SPORTS-RELATED
CONCUSSIONS IN YOUTH

Improving the Science, Changing the Culture

Committee on Sports-Related Concussions in Youth

Board on Children, Youth, and Families

Robert Graham, Frederick P. Rivara, Morgan A. Ford,
and Carol Mason Spicer, Editors

         INSTITUTE OF MEDICINE AND
NATIONAL RESEARCH COUNCIL
                          OF THE NATIONAL ACADEMIES

THE NATIONAL ACADEMIES PRESS
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SPORTS-RELATED CONCUSSIONS IN YOUTH Improving the Science, Changing the Culture Committee on Sports-Related Concussions in Youth Board on Children, Youth, and Families Robert Graham, Frederick P. Rivara, Morgan A. Ford, and Carol Mason Spicer, Editors

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THE NATIONAL ACADEMIES PRESS  500 Fifth Street, NW  Washington, DC 20001 NOTICE: The project that is the subject of this report was approved by the Govern- ing Board of the National Research Council, whose members are drawn from the councils of the National Academy of Sciences, the National Academy of Engineer- ing, and the Institute of Medicine. The members of the committee responsible for the report were chosen for their special competences and with regard for appropri- ate balance. This study was supported by contracts between the National Academy of Sciences and the Centers for Disease Control and Prevention (CDC) (200-2011-38807); the CDC Foundation (Unnumbered Award) with support from the National Foot- ball League; the Department of Defense (HT0011-12-C-0023); the Department of Education (ED-OSE-12-P-0049); the Health Resources and Services Administration (HHSH250200976014I); the National Athletic Trainers’ Association Research and Education Foundation (0512SETGRANT); and the National Institutes of Health (HHSN263201200074I). Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the views of the organizations or agencies that provided support for the project. International Standard Book Number-13: 978-0-309-28800-2 International Standard Book Number-10: 0-309-28800-2 Additional copies of this report are available for sale from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. For more information about the Institute of Medicine, visit the IOM home page at: www.iom.edu. Copyright 2014 by the National Academy of Sciences. All rights reserved. Printed in the United States of America The serpent has been a symbol of long life, healing, and knowledge among almost all cultures and religions since the beginning of recorded history. The serpent ad- opted as a logotype by the Institute of Medicine is a relief carving from ancient Greece, now held by the Staatliche Museen in Berlin. Suggested citation: Institute of Medicine (IOM) and National Research Council (NRC). 2014. Sports-related concussions in youth: Improving the science, changing the culture. Washington, DC: The National Academies Press.

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Acad- emy has a mandate that requires it to advise the federal government on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding en- gineers. It is autonomous in its administration and in the selection of its members, sharing with the National Academy of Sciences the responsibility for advising the federal government. The National Academy of Engineering also sponsors engineer- ing programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. C. D. Mote, Jr., is presi- dent of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Insti- tute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sci- ences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in providing services to the government, the public, and the scientific and engineering communities. The Coun- cil is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. C. D. Mote, Jr., are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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COMMITTEE ON SPORTS-RELATED CONCUSSIONS IN YOUTH ROBERT GRAHAM (Chair), Director, National Program Office, Aligning Forces for Quality, and Research Professor of Health Policy, School of Public Health and Health Services, George Washington University, Washington, DC FREDERICK P. RIVARA (Vice Chair), Seattle Children’s Guild Endowed Chair in Pediatrics and Professor, Pediatrics, School of Medicine, University of Washington, Seattle KRISTY B. ARBOGAST, Engineering Core Director, Center for Injury Research and Prevention, Children’s Hospital of Philadelphia, and Associate Professor of Pediatrics, University of Pennsylvania DAVID A. BRENT, Academic Chief, Child and Adolescent Psychiatry, Western Psychiatric Institute and Clinic, and Professor of Psychiatry, Pediatrics, and Epidemiology, School of Medicine, University of Pittsburgh B. J. CASEY, Sackler Professor of Developmental Psychobiology and Director, Sackler Institute for Developmental Psychobiology, Weill Medical College of Cornell University, New York, New York TRACEY COVASSIN, Associate Professor of Kinesiology and Undergraduate Athletic Training Program Director, Michigan State University, Lansing JOE DOYLE, former Regional Manager, American Development Model, Rocky Mountain and Pacific Districts, USA Hockey, Colorado Springs, Colorado ERIC J. HUANG, Professor of Pathology and Neuropathology, Department of Pathology, School of Medicine, University of California, San Francisco ARTHUR C. MAERLENDER, Director, Pediatric Neuropsychological Services, and Assistant Professor, Department of Psychiatry, Geisel School of Medicine, Dartmouth College, Hanover, New Hampshire SUSAN S. MARGULIES, George H. Stephenson Professor in Bioengineering, Department of Bioengineering, University of Pennsylvania, Philadelphia DENNIS L. MOLFESE, Mildred Francis Thompson Professor and Director, Center for Brain, Biology, and Behavior, Department of Psychology, University of Nebraska, Lincoln MAYUMI L. PRINS, Associate Professor in Residence and Director, Brain Injury Research Center Education Program, David Geffen School of Medicine, University of California, Los Angeles v

