Review

. 2022 Jan;43(1):129-148.

doi: 10.1002/hbm.25015. Epub 2020 Apr 20.

The ENIGMA Stroke Recovery Working Group: Big data neuroimaging to study brain-behavior relationships after stroke

Sook-Lei Liew^{1

2

3

4}, Artemis Zavaliangos-Petropulu^{2

4

5}, Neda Jahanshad^{2

5}, Catherine E Lang⁶, Kathryn S Hayward^{7

8}, Keith R Lohse^{9

10}, Julia M Juliano⁴, Francesca Assogna¹¹, Lee A Baugh^{12

13}, Anup K Bhattacharya¹⁴, Bavrina Bigjahan^{2

15}, Michael R Borich¹⁶, Lara A Boyd^{17

18}, Amy Brodtmann¹⁹, Cathrin M Buetefisch^{16

20}, Winston D Byblow²¹, Jessica M Cassidy²², Adriana B Conforto^{23

24}, R Cameron Craddock²⁵, Michael A Dimyan^{26

27}, Adrienne N Dula^{25

28}, Elsa Ermer²⁶, Mark R Etherton^{29

30}, Kelene A Fercho^{12

31}, Chris M Gregory³², Shahram Hadidchi^{33

34}, Jess A Holguin¹, Darryl H Hwang¹⁵, Simon Jung³⁵, Steven A Kautz^{32

36}, Mohamed Salah Khlif¹⁹, Nima Khoshab³⁷, Bokkyu Kim^{38

39}, Hosung Kim², Amy Kuceyeski^{40

41}, Martin Lotze⁴², Bradley J MacIntosh^{43

44}, John L Margetis¹, Feroze B Mohamed⁴⁵, Fabrizio Piras¹¹, Ander Ramos-Murguialday^{46

47}, Geneviève Richard^{48

49

50}, Pamela Roberts⁵¹, Andrew D Robertson^{52

53}, Jane M Rondina⁵⁴, Natalia S Rost⁵⁵, Nerses Sanossian⁵⁶, Nicolas Schweighofer³⁹, Na Jin Seo^{32

36

57}, Mark S Shiroishi⁵⁸, Surjo R Soekadar^{59

60}, Gianfranco Spalletta^{11

61}, Cathy M Stinear⁶², Anisha Suri⁶³, Wai Kwong W Tang⁶⁴, Gregory T Thielman^{65

