ENIGMA's simple seven: Recommendations to enhance the reproducibility of resting-state fMRI in traumatic brain injury

Karen Caeyenberghs; Phoebe Imms; Andrei Irimia; Martin M Monti; Carrie Esopenko; Nicola L de Souza; Juan F Dominguez D; Mary R Newsome; Ekaterina Dobryakova; Andrew Cwiek; Hollie A C Mullin; Nicholas J Kim; Andrew R Mayer; Maheen M Adamson; Kevin Bickart; Katherine M Breedlove; Emily L Dennis; Seth G Disner; Courtney Haswell; Cooper B Hodges; Kristen R Hoskinson; Paula K Johnson; Marsh Königs; Lucia M Li; Spencer W Liebel; Abigail Livny; Rajendra A Morey; Alexandra M Muir; Alexander Olsen; Adeel Razi; Matthew Su; David F Tate; Carmen Velez; Elisabeth A Wilde; Brandon A Zielinski; Paul M Thompson; Frank G Hillary

doi:10.1016/j.nicl.2024.103585

ENIGMA's simple seven: Recommendations to enhance the reproducibility of resting-state fMRI in traumatic brain injury

Neuroimage Clin. 2024 Mar 5:42:103585. doi: 10.1016/j.nicl.2024.103585. Online ahead of print.

Authors

Karen Caeyenberghs¹, Phoebe Imms², Andrei Irimia³, Martin M Monti⁴, Carrie Esopenko⁵, Nicola L de Souza⁶, Juan F Dominguez D⁷, Mary R Newsome⁸, Ekaterina Dobryakova⁹, Andrew Cwiek¹⁰, Hollie A C Mullin¹¹, Nicholas J Kim¹², Andrew R Mayer¹³, Maheen M Adamson¹⁴, Kevin Bickart¹⁵, Katherine M Breedlove¹⁶, Emily L Dennis¹⁷, Seth G Disner¹⁸, Courtney Haswell¹⁹, Cooper B Hodges²⁰, Kristen R Hoskinson²¹, Paula K Johnson²², Marsh Königs²³, Lucia M Li²⁴, Spencer W Liebel²⁵, Abigail Livny²⁶, Rajendra A Morey²⁷, Alexandra M Muir²⁸, Alexander Olsen²⁹, Adeel Razi³⁰, Matthew Su³¹, David F Tate³², Carmen Velez³³, Elisabeth A Wilde³⁴, Brandon A Zielinski³⁵, Paul M Thompson³⁶, Frank G Hillary³⁷

