Journal of the American Heart Association: Cardiovascular and Cerebrovascular Disease (May 2022)
Chronic Stroke Sensorimotor Impairment Is Related to Smaller Hippocampal Volumes: An ENIGMA Analysis
- Artemis Zavaliangos‐Petropulu,
- Bethany Lo,
- Miranda R. Donnelly,
- Nicolas Schweighofer,
- Keith Lohse,
- Neda Jahanshad,
- Giuseppe Barisano,
- Nerisa Banaj,
- Michael R. Borich,
- Lara A. Boyd,
- Cathrin M. Buetefisch,
- Winston D. Byblow,
- Jessica M. Cassidy,
- Charalambos C. Charalambous,
- Adriana B. Conforto,
- Julie A. DiCarlo,
- Adrienne N. Dula,
- Natalia Egorova‐Brumley,
- Mark R. Etherton,
- Wuwei Feng,
- Kelene A. Fercho,
- Fatemeh Geranmayeh,
- Colleen A. Hanlon,
- Kathryn S. Hayward,
- Brenton Hordacre,
- Steven A. Kautz,
- Mohamed Salah Khlif,
- Hosung Kim,
- Amy Kuceyeski,
- David J. Lin,
- Jingchun Liu,
- Martin Lotze,
- Bradley J. MacIntosh,
- John L. Margetis,
- Feroze B. Mohamed,
- Fabrizio Piras,
- Ander Ramos‐Murguialday,
- Kate P. Revill,
- Pamela S. Roberts,
- Andrew D. Robertson,
- Heidi M. Schambra,
- Na Jin Seo,
- Mark S. Shiroishi,
- Cathy M. Stinear,
- Surjo R. Soekadar,
- Gianfranco Spalletta,
- Myriam Taga,
- Wai Kwong Tang,
- Gregory T. Thielman,
- Daniela Vecchio,
- Nick S. Ward,
- Lars T. Westlye,
- Emilio Werden,
- Carolee Winstein,
- George F. Wittenberg,
- Steven L. Wolf,
- Kristin A. Wong,
- Chunshui Yu,
- Amy Brodtmann,
- Steven C. Cramer,
- Paul M. Thompson,
- Sook‐Lei Liew
Affiliations
- Artemis Zavaliangos‐Petropulu
- Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA
- Bethany Lo
- Chan Division of Occupational Science and Occupational Therapy University of Southern California Los Angeles CA
- Miranda R. Donnelly
- Chan Division of Occupational Science and Occupational Therapy University of Southern California Los Angeles CA
- Nicolas Schweighofer
- Biokinesiology and Physical Therapy University of Southern California Los Angeles CA
- Keith Lohse
- Physical Therapy and Neurology Washington University School of Medicine in Saint Louis MO
- Neda Jahanshad
- Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA
- Giuseppe Barisano
- Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA
- Nerisa Banaj
- Laboratory of Neuropsychiatry IRCCS Santa Lucia Foundation Rome Italy
- Michael R. Borich
- Division of Physical Therapy Department of Rehabilitation Medicine Emory University School of Medicine Atlanta GA
- Lara A. Boyd
- Department of Physical Therapy University of British Columbia Vancouver Canada
- Cathrin M. Buetefisch
- Department of Neurology School of Medicine Emory University Atlanta GA
- Winston D. Byblow
- Department of Exercise Sciences, and Centre for Brain Research University of Auckland New Zealand
- Jessica M. Cassidy
- Department of Allied Health Sciences University of North Carolina at Chapel Hill NC
- Charalambos C. Charalambous
- Department of Basic and Clinical Sciences University of Nicosia Medical School Nicosia Cyprus
- Adriana B. Conforto
- Hospital das Clínicas São Paulo University São Paulo Brazil
- Julie A. DiCarlo
- Center for Neurotechnology and Neurorecovery (CNTR) Massachusetts General Hospital Boston MA
- Adrienne N. Dula
- Department of Neurology Dell Medical School University of Texas at Austin TX
- Natalia Egorova‐Brumley
- Melbourne School of Psychological Sciences University of Melbourne Parkville Victoria Australia
- Mark R. Etherton
- Department of Neurology J. Philip Kistler Stroke Research Center Massachusetts General Hospital Boston MA
- Wuwei Feng
- Department of Neurology Duke University School of Medicine Durham NC
- Kelene A. Fercho
- Basic Biomedical Sciences University of South Dakota Vermillion SD
- Fatemeh Geranmayeh
- Brain Sciences Imperial College London London United Kingdom
- Colleen A. Hanlon
- Wake Forest School of Medicine Winston Salem NC
- Kathryn S. Hayward
- Departments of Physiotherapy and Medicine, University of Melbourne Heidelberg Victoria Australia
- Brenton Hordacre
- Innovation, Implementation and Clinical Translation (IIMPACT) in Health Allied Health and Human Performance University of South Australia Adelaide South Australia Australia
- Steven A. Kautz
- Ralph H Johnson Veterans Affairs Medical Center Charleston SC
- Mohamed Salah Khlif
- The Florey Institute of Neuroscience and Mental Health Heidelberg Victoria Australia
- Hosung Kim
- Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA
- Amy Kuceyeski
- Department of Radiology Weill Cornell Medicine New York NY
- David J. Lin
- Center for Neurotechnology and Neurorecovery (CNTR) Massachusetts General Hospital Boston MA
- Jingchun Liu
- Department of Radiology Tianjin Medical University General Hospital Tianjin China
- Martin Lotze
- Functional Imaging Institute for Diagnostic Radiology and Neuroradiology University Medicine Greifswald Germany
- Bradley J. MacIntosh
- Hurvitz Brain Sciences Program Sunnybrook Research Institute Toronto Canada
- John L. Margetis
- Chan Division of Occupational Science and Occupational Therapy University of Southern California Los Angeles CA
