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What tests and measures accurately diagnose persisting post-concussive symptoms in children, adolescents and adults following sport-related concussion? A systematic review
  1. Keith Owen Yeates1,2,3,
  2. Anu M Räisänen4,5,
  3. Zahra Premji6,
  4. Chantel T Debert7,
  5. Pierre Frémont8,
  6. Sidney Hinds9,
  7. Jonathan D Smirl5,10,
  8. Karen Barlow11,
  9. Gavin A Davis12,13,
  10. Ruben J Echemendia14,15,
  11. Nina Feddermann-Demont16,17,
  12. Colm Fuller18,19,
  13. Isabelle Gagnon20,21,
  14. Christopher C Giza22,23,
  15. Grant L Iverson24,25,
  16. Michael Makdissi26,27,
  17. Kathryn J Schneider5
  1. 1 Department of Psychology, University of Calgary, Calgary, Alberta, Canada
  2. 2 Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada
  3. 3 Alberta Children's Hospital Research Institute, University of Calgary, Calgary, Alberta, Canada
  4. 4 Department of Physical Therapy Education - Oregon, Western University of Health Sciences, College of Health Sciences - Northwest, Lebanon, Oregon, USA
  5. 5 Sport Injury Prevention Research Centre, Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada
  6. 6 Libraries, University of Victoria, Victoria, British Columbia, Canada
  7. 7 Department of Clinical Neuroscience, Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
  8. 8 Department of Rehabilitation, Laval University, Quebec, Quebec, Canada
  9. 9 Uniformed Services University, Bethesda, Maryland, USA
  10. 10 Faculty of Kinesiology, University of Calgary, Calgary, Alberta, Canada
  11. 11 Child Health Research Centre, Faculty of Medicine, University of Queensland, Brisbane, Queensland, Australia
  12. 12 Murdoch Children's Research Institute, Parkville, Victoria, Australia
  13. 13 Cabrini Health, Malvern, Victoria, Australia
  14. 14 Department of Psychology, University of Missouri, Kansas City, Missouri, USA
  15. 15 Psychological and Neurobehavioral Associates, Inc, State College, Pennsylvania, USA
  16. 16 Department of Neurology, University Hospital Zurich, Zurich, Switzerland
  17. 17 Sports Neuroscience, University of Zurich, Zurich, Switzerland
  18. 18 College of Medicine and Health, University College Cork, Cork, Ireland
  19. 19 Sports Medicine Department, Sports Surgery Clinic, Dublin, Ireland
  20. 20 School of Physical and Occupational Therapy, Faculty of Medicine and Health Sciences, McGill University, Montreal, Quebec, Canada
  21. 21 Trauma Center, Montreal Children’s Hospital, McGill University Health Center, Montreal, Quebec, Canada
  22. 22 Department of Neurosurgery, UCLA Steve Tisch BrainSPORT Program, Los Angeles, California, USA
  23. 23 Department of Pediatrics/Pediatric Neurology, Mattel Children's Hospital UCLA, Los Angeles, California, USA
  24. 24 Department of Physical Medicine and Rehabilitation, Harvard Medical School, Boston, Massachusetts, USA
  25. 25 Sports Concussion Program, MassGeneral Hospital for Children, Boston, Massachusetts, USA
  26. 26 Melbourne Brain Centre, Florey Institute of Neuroscience and Mental Health - Austin Campus, Heidelberg, Victoria, Australia
  27. 27 Australian Football League, Melbourne, Victoria, Australia
  1. Correspondence to Dr Keith Owen Yeates, Psychology, University of Calgary, Calgary, Canada; kyeates{at}ucalgary.ca

Abstract

Objective To determine what tests and measures accurately diagnose persisting post-concussive symptoms (PPCS) in children, adolescents and adults following sport-related concussion (SRC).

Design A systematic literature review.

Data sources MEDLINE, Embase, PsycINFO, Cochrane Central Register of Controlled Trials, CINAHL and SPORTDiscus through March 2022.