Affiliations

¹ Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Australia. Electronic address: k.caeyenberghs@deakin.edu.au.
² Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA, USA. Electronic address: imms@usc.edu.
³ Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA, USA; Alfred E. Mann Department of Biomedical Engineering, Andrew & Erna Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA; Department of Quantitative & Computational Biology, Dana and David Dornsife College of Arts & Sciences, University of Southern California, Los Angeles, CA, USA. Electronic address: irimia@usc.edu.
⁴ Department of Psychology, UCLA, USA; Brain Injury Research Center (BIRC), Department of Neurosurgery, UCLA, USA. Electronic address: monti@psych.ucla.edu.
⁵ Department of Rehabilitation and Human Performance, Icahn School of Medicine at Mount Sinai, NY, USA. Electronic address: carrie.esopenko@mountsinai.org.
⁶ Department of Rehabilitation and Human Performance, Icahn School of Medicine at Mount Sinai, NY, USA. Electronic address: nicola.desouza@mountsinai.org.
⁷ Cognitive Neuroscience Unit, School of Psychology, Deakin University, Geelong, Australia. Electronic address: juan.dominguezduque@deakin.edu.au.
⁸ Michael E. DeBakey VA Medical Center, Houston, TX, USA; H. Ben Taub Department of Physical Medicine and Rehabilitation, Baylor College of Medicine, Houston, TX, USA; TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA. Electronic address: m.newsome@hsc.utah.edu.
⁹ Center for Traumatic Brain Injury, Kessler Foundation, East Hanover, NJ, USA; Rutgers New Jersey Medical School, Newark, NJ, USA. Electronic address: edobryakova@kesslerfoundation.org.
¹⁰ Department of Psychology, Penn State University, State College, PA, USA. Electronic address: apc5912@psu.edu.
¹¹ Department of Psychology, Penn State University, State College, PA, USA. Electronic address: ham5439@psu.edu.
¹² Ethel Percy Andrus Gerontology Center, Leonard Davis School of Gerontology, University of Southern California, Los Angeles, CA, USA; Alfred E. Mann Department of Biomedical Engineering, Andrew & Erna Viterbi School of Engineering, University of Southern California, Los Angeles, CA, USA. Electronic address: kimnj@usc.edu.
¹³ Mind Research Network, Albuquerque, NM, USA; Departments of Neurology and Psychiatry, University of New Mexico School of Medicine, Albuquerque, NM, USA. Electronic address: amayer@mrn.org.
¹⁴ Women's Operational Military Exposure Network (WOMEN) & Rehabilitation Department, VA Palo Alto, Palo Alto, CA, USA; Rehabilitation Service, VA Palo Alto, Palo Alto, CA, USA; Neurosurgery, Stanford School of Medicine, Stanford, CA, USA. Electronic address: madamson@stanford.edu.
¹⁵ UCLA Steve Tisch BrainSPORT Program, USA; Department of Neurology, David Geffen School of Medicine at UCLA, USA. Electronic address: KBickart@mednet.ucla.edu.
¹⁶ Center for Clinical Spectroscopy, Brigham and Women's Hospital, Boston, MA, USA; Department of Radiology, Harvard Medical School, Boston, MA, USA. Electronic address: kbreedlove@bwh.harvard.edu.
¹⁷ TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA; George E. Wahlen Veterans Affairs Medical Center, Salt Lake City, UT, USA. Electronic address: emily.dennis@hsc.utah.edu.
¹⁸ Minneapolis VA Health Care System, Minneapolis, MN, USA; Department of Psychiatry and Behavioral Sciences, University of Minnesota Medical School, Minneapolis, MN, USA. Electronic address: disne014@umn.edu.
¹⁹ Department of Psychiatry and Behavioral Sciences, Duke University, Durham, NC, USA. Electronic address: courtney.haswell@duke.edu.
²⁰ TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA; George E. Wahlen Veterans Affairs Medical Center, Salt Lake City, UT, USA; Department of Psychology, Brigham Young University, Provo, UT, USA. Electronic address: cooper.hodges@hsc.utah.edu.
²¹ Center for Biobehavioral Health, The Abigail Wexner Research Institute at Nationwide Children's Hospital, Columbus, OH, USA; Department of Pediatrics, The Ohio State University College of Medicine, OH, USA. Electronic address: Kristen.Hoskinson@nationwidechildrens.org.
²² TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA; Neuroscience Center, Brigham Young University, Provo, UT, USA. Electronic address: paula.v.johnson@utah.edu.
²³ Emma Children's Hospital, Amsterdam UMC, University of Amsterdam, Emma Neuroscience Group, The Netherlands; Amsterdam Reproduction and Development, Amsterdam, The Netherlands. Electronic address: m.konigs@amsterdamumc.nl.
²⁴ C3NL, Imperial College London, United Kingdom; UK DRI Centre for Health Care and Technology, Imperial College London, United Kingdom. Electronic address: lucia.li@imperial.ac.uk.
²⁵ TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA; George E. Wahlen Veterans Affairs Medical Center, Salt Lake City, UT, USA. Electronic address: Spencer.Liebel@hsc.utah.edu.
²⁶ Division of Diagnostic Imaging, Sheba Medical Center, Tel-Hashomer, Israel; Sagol School of Neuroscience, Tel-Aviv University, Tel-Aviv, Israel; Sackler Faculty of Medicine, Tel-Aviv University, Tel-Aviv, Israel. Electronic address: abigail.livnyezer@gmail.com.
²⁷ Department of Psychiatry and Behavioral Sciences, Duke University, Durham, NC, USA; Duke-UNC Brain Imaging and Analysis Center, Duke University, Durham, NC, USA; VA Mid-Atlantic Mental Illness Research Education and Clinical Center, Durham, NC, USA. Electronic address: rajendra.morey@duke.edu.
²⁸ Department of Psychology, Brigham Young University, Provo, UT, USA. Electronic address: muira@usc.edu.
²⁹ Department of Psychology, Norwegian University of Science and Technology, Trondheim, Norway; Clinic of Rehabilitation, St. Olavs Hospital, Trondheim University Hospital, Trondheim, Norway; NorHEAD - Norwegian Centre for Headache Research, Norwegian University of Science and Technology, Trondheim, Norway. Electronic address: alexander.olsen@ntnu.no.
³⁰ Turner Institute for Brain and Mental Health, School of Psychological Sciences, Monash University, Clayton, VIC 3800, Australia; Wellcome Centre for Human Neuroimaging, University College London, WC1N 3AR London, United Kingdom; CIFAR Azrieli Global Scholars Program, CIFAR, Toronto, ON, Canada. Electronic address: adeel.razi@monash.edu.
³¹ H. Ben Taub Department of Physical Medicine and Rehabilitation, Baylor College of Medicine, Houston, TX, USA. Electronic address: ms161@rice.edu.
³² TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA; George E. Wahlen Veterans Affairs Medical Center, Salt Lake City, UT, USA. Electronic address: David.Tate@hsc.utah.edu.
³³ TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA; George E. Wahlen Veterans Affairs Medical Center, Salt Lake City, UT, USA. Electronic address: carmen.velez@hsc.utah.edu.
³⁴ H. Ben Taub Department of Physical Medicine and Rehabilitation, Baylor College of Medicine, Houston, TX, USA; TBI and Concussion Center, Department of Neurology, University of Utah, Salt Lake City, UT, USA; George E. Wahlen Veterans Affairs Medical Center, Salt Lake City, UT, USA. Electronic address: elisabeth.wilde@hsc.utah.edu.
³⁵ Departments of Pediatrics, Neurology, and Neuroscience, University of Florida, Gainesville, FL, USA; Departments of Pediatrics, Neurology, and Radiology, University of Utah, Salt Lake City, UT, USA. Electronic address: zielinskib@ufl.edu.
³⁶ Imaging Genetics Center, Mark and Mary Stevens Neuroimaging & Informatics Institute, University of Southern California, Marina del Rey, CA, USA. Electronic address: pthomp@usc.edu.
³⁷ Department of Psychology, Penn State University, State College, PA, USA; Department of Neurology, Hershey Medical Center, PA, USA. Electronic address: fhillary@psu.edu.

