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The Diagnosis and Management of Concussion in Children and Adolescents

      Abstract

      Background

      Concussion is a complex brain injury that results in more than 100,000 emergency department visits for school-aged children each year in the United States. All 50 US states have passed concussion legislation designed to promote safety in youth sports. Most of these laws require medical clearance by a licensed health care provider before returning to sport, which may have contributed to an increase in pediatric subspecialty referrals, particularly referrals to the child neurologist.

      Methods

      We reviewed the literature on pediatric concussion.

      Results

      This review summarizes the current knowledge and recommendations for concussion diagnosis and management in children and adolescents, athletes and nonathletes. It highlights concussion epidemiology, pathophysiology, advances in neuroimaging, and potential health risks including second impact syndrome and chronic traumatic encephalopathy. It also underscores clinical areas where evidence is lacking.

      Conclusions

      The diagnosis and management of concussion requires specific considerations in children. Further concussion research must be done to minimize injury risk and to optimize medical care for this common problem.

      Keywords

      Introduction

      While playing a junior high school football game in 2006, 13-year-old Zackery Lystedt tackled an opposing player late in the second quarter. The collision caused his head to strike the ground. He was removed from the game with a severe headache. Zackery returned to play in the third quarter, and near the end of the game he collapsed on the field. Airlifted to a level 1 trauma center, doctors performed an emergent neurosurgical procedure to alleviate cerebral edema. It would be nearly 3 years before Zackery would stand again, with assistance.
      Centers for Disease Control and Prevention
      Zack's Story: CDC highlights Washington sports concussion law.
      Discouraged that their son was not properly evaluated following his initial on-field head injury, Zackery's family worked with many individuals including members of the Washington State Congress and the Centers for Disease Control and Prevention to enact a bill that could help prevent similar injuries in youth athletes. On May 14, 2009, the Zackery Lystedt Law was passed in Washington State.

      Zackery Lystedt Law, Washington State House Bill 1824, Rodne, Quall, Anderson et al., (2009).

      The law requires that student athletes be removed from competition when a head injury is suspected. The athlete may return to play only after receiving written clearance from a licensed healthcare provider.

      Zackery Lystedt Law, Washington State House Bill 1824, Rodne, Quall, Anderson et al., (2009).

      Following passage of the Zackery Lystedt Law, other states began enacting similar youth concussion legislation. As of February 2014, all 50 states and the District of Columbia had passed concussion laws designed to help protect youth athletes.
      National Conference of State Legislatures
      Traumatic Brain Injury Legislation.
      Most of these laws require that a licensed health care provider evaluates the athlete following injury and medically clear him or her before returning to sport. The new legislation promotes safety in youth sports. It also may promote greater health care utilization. From 2006 to 2012, states with concussion laws in effect had a 10% increase in health care utilization for concussions compared with states without active legislation, and the rates of pediatric concussion referrals to neurologists have increased steadily compared with the 2008-2009 rates, up 36% in 2009-2010, 84% in 2010-2011, and 150% in 2011-2012.
      • Gibson T.B.
      • Herring S.A.
      • Kutcher J.S.
      • Broglio S.P.
      Analyzing the Effect of State Legislation on Health Care Utilization for Children With Concussion.
      The following review summarizes the current knowledge and consensus guidelines in youth concussion. It is written to aid health professionals in the diagnosis and clinical management of the pediatric patient with concussion.

      Concussion definition and epidemiology

      The American Academy of Neurology defines concussion as a biomechanically induced clinical syndrome related to alterations in brain function that can affect memory and orientation.
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      • Kutcher J.S.
      • Ashwal S.
      • et al.
      Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology.
      The injury can be caused by a direct blow to the head, face, or neck or by a blow elsewhere to the body with force transmitted to the head.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      Loss of consciousness occurs in only 8%-19% of concussions and is not a defining feature.
      • Collins M.W.
      • Iverson G.L.
      • Lovell M.R.
      • McKeag D.B.
      • Norwig J.
      • Maroon J.
      On-field predictors of neuropsychological and symptom deficit following sports-related concussion.
      • Schulz M.R.
      • Marshall S.W.
      • Mueller F.O.
      • et al.
      Incidence and risk factors for concussion in high school athletes, North Carolina, 1996-1999.
      Concussion symptoms typically resolve within 7-10 days, but a minority of patients report symptoms that persist for months, even years.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      Children may take longer to recover than adults. Most clinicians consider concussion to represent a subset of mild traumatic brain injury (TBI), defined as a Glasgow Coma Scale score of 13-15, loss of consciousness of less than 30 minutes (if present), and posttraumatic amnesia of 24 hours (if present).
      • Carroll L.J.
      • Cassidy J.D.
      • Holm L.
      • Kraus J.
      • Coronado V.G.
      Methodological issues and research recommendations for mild traumatic brain injury: the WHO Collaborating Centre Task Force on Mild Traumatic Brain Injury.
      Symptom grading scales for concussion severity are no longer recommended because they are poorly predictive of outcome.
      • Giza C.C.
      • Kutcher J.S.
      • Ashwal S.
      • et al.
      Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology.
      “Subconcussive” impacts, defined as biomechanically induced injuries to the brain that do not result in clinical symptoms, may have a cumulative effect leading to chronic traumatic brain injury in some adult patients.
      • Rabadi M.H.
      • Jordan B.D.
      The cumulative effect of repetitive concussion in sports.
      Little is known about subconcussive injuries in youth.
      It is estimated that 1.6-3.8 million sport-related TBIs occur in the United States each year; the majority of these injuries represent mild TBI and concussion.
      • Langlois J.A.
      • Rutland-Brown W.
      • Wald M.M.
      The epidemiology and impact of traumatic brain injury: a brief overview.
      Concussions result in more than 100,000 emergency department visits each year for school-aged children in the United States.
      • Meehan III, W.P.
      • Mannix R.
      Pediatric concussions in United States emergency departments in the years 2002 to 2006.
      Approximately 1 in every 220 pediatric patients seen in the emergency department is diagnosed with concussion, and 30%-50% of the concussions are sports-related.
      • Meehan III, W.P.
      • Mannix R.
      Pediatric concussions in United States emergency departments in the years 2002 to 2006.
      • Bakhos L.L.
      • Lockhart G.R.
      • Myers R.
      • Linakis J.G.
      Emergency department visits for concussion in young child athletes.
      Additionally, concussion represents approximately 9% of all high school sports injuries.
      • Gessel L.M.
      • Fields S.K.
      • Collins C.L.
      • Dick R.W.
      • Comstock R.D.
      Concussions among United States high school and collegiate athletes.
      The overall incidence of youth concussion is not known because some injuries go unrecognized and some patients do not seek medical care.
      • Langlois J.A.
      • Rutland-Brown W.
      • Wald M.M.
      The epidemiology and impact of traumatic brain injury: a brief overview.
      Although boys may have more sports-related concussions overall, girls appear to have a higher concussion risk when comparing similar sports.
      • Lincoln A.E.
      • Caswell S.V.
      • Almquist J.L.
      • Dunn R.E.
      • Norris J.B.
      • Hinton R.Y.
      Trends in concussion incidence in high school sports: a prospective 11-year study.
      • Marar M.
      • McIlvain N.M.
      • Fields S.K.
      • Comstock R.D.
      Epidemiology of concussions among United States high school athletes in 20 sports.
      • Powell J.W.
      • Barber-Foss K.D.
      Traumatic brain injury in high school athletes.
      Sports differ in terms of concussion risks between genders: football, ice hockey, lacrosse, and wrestling have the highest risks for boys; soccer, lacrosse, ice hockey, field hockey, and basketball have the highest risks for girls.
      • Marar M.
      • McIlvain N.M.
      • Fields S.K.
      • Comstock R.D.
      Epidemiology of concussions among United States high school athletes in 20 sports.
      • Agel J.
      • Harvey E.J.
      A 7-year review of men's and women's ice hockey injuries in the NCAA.
      It is unclear whether age or level of competition affects concussion risk, but concussion rates tend to be higher in games than in practices.
      • Gessel L.M.
      • Fields S.K.
      • Collins C.L.
      • Dick R.W.
      • Comstock R.D.
      Concussions among United States high school and collegiate athletes.
      • Marar M.
      • McIlvain N.M.
      • Fields S.K.
      • Comstock R.D.
      Epidemiology of concussions among United States high school athletes in 20 sports.
      • Guskiewicz K.M.
      • Weaver N.L.
      • Padua D.A.
      • Garrett Jr., W.E.
      Epidemiology of concussion in collegiate and high school football players.