Eligibility criteria Original, empirical, peer-reviewed findings (cohort studies, case-control studies, cross-sectional studies and case series) published in English and focused on SRC. Studies needed to compare individuals with PPCS to a comparison group or their own baseline prior to concussion, on tests or measures potentially affected by concussion or associated with PPCS. Results: Of 3298 records screened, 26 articles were included in the qualitative synthesis, including 1016 participants with concussion and 531 in comparison groups; 7 studies involved adults, 8 involved children and adolescents and 11 spanned both age groups. No studies focused on diagnostic accuracy. Studies were heterogeneous in participant characteristics, definitions of concussion and PPCS, timing of assessment and the tests and measures examined. Some studies found differences between individuals with PPCS and comparison groups or their own pre-injury assessments, but definitive conclusions were not possible because most studies had small convenience samples, cross-sectional designs and were rated high risk of bias.

Conclusion The diagnosis of PPCS continues to rely on symptom report, preferably using standardised symptom rating scales. The existing research does not indicate that any other specific tool or measure has satisfactory accuracy for clinical diagnosis. Future research drawing on prospective, longitudinal cohort studies could help inform clinical practice.

  • Diagnosis
  • Brain Concussion

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Footnotes

  • Twitter @amraisanen, @pfremo, @griz1, @Kat_Schneider7

  • Contributors All authors made a substantial contribution to the conception or design of the work, or to the acquisition, analysis, or interpretation of data for the work; drafted the paper or revised it critically for important intellectual content; and provided final approval of the version to be published and agree to be accountable for all aspects of the work. Based on the CRediT taxonomy, specific contributions were as follows. KOY: conceptualisation, data curation, formal analysis, investigation, methodology, project administration and writing original draft. AMR and ZP: conceptualisation, data curation, formal analysis, investigation, methodology, project administration and writing—review and editing. KJS: conceptualisation, data curation, funding acquisition, investigation, methodology, project administration and writing—review and editing. All other authors: conceptualisation, data curation, investigation, methodology and writing—review and editing.

  • Funding This systematic review was prepared for presentation at the 6th International Conference on Concussion in Sport in Amsterdam, October 2022. An education grant was received from the Concussion in Sport International Consensus Conference Organising Committee through Publi Creations for partial administrative and operational costs associated with the preparation of the systematic review.