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NEHA P. RAUKAR, Assistant Professor of Emergency Medicine, and Director, Division of Sports Medicine, Warren Alpert School of Medicine, Brown University, Providence, Rhode Island NANCY R. TEMKIN, Professor, Departments of Biostatistics and Neurological Surgery, University of Washington, Seattle KASISOMAYAJULA VISWANATH, Associate Professor of Social and Behavioral Sciences, Harvard School of Public Health, and Director, Health Communication Core, Dana-Farber/Harvard Cancer Center, Boston, Massachusetts KEVIN D. WALTER, Associate Professor, Departments of Orthopaedic Surgery and Pediatrics, Medical College of Wisconsin, Milwaukee JOSEPH L. WRIGHT, Senior Vice President, Community Affairs, Children’s National Medical Center, and Professor of Pediatrics (Vice Chair), Emergency Medicine and Health Policy, George Washington University, Washington, DC Study Staff MORGAN A. FORD, Study Director CAROL MASON SPICER, Associate Program Officer WENDY KEENAN, Program Associate (through April 2013) SAMANTHA ROBOTHAM, Senior Program Assistant PAMELLA ATAYI, Administrative Assistant KIMBER BOGARD, Director, Board on Children, Youth, and Families vi

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Reviewers This report has been reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise, in accordance with procedures approved by the National Research Council’s Report Review Committee. The purpose of this independent review is to provide candid and critical comments that will assist the institution in making its published report as sound as possible and to ensure that the report meets institutional standards for objectivity, evidence, and responsiveness to the study charge. The review comments and draft manuscript remain confidential to protect the integrity of the deliberative process. We wish to thank the following individuals for their review of this report: Gordon Bloom, McGill University R. Dawn Comstock, University of Colorado, Denver Joseph J. Trey Crisco, Brown University John DiFiori, University of California, Los Angeles Corey S. Goodman, venBio LLC Michael V. Johnston, Johns Hopkins University Matthew W. Kreuter, Washington University Brad G. Kurowski, University of Cincinnati Karen McAvoy, Rocky Mountain Youth Sports Medicine Institute Tamara C. Valovich McLeod, A.T. Still University Barclay Morrison, Columbia University Cara Camiolo Reddy, University of Pittsburgh Thomas L. Schwenk, University of Nevada vii

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viii REVIEWERS CAPT Jack W. Tsao, Uniformed Services University of the Health Sciences Keith O. Yeates, Nationwide Children’s Hospital Although the reviewers listed above have provided many constructive comments and suggestions, they were not asked to endorse the conclusions or recommendations nor did they see the final draft of the report before its release. The review of this report was overseen by Bradford H. Gray, The Urban Institute, and Floyd E. Bloom, The Scripps Research Institute. Ap- pointed by the National Research Council and the Institute of Medicine, they were responsible for making certain that an independent examination of this report was carried out in accordance with institutional procedures and that all review comments were carefully considered. Responsibility for the final content of this report rests entirely with the authoring committee and the institution.