      Pathophysiology

      Concussion represents a functional, rather than a structural, brain injury.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      Seminal studies have demonstrated that acceleration-deceleration and rotational forces related to head impact can induce concussion.
      • Ommaya A.K.
      • Gennarelli T.A.
      Cerebral concussion and traumatic unconsciousness. Correlation of experimental and clinical observations of blunt head injuries.
      • Denny-Brown D.
      • Russell W.R.
      Experimental cerebral concussion.
      The pathophysiology of brain dysfunction results from an abnormal neurometabolic cascade. This begins with the disruption of neuronal cell membranes, potassium efflux, and glutamate release.
      • Katayama Y.
      • Becker D.P.
      • Tamura T.
      • Hovda D.A.
      Massive increases in extracellular potassium and the indiscriminate release of glutamate following concussive brain injury.
      Ion pumps use adenosine triphosphate to restore the normal cellular membrane potentials. The increase in cellular adenosine triphosphate metabolism following injury can produce a relative energy deficit, with a consequent depression of neuronal activity.
      • Yoshino A.
      • Hovda D.A.
      • Kawamata T.
      • Katayama Y.
      • Becker D.P.
      Dynamic changes in local cerebral glucose utilization following cerebral conclusion in rats: evidence of a hyper- and subsequent hypometabolic state.
      Additionally, intracellular calcium accumulation, mitochondrial dysfunction, free radical production, impaired glucose metabolism, cytoskeletal injury, abnormal axonal transport, and alterations in neurotransmission all can contribute to the altered neurometabolic state.
      • Yoshino A.
      • Hovda D.A.
      • Kawamata T.
      • Katayama Y.
      • Becker D.P.
      Dynamic changes in local cerebral glucose utilization following cerebral conclusion in rats: evidence of a hyper- and subsequent hypometabolic state.
      • Vagnozzi R.
      • Marmarou A.
      • Tavazzi B.
      • et al.
      Changes of cerebral energy metabolism and lipid peroxidation in rats leading to mitochondrial dysfunction after diffuse brain injury.
      • Xiong Y.
      • Gu Q.
      • Peterson P.L.
      • Muizelaar J.P.
      • Lee C.P.
      Mitochondrial dysfunction and calcium perturbation induced by traumatic brain injury.
      • Pettus E.H.
      • Christman C.W.
      • Giebel M.L.
      • Povlishock J.T.
      Traumatically induced altered membrane permeability: its relationship to traumatically induced reactive axonal change.
      • Miller L.P.
      • Lyeth B.G.
      • Jenkins L.W.
      • et al.
      Excitatory amino acid receptor subtype binding following traumatic brain injury.
      • Gorman L.K.
      • Fu K.
      • Hovda D.A.
      • Murray M.
      • Traystman R.J.
      Effects of traumatic brain injury on the cholinergic system in the rat.
      • Pappius H.M.
      Significance of biogenic amines in functional disturbances resulting from brain injury.
      Regional changes in cerebral blood flow may exacerbate the energy crisis.
      • Yuan X.Q.
      • Prough D.S.
      • Smith T.L.
      • Dewitt D.S.
      The effects of traumatic brain injury on regional cerebral blood flow in rats.
      These physiologic perturbations correlate with clinical features of concussion including the increase in concussion vulnerability early after injury and the gradually resolving neurocognitive symptoms.
      • Giza C.C.
      • Hovda D.A.
      The new neurometabolic cascade of concussion.
      Injury to the young, developing brain may be associated with greater risk of long-term functional impairments because of altered neuronal plasticity and immature myelination.
      • Fineman I.
      • Giza C.C.
      • Nahed B.V.
      • Lee S.M.
      • Hovda D.A.
      Inhibition of neocortical plasticity during development by a moderate concussive brain injury.
      • Ajao D.O.
      • Pop V.
      • Kamper J.E.
      • et al.
      Traumatic brain injury in young rats leads to progressive behavioral deficits coincident with altered tissue properties in adulthood.
      Following a concussive injury, there is a brief temporal window of increased concussion vulnerability in the animal model that appears to resolve gradually during 7-10 days. Longhi and colleagues demonstrated that adult mice with concussive injuries had significantly greater functional impairments with repeat injuries at 3 or 5 days compared with 7 days, suggesting that the vulnerability to repeat concussion in the animal model diminishes within 7 days from the initial TBI.
      • Longhi L.
      • Saatman K.E.
      • Fujimoto S.
      • et al.
      Temporal window of vulnerability to repetitive experimental concussive brain injury.
      Vestibular dysfunction and axonal injury were worse when the impacts were spaced only 3 days apart. In juvenile rats, repeat concussions spaced 1 day apart caused greater cumulative memory impairments, whereas concussions spaced 5 days apart led to memory impairments that were similar to the initial injury.
      • Prins M.L.
      • Alexander D.
      • Giza C.C.
      • Hovda D.A.
      Repeated mild traumatic brain injury: mechanisms of cerebral vulnerability.
      Fewer data about the duration of increased concussion vulnerability are available in humans. Maugans and colleagues found diminished cerebral blood flow in concussed children aged 11-15 years compared with controls.
      • Maugans T.A.
      • Farley C.
      • Altaye M.
      • Leach J.
      • Cecil K.M.
      Pediatric sports-related concussion produces cerebral blood flow alterations.
      Cerebral blood flow values in their study improved over time; 27% matched the control values by 14 days postinjury, 64% after 30 days.
      Loss of cell membrane integrity with concussion may cause leakage of some neuronal and glial cell components. The cellular components that are detectable in serum could serve as biomarkers for the concussive injury and injury recovery. Biomarker studies have yielded inconsistent results evaluating S100 calcium-binding protein B, neuron-specific enolase, tau protein, neurofilament light protein, amyloid beta protein, myelin basic protein, and glial fibrillary acidic protein.
      • Babcock L.
      • Byczkowski T.
      • Wade S.L.
      • Ho M.
      • Bazarian J.J.
      Inability of S100B to predict postconcussion syndrome in children who present to the emergency department with mild traumatic brain injury: a brief report.
      • Berger R.P.
      • Beers S.R.
      • Richichi R.
      • Wiesman D.
      • Adelson P.D.
      Serum biomarker concentrations and outcome after pediatric traumatic brain injury.
      • Geyer C.
      • Ulrich A.
      • Grafe G.
      • Stach B.
      • Till H.
      Diagnostic value of S100B and neuron-specific enolase in mild pediatric traumatic brain injury.
      • Mannix R.
      • Eisenberg M.
      • Berry M.
      • Meehan III, W.P.
      • Hayes R.L.
      Serum biomarkers predict acute symptom burden in children after concussion: a preliminary study.
      • Shahim P.
      • Tegner Y.
      • Wilson D.H.
      • et al.
      Blood biomarkers for brain injury in concussed professional ice hockey players.
      S100 calcium-binding protein B and neuron-specific enolase levels drawn within 6 hours of mild TBI did not differ between symptomatic and asymptomatic children aged 6 months to 15 years.
      • Geyer C.
      • Ulrich A.
      • Grafe G.
      • Stach B.
      • Till H.
      Diagnostic value of S100B and neuron-specific enolase in mild pediatric traumatic brain injury.
      S100 calcium-binding protein B levels drawn within 6 hours of concussion did not predict postconcussion symptoms 3 months later.
      • Babcock L.
      • Byczkowski T.
      • Wade S.L.
      • Ho M.
      • Bazarian J.J.
      Inability of S100B to predict postconcussion syndrome in children who present to the emergency department with mild traumatic brain injury: a brief report.
      In contrast, elevated serum glial fibrillary acidic protein levels measured within 24 hours of injury predicted greater symptom burdens at 1 month following concussive injury in a cohort of children aged 11-17 years.
      • Mannix R.
      • Eisenberg M.
      • Berry M.
      • Meehan III, W.P.
      • Hayes R.L.
      Serum biomarkers predict acute symptom burden in children after concussion: a preliminary study.
      Immediately after concussion, professional hockey players had increases in serum tau protein and S100 calcium-binding protein B levels compared with their preseason values, but neuron-specific enolase levels did not differ.
      • Shahim P.
      • Tegner Y.
      • Wilson D.H.
      • et al.
      Blood biomarkers for brain injury in concussed professional ice hockey players.
      Currently, serum biomarkers are not recommended for clinical diagnosis or management.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      • Broglio S.P.
      • Cantu R.C.
      • Gioia G.A.
      • et al.
      National Athletic Trainers' Association position statement: management of sport concussion.
      • Papa L.
      • Ramia M.M.
      • Edwards D.
      • Johnson B.D.
      • Slobounov S.
      Systematic Review of Clinical Studies Examining Biomarkers of Brain Injury in Athletes Following Sports-Related Concussion.

