semantic variant PPA;
TP=
temporal pole

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.

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

  • Class of Evidence: NPub.org/coe

  • Received January 14, 2022.
  • Accepted in final form June 15, 2022.
  • © 2022 American Academy of Neurology
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