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March 14, 2023; 100 (11) Research Article

Advanced Brain Age and Chronic Poststroke Aphasia Severity

View ORCID ProfileNatalie Busby, Janina Wilmskoetter, Ezequiel Gleichgerrcht, Chris Rorden, Rebecca Roth, Roger Newman-Norlund, Argye Elizabeth Hillis, Simon S. Keller, Christophe de Bezenac, Sigfus Kristinsson, Julius Fridriksson, Leonardo Bonilha
First published December 16, 2022, DOI: https://doi.org/10.1212/WNL.0000000000201693
Natalie Busby
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Janina Wilmskoetter
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Ezequiel Gleichgerrcht
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Chris Rorden
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Rebecca Roth
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Roger Newman-Norlund
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Argye Elizabeth Hillis
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Simon S. Keller
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Christophe de Bezenac
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Sigfus Kristinsson
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Julius Fridriksson
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Leonardo Bonilha
From the Departments of Communication Sciences and Disorders (N.B., J.F.), and Psychology (C.R., R.N.N.), University of South Carolina, Columbia; Department of Health and Rehabilitation Sciences (J.W., E.G., S.K., J.F.), Medical University of South Carolina, Charleston; Department of Neurology (R.R., L.B.), Emory University, Atlanta, GA; Department of Neurology (A.E.H.), Johns Hopkins University School of Medicine, Baltimore, MD; Department of Pharmacology and Therapeutics (S.S.K., C.d.B.), Institute of Systems, Molecular and Integrative Biology, University of Liverpool, United Kingdom; The Walton Centre NHS Foundation Trust (S.S.K., C.d.B.), Liverpool, United Kingdom.
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Advanced Brain Age and Chronic Poststroke Aphasia Severity
Natalie Busby, Janina Wilmskoetter, Ezequiel Gleichgerrcht, Chris Rorden, Rebecca Roth, Roger Newman-Norlund, Argye Elizabeth Hillis, Simon S. Keller, Christophe de Bezenac, Sigfus Kristinsson, Julius Fridriksson, Leonardo Bonilha
Neurology Mar 2023, 100 (11) e1166-e1176; DOI: 10.1212/WNL.0000000000201693

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Abstract

Background and Objectives Chronic poststroke language impairment is typically worse in older individuals or those with large stroke lesions. However, there is unexplained variance that likely depends on intact tissue beyond the lesion. Brain age is an emerging concept, which is partially independent from chronologic age. Advanced brain age is associated with cognitive decline in healthy older adults; therefore, we aimed to investigate the relationship with stroke aphasia. We hypothesized that advanced brain age is a significant factor associated with chronic poststroke language impairments, above and beyond chronologic age, and lesion characteristics.

Methods This cohort study retrospectively evaluated participants from the Predicting Outcomes of Language Rehabilitation in Aphasia clinical trial (NCT03416738), recruited through local advertisement in South Carolina (US). Primary inclusion criteria were left hemisphere stroke and chronic aphasia (≥12 months after stroke). Participants completed baseline behavioral testing including the Western Aphasia Battery–Revised (WAB-R), Philadelphia Naming Test (PNT), Pyramids and Palm Trees Test (PPTT), and Wechsler Adult Intelligence Scale Matrices subtest, before completing 6 weeks of language therapy. The PNT was repeated 1 month after therapy. We leveraged modern neuroimaging techniques to estimate brain age and computed a proportional difference between chronologic age and estimated brain age. Multiple linear regression models were used to evaluate the relationship between proportional brain age difference (PBAD) and behavior.

Results Participants (N = 93, 58 males and 35 females, average age = 61 years) had estimated brain ages ranging from 14 years younger to 23 years older than chronologic age. Advanced brain age predicted performance on semantic tasks (PPTT) and language tasks (WAB-R). For participants with advanced brain aging (n = 47), treatment gains (improvement on the PNT) were independently predicted by PBAD (T = −2.0474, p = 0.0468, 9% of variance explained).

Discussion Through the application of modern neuroimaging techniques, advanced brain aging was associated with aphasia severity and performance on semantic tasks. Notably, therapy outcome scores were also associated with PBAD, albeit only among participants with advanced brain aging. These findings corroborate the importance of brain age as a determinant of poststroke recovery and underscore the importance of personalized health factors in determining recovery trajectories, which should be considered during the planning or implementation of therapeutic interventions.

Glossary

TE=
echo time;
TI=
inversion time;
PBAD=
proportional brain age difference;
PNT=
Philadelphia Naming Test;
PPTT=
Pyramids and Palm Trees Test;
POLAR=
Predicting Outcomes of Language Rehabilitation in Aphasia;
TR=
repetition time;
WAB-AQ=
Western Aphasia Battery–Aphasia Quotient;
WAB-R=
Western Aphasia Battery–Revised;
WAIS=
Wechsler Adult Intelligence Scale

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 Editor-in-Chief José Merino, MD, MPhil, FAAN.

  • Received May 16, 2022.
  • Accepted in final form October 31, 2022.
  • © 2022 American Academy of Neurology
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