Abstract

Resting state functional magnetic resonance imaging (rsfMRI) provides researchers and clinicians with a powerful tool to examine functional connectivity across large-scale brain networks, with ever-increasing applications to the study of neurological disorders, such as traumatic brain injury (TBI). While rsfMRI holds unparalleled promise in systems neurosciences, its acquisition and analytical methodology across research groups is variable, resulting in a literature that is challenging to integrate and interpret. The focus of this narrative review is to address the primary methodological issues including investigator decision points in the application of rsfMRI to study the consequences of TBI. As part of the ENIGMA Brain Injury working group, we have collaborated to identify a minimum set of recommendations that are designed to produce results that are reliable, harmonizable, and reproducible for the TBI imaging research community. Part one of this review provides the results of a literature search of current rsfMRI studies of TBI, highlighting key design considerations and data processing pipelines. Part two outlines seven data acquisition, processing, and analysis recommendations with the goal of maximizing study reliability and between-site comparability, while preserving investigator autonomy. Part three summarizes new directions and opportunities for future rsfMRI studies in TBI patients. The goal is to galvanize the TBI community to gain consensus for a set of rigorous and reproducible methods, and to increase analytical transparency and data sharing to address the reproducibility crisis in the field.

Keywords: Functional MRI; Functional connectivity; Lesions; Reproducibility; Resting state fMRI; Traumatic brain injury.

Publication types

Review