      Neuroimaging

      As concussion represents a functional brain injury, standard neuroimaging, computed tomography (CT) and magnetic resonance imaging (MRI), is normal.
      • Giza C.C.
      • Kutcher J.S.
      • Ashwal S.
      • et al.
      Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      • Broglio S.P.
      • Cantu R.C.
      • Gioia G.A.
      • et al.
      National Athletic Trainers' Association position statement: management of sport concussion.
      • Halstead M.E.
      • Walter K.D.
      American Academy of Pediatrics. Clinical report–sport-related concussion in children and adolescents.
      • Harmon K.G.
      • Drezner J.
      • Gammons M.
      • et al.
      American Medical Society for Sports Medicine position statement: concussion in sport.
      We do not recommend neuroimaging to diagnose acute concussion. Imaging should be considered when a moderate or severe TBI or intracranial hemorrhage is suspected, there is evidence of a skull fracture, or when multiple or severe bodily injuries are also present.
      • Giza C.C.
      • Kutcher J.S.
      • Ashwal S.
      • et al.
      Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology.
      • Jagoda A.S.
      • Bazarian J.J.
      • Bruns Jr., J.J.
      • et al.
      Clinical policy: neuroimaging and decisionmaking in adult mild traumatic brain injury in the acute setting.
      Imaging also should be considered for concussed patients who use anticoagulation medicines or have an increased risk of bleeding.
      • Jagoda A.S.
      • Bazarian J.J.
      • Bruns Jr., J.J.
      • et al.
      Clinical policy: neuroimaging and decisionmaking in adult mild traumatic brain injury in the acute setting.
      The term “complicated mild TBI” refers to patients who have clinically mild brain injuries and signs of traumatic injury with conventional neuroimaging.
      • Iverson G.L.
      • Lovell M.R.
      • Smith S.
      • Franzen M.D.
      Prevalence of abnormal CT-scans following mild head injury.
      • Williams D.H.
      • Levin H.S.
      • Eisenberg H.M.
      Mild head injury classification.
      The incidence of complicated mild TBI among adult patients ranges from 9% to 27%.
      • Iverson G.L.
      • Lovell M.R.
      • Smith S.
      • Franzen M.D.
      Prevalence of abnormal CT-scans following mild head injury.
      • Jeret J.S.
      • Mandell M.
      • Anziska B.
      • et al.
      Clinical predictors of abnormality disclosed by computed tomography after mild head trauma.
      • Yuh E.L.
      • Mukherjee P.
      • Lingsma H.F.
      • et al.
      Magnetic resonance imaging improves 3-month outcome prediction in mild traumatic brain injury.
      The incidence in children is not known. The MRI susceptibility-weighted imaging sequence has better sensitivity than CT in detecting small brain contusions, hemorrhagic axonal injury, and other traumatic hemorrhagic injuries.
      • Beauchamp M.H.
      • Ditchfield M.
      • Babl F.E.
      • et al.
      Detecting traumatic brain lesions in children: CT versus MRI versus susceptibility weighted imaging (SWI).
      Among 135 patients with mild TBI and normal CT scans, 28% had intracranial injury detected by MRI. Patients with MRI-detected hemorrhage had poorer 3-month clinical outcomes than those without hemorrhage.
      • Yuh E.L.
      • Mukherjee P.
      • Lingsma H.F.
      • et al.
      Magnetic resonance imaging improves 3-month outcome prediction in mild traumatic brain injury.
      Cerebral atrophy is found inconsistently among patients with mild TBI. Most studies demonstrating atrophy have included moderate and severe TBI patients or patients with extensive mild TBI exposure.
      • Shenton M.E.
      • Hamoda H.M.
      • Schneiderman J.S.
      • et al.
      A review of magnetic resonance imaging and diffusion tensor imaging findings in mild traumatic brain injury.
      In a study of collegiate football players, hippocampal volume loss correlated with the number of years playing football and the number of prior sports concussions.
      • Singh R.
      • Meier T.B.
      • Kuplicki R.
      • et al.
      Relationship of collegiate football experience and concussion with hippocampal volume and cognitive outcomes.
      Football players without a history of concussion also had smaller hippocampal volumes compared with control subjects who did not play football. Investigators have not found consistent correlations between MRI volume abnormalities and neurocognitive outcomes.
      • Yuh E.L.
      • Mukherjee P.
      • Lingsma H.F.
      • et al.
      Magnetic resonance imaging improves 3-month outcome prediction in mild traumatic brain injury.
      • Lee H.
      • Wintermark M.
      • Gean A.D.
      • Ghajar J.
      • Manley G.T.
      • Mukherjee P.
      Focal lesions in acute mild traumatic brain injury and neurocognitive outcome: CT versus 3T MRI.
      Various advanced neuroimaging techniques have demonstrated microstructural and functional brain abnormalities in concussed patients. Unfortunately, few findings have been consistent across studies. Diffusion tensor imaging, used to evaluate axonal integrity, has shown both decreased and increased fractional anisotropy following concussion.
      • Arfanakis K.
      • Haughton V.M.
      • Carew J.D.
      • Rogers B.P.
      • Dempsey R.J.
      • Meyerand M.E.
      Diffusion tensor MR imaging in diffuse axonal injury.
      • Inglese M.
      • Makani S.
      • Johnson G.
      • et al.
      Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study.
      • Bazarian J.J.
      • Zhu T.
      • Blyth B.
      • Borrino A.
      • Zhong J.
      Subject-specific changes in brain white matter on diffusion tensor imaging after sports-related concussion.
      • Virji-Babul N.
      • Borich M.R.
      • Makan N.
      • et al.
      Diffusion tensor imaging of sports-related concussion in adolescents.
      Many brain regions have been implicated, but the frontal and temporal association pathways seem particularly vulnerable to axonal injury.
      • Niogi S.N.
      • Mukherjee P.
      Diffusion tensor imaging of mild traumatic brain injury.
      Functional MRI, single photon emission CT, and positron emission tomography studies also have shown inconsistent abnormalities following concussion.
      • Lin A.P.
      • Liao H.J.
      • Merugumala S.K.
      • Prabhu S.P.
      • Meehan III, W.P.
      • Ross B.D.
      Metabolic imaging of mild traumatic brain injury.
      Task-based blood-oxygen-level dependent functional MRI has demonstrated hyperactivation in several brain networks after injury, but the apparent lack of neurocognitive deficits at the time of imaging makes its significance uncertain.
      • McAllister T.W.
      • Saykin A.J.
      • Flashman L.A.
      • et al.
      Brain activation during working memory 1 month after mild traumatic brain injury: a functional MRI study.
      • Jantzen K.J.
      • Anderson B.
      • Steinberg F.L.
      • Kelso J.A.
      A prospective functional MR imaging study of mild traumatic brain injury in college football players.
      • Dettwiler A.
      • Murugavel M.
      • Putukian M.
      • Cubon V.
      • Furtado J.
      • Osherson D.
      Persistent differences in patterns of brain activation after sports-related concussion: a longitudinal functional magnetic resonance imaging study.
      Resting state functional MRI in adolescents shows both increased and decreased connectivity in various brain networks.
      • Borich M.
      • Babul A.N.
      • Huang P.H.
      • Boyd L.
      • Virji-Babul N.
      Alterations in resting state brain networks in concussed adolescent athletes.
      MRI spectroscopy studies have shown decreased N-acetylaspartate peaks, especially in the corpus callosum, during concussion recovery.
      • Johnson B.
      • Gay M.
      • Zhang K.
      • et al.
      The use of magnetic resonance spectroscopy in the subacute evaluation of athletes recovering from single and multiple mild traumatic brain injury.
      • Vagnozzi R.
      • Signoretti S.
      • Cristofori L.
      • et al.
      Assessment of metabolic brain damage and recovery following mild traumatic brain injury: a multicentre, proton magnetic resonance spectroscopic study in concussed patients.
      Although some of the data are compelling, we do not currently recommend advanced imaging modalities for the assessment of patients with concussion beyond the research setting.