66}, Daniela Vecchio¹¹, Arno Villringer^{67

68

69}, Nick S Ward⁷⁰, Emilio Werden¹⁹, Lars T Westlye^{48

49}, Carolee Winstein^{39

71}, George F Wittenberg^{72

73}, Kristin A Wong⁷⁴, Chunshui Yu^{75

76}, Steven C Cramer⁷⁷, Paul M Thompson^{2

5}

Affiliations

¹ Chan Division of Occupational Science and Occupational Therapy, University of Southern California, Los Angeles, California, USA.
² Department of Neurology, USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
³ Department of Biomedical Engineering, University of Southern California, Los Angeles, California, USA.
⁴ Neuroscience Graduate Program, University of Southern California, Los Angeles, California, USA.
⁵ Imaging Genetics Center, USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁶ Program in Physical Therapy, Washington University School of Medicine, St. Louis, Missouri, USA.
⁷ Department of Physiotherapy, and Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria, Australia.
⁸ NHMRC Centre of Research Excellence in Stroke Rehabilitation and Brain Recovery, University of Melbourne, Parkville, Victoria, Australia.
⁹ Department of Health, Kinesiology, and Recreation, University of Utah, Salt Lake City, Utah, USA.
¹⁰ Department of Physical Therapy and Athletic Training, University of Utah, Salt Lake City, Utah, USA.
¹¹ Laboratory of Neuropsychiatry, Department of Clinical and Behavioral Neurology, IRCCS Santa Lucia Foundation, Rome, Italy.
¹² Division of Basic Biomedical Sciences, Sanford School of Medicine, University of South Dakota, Vermillion, South Dakota, USA.
¹³ Sioux Falls VA Health Care System, Sioux Falls, South Dakota, USA.
¹⁴ Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, Missouri, USA.
¹⁵ Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
¹⁶ Department of Rehabilitation Medicine, Emory University, Atlanta, Georgia, USA.
¹⁷ Department of Physical Therapy, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada.
¹⁸ Djavad Mowafaghian Centre for Brain Health, Vancouver, British Columbia, Canada.
¹⁹ Florey Institute for Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria, Australia.
²⁰ Department of Neurology, Emory University, Atlanta, Georgia, USA.
²¹ Department of Exercise Sciences, Centre for Brain Research, University of Auckland, Auckland, New Zealand.
²² Division of Physical Therapy, Department Allied Health Sciences, University of North Carolina, Chapel Hill, Chapel Hill, North Carolina, USA.
²³ Neurology Clinical Division, Hospital das Clínicas/São Paulo University, São Paulo, Brazil.
²⁴ Hospital Israelita Albert Einstein, São Paulo, Brazil.
²⁵ Department of Diagnostic Medicine, The University of Texas at Austin Dell Medical School, Austin, Texas, USA.
²⁶ Department of Neurology and Neurorehabilitation, School of Medicine, University of Maryland, Baltimore, Baltimore, Maryland, USA.
²⁷ VA Maryland Health Care System, Baltimore, Maryland, USA.
²⁸ Department of Neurology, Dell Medical School at University of Texas at Austin, Austin, Texas, USA.
²⁹ Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts, USA.
³⁰ J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, Massachusetts, USA.
³¹ Federal Aviation Administration, Civil Aerospace Medical Institute, Oklahoma City, Oklahoma, USA.
³² Department of Health Sciences and Research, Medical University of South Carolina, Charleston, South Carolina, USA.
³³ Department of Radiology, Wayne State University/Detroit Medical Center, Detroit, Michigan, USA.
³⁴ Department of Internal Medicine, Wayne State University/Detroit Medical Center, Detroit, Michigan, USA.
³⁵ Department of Neurology, University of Bern, Bern, Switzerland.
³⁶ Ralph H Johnson VA Medical Center, Charleston, South Carolina, USA.
³⁷ Department of Anatomy and Neurobiology, University of California, Irvine, California, USA.
³⁸ Department of Physical Therapy Education, State University of New York Upstate Medical University, Syracuse, New York, USA.
³⁹ Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, California, USA.
⁴⁰ Department of Radiology, Weill Cornell Medicine, New York, New York, USA.
⁴¹ Brain and Mind Research Institute, Weill Cornell Medicine, New York, New York, USA.
⁴² Functional Imaging Unit, Center for Diagnostic Radiology, School of Medicine, University of Greifswald, Greifswald, Germany.
⁴³ Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada.
⁴⁴ Physical Sciences Platform, Brain Sciences Program, Sunnybrook Research Institute, Toronto, Ontario, Canada.
⁴⁵ Department of Radiology, Thomas Jefferson University, Philadelphia, Pennsylvania, USA.
⁴⁶ TECNALIA, Basque Research and Technology Alliance (BRTA), Neurotechnology Laboratory, Derio, Spain.
⁴⁷ Institute of Medical Psychology and Behavioural Neurobiology, University of Tubingen, Tübingen, Germany.
⁴⁸ Department of Psychology, University of Oslo, Oslo, Norway.
⁴⁹ NORMENT, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.
⁵⁰ Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
⁵¹ Department of Physical Medicine and Rehabilitation, Cedars-Sinai, Los Angeles, California, USA.
⁵² Department of Kinesiology, University of Waterloo, Waterloo, Ontario, Canada.
⁵³ Schlegel-UW Research Institute for Aging, University of Waterloo, Waterloo, Ontario, Canada.
⁵⁴ Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, London, UK.
⁵⁵ Stroke Division, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA.
⁵⁶ Division of Neurocritical Care and Stroke, Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁵⁷ Division of Occupational Therapy, Department of Health Professions, Medical University of South Carolina, Charleston, South Carolina, USA.
⁵⁸ Division of Neuroradiology, Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁵⁹ Department of Psychiatry and Psychotherapy, Clinical Neurotechnology Laboratory, Charité - University Medicine Berlin, Berlin, Germany.
⁶⁰ Applied Neurotechnology Laboratory, Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.
⁶¹ Division of Neuropsychiatry, Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas, USA.
⁶² Department of Medicine, University of Auckland, Auckland, New Zealand.
⁶³ Department of Electrical and Computer Engineering, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
⁶⁴ Department of Psychiatry, The Chinese University of Hong Kong, Hong Kong, People's Republic of China.
⁶⁵ Physical Therapy and Neuroscience, University of the Sciences, Philadelphia, Pennsylvania, USA.
⁶⁶ Samson College, Quezon City, Philippines.
⁶⁷ Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
⁶⁸ Department of Cognitive Neurology, University Hospital Leipzig, Leipzig, Germany.
⁶⁹ Center for Stroke Research, Charité-Universitätsmedizin Berlin, Berlin, Germany.
⁷⁰ UCL Queen Square Institute of Neurology, University College London, London, UK.
⁷¹ Department of Neurology, University of Southern California, Los Angeles, California, USA.
⁷² Department of Neurology, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
⁷³ Department of Veterans Affairs, University Drive Campus, Pittsburgh, Pennsylvania, USA.
⁷⁴ Department of Physical Medicine and Rehabilitation, Dell Medical School, University of Texas Austin, Austin, Texas, USA.
⁷⁵ Department of Radiology, Tianjin Medical University General Hospital, Tianjin, China.
⁷⁶ Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, China.
⁷⁷ Department of Neurology, UCLA and California Rehabilitation Institute, Los Angeles, California, USA.