  • Competing interests KOY is editor-in-chief of the journal Neuropsychology for which he receives an editorial stipend from the American Psychological Association. He is an unpaid consulting editor for Archives of Clinical Neuropsychology and Journal of Head Trauma Rehabilitation. He is an unpaid member of the Scientific Advisory Committee for Brain Injury Canada. He is the chair of the Canadian Concussion Network, which is funded by a grant from Canadian Institutes of Health Research (CIHR) to the University of Calgary; he is principal applicant on the grant but receives no income from it. He is a principal investigator (PI) on another grant from CIHR from which he derives no income. He is a co-investigator on research grants from CIHR, the US National Institutes of Health (NIH), Brain Canada Foundation and National Football League Scientific Advisory Board; he derives income only from the grant from NIH. He serves as a member of a CIHR grant review panel for which he receives an honorarium. He receives book royalties from Guilford Press and Cambridge University Press. He has received travel support and honorarium for presentations to multiple organisations. He has served or serves on the following committees/boards for which he receives honorarium: Independent Data Monitoring Committee (IDMC), Care for Post-Concussive Symptoms Effectiveness (CARE4PCS-2) Trial, National Institute for Child Health and Human Development; Observational Study Monitoring Board (OSMB), Approaches and Decisions in Acute Pediatric TBI (ADAPT) Trial, National Institute of Neurological Disorders and Stroke; National Research Advisory Council, National Pediatric Rehabilitation Resource Center, Center for Pediatric Rehabilitation: Growing Research, Education, and Sharing Science (C-PROGRESS), Virginia Tech University. AMR received a stipend for the clerical and administrative aspects of the systematic review. She has received research grants from the Tonal Strength Institute and Alberta Bone and Joint Strategic Clinical Network. ZP has no disclosures. CD was a pharmaceutical funded invited expert panelist (Teva) for CGRP monoclonal antibody treatment in chronic migraine and received a pharmaceutical funded grant for growth hormone deficiency following concussion. She has grants as PI or co-investigator from the Canadian Department of National Defense, CIHR, Tri-council funding New Frontiers, Alberta Provincial government and Foundations for Physical Medicine and Rehabilitation. She holds a patent for urine metabolites in the diagnosis of concussion. PF is a co-investigator on a research grant from the NFL’s 'Play Smart. Play Safe' Initiative and an Executive committee member of the Canadian Concussion Network (financed by CIHR). He received honorarium for an expert group discussion on blood biomarkers for concussion in December 2020. SH provides client consultation services for military/veteran health, neuroscience, health, sports medicine, neurodegenerative disease, neurotrauma, nuclear medicine, molecular imaging, nuclear and radiation accidents and incidents, and health equity. Consult services includes support to Prevent Biometrics; advisor to Synaptek; advisor/consultant for the Collaborative Neuropathology Network Characterizing Outcomes of TBI (CONNECT-TBI); advisor to NanoDX; and reviewer for Peer Reviewed Alzheimer’s Disease Research Program. SH is chief of Health Equity and Deputy Medical Director for the NFL Players Association, Medical Director for the MLS Players Association. He receives grant support (no income) from the following: Co-PI, Long-term Impact of Military-relevant Brain Injury Consortium – Chronic Effects of Neurotrauma Consortium (LIMBIC-CENC); Advisory Board member to Concussion Legacy Foundation Project Enlist; Advisory Board member to the University of Michigan Concussion Center; advisor to Gryphon Bio; ad hoc reviewer for VA Brain Health Research; invited reviewer to Congressionally Directed Medical Research Programs; National Academy of Science, Engineering, and Medicine 'Accelerating Progress in TBI Research and Care'; NASEM TBI Forum committee member (currently inactive); contributor to Post-traumatic Epilepsy Former Department of Defense work: NFL Scientific Advisory Board member; NCAA-DoD CARE Medical Advisory Board Member; DoD Brain Health Research Coordinating Officer and Medical Advisor to the Principal Assistant for Research and Technology (PAR&T), United States Army Medical Research and Development Command (USAMRDC); Ex Officio National Advisory Neurological Disorders and Stroke (NANDSC) Council Member. KJS has no disclosures. KB receives funding from the Motor Accident Insurance Commission, Queensland Australia. She is a committee member on the Medical Advisory Board, Concussion Australia. She is Chief Investigator, for the first Australia and New Zealand Guidelines for the assessment and management of mild traumatic brain injury and persisting post-concussion symptoms, supported by the Medical Research Future Fund Australia. She has received travel support and honorarium for presentations to organisations. GAD is a member of the Scientific Committee of the 6th International Conference on Concussion in Sport; an honorary member of the AFL Concussion Scientific Committee; Section Editor, Sport and Rehabilitation, NEUROSURGERY; and has attended meetings organised by sporting organisations including the NFL, NRL, IIHF, IOC and FIFA; however, he has not received any payment, research funding, or other monies from these groups other than for travel costs. RJE is a paid consultant for the NHL and co-chair of the NHL/NHLPA Concussion Subcommittee. He is also a paid consultant and chair of the Major League Soccer concussion committee, and a consultant to the US Soccer Federation. He previously served as a neuropsychology consultant to Princeton University Athletic Medicine and EyeGuide. He is