      Concussion symptoms and diagnosis

      Signs and symptoms

      Concussion is a clinical diagnosis. The injury can cause a variety of somatic, neurobehavioral, and cognitive signs and symptoms.
      • Piland S.G.
      • Motl R.W.
      • Guskiewicz K.M.
      • McCrea M.
      • Ferrara M.S.
      Structural validity of a self-report concussion-related symptom scale.
      Headache is probably the most common postconcussion symptom (affecting approximately 65%-93% of patients), followed by fatigue, dizziness, and slowed mentation (Table 1).
      • Eisenberg M.A.
      • Meehan III, W.P.
      • Mannix R.
      Duration and Course of Post-Concussive Symptoms.
      • Grubenhoff J.A.
      • Kirkwood M.W.
      • Deakyne S.
      • Wathen J.
      Detailed concussion symptom analysis in a paediatric ED population.
      • Lee Y.M.
      • Odom M.J.
      • Zuckerman S.L.
      • Solomon G.S.
      • Sills A.K.
      Does age affect symptom recovery after sports-related concussion? A study of high school and college athletes.
      • Meehan III, W.P.
      • d'Hemecourt P.
      • Comstock R.D.
      High school concussions in the 2008-2009 academic year: mechanism, symptoms, and management.
      Some symptoms develop rapidly after impact, whereas other symptoms can be delayed in onset or can evolve over hours or days following injury.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      If symptoms that had been stable abruptly worsen, the patient should be evaluated for more severe brain injury, specifically intracranial hemorrhage.
      Table 1Symptom Frequency in Pediatric Concussion
      Concussion SymptomsFrequency (%)
      Percentages obtained from references.68-71
      Headache65-93
      Fatigue55-82
      Dizziness, balance problems32-75
      Slowed mentation44-60
      Drowsiness27-60
      Difficulty concentrating30-57
      Nausea29-55
      Light sensitivity15-52
      Noise sensitivity17-49
      Forgetfulness34-42
      Blurry vision23-39
      Sleep disturbance12-38
      Irritability9-34
      Depression/sadness17-24
      Vomiting5-23
      Tinnitus8-19
      Percentages obtained from references.
      • Eisenberg M.A.
      • Meehan III, W.P.
      • Mannix R.
      Duration and Course of Post-Concussive Symptoms.
      • Grubenhoff J.A.
      • Kirkwood M.W.
      • Deakyne S.
      • Wathen J.
      Detailed concussion symptom analysis in a paediatric ED population.
      • Lee Y.M.
      • Odom M.J.
      • Zuckerman S.L.
      • Solomon G.S.
      • Sills A.K.
      Does age affect symptom recovery after sports-related concussion? A study of high school and college athletes.
      • Meehan III, W.P.
      • d'Hemecourt P.
      • Comstock R.D.
      High school concussions in the 2008-2009 academic year: mechanism, symptoms, and management.
      Concussion symptoms are nonspecific; many individuals who do not have a concussion experience headaches, dizziness, mood swings, or sadness. Baseline testing of healthy collegiate athletes demonstrated that 52%-83% of males and 75%-85% of females endorse one or more of the symptoms listed in the Post-Concussion Symptom Scale.
      • Valovich McLeod T.C.
      • Bay R.C.
      • Lam K.C.
      • Chhabra A.
      Representative baseline values on the Sport Concussion Assessment Tool 2 (SCAT2) in adolescent athletes vary by gender, grade, and concussion history.
      • Shehata N.
      • Wiley J.P.
      • Richea S.
      • Benson B.W.
      • Duits L.
      • Meeuwisse W.H.
      Sport concussion assessment tool: baseline values for varsity collision sport athletes.
      Similar assessments among high school athletes showed that 60% of males and 48% of females without concussion acknowledge at least one symptom, whereas nearly 10% of athletes acknowledge eight or more symptoms.
      • Jinguji T.M.
      • Bompadre V.
      • Harmon K.G.
      • et al.
      Sport Concussion Assessment Tool-2: baseline values for high school athletes.
      Individuals with premorbid depression or anxiety tend to report more baseline symptoms at greater levels of severity than individuals without depression or anxiety.
      • Putukian M.
      • Echemendia R.
      • Dettwiler-Danspeckgruber A.
      • et al.
      Prospective clinical assessment using sideline concussion assessment tool-2 testing in the evaluation of sport-related concussion in college athletes.
      The presence of premorbid symptoms can make the postinjury assessment difficult. Kutcher and Giza propose a clinical classification system for concussion based on the degree of diagnostic certainty, stratifying patients as “possible,” “probable,” or “definite” concussion.
      • Kutcher J.S.
      • Giza C.C.
      Sports concussion diagnosis and management.

      On-field and acute assessment

      When an acute concussion is suspected, three questions should be asked: (1) Is there a moderate or severe TBI? (2) Is there a cervical spine injury? (3) Is there a concussion?
      • Putukian M.
      • Raftery M.
      • Guskiewicz K.
      • et al.
      Onfield assessment of concussion in the adult athlete.
      Signs and symptoms of a moderate or severe TBI can include severe headache, prolonged loss of consciousness (>30 minutes), prolonged posttraumatic amnesia (>24 hours), progressive worsening of symptoms, impaired alertness, seizures, or focal neurological deficits.
      • Giza C.C.
      • Kutcher J.S.
      • Ashwal S.
      • et al.
      Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology.
      • Jagoda A.S.
      • Bazarian J.J.
      • Bruns Jr., J.J.
      • et al.
      Clinical policy: neuroimaging and decisionmaking in adult mild traumatic brain injury in the acute setting.
      The presence of these signs or symptoms warrants evaluation in an emergency department.
      • Putukian M.
      • Raftery M.
      • Guskiewicz K.
      • et al.
      Onfield assessment of concussion in the adult athlete.
      If a cervical spine injury is suspected or if the patient is unconscious, the spine should be stabilized.
      • Halstead M.E.
      • Walter K.D.
      American Academy of Pediatrics. Clinical report–sport-related concussion in children and adolescents.
      Absent evidence of a more severe TBI or spinal injury, further evaluation for concussion can proceed. Considered benign, acute motor phenomena can occur immediately following impact and may include tonic posturing, myoclonus, or righting movements (apparent attempt to return to an upright position while unconscious).
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      Loss of consciousness longer than 60 seconds increases the likelihood of tonic posturing.
      • McCrory P.R.
      • Berkovic S.F.
      Video analysis of acute motor and convulsive manifestations in sport-related concussion.
      Because concussion symptoms can evolve, serial evaluations should be performed over the next several hours.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      • Harmon K.G.
      • Drezner J.
      • Gammons M.
      • et al.
      American Medical Society for Sports Medicine position statement: concussion in sport.
      • Putukian M.
      • Raftery M.
      • Guskiewicz K.
      • et al.
      Onfield assessment of concussion in the adult athlete.
      Whenever a concussion is suspected, the youth athlete should be removed from play and cannot return to play that day and until cleared by an appropriate health care professional.
      • Giza C.C.
      • Kutcher J.S.
      • Ashwal S.
      • et al.
      Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      • Broglio S.P.
      • Cantu R.C.
      • Gioia G.A.
      • et al.
      National Athletic Trainers' Association position statement: management of sport concussion.
      • Halstead M.E.
      • Walter K.D.
      American Academy of Pediatrics. Clinical report–sport-related concussion in children and adolescents.
      • Harmon K.G.
      • Drezner J.
      • Gammons M.
      • et al.
      American Medical Society for Sports Medicine position statement: concussion in sport.
      • Putukian M.
      • Raftery M.
      • Guskiewicz K.
      • et al.
      Onfield assessment of concussion in the adult athlete.
      In the acute setting, nonsteroidal anti-inflammatory medications are avoided due to bleeding risk, as are medications that can affect mental status.