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Acknowledgments The Institute of Medicine-National Research Council (IOM-NRC) Committee on Sports-Related Concussions in Youth and its supporting staff thank the colleagues, organizations, and agencies that shared their expertise and information during the committee’s information-gathering meetings (see Appendix A for the names of the speakers). Their contribu- tions informed the committee’s deliberations and enhanced the quality of this report. The study sponsors gladly provided information and responded to questions. The committee also thanks the National Collegiate Athletic Association and the Datalys Center for Sports Injury Research and Pre- vention, Inc., and Dawn Comstock (University of Colorado, Denver) for responding to questions and providing concussion incidence data for use in the committee’s report. The IOM-NRC staff, including board director Kimber Bogard, study director Morgan Ford, associate program officer Carol Mason Spicer, as well as Wendy Keenan, Samantha Robotham, Pamella Atayi, Colin Fink, and Daniel Bearss, were central in shepherding the report though all its stages. The committee would also like to thank study consultant Stefan Duma (Virginia Tech–Wake Forest University), for preparing a background paper to inform the committee’s deliberations on the effectiveness of helmets to reduce sports-related concussions in youth. The committee and staff extend their gratitude to Laura DeStefano, Nicole Joy, and Abbey Meltzer, IOM Office of Reports and Communications, and Jennifer Walsh, Office of News and Public Information, for their assistance with report release and communication activities. Last but not least, the committee and staff thank Clyde Behney, Interim Leonard D. Schaeffer Executive Officer of the IOM, for the guidance he provided throughout this important study. ix

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Contents Abbreviations and acronyms xvii SUMMARY 1 1 INTRODUCTION 19 Committee’s Approach to Its Charge, 22 Overview of Core Issues, 25 Report Organization, 46 Findings, 47 References, 48 2 neuroscience, biomechanics, and risks of concussion in the developing brain 55 Normal Brain Development, 55 Biomechanics of Concussion, 59 Neurochemistry of Concussion, 67 Risk Factors for Concussion in the Developing Brain, 80 Findings, 83 References, 84 3  concussion recognition, diagnosis, and acute management 99 Sideline Assessment, 99 Clinical Evaluation, 102 Neuropsychological Testing, 114 xi

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xii CONTENTS Acute Concussion Management, 154 Findings, 162 References, 164 4  treatment and management of prolonged symptoms and post-concussion syndrome 181 Diagnostic Definition, 182 Short-Term Predictors of a Prolonged Symptomatic Period Post Concussion, 182 Symptomatology in Prolonged Recovery and Post-Concussion Syndrome, 185 Clinical Management of Prolonged Symptoms and Post-Concussion Syndrome, 191 Effects of Prolonged Recovery on Family, 193 Access to Care for Individuals with Prolonged Recovery, 194 Findings, 195 References, 195 5  Consequences of repetitive head impacts and multiple concussionS 203 Neuropsychological and Neurophysiological Consequences, 203 Multiple Concussions and Depression and Suicide, 212 Experimental Models, 215 Biomarkers and Risk Factors, 218 Long-Term Neurodegenerative Consequences, 220 Findings, 226 References, 227 6 protection and prevention strategies 239 Protective Equipment, 239 Sports Rules, 257 Concussion Education, 260 State Concussion Legislation, 265 Findings, 272 References, 273 7 Conclusions and Recommendations 285 Surveillance, 285 Evidence-Based Guidelines for Concussion Diagnosis and Management, 286 Short- and Long-Term Consequences of Concussions and Repetitive Head Impacts, 287 Age-Appropriate Rules and Playing Standards, 288

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CONTENTS xiii Biomechanics, Protective Equipment, and Safety Standards, 289 Culture Change, 289 Partnerships, 290 AppendixES A PUBLIC WORKSHOP AGENDAS 293 B biographical sketches of committee members 299 C CLINICAL EVALUATION TOOLS 309

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Boxes, Figures, and Tables Boxes S-1 Committee’s Recommendations, 14 1-1 Statement of Task, 21 2-1  Overview of Commonly Used Experimental Models of Traumatic Brain Injury, 68 3-1 Imaging Techniques, 103 Figures 1-1 Relationship of concussions to the spectrum of traumatic brain injury, 23 2-1 Profiles of parameters of human brain development and the estimated age ranges for research animal models, 56 2-2 Neurochemical cascade observed after moderate traumatic brain injuries, 69 3-1 Factors that impact the results of neuropsychological tests, 117 4-1 Symptom recovery curve, 187 4-2 Cognitive recovery curve, 188 xv