currently a co-PI for a grant funded by the NFL (NFL-Long) through Boston Children’s Hospital. He occasionally provides expert testimony in matters related to MTBI and sports concussion, and occasionally receives honoraria and travel support/reimbursement for professional meetings. NF-D is a member of the International independent FIFA Concussion Advisory Group; GOTS Concussion Committee Innovation and Technology Panel, UK Department for Digital, Culture, Media and Sport; Concussion in Sport Group (CISG); NINDS CDE Sports Concussion CDE Subacute Subgroup (National Institutes of Health); IFAB Concussion Expert Group; Swiss Neurology Society; Swiss Society for Clinical Neurophysiology; European NeuroOphthalmology Society; and Concussion in Sport Group (CISG). She is an Editorial Board Member for the Journal of Concussion, Journal of Science and Medicine in Football. CF is a PhD candidate at the School of Medicine & Health at University College Cork, Ireland. He is currently head of physiotherapy at the sports medicine department of the Sports Surgery Clinic (SSC), Dublin Ireland. SSC have paid the fees of his PhD and contributed towards the cost of him attending the 6th International Conference on Concussion in Sport in Amsterdam, 2022. From October 2017 to July 2020, he worked as national team lead physiotherapist for the IRFU Senior Men’s rugby team. He is a member of the Irish Society of Chartered Physiotherapists. Since 2022, he is a founder and shareholder (10%) of Fizfit Ltd., a start-up which focused on recovery and activation products for musculoskeletal health. IG has paid employment relationships with McGill University and the McGill University Health Center. She has received grants in the last 3 years from: Canadian Institutes of Health Research; Fonds de recherche du Québec – Santé; Research Institute of the McGill University Health Center; McGill University; and Institut National du Sport du Québec. CCG discloses the following grants and research support: Hit-IQ (2022-2023); NIH NINDS (R01 NS110757 2019-2024); NINDS (U54 NS121688 2021-2026); UCLA Brain Injury Research Center, UCLA Steve Tisch BrainSPORT program, Easton Clinic for Brain Health/Je os a clinical consultant (provide clinical care to athletes) for the NBA, NFL-Neurological Care Program, NHL/NHLPA, and Los Angeles Lakers. He is a member of the Advisory Board (non-compensated) for Major League Soccer, National Basketball Association, and US Soccer Federation. He is a member of the Advisory Board (Compensated) for Highmark Interactive; he occasionally serves as an expert witness in medicolegal cases. He is a shareholder in Highmark Interactive stock options. He receives book royalties from Blackwell/Wiley Publishing. GLI serves as a scientific advisor for NanoDX®, Sway Operations, LLC, and Highmark, Inc. He has a clinical and consulting practice in forensic neuropsychology, including expert testimony, involving individuals who have sustained mild TBIs (including former athletes), and on the topic of suicide. He has received past research support or funding from several test publishing companies, including ImPACT Applications, Inc., CNS Vital Signs, and Psychological Assessment Resources (PAR, Inc.). He receives royalties from the sales of one neuropsychological test (WCST-64). He has received travel support and honorariums for presentations at conferences and meetings. He has received research funding as a principal investigator from the National Football League, and subcontract grant funding as a collaborator from the Harvard Integrated Program to Protect and Improve the Health of National Football League Players Association Members. He has received research funding from the Wounded Warrior Project™. He acknowledges unrestricted philanthropic support from ImPACT Applications, Inc., the Mooney-Reed Charitable Foundation, the National Rugby League, Boston Bolts, and the Schoen Adams Research Institute at Spaulding Rehabilitation. MM is a sport and exercise medicine physician working in private consulting practice and is the Chief Medical Officer for the Australian Football League. He is a shareholder of Olympic Park Sports Medicine Centre in Melbourne, Australia. He is ex-senior physician at the Hawthorn Football Club (AFL) and ex-Chief Executive Officer of the AFL Doctors Association. He has received research grants from the Australian Football League. He has received travel support from the Australian Football League, FIFA and the International Olympic Committee to attend and present at international conferences. He is a member of the Scientific Committee for the 6th International Conference on Concussion in Sport. He is an honorary member of the International Concussion in Sport Group,and the Australian Rugby Union Concussion Advisory Group. He is an independent concussion consultant for World Rugby. KS has received grant funding from CIHR, National Football League Scientific Advisory Board, International Olympic Committee Medical and Scientific Research Fund, World Rugby, Mitacs Accelerate, University of Calgary) with funds paid to her institution and not to her personally. She is an Associate Editor of BJSM (unpaid) and has received travel and accommodation support for meetings where she has presented. She coordinated the writing of the systematic reviews that informed the 6th International Conference on Concussion in Sport, for which she has received an educational grant to assist with the administrative costs associated with the writing of the reviews. She is a member of the AFL Concussion Scientific Committee (unpaid position) and Brain Canada advisory committee (unpaid positions). She works as a physiotherapy consultant and treats athletes of all levels of sport from grass roots to professional.

  • Provenance and peer review Not commissioned; externally peer reviewed.

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