      Clinical assessment tools

      Several assessment tools have been developed to assist with concussion diagnosis and serial evaluation. These tools are meant to complement the clinical history and neurological examination, not to replace them. No tool should be used in isolation to diagnose a concussion or to clear a patient to return to activity. We describe several of the more commonly used instruments below. Our inclusion of an instrument should not be read as an endorsement or a recommendation for its use.
      The Standardized Assessment of Concussion evaluates orientation, concentration, immediate memory and delayed memory.
      • McCrea M.
      • Kelly J.P.
      • Kluge J.
      • Ackley B.
      • Randolph C.
      Standardized assessment of concussion in football players.
      It has a sensitivity of 80%-95% and specificity of 76%-91%.
      • McCrea M.
      Standardized Mental Status Testing on the Sideline After Sport-Related Concussion.
      • McCrea M.
      • Barr W.B.
      • Guskiewicz K.
      • et al.
      Standard regression-based methods for measuring recovery after sport-related concussion.
      The Sport Concussion Assessment Tool 3rd Edition, developed by the Concussion in Sport Group at the 2012 Zurich conference, can be used in athletes 13 years of age and older.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      It comprises several subtests including the Glasgow Coma Scale, the Maddocks Score (sport-related recall), a symptom scale, cognitive assessment, delayed recall, neck examination, and balance and coordination testing. For athletes 5-12 years old, a child Sport Concussion Assessment Tool 3rd Edition is available with age-appropriate questions and a section for parent report of the child's symptoms.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      Computerized neurocognitive tests can be helpful in concussion evaluation, particularly when preseason scoring is available. The costs of computerized testing can be a limiting factor, as most charge a fee per administration. The Immediate Post-Concussion Assessment and Cognitive Testing is a widely used computerized neurocognitive test. Different approaches at validating the Immediate Post-Concussion Assessment and Cognitive Testing have produced a range of diagnostic sensitivities (79%-91%) and specificities (69%-89%).
      • Broglio S.P.
      • Macciocchi S.N.
      • Ferrara M.S.
      Sensitivity of the concussion assessment battery.
      • Schatz P.
      • Pardini J.E.
      • Lovell M.R.
      • Collins M.W.
      • Podell K.
      Sensitivity and specificity of the ImPACT Test Battery for concussion in athletes.
      • Schatz P.
      • Sandel N.
      Sensitivity and specificity of the online version of ImPACT in high school and collegiate athletes.
      Test-retest reliability also varies.
      • Broglio S.P.
      • Ferrara M.S.
      • Macciocchi S.N.
      • Baumgartner T.A.
      • Elliott R.
      Test-retest reliability of computerized concussion assessment programs.
      • Resch J.
      • Driscoll A.
      • McCaffrey N.
      • et al.
      ImPact test-retest reliability: reliably unreliable?.
      • Elbin R.J.
      • Schatz P.
      • Covassin T.
      One-year test-retest reliability of the online version of ImPACT in high school athletes.
      Other computerized neurocognitive tests include the Automated Neuropsychological Assessment Metrics, CogSport/Axon, and the Concussion Resolution Index.
      • Collie A.
      • Darby D.
      • Maruff P.
      Computerised cognitive assessment of athletes with sports related head injury.
      • Collie A.
      • Maruff P.
      • Makdissi M.
      • McCrory P.
      • McStephen M.
      • Darby D.
      CogSport: reliability and correlation with conventional cognitive tests used in postconcussion medical evaluations.
      • Erlanger D.
      • Saliba E.
      • Barth J.
      • Almquist J.
      • Webright W.
      • Freeman J.
      Monitoring Resolution of Postconcussion Symptoms in Athletes: Preliminary Results of a Web-Based Neuropsychological Test Protocol.
      • Cernich A.
      • Reeves D.
      • Sun W.
      • Bleiberg J.
      Automated Neuropsychological Assessment Metrics sports medicine battery.
      Formalized measures of balance impairment and coordination impairment are available for on-field and office assessments. The Balance Error Scoring System is a clinical assessment measuring the number of balance corrections made while standing with the eyes closed: double-leg stances and single-leg stance (on a firm surface and on a piece of medium-density foam). Its sensitivity is 34%-60%,
      • McCrea M.
      • Barr W.B.
      • Guskiewicz K.
      • et al.
      Standard regression-based methods for measuring recovery after sport-related concussion.
      • Furman G.R.
      • Lin C.C.
      • Bellanca J.L.
      • Marchetti G.F.
      • Collins M.W.
      • Whitney S.L.
      Comparison of the balance accelerometer measure and balance error scoring system in adolescent concussions in sports.
      but a learning effect in young athletes can be seen.
      • Valovich McLeod T.C.
      • Perrin D.H.
      • Guskiewicz K.M.
      • Shultz S.J.
      • Diamond R.
      • Gansneder B.M.
      Serial administration of clinical concussion assessments and learning effects in healthy young athletes.
      The Sensory Organization Test measures balance but requires an expensive force plate system; the King-Devick test assesses visual-spatial and ocular motor function through reading numbers at varying spaces and positions; and the “drop-stick” test is a simple measure of reaction time.
      • Galetta K.M.
      • Brandes L.E.
      • Maki K.
      • et al.
      The King-Devick test and sports-related concussion: study of a rapid visual screening tool in a collegiate cohort.
      • Eckner J.T.
      • Kutcher J.S.
      • Broglio S.P.
      • Richardson J.K.
      Effect of sport-related concussion on clinically measured simple reaction time.
      • Guskiewicz K.M.
      • Ross S.E.
      • Marshall S.W.
      Postural Stability and Neuropsychological Deficits After Concussion in Collegiate Athletes.
      A combination of assessment tools may help to improve concussion diagnostic accuracy, but further research is required, especially in children.
      • McCrea M.
      • Barr W.B.
      • Guskiewicz K.
      • et al.
      Standard regression-based methods for measuring recovery after sport-related concussion.
      • Davis G.A.
      • Purcell L.K.
      The evaluation and management of acute concussion differs in young children.
      • Lau B.C.
      • Collins M.W.
      • Lovell M.R.
      Sensitivity and specificity of subacute computerized neurocognitive testing and symptom evaluation in predicting outcomes after sports-related concussion.

      Persistent symptoms

      The duration of postconcussion symptoms can vary. Most patients with concussion recover within 7-10 days of injury, although concussion symptoms in children may resolve more slowly.
      • Field M.
      • Collins M.W.
      • Lovell M.R.
      • Maroon J.
      Does age play a role in recovery from sports-related concussion? A comparison of high school and collegiate athletes.
      • Makdissi M.
      • Darby D.
      • Maruff P.
      • Ugoni A.
      • Brukner P.
      • McCrory P.R.
      Natural history of concussion in sport: markers of severity and implications for management.
      • McCrea M.
      • Guskiewicz K.M.
      • Marshall S.W.
      • et al.
      Acute effects and recovery time following concussion in collegiate football players: the NCAA Concussion Study.
      • Pellman E.J.
      • Lovell M.R.
      • Viano D.C.
      • Casson I.R.
      Concussion in professional football: recovery of NFL and high school athletes assessed by computerized neuropsychological testing–Part 12.
      The mean duration of postconcussion symptoms among patients age 8-23 years who were referred to a concussion clinic was 43 ± 55 days.
      • Brown N.J.
      • Mannix R.C.
      • O'Brien M.J.
      • Gostine D.
      • Collins M.W.
      • Meehan III, W.P.
      Effect of cognitive activity level on duration of post-concussion symptoms.
      In a prospective study of patients aged 11-22 years who presented to an emergency department with acute concussion, irritability and sleep disturbances lasted a median of 16 days, whereas frustration and poor concentration lasted 14 days.
      • Eisenberg M.A.
      • Meehan III, W.P.
      • Mannix R.
      Duration and Course of Post-Concussive Symptoms.
      One month after injury, 24.8% of patients had headaches, 21.6% reported fatigue, and 18.3% complained of persistent difficulties with thinking. Three months after injury, 15% continued to report at least one postconcussion symptom.
      A minority of patients report postconcussion symptoms that persist for months and, sometimes, for years. Among patients with concussion who initially presented to an emergency department, 11%-15% continued to have symptoms three months later, and 2.3% reported symptoms one year after injury.
      • Eisenberg M.A.
      • Meehan III, W.P.
      • Mannix R.
      Duration and Course of Post-Concussive Symptoms.
      • Barlow K.M.
      • Crawford S.
      • Stevenson A.
      • Sandhu S.S.
      • Belanger F.
      • Dewey D.
      Epidemiology of postconcussion syndrome in pediatric mild traumatic brain injury.
      The incidence of persistent symptoms differs across studies, ranging from 1.4% to 38%, based on the patient population assessed and the diagnostic criteria used.
      • Barlow K.M.
      • Crawford S.
      • Stevenson A.
      • Sandhu S.S.
      • Belanger F.
      • Dewey D.
      Epidemiology of postconcussion syndrome in pediatric mild traumatic brain injury.
      • Babcock L.
      • Byczkowski T.
      • Wade S.L.
      • Ho M.
      • Mookerjee S.
      • Bazarian J.J.
      Predicting postconcussion syndrome after mild traumatic brain injury in children and adolescents who present to the emergency department.
      • Chrisman S.P.
      • Rivara F.P.
      • Schiff M.A.
      • Zhou C.
      • Comstock R.D.
      Risk factors for concussive symptoms 1 week or longer in high school athletes.
      • Eisenberg M.A.
      • Andrea J.
      • Meehan W.
      • Mannix R.
      Time interval between concussions and symptom duration.
      • Mittenberg W.
      • Strauman S.
      Diagnosis of mild head injury and the postconcussion syndrome.
      A survey of physician members of the American College of Sports Medicine demonstrated a lack of consensus about how many postconcussion symptoms must be present and how long they must persist to constitute abnormal.
      • Rose S.
      • Fischer A.
      • Heyer G.
      How long is too long? The lack of consensus regarding the Postconcussion Syndrome diagnosis.
      The 2012 consensus statement on concussion in sport defines postconcussion symptoms that last beyond 10 days as persistent,
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      whereas the American Medical Society for Sports Medicine requires that symptoms last “weeks to months”.
      • Harmon K.G.
      • Drezner J.
      • Gammons M.
      • et al.
      American Medical Society for Sports Medicine position statement: concussion in sport.
      Several definitions for the abnormal persistence of postconcussion symptoms have been put forth, with symptom durations ranging from 7 days to 3 months.
      • Kraus J.F.
      • Hsu P.
      • Schafer K.
      • Afifi A.A.
      Sustained outcomes following mild traumatic brain injury: Results of a five-emergency department longitudinal study.
      • McCrea M.
      • Guskiewicz K.
      • Randolph C.
      • et al.
      Incidence, clinical course, and predictors of prolonged recovery time following sport-related concussion in high school and college athletes.
      • Meehan III, W.P.
      • Mannix R.C.
      • Stracciolini A.
      • Elbin R.J.
      • Collins M.W.
      Symptom severity predicts prolonged recovery after sport-related concussion, but age and amnesia do not.
      When postconcussion symptoms persist, it can be difficult to distinguish the symptoms related to brain injury from the premorbid symptoms. Physical complaints such as headache and dizziness tend to present shortly after impact, whereas emotional complaints such as frustration, irritability, and restlessness may develop later during the recovery process.
      • Eisenberg M.A.
      • Meehan III, W.P.
      • Mannix R.
      Duration and Course of Post-Concussive Symptoms.
      Premorbid depression or anxiety can potentiate postconcussion symptoms (and symptom reporting).
      • Corwin D.J.
      • Zonfrillo M.R.
      • Master C.L.
      • et al.
      Characteristics of prolonged concussion recovery in a pediatric subspecialty referral population.
      Additionally, a subset of children may exaggerate or feign symptoms after concussion, further complicating clinical assessment. Kirkwood and colleagues used the Medical Symptom Validity Test to detect symptom exaggeration in a cohort of pediatric patients with concussion.
      • Kirkwood M.W.
      • Peterson R.L.
      • Connery A.K.
      • Baker D.A.
      • Grubenhoff J.A.
      Postconcussive symptom exaggeration after pediatric mild traumatic brain injury.
      Among 191 participants, 23 (12%) failed the validity test, and those who failed endorsed significantly more symptoms than those who passed. We agree with the authors that validity testing should become a standard part of the neuropsychological battery for concussion. The very high pass rate also should be highlighted: 88% of patients had no evidence of feigning or exaggerating their postconcussion symptoms. Last, some of the families in our care seem to expect that concussion symptoms will persist, which may be related to the recent increase in media attention about poor concussion outcomes among professional athletes. Following a typical concussion, we recommend that the clinician convey early (and reinforce often) during the course of treatment that a full and normal recovery is expected.