PMID: 32310331
PMCID: PMC8675421
DOI: 10.1002/hbm.25015

Review

The ENIGMA Stroke Recovery Working Group: Big data neuroimaging to study brain-behavior relationships after stroke

Sook-Lei Liew et al. Hum Brain Mapp. 2022 Jan.

. 2022 Jan;43(1):129-148.

doi: 10.1002/hbm.25015. Epub 2020 Apr 20.

Authors

Affiliations

¹ Chan Division of Occupational Science and Occupational Therapy, University of Southern California, Los Angeles, California, USA.
² Department of Neurology, USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
³ Department of Biomedical Engineering, University of Southern California, Los Angeles, California, USA.
⁴ Neuroscience Graduate Program, University of Southern California, Los Angeles, California, USA.
⁵ Imaging Genetics Center, USC Stevens Neuroimaging and Informatics Institute, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁶ Program in Physical Therapy, Washington University School of Medicine, St. Louis, Missouri, USA.
⁷ Department of Physiotherapy, and Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria, Australia.
⁸ NHMRC Centre of Research Excellence in Stroke Rehabilitation and Brain Recovery, University of Melbourne, Parkville, Victoria, Australia.
⁹ Department of Health, Kinesiology, and Recreation, University of Utah, Salt Lake City, Utah, USA.
¹⁰ Department of Physical Therapy and Athletic Training, University of Utah, Salt Lake City, Utah, USA.
¹¹ Laboratory of Neuropsychiatry, Department of Clinical and Behavioral Neurology, IRCCS Santa Lucia Foundation, Rome, Italy.
¹² Division of Basic Biomedical Sciences, Sanford School of Medicine, University of South Dakota, Vermillion, South Dakota, USA.
¹³ Sioux Falls VA Health Care System, Sioux Falls, South Dakota, USA.
¹⁴ Mallinckrodt Institute of Radiology, Washington University School of Medicine, St. Louis, Missouri, USA.
¹⁵ Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
¹⁶ Department of Rehabilitation Medicine, Emory University, Atlanta, Georgia, USA.
¹⁷ Department of Physical Therapy, Faculty of Medicine, University of British Columbia, Vancouver, British Columbia, Canada.
¹⁸ Djavad Mowafaghian Centre for Brain Health, Vancouver, British Columbia, Canada.
¹⁹ Florey Institute for Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria, Australia.
²⁰ Department of Neurology, Emory University, Atlanta, Georgia, USA.
²¹ Department of Exercise Sciences, Centre for Brain Research, University of Auckland, Auckland, New Zealand.
²² Division of Physical Therapy, Department Allied Health Sciences, University of North Carolina, Chapel Hill, Chapel Hill, North Carolina, USA.
²³ Neurology Clinical Division, Hospital das Clínicas/São Paulo University, São Paulo, Brazil.
²⁴ Hospital Israelita Albert Einstein, São Paulo, Brazil.
²⁵ Department of Diagnostic Medicine, The University of Texas at Austin Dell Medical School, Austin, Texas, USA.
²⁶ Department of Neurology and Neurorehabilitation, School of Medicine, University of Maryland, Baltimore, Baltimore, Maryland, USA.
²⁷ VA Maryland Health Care System, Baltimore, Maryland, USA.
²⁸ Department of Neurology, Dell Medical School at University of Texas at Austin, Austin, Texas, USA.
²⁹ Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts, USA.
³⁰ J. Philip Kistler Stroke Research Center, Harvard Medical School, Boston, Massachusetts, USA.
³¹ Federal Aviation Administration, Civil Aerospace Medical Institute, Oklahoma City, Oklahoma, USA.
³² Department of Health Sciences and Research, Medical University of South Carolina, Charleston, South Carolina, USA.
³³ Department of Radiology, Wayne State University/Detroit Medical Center, Detroit, Michigan, USA.
³⁴ Department of Internal Medicine, Wayne State University/Detroit Medical Center, Detroit, Michigan, USA.
³⁵ Department of Neurology, University of Bern, Bern, Switzerland.
³⁶ Ralph H Johnson VA Medical Center, Charleston, South Carolina, USA.
³⁷ Department of Anatomy and Neurobiology, University of California, Irvine, California, USA.