- Feroze B. Mohamed
- Department of Radiology Jefferson Integrated MR Center Thomas Jefferson University Philadelphia PA
- Fabrizio Piras
- Laboratory of Neuropsychiatry IRCCS Santa Lucia Foundation Rome Italy
- Ander Ramos‐Murguialday
- Institute of Medical Psychology and Behavioral Neurobiology University of Tübingen Germany
- Kate P. Revill
- Department of Psychology Emory University Atlanta GA
- Pamela S. Roberts
- Chan Division of Occupational Science and Occupational Therapy University of Southern California Los Angeles CA
- Andrew D. Robertson
- Department of Kinesiology and Health Sciences University of Waterloo Ontario Canada
- Heidi M. Schambra
- Departments of Neurology & Rehabilitation Medicine NYU Langone New York NY
- Na Jin Seo
- Ralph H Johnson Veterans Affairs Medical Center Charleston SC
- Mark S. Shiroishi
- Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA
- Cathy M. Stinear
- Department of Medicine University of Auckland New Zealand
- Surjo R. Soekadar
- Clinical Neurotechnology Laboratory Department of Psychiatry and Neurosciences (CCM) Charité ‐ Universitätsmedizin Berlin Berlin Germany
- Gianfranco Spalletta
- Laboratory of Neuropsychiatry IRCCS Santa Lucia Foundation Rome Italy
- Myriam Taga
- NYU Langone Department of Neurology New York NY
- Wai Kwong Tang
- Department of Psychiatry The Chinese University of Hong Kong China
- Gregory T. Thielman
- Department of Physical Therapy and Neuroscience University of the Sciences Philadelphia PA
- Daniela Vecchio
- Laboratory of Neuropsychiatry IRCCS Santa Lucia Foundation Rome Italy
- Nick S. Ward
- University College London Queen Square Institute of Neurology London United Kingdom
- Lars T. Westlye
- Department of Psychology University of Oslo Norway
- Emilio Werden
- The Florey Institute of Neuroscience and Mental Health Heidelberg Victoria Australia
- Carolee Winstein
- Biokinesiology and Physical Therapy University of Southern California Los Angeles CA
- George F. Wittenberg
- Department of Neurology University of Pittsburgh PA
- Steven L. Wolf
- Division of Physical Therapy Department of Rehabilitation Medicine Emory University School of Medicine Atlanta GA
- Kristin A. Wong
- Department of Physical Medicine & Rehabilitation Dell Medical School University of Texas at Austin TX
- Chunshui Yu
- Department of Radiology Tianjin Medical University General Hospital Tianjin China
- Amy Brodtmann
- The Florey Institute of Neuroscience and Mental Health Heidelberg Victoria Australia
- Steven C. Cramer
- Department of Neurology University of California Los Angeles David Geffen School of Medicine Los Angeles CA
- Paul M. Thompson
- Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA
- Sook‐Lei Liew
- Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA
- DOI
- https://doi.org/10.1161/JAHA.121.025109
- Journal volume & issue
-
Vol. 11,
no. 10
Abstract
Background Persistent sensorimotor impairments after stroke can negatively impact quality of life. The hippocampus is vulnerable to poststroke secondary degeneration and is involved in sensorimotor behavior but has not been widely studied within the context of poststroke upper‐limb sensorimotor impairment. We investigated associations between non‐lesioned hippocampal volume and upper limb sensorimotor impairment in people with chronic stroke, hypothesizing that smaller ipsilesional hippocampal volumes would be associated with greater sensorimotor impairment. Methods and Results Cross‐sectional T1‐weighted magnetic resonance images of the brain were pooled from 357 participants with chronic stroke from 18 research cohorts of the ENIGMA (Enhancing NeuoImaging Genetics through Meta‐Analysis) Stroke Recovery Working Group. Sensorimotor impairment was estimated from the FMA‐UE (Fugl‐Meyer Assessment of Upper Extremity). Robust mixed‐effects linear models were used to test associations between poststroke sensorimotor impairment and hippocampal volumes (ipsilesional and contralesional separately; Bonferroni‐corrected, P<0.025), controlling for age, sex, lesion volume, and lesioned hemisphere. In exploratory analyses, we tested for a sensorimotor impairment and sex interaction and relationships between lesion volume, sensorimotor damage, and hippocampal volume. Greater sensorimotor impairment was significantly associated with ipsilesional (P=0.005; β=0.16) but not contralesional (P=0.96; β=0.003) hippocampal volume, independent of lesion volume and other covariates (P=0.001; β=0.26). Women showed progressively worsening sensorimotor impairment with smaller ipsilesional (P=0.008; β=−0.26) and contralesional (P=0.006; β=−0.27) hippocampal volumes compared with men. Hippocampal volume was associated with lesion size (P<0.001; β=−0.21) and extent of sensorimotor damage (P=0.003; β=−0.15). Conclusions The present study identifies novel associations between chronic poststroke sensorimotor impairment and ipsilesional hippocampal volume that are not caused by lesion size and may be stronger in women.
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