      Treatment and management

      Physical and cognitive rest

      Current position and consensus statements published by the American Academy of Neurology, the American Academy of Pediatrics, the American Medical Society for Sports Medicine, the National Athletic Trainers' Association, and the 4th International Conference on Concussion in Sport have been united in their recommendations for physical and cognitive rest as the cornerstones of acute concussion management.
      • Giza C.C.
      • Kutcher J.S.
      • Ashwal S.
      • et al.
      Summary of evidence-based guideline update: evaluation and management of concussion in sports: report of the Guideline Development Subcommittee of the American Academy of Neurology.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      • Broglio S.P.
      • Cantu R.C.
      • Gioia G.A.
      • et al.
      National Athletic Trainers' Association position statement: management of sport concussion.
      • Halstead M.E.
      • Walter K.D.
      American Academy of Pediatrics. Clinical report–sport-related concussion in children and adolescents.
      • Harmon K.G.
      • Drezner J.
      • Gammons M.
      • et al.
      American Medical Society for Sports Medicine position statement: concussion in sport.
      The child with a suspected concussion should be removed from sport and other physical activities until evaluated by a health care professional. If a concussion is diagnosed, the child should not return to activity that day. Following concussion, athletes can have slowed reaction times, balance impairments, and cognitive symptoms, placing them at increased risk of repeat injury and in rare instances catastrophic injury (described later in this article, see second impact syndrome). Legislation in most states mandates that youth athletes be medically cleared before returning to their sport. Cognitive and physical activities should be limited until symptoms abate during rest. It is not practical (nor realistic) to prescribe complete rest, but physical or cognitive overexertion can worsen postconcussion symptoms. Once symptoms have resolved at rest, activities can be reintroduced gradually. General and sport-specific return-to-play protocols are available for youth athletes.
      • May K.H.
      • Marshall D.L.
      • Burns T.G.
      • Popoli D.M.
      • Polikandriotis J.A.
      Pediatric sports specific return to play guidelines following concussion.
      These protocols advance physical activity through five graded stages, with each stage usually taking at least one day to complete.
      • Broglio S.P.
      • Cantu R.C.
      • Gioia G.A.
      • et al.
      National Athletic Trainers' Association position statement: management of sport concussion.
      • Halstead M.E.
      • Walter K.D.
      American Academy of Pediatrics. Clinical report–sport-related concussion in children and adolescents.
      Fewer data are available for advancing physical activity in youth who are not athletes. But an analogous approach, advancing activity intensity over several days, can be used if the patient is appropriately monitored.
      Although expert consensus advocates limiting physical and cognitive activities after concussion, little is known about the therapeutic benefits of rest during acute recovery. A randomized trial of patients with acute concussion, aged 11-22 years, found no differences between those given instructions for strict rest for 5 days versus those instructed to rest for 1-2 days and then gradually return to activity.
      • Thomas D.G.
      • Apps J.N.
      • Hoffmann R.G.
      • McCrea M.
      • Hammeke T.
      Benefits of Strict Rest After Acute Concussion: A Randomized Controlled Trial.
      In contrast, initiation of cognitive and physical rest, either immediately after injury or greater than 30 days after injury, led to postconcussion symptom improvements in high school and college athletes, but there was no control group for comparison.
      • Moser R.S.
      • Glatts C.
      • Schatz P.
      Efficacy of immediate and delayed cognitive and physical rest for treatment of sports-related concussion.
      A retrospective study demonstrated that pediatric patients with higher activity levels following concussion had poorer visual memory and reaction time scores on computerized testing than those engaging in moderate activity levels.
      • Majerske C.W.
      • Mihalik J.P.
      • Ren D.
      • et al.
      Concussion in sports: postconcussive activity levels, symptoms, and neurocognitive performance.
      Brown and colleagues conducted a prospective cohort study that demonstrated benefits from cognitive rest.
      • Brown N.J.
      • Mannix R.C.
      • O'Brien M.J.
      • Gostine D.
      • Collins M.W.
      • Meehan III, W.P.
      Effect of cognitive activity level on duration of post-concussion symptoms.
      The 335 patients, 8-23 years of age, were divided into four quartiles based on self-reported levels of cognitive activity. Those with the highest amounts of cognitive activity had the longest recovery periods. There were no differences between the other three quartiles, suggesting that complete cognitive rest may be similar to moderate levels of rest in terms of therapeutic benefit.
      Arguably, school-aged children should be able to tolerate the full school day before attempts are made to return to sports or other strenuous activities. We discourage prolonged school absences, although intense postconcussion symptoms may delay school return for some students. Academic accommodations should be requested when needed. Schools vary in how they monitor and accommodate returning students with concussion, so recommendations for academic accommodations should be written clearly in a health care professionals note and should focus on the specific school-related triggers that exacerbate concussion symptoms.
      • Halstead M.E.
      • McAvoy K.
      • Devore C.D.
      • Carl R.
      • Lee M.
      • Logan K.
      Returning to learning following a concussion.
      • Heyer G.L.
      • Weber K.D.
      • Rose S.C.
      • Perkins S.Q.
      • Schmittauer C.E.
      High School Principals' Resources, Knowledge, and Practices regarding the Returning Student with Concussion.
      • McGrath N.
      Supporting the student-athlete's return to the classroom after a sport-related concussion.
      Examples of symptom-specific accommodations are provided in Table 2. Optimizing the “return to learning” process may require input from several health care and education professionals working with the patient and family, including the physician, the athletic trainer, teachers, the school nurse, the school psychologist, and the school principal.
      • Halstead M.E.
      • McAvoy K.
      • Devore C.D.
      • Carl R.
      • Lee M.
      • Logan K.
      Returning to learning following a concussion.
      In rare cases when postconcussion symptoms persist, formalized educational plans may become necessary.
      Table 2Potential School Accommodations Following Concussion
      Accommodations from references.119-121
      Overall workload
       Excuse school absences
       Shorten school days
       Provide rest breaks during class or between classes
       Excuse assignments or examinations
       Extend assignment deadlines
       Postpone examinations (especially standardized tests)
      Physical exertion
       Provide extra time to get from class to class
       Excuse from participation in gym class and sports
       Minimize flights of stairs and weight of backpack
      Poor concentration and slowed mentation
       Provide additional time for examinations and homework assignments
       Seat closer to teacher
       Provide class notes
       Allow examinations to be taken in separate, quiet room
      Noise and light sensitivity
       Provide a quiet room to each lunch
       Minimize band, choir, or shop classes
       Allow ear plugs (outside of classroom)
       Allow hat or sunglasses
       Seat in area of classroom with dim light
       Minimize use of computer screens
      Visual symptoms
       Minimize reading (may need reading assistant) or allow breaks while reading
       Provide a note-taker or scribe
       Minimize use of computer screens
      Accommodations from references.
      • Halstead M.E.
      • McAvoy K.
      • Devore C.D.
      • Carl R.
      • Lee M.
      • Logan K.
      Returning to learning following a concussion.
      • Heyer G.L.
      • Weber K.D.
      • Rose S.C.
      • Perkins S.Q.
      • Schmittauer C.E.
      High School Principals' Resources, Knowledge, and Practices regarding the Returning Student with Concussion.
      • McGrath N.
      Supporting the student-athlete's return to the classroom after a sport-related concussion.