³⁸ Department of Physical Therapy Education, State University of New York Upstate Medical University, Syracuse, New York, USA.
³⁹ Division of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, California, USA.
⁴⁰ Department of Radiology, Weill Cornell Medicine, New York, New York, USA.
⁴¹ Brain and Mind Research Institute, Weill Cornell Medicine, New York, New York, USA.
⁴² Functional Imaging Unit, Center for Diagnostic Radiology, School of Medicine, University of Greifswald, Greifswald, Germany.
⁴³ Department of Medical Biophysics, University of Toronto, Toronto, Ontario, Canada.
⁴⁴ Physical Sciences Platform, Brain Sciences Program, Sunnybrook Research Institute, Toronto, Ontario, Canada.
⁴⁵ Department of Radiology, Thomas Jefferson University, Philadelphia, Pennsylvania, USA.
⁴⁶ TECNALIA, Basque Research and Technology Alliance (BRTA), Neurotechnology Laboratory, Derio, Spain.
⁴⁷ Institute of Medical Psychology and Behavioural Neurobiology, University of Tubingen, Tübingen, Germany.
⁴⁸ Department of Psychology, University of Oslo, Oslo, Norway.
⁴⁹ NORMENT, Division of Mental Health and Addiction, Oslo University Hospital, Oslo, Norway.
⁵⁰ Institute of Clinical Medicine, University of Oslo, Oslo, Norway.
⁵¹ Department of Physical Medicine and Rehabilitation, Cedars-Sinai, Los Angeles, California, USA.
⁵² Department of Kinesiology, University of Waterloo, Waterloo, Ontario, Canada.
⁵³ Schlegel-UW Research Institute for Aging, University of Waterloo, Waterloo, Ontario, Canada.
⁵⁴ Department of Clinical and Movement Neurosciences, UCL Queen Square Institute of Neurology, University College London, London, UK.
⁵⁵ Stroke Division, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts, USA.
⁵⁶ Division of Neurocritical Care and Stroke, Department of Neurology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁵⁷ Division of Occupational Therapy, Department of Health Professions, Medical University of South Carolina, Charleston, South Carolina, USA.
⁵⁸ Division of Neuroradiology, Department of Radiology, Keck School of Medicine, University of Southern California, Los Angeles, California, USA.
⁵⁹ Department of Psychiatry and Psychotherapy, Clinical Neurotechnology Laboratory, Charité - University Medicine Berlin, Berlin, Germany.
⁶⁰ Applied Neurotechnology Laboratory, Department of Psychiatry and Psychotherapy, University of Tübingen, Tübingen, Germany.
⁶¹ Division of Neuropsychiatry, Menninger Department of Psychiatry and Behavioral Sciences, Baylor College of Medicine, Houston, Texas, USA.
⁶² Department of Medicine, University of Auckland, Auckland, New Zealand.
⁶³ Department of Electrical and Computer Engineering, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
⁶⁴ Department of Psychiatry, The Chinese University of Hong Kong, Hong Kong, People's Republic of China.
⁶⁵ Physical Therapy and Neuroscience, University of the Sciences, Philadelphia, Pennsylvania, USA.
⁶⁶ Samson College, Quezon City, Philippines.
⁶⁷ Department of Neurology, Max Planck Institute for Human Cognitive and Brain Sciences, Leipzig, Germany.
⁶⁸ Department of Cognitive Neurology, University Hospital Leipzig, Leipzig, Germany.
⁶⁹ Center for Stroke Research, Charité-Universitätsmedizin Berlin, Berlin, Germany.
⁷⁰ UCL Queen Square Institute of Neurology, University College London, London, UK.
⁷¹ Department of Neurology, University of Southern California, Los Angeles, California, USA.
⁷² Department of Neurology, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
⁷³ Department of Veterans Affairs, University Drive Campus, Pittsburgh, Pennsylvania, USA.
⁷⁴ Department of Physical Medicine and Rehabilitation, Dell Medical School, University of Texas Austin, Austin, Texas, USA.
⁷⁵ Department of Radiology, Tianjin Medical University General Hospital, Tianjin, China.
⁷⁶ Tianjin Key Laboratory of Functional Imaging, Tianjin Medical University General Hospital, Tianjin, China.
⁷⁷ Department of Neurology, UCLA and California Rehabilitation Institute, Los Angeles, California, USA.

