Chronic Stroke Sensorimotor Impairment Is Related to Smaller Hippocampal Volumes: An ENIGMA Analysis

Author:

Zavaliangos‐Petropulu Artemis12ORCID,Lo Bethany3ORCID,Donnelly Miranda R.3,Schweighofer Nicolas4ORCID,Lohse Keith5,Jahanshad Neda1,Barisano Giuseppe12ORCID,Banaj Nerisa6ORCID,Borich Michael R.7ORCID,Boyd Lara A.8,Buetefisch Cathrin M.9,Byblow Winston D.10,Cassidy Jessica M.11ORCID,Charalambous Charalambos C.1213ORCID,Conforto Adriana B.1415,DiCarlo Julie A.16ORCID,Dula Adrienne N.17ORCID,Egorova‐Brumley Natalia18,Etherton Mark R.19ORCID,Feng Wuwei20ORCID,Fercho Kelene A.2122,Geranmayeh Fatemeh23ORCID,Hanlon Colleen A.24,Hayward Kathryn S.2526ORCID,Hordacre Brenton27,Kautz Steven A.2829,Khlif Mohamed Salah26,Kim Hosung1,Kuceyeski Amy30ORCID,Lin David J.16,Liu Jingchun31,Lotze Martin32,MacIntosh Bradley J.3334ORCID,Margetis John L.3,Mohamed Feroze B.35,Piras Fabrizio6ORCID,Ramos‐Murguialday Ander3637ORCID,Revill Kate P.38ORCID,Roberts Pamela S.339,Robertson Andrew D.40ORCID,Schambra Heidi M.41ORCID,Seo Na Jin2842ORCID,Shiroishi Mark S.143ORCID,Stinear Cathy M.44ORCID,Soekadar Surjo R.45,Spalletta Gianfranco6,Taga Myriam46,Tang Wai Kwong47ORCID,Thielman Gregory T.48,Vecchio Daniela6ORCID,Ward Nick S.49,Westlye Lars T.5051ORCID,Werden Emilio2652,Winstein Carolee4ORCID,Wittenberg George F.5354ORCID,Wolf Steven L.755ORCID,Wong Kristin A.56,Yu Chunshui31ORCID,Brodtmann Amy26ORCID,Cramer Steven C.5758,Thompson Paul M.1,Liew Sook‐Lei134ORCID

Affiliation:

1. Mark and Mary Stevens Neuroimaging and Informatics Institute Keck School of Medicine, University of Southern California Los Angeles CA

2. Neuroscience Graduate Program University of Southern California Los Angeles CA

3. Chan Division of Occupational Science and Occupational Therapy University of Southern California Los Angeles CA

4. Biokinesiology and Physical Therapy University of Southern California Los Angeles CA

5. Physical Therapy and Neurology Washington University School of Medicine in Saint Louis MO

6. Laboratory of Neuropsychiatry IRCCS Santa Lucia Foundation Rome Italy

7. Division of Physical Therapy Department of Rehabilitation Medicine Emory University School of Medicine Atlanta GA

8. Department of Physical Therapy University of British Columbia Vancouver Canada

9. Department of Neurology School of Medicine Emory University Atlanta GA

10. Department of Exercise Sciences, and Centre for Brain Research University of Auckland New Zealand

11. Department of Allied Health Sciences University of North Carolina at Chapel Hill NC

12. Department of Basic and Clinical Sciences University of Nicosia Medical School Nicosia Cyprus

13. Center for Neuroscience and Integrative Brain Research (CENIBRE) Nicosia Cyprus

14. Hospital das Clínicas São Paulo University São Paulo Brazil

15. Hospital Israelita Albert Einstein São Paulo Brazil

16. Center for Neurotechnology and Neurorecovery (CNTR) Massachusetts General Hospital Boston MA

17. Department of Neurology Dell Medical School University of Texas at Austin TX

18. Melbourne School of Psychological Sciences University of Melbourne Parkville Victoria Australia

19. Department of Neurology J. Philip Kistler Stroke Research Center Massachusetts General Hospital Boston MA

20. Department of Neurology Duke University School of Medicine Durham NC

21. Basic Biomedical Sciences University of South Dakota Vermillion SD

22. Federal Aviation Administration Civil Aerospace Medical Institute Oklahoma City OK

23. Brain Sciences Imperial College London London United Kingdom

24. Wake Forest School of Medicine Winston Salem NC

25. Departments of Physiotherapy and Medicine, University of Melbourne Heidelberg Victoria Australia

26. The Florey Institute of Neuroscience and Mental Health Heidelberg Victoria Australia

27. Innovation, Implementation and Clinical Translation (IIMPACT) in Health Allied Health and Human Performance University of South Australia Adelaide South Australia Australia

28. Ralph H Johnson Veterans Affairs Medical Center Charleston SC

29. Department of Health Sciences & Research Medical University of South Carolina Charleston SC

30. Department of Radiology Weill Cornell Medicine New York NY

31. Department of Radiology Tianjin Medical University General Hospital Tianjin China

32. Functional Imaging Institute for Diagnostic Radiology and Neuroradiology University Medicine Greifswald Germany

33. Hurvitz Brain Sciences Program Sunnybrook Research Institute Toronto Canada

34. Department of Medical Biophysics University of Toronto Ontario Canada

35. Department of Radiology Jefferson Integrated MR Center Thomas Jefferson University Philadelphia PA

36. Institute of Medical Psychology and Behavioral Neurobiology University of Tübingen Germany

37. Health Division TECNALIA San Sebastian Spain

38. Department of Psychology Emory University Atlanta GA

39. Department of Physical Medicine and Rehabilitation Cedars‐Sinai Los Angeles CA

40. Department of Kinesiology and Health Sciences University of Waterloo Ontario Canada

41. Departments of Neurology & Rehabilitation Medicine NYU Langone New York NY

42. Department of Rehabilitation Sciences Department of Health Science and Research Medical University of South Carolina Charleston SC

43. Department of Radiology Keck School of Medicine University of Southern California Los Angeles CA

44. Department of Medicine University of Auckland New Zealand

45. Clinical Neurotechnology Laboratory Department of Psychiatry and Neurosciences (CCM) Charité ‐ Universitätsmedizin Berlin Berlin Germany

46. NYU Langone Department of Neurology New York NY

47. Department of Psychiatry The Chinese University of Hong Kong China

48. Department of Physical Therapy and Neuroscience University of the Sciences Philadelphia PA

49. University College London Queen Square Institute of Neurology London United Kingdom

50. Department of Psychology University of Oslo Norway

51. Department of Mental Health and Addiction Oslo University Hospital Oslo Norway

52. Melbourne Dementia Research Center University of Melbourne Victoria Australia

53. Department of Neurology University of Pittsburgh PA

54. Department of Veterans Affairs Geriatrics Research Educational & Clinical Center Veterans Affairs Pittsburgh Healthcare System (VAPHS) Pittsburgh PA

55. Department of Medicine Emory University School of Medicine Atlanta GA

56. Department of Physical Medicine & Rehabilitation Dell Medical School University of Texas at Austin TX

57. Department of Neurology University of California Los Angeles David Geffen School of Medicine Los Angeles CA

58. California Rehabilitation Hospital Los Angeles CA

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.

Publisher

Ovid Technologies (Wolters Kluwer Health)

Subject

Cardiology and Cardiovascular Medicine

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