      Medical management

      Several concussion symptoms are amenable to medical therapy. Symptom-specific treatments can be used as needed during the recovery period. Unfortunately, the effectiveness of these treatments has not been well-studied in concussion patients.
      Sleep disturbances are common following concussion.
      • Paniak C.
      • Reynolds S.
      • Phillips K.
      • Toller-Lobe G.
      • Melnyk A.
      • Nagy J.
      Patient complaints within 1 month of mild traumatic brain injury: a controlled study.
      Patients may experience excessive sleep, daytime drowsiness, difficulty falling asleep, or frequent nighttime waking. Addressing sleep complaints begins with a discussion of good sleep hygiene.
      • Meehan III, W.P.
      Medical therapies for concussion.
      Patients should be counseled about removing distracting stimuli (e.g., televisions, computers, telephones, video games) from the bedroom; sleeping in a quiet, dark, and comfortable room; avoiding caffeine, especially in the afternoon and evening; and eliminating daytime naps. Sleep aids such as melatonin may be helpful for the patient with erratic sleep patterns. Prescription sedatives and anxiolytics should be avoided because of their negative effects on arousal and cognition.
      Headaches are probably the most common postconcussion complaint. During the acute recovery period, simple analgesics are often adequate in relieving pain. Limited evidence is available for the use of migraine-specific triptans for posttraumatic headache. In an observational study of US soldiers with chronic posttraumatic headache, 51 (70%) who used triptans experienced headache relief within 2 hours.
      • Erickson J.C.
      Treatment outcomes of chronic post-traumatic headaches after mild head trauma in US soldiers: an observational study.
      If headaches persist, analgesic and triptan use should be limited to avoid medication overuse headache, which can contribute to chronic posttraumatic headaches in some patients.
      • Heyer G.L.
      • Idris S.A.
      Does analgesic overuse contribute to chronic post-traumatic headaches in adolescent concussion patients?.
      We do not recommend opioids in the routine management of headaches following concussion.
      The abnormal persistence of postconcussion symptoms poses a variety of therapeutic challenges. When persistent headaches develop, prophylactic headache medicines can be considered. Kuczynski and colleagues reported headache treatment outcomes for several medications from a pediatric posttraumatic headache cohort with a median time since TBI of 6.9 months. They found that headaches improved in 75% of those treated with melatonin and 68% of those treated with amitriptyline, and lower response rates were seen with nortriptyline and topiramate.
      • Kuczynski A.
      • Crawford S.
      • Bodell L.
      • Dewey D.
      • Barlow K.M.
      Characteristics of post-traumatic headaches in children following mild traumatic brain injury and their response to treatment: a prospective cohort.
      The choice of which medicine to prescribe depends on the patient's associated symptoms. Amitriptyline can be helpful when complaints about diminished nighttime sleep are present. It is effective in treating both migraine and tension-type headaches.
      • Pinchefsky E.
      • Dubrovsky A.S.
      • Friedman D.
      • Shevell M.
      Part II-Management of Pediatric Posttraumatic Headaches.
      Topiramate can also be effective, but cognitive slowing may be a limiting factor as the dose is advanced. Beta-blockers may be troublesome for the athlete requiring an elevated heart rate. Certain medications such as beta-blockers, glucocorticoids, and narcotics may be banned by some sporting bodies.
      Emotional and cognitive symptoms should be assessed at each visit. Referral to a neuropsychologist who is familiar with concussion management can help to determine the need for neurocognitive testing and to manage mood swings, irritability, anxiety, and depression. For ongoing or severe depression or anxiety, selective serotonin reuptake inhibitors, tricyclic antidepressants, or referral to a psychiatrist can be considered.
      • Warden D.L.
      • Gordon B.
      • McAllister T.W.
      • et al.
      Guidelines for the pharmacologic treatment of neurobehavioral sequelae of traumatic brain injury.
      When managing cognitive symptoms such as mental fatigue and impairments in attention and memory in TBI patients, studies of methylphenidate have shown mixed results.
      • Johansson B.
      • Wentzel A.P.
      • Andrell P.
      • Odenstedt J.
      • Mannheimer C.
      • Ronnback L.
      Evaluation of dosage, safety and effects of methylphenidate on post-traumatic brain injury symptoms with a focus on mental fatigue and pain.
      • Williams S.E.
      • Ris M.D.
      • Ayyangar R.
      • Schefft B.K.
      • Berch D.
      Recovery in pediatric brain injury: is psychostimulant medication beneficial?.
      Amantadine has been used for post-TBI cognitive and behavioral symptoms, but the results have also been inconsistent.
      • Schneider W.N.
      • Drew-Cates J.
      • Wong T.M.
      • Dombovy M.L.
      Cognitive and behavioural efficacy of amantadine in acute traumatic brain injury: an initial double-blind placebo-controlled study.
      • Beers S.R.
      • Skold A.
      • Dixon C.E.
      • Adelson P.D.
      Neurobehavioral effects of amantadine after pediatric traumatic brain injury: a preliminary report.
      Moderate and severe TBI patients are included in some of these studies, highlighting the need for dedicated concussion treatment trials.
      For chronic and intractable postconcussion symptoms, other nonpharmacologic therapies may be useful. Active physical rehabilitation has been shown to benefit some children. In a study of 16 patients aged 8-17 years who had persistent postconcussion symptoms ranging from 4-18 weeks’ duration, escalating amounts of exercise led to improved symptoms and increased exercise tolerance.
      • Gagnon I.
      • Galli C.
      • Friedman D.
      • Grilli L.
      • Iverson G.L.
      Active rehabilitation for children who are slow to recover following sport-related concussion.
      When persistent vertigo is present, referral to a vestibular therapist may be helpful.
      • Alsalaheen B.A.
      • Mucha A.
      • Morris L.O.
      • et al.
      Vestibular rehabilitation for dizziness and balance disorders after concussion.
      • Schneider K.J.
      • Meeuwisse W.H.
      • Nettel-Aguirre A.
      • et al.
      Cervicovestibular rehabilitation in sport-related concussion: a randomised controlled trial.
      Cognitive therapy, meditation, biofeedback, and psychotherapy may be beneficial to those with memory and coping difficulties, anxiety, or panic attacks.
      • Makdissi M.
      • Cantu R.C.
      • Johnston K.M.
      • McCrory P.
      • Meeuwisse W.H.
      The difficult concussion patient: what is the best approach to investigation and management of persistent (>10 days) postconcussive symptoms?.
      When postconcussion symptoms persist and interfere with daily activities, we recommend referral to a multidisciplinary concussion clinic when possible.

      Other complications

      Posttraumatic seizures and epilepsy

      Posttraumatic seizures are classified as early (1 week or less following injury) or late (after 1 week). Any TBI increases both early and late seizure risk. The risk increases further in patients with lower Glasgow Coma Scale scores at presentation.
      • Christensen J.
      • Pedersen M.G.
      • Pedersen C.B.
      • Sidenius P.
      • Olsen J.
      • Vestergaard M.
      Long-term risk of epilepsy after traumatic brain injury in children and young adults: a population-based cohort study.
      • Annegers J.F.
      • Hauser W.A.
      • Coan S.P.
      • Rocca W.A.
      A population-based study of seizures after traumatic brain injuries.
      • Emanuelson I.
      • Uvebrant P.
      Occurrence of epilepsy during the first 10 years after traumatic brain injury acquired in childhood up to the age of 18 years in the south western Swedish population-based series.
      • Lewis R.J.
      • Yee L.
      • Inkelis S.H.
      • Gilmore D.
      Clinical predictors of post-traumatic seizures in children with head trauma.
      • Hahn Y.S.
      • Fuchs S.
      • Flannery A.M.
      • Barthel M.J.
      • McLone D.G.
      Factors influencing posttraumatic seizures in children.
      In a large Danish population study, prior concussion imparted a twofold increased risk of epilepsy in children.
      • Christensen J.
      • Pedersen M.G.
      • Pedersen C.B.
      • Sidenius P.
      • Olsen J.
      • Vestergaard M.
      Long-term risk of epilepsy after traumatic brain injury in children and young adults: a population-based cohort study.
      Risk was greatest within the first year after concussion, but remained increased for more than 10 years. In contrast, the epilepsy risk normalized within 5 years of injury among the Mayo Clinic's Olmsted County population.
      • Annegers J.F.
      • Hauser W.A.
      • Coan S.P.
      • Rocca W.A.
      A population-based study of seizures after traumatic brain injuries.