PMID: 32310331
PMCID: PMC8675421
DOI: 10.1002/hbm.25015

Abstract

The goal of the Enhancing Neuroimaging Genetics through Meta-Analysis (ENIGMA) Stroke Recovery working group is to understand brain and behavior relationships using well-powered meta- and mega-analytic approaches. ENIGMA Stroke Recovery has data from over 2,100 stroke patients collected across 39 research studies and 10 countries around the world, comprising the largest multisite retrospective stroke data collaboration to date. This article outlines the efforts taken by the ENIGMA Stroke Recovery working group to develop neuroinformatics protocols and methods to manage multisite stroke brain magnetic resonance imaging, behavioral and demographics data. Specifically, the processes for scalable data intake and preprocessing, multisite data harmonization, and large-scale stroke lesion analysis are described, and challenges unique to this type of big data collaboration in stroke research are discussed. Finally, future directions and limitations, as well as recommendations for improved data harmonization through prospective data collection and data management, are provided.

Keywords: MRI; big data; lesions; neuroinformatics; stroke.

PubMed Disclaimer

Conflict of interest statement

Neda Jahanshad and Paul Thompson are MPIs of a research‐related grant from Biogen, Inc. for work unrelated to the contents of this manuscript. Steven C. Cramer is a consultant for Abbvie, Constant Therapeutics, MicroTransponder, Neurolutions, Regenera, SanBio, Stemedica, Fujifilm Toyama Chemical Co., Biogen, and TRCare.

Figures

**FIGURE 1**
ENIGMA Stroke Recovery workflow. Workflow for ENIGMA Stroke Recovery from data intake to data analysis

**FIGURE 2**
Optimized lesion segmentation pipeline. Example of a future neuroinformatics system for lesion segmentation, with only one point of manual input (manual segmentation of failed lesion masks, indicated in bold)

**FIGURE A1**
Examples of quality control decisions. (A) An axial view of a participant's left (blue) and right (red) caudate that are both scored as PASS. (B) An axial view of an under segmented right caudate (FAIL). Lesion overlap in the caudate caused ambiguous gray matter boundaries, resulting in a failed segmentation. (C) FreeSurfer can fail to segment correctly even without the presence of a lesion. This is an axial view of under segmented left and right caudate segmentation that were scored as FAIL. (D) A coronal view of a participant's left and right caudate that are both scored as PASS. (E) A coronal view of a participant with a lesion that overlaps with the left caudate creates ambiguous boundaries. In this case, FreeSurfer overestimated the left caudate, mistaking the lesion as a gray matter boundary (FAIL)

See this image and copyright information in PMC

References

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The ENIGMA Stroke Recovery Working Group: Big data neuroimaging to study brain-behavior relationships after stroke

Affiliations

The ENIGMA Stroke Recovery Working Group: Big data neuroimaging to study brain-behavior relationships after stroke

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

Publication types

MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

Other Literature Sources

Medical

Miscellaneous