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xvi BOXES, FIGURES, AND TABLES 4-3 Postural stability recovery curve, 189 6-1 Injury risk curve relating a mechanical parameter such as head acceleration to the probability of injury, 243 6-2  graph showing the types of health care providers permitted Bar to make return-to-play decisions, according to state laws as of December 2012, 268 C-1 Standardized assessment of concussion, 311 C-2 Demonstration and test cards for King-Devick (K-D) test, 313 C-3 Page one of the acute concussion evaluation form, 317 C-4 Concussion symptom inventory, 318 C-5 Graded symptom checklist, 319 C-6 Post-concussion scale, 322 Tables S-1 Reported Concussion Rates by Sport, Sex, and Competition Level (High School and College) (Rates per 10,000 Athletic Exposures), 4 1-1 Primary Surveillance Systems for Sports-Related Concussion Data, 30 1-2 Reported Concussion Rates by Sport, Sex, and Competition Level (High School and College) (Rates per 10,000 Athletic Exposures), 34 1-3 Sports- and Recreation-Related Activities Most Commonly Associated with Emergency Department Visits for Nonfatal TBIs by Age and Sex—NEISS-AIP, United States, 2001-2009, 40 3-1 Signs and Symptoms of Concussions Relevant to Sideline Assessment, 100 3-2 Sideline Concussion Screening Tools, 102 3-3 Concussion Symptoms by Category, 105 3-4 Measures of Post-Concussion Symptomatology, 112 3-5 Common Computerized Neuropsychological Tests, 130 3-6 Reliability Studies on Common Neuropsychological Tests, 132 3-7 Validity Studies on Common Neuropsychological Tests, 142 3-8 Graded Return-to-Play Protocol, 160 C-1 Glasgow Coma Scale, 310

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Abbreviations and Acronyms ACE Acute Concussion Evaluation AE athletic exposure AIS Abbreviated Injury Scale ALS amyotrophic lateral sclerosis ANAM Automated Neuropsychological Assessment Metrics APOE apolipoprotein E APP amyloid precursor protein ATD anthropomorphic test device ATP adenosine triphosphate BESS Balance Error Scoring System CBF cerebral blood flow CBT cognitive behavioral therapy CCAT Computerized Cognitive Assessment Tool CCI controlled cortical impact CDC Centers for Disease Control and Prevention CI confidence interval CMRglc cerebral metabolic rate of glucose consumption CNS central nervous system CPSC Consumer Product Safety Commission CRI Concussion Resolution Index CSI Concussion Symptom Inventory CT computed tomography CTE chronic traumatic encephalopathy xvii

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xviii ABBREVIATIONS AND ACRONYMS CTP cleaved tau protein DNA deoxyribonucleic acid DTI diffusion tensor imaging ED emergency department EE enriched environment EEG electroencephalogram ERP event-related potential FA fractional anisotropy fMRI functional magnetic resonance imaging FTLD frontotemporal lobar degeneration GCS Glasgow Coma Scale GSC/GSS Graded Symptom Checklist/Scale HBI Health and Behavior Inventory HIT Head Impact Telemetry ICC intraclass correlation coefficient IEP individualized educational plan ImPACT Immediate Post-Concussion Assessment and Cognitive Testing iNOS inducible isoform of nitric oxide synthase IOM Institute of Medicine MACE Military Acute Concussion Evaluation MD mean diffusivity MRI magnetic resonance imaging MRS magnetic resonance spectroscopy mTBI mild traumatic brain injury MWM Morris water maze NAA N-Acetylaspartic acid NC non-concussed NCAA National Collegiate Athletic Association NCAA ISS National Collegiate Athletic Association Injury Surveillance System NEISS-AIP National Electronic Injury Surveillance System—All Injury Program NFHS National Federation of State High School Associations

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ABBREVIATIONS AND acronyms xix NFL National Football League NFT neurofibrillary tangle NHIS National Health Interview Survey NHL National Hockey League NMDA N-methyl-D-aspartate NOCSAE National Operating Committee on Standards for Athletic Equipment NOR novel object recognition NSE neuron-specific enolase OR odds ratio OSSAA Oklahoma Secondary School Activities Association PARP poly-ADP ribose polymerase PCS post-concussion syndrome PCSI Post-Concussion Symptom Inventory PCSS Post-Concussion Symptom Scale PET positron emission tomography PR prolonged recovery PTSD posttraumatic stress disorder QEEG quantitative EEG RCT randomized controlled trial RIO Reporting Information Online ROS reactive oxygen species RPCSQ Rivermead Post-Concussion Symptoms Questionnaire SAC Standardized Assessment of Concussion SAT Scholastic Aptitude Test SCAT Sport Concussion Assessment Tool SLAM Sports as a Laboratory Assessment Model SOT Sensory Organization Test TBI traumatic brain injury TR typical recovery VA Department of Veterans Affairs

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