      Second impact syndrome

      While still symptomatic from a concussion, the brain is prone to autoregulatory dysfunction and abnormal ion fluxes.
      • Reilly P.L.
      Brain injury: the pathophysiology of the first hours.'Talk and Die revisited'.
      A second impact during the vulnerable recovery period has been implicated as a cause of malignant cerebral edema and herniation.
      • Wetjen N.M.
      • Pichelmann M.A.
      • Atkinson J.L.
      Second impact syndrome: concussion and second injury brain complications.
      The mortality rate from the so-called “second impact syndrome” (SIS) approaches 100%.
      • McCrory P.R.
      • Berkovic S.F.
      Second impact syndrome.
      Controversy exists, however, about the nature, and even the existence, of SIS. Traumatic intracranial hemorrhage or diffuse cerebral edema can cause progressive symptomatic deterioration following brain injury, even in the absence of a first impact.
      • McCrory P.R.
      • Berkovic S.F.
      Second impact syndrome.
      • Bruce D.A.
      • Alavi A.
      • Bilaniuk L.
      • Dolinskas C.
      • Obrist W.
      • Uzzell B.
      Diffuse cerebral swelling following head injuries in children: the syndrome of “malignant brain edema”.
      • Bruce D.A.
      Delayed deterioration of consciousness after trivial head injury in childhood.
      • Kim J.
      • Kemp S.
      • Kullas K.
      • Hitos K.
      • Dexter M.A.
      Injury patterns in patients who “talk and die”.
      • Reilly P.L.
      • Graham D.I.
      • Adams J.H.
      • Jennett B.
      Patients with head injury who talk and die.
      Mutations in the CACNA1A gene, which encodes a voltage-gated calcium channel subunit, have been implicated as a cause of delayed cerebral edema following minor head trauma.
      • Kors E.E.
      • Terwindt G.M.
      • Vermeulen F.L.
      • et al.
      Delayed cerebral edema and fatal coma after minor head trauma: role of the CACNA1A calcium channel subunit gene and relationship with familial hemiplegic migraine.
      McCrory and Berkovic classified 17 published SIS patients as “definite,” “probable,” “possible,” and “not SIS.”
      • McCrory P.R.
      • Berkovic S.F.
      Second impact syndrome.
      Twelve patients failed to meet SIS criteria (i.e., classified as “not SIS”) based on the absence of a witnessed second impact or the absence of neuroimaging or neuropathologic evidence of unexplained cerebral edema. The remaining five patients were classified as “probable SIS”; all were boys aged 16-19 years with the second impact occurring within 1 week of the initial TBI. Subsequent case series have reported patients who sustained a second impact causing acute cerebral edema with small subdural hemorrhages, all while symptomatic from a first concussion.
      • Cantu R.C.
      • Gean A.D.
      Second-impact syndrome and a small subdural hematoma: an uncommon catastrophic result of repetitive head injury with a characteristic imaging appearance.
      • Mori T.
      • Katayama Y.
      • Kawamata T.
      Acute hemispheric swelling associated with thin subdural hematomas: pathophysiology of repetitive head injury in sports.
      In most cases, the second injury occurred within 1 month of the first. All patients had catastrophic clinical outcomes. Many factors increase the risk of repeat injury while symptomatic with a concussion including delayed reaction times, balance impairments, and cognitive difficulties. While debate about the nature of SIS continues, risk of further injury can be minimized by removing the patient from all sports and activities until symptoms resolve.

      Chronic traumatic encephalopathy

      Chronic traumatic encephalopathy (CTE) is a progressive neurodegenerative disorder characterized by a unique pattern of hyperphosphorylated tau deposition in the brain.
      • McKee A.C.
      • Stern R.A.
      • Nowinski C.J.
      • et al.
      The spectrum of disease in chronic traumatic encephalopathy.
      • Omalu B.I.
      • DeKosky S.T.
      • Minster R.L.
      • Kamboh M.I.
      • Hamilton R.L.
      • Wecht C.H.
      Chronic traumatic encephalopathy in a National Football League player.
      An association has been inferred between lifetime burden of head injury and CTE development.
      • McCrory P.
      • Meeuwisse W.H.
      • Aubry M.
      • et al.
      Consensus statement on concussion in sport: the 4th International Conference on Concussion in Sport held in Zurich, November 2012.
      • Gardner A.
      • Iverson G.L.
      • McCrory P.
      Chronic traumatic encephalopathy in sport: a systematic review.
      • McCrory P.
      • Meeuwisse W.H.
      • Kutcher J.S.
      • Jordan B.D.
      • Gardner A.
      What is the evidence for chronic concussion-related changes in retired athletes: behavioural, pathological and clinical outcomes?.
      CTE symptoms include irritability, impulsivity, attention difficulties, executive dysfunction, memory impairments, depression, and gait disturbances.
      • McKee A.C.
      • Stern R.A.
      • Nowinski C.J.
      • et al.
      The spectrum of disease in chronic traumatic encephalopathy.
      • McKee A.C.
      • Cantu R.C.
      • Nowinski C.J.
      • et al.
      Chronic traumatic encephalopathy in athletes: progressive tauopathy after repetitive head injury.
      To date, ascertainment of symptoms has been limited to postmortem interviews with family members. Prospective CTE studies have not yet been conducted, and the potential effects of comorbidities have not yet been addressed.
      • Gardner A.
      • Iverson G.L.
      • McCrory P.
      Chronic traumatic encephalopathy in sport: a systematic review.
      • McCrory P.
      • Meeuwisse W.H.
      • Kutcher J.S.
      • Jordan B.D.
      • Gardner A.
      What is the evidence for chronic concussion-related changes in retired athletes: behavioural, pathological and clinical outcomes?.
      Some investigators have concluded that CTE increases the risk of suicide; however, this has not been borne out by an increase in the suicide rate among athletes who participate in collision sports.
      • Iverson G.L.
      Chronic traumatic encephalopathy and risk of suicide in former athletes.
      For example, the suicide rate among retired professional American football players is lower than average at 41% of the rate in the general population.
      • Baron S.L.
      • Hein M.J.
      • Lehman E.
      • Gersic C.M.
      Body mass index, playing position, race, and the cardiovascular mortality of retired professional football players.
      The neuropathologic changes of CTE may begin in the school-aged brain. McKee and colleagues found evidence of CTE in the brains of six individuals with high school football as their only clear source of concussion exposure; the youngest brain with CTE pathology was 17 years old.
      • McKee A.C.
      • Stern R.A.
      • Nowinski C.J.
      • et al.
      The spectrum of disease in chronic traumatic encephalopathy.
      More research is needed to establish the risk of developing CTE brain changes during childhood, especially with high school-level collision sports. Although further study is necessary, Love and Solomon deny a compelling reason to withhold a high school athlete from sports because of a concern for CTE.
      • Love S.
      • Solomon G.S.
      Talking With Parents of High School Football Players About Chronic Traumatic Encephalopathy: A Concise Summary.

      Retirement and disqualification from sports

      Currently, the only modifiable risk factor for the development of neurocognitive and behavioral symptoms following concussion is the prevention of future concussions. Unfortunately, there are no consensus guidelines or well-accepted criteria available about retiring the youth athlete from sports after frequent or severe concussions. Features that should prompt consideration for sports retirement include a severe and prolonged course of concussion recovery, progressively longer recovery times with successive concussions, progressively lower force of impact required to cause concussion, persistent functional impairment in school or work, evidence of neurocognitive dysfunction on formal neuropsychiatric testing, an abnormality on neurological exam attributable to head injury, or structural brain injury on standard neuroimaging.
      • Harmon K.G.
      • Drezner J.
      • Gammons M.
      • et al.
      American Medical Society for Sports Medicine position statement: concussion in sport.
      • Cantu R.C.
      • Register-Mihalik J.K.
      Considerations for return-to-play and retirement decisions after concussion.
      • Sedney C.L.
      • Orphanos J.
      • Bailes J.E.
      When to consider retiring an athlete after sports-related concussion.
      Neuropsychological evaluation can be beneficial in quantifying the subjective complaints of persistent cognitive and behavioral problems, data that may influence the decision to retire the athlete. Team sports and individual sports provide important structure for character building, and there are health benefits from sports-related exercise. Decisions about the retirement and disqualification of a patient from youth sports should weigh the risks of further injury with the risks of no longer participating in that activity.

      Conclusion

      As health care utilization for concussions continues to rise, physicians from a variety of medical specialties, including child neurology, can expect to see more referrals for patients with concussion. In the past decade, much has been done to better understand concussion and concussion prevention. This review provided a glimpse of that progress. Although the research focusing on concussion in youth has gained some momentum, evidence-based recommendations for concussion diagnosis and management are still lacking. Consensus and expert statements are available to guide several aspects of clinical management. Further research is necessary to facilitate primary concussion prevention and to elucidate how best to treat concussions when they occur.

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