Clinical manifestations

Presentation and course

Clinical manifestations of concussion are variable and can be numerous. Symptom onset occurs within minutes to days after an injury. Common concussive symptoms (as per the ACE materials available to the public at HEADS UP to Health Care Providers: Tools for Providers) are included in Table 1.

Table 1. Common Concussive Symptoms

Physical	Cognitive	Emotional	Sleep
Headache	Feeling mentally foggy	Irritability	Drowsiness
Nausea	Problems concentrating	Sadness	Sleeping more than usual
Fatigue	Problems remembering	Feeling more emotional	Sleeping less than usual
Visual problems	Feeling more slowed down	Nervousness	Trouble falling asleep
Balance problems
Sensitivity to light/noise
Numbness/tingling
Vomiting
Dizziness

In children with concussion presenting to the emergency department, headache, nausea, dizziness, blurry/double vision, and not feeling “sharp” were the most common symptoms and were associated with altered mental status (38). Although physical symptoms are more prominent early after injury, a study indicates that emotional and sleep symptoms are more likely to develop over days to weeks following the injury (29).

Commonly accepted “red flags” that may indicate a more severe brain injury and require further evaluation include focal neurologic signs such as weakness or sensory symptoms, loss of consciousness longer than 5 minutes, excessive symptoms such as severe headache, persistent emesis, confusion lasting longer than 30 minutes, altered mental status, as well as clinical judgment.

Although the core symptoms of concussion are the same among all age groups, it is important to consider the developmental expectations and the communication ability of each child. For example, a 3 year old may not be able to verbalize “I have a headache, blurry vision, feel tired, and am having difficulty concentrating.” The parent, however, may note that their 3 year old is acting “more clingy than usual,” “wants to stay inside,” “is not as playful,” etc. A prospective study indicates that compared to school-age children, preschool children are less likely to report concussive symptoms, and symptoms reported were those able to be observed easily by the parent/caregiver (85). They even tend to show more changes in mood and behavior over time (123).

Although the role of gender in concussion recovery is unclear, one study suggests female athletes reported more baseline symptoms, greater postconcussion symptom severity, and took longer to return to baseline symptoms after injury (125; 126).

Prognosis and complications

Most evidence indicates more pronounced recovery from symptoms within the first week after the injury (64). Evaluating a large cohort of high school and college athletes over 10 years of age, only 10% reported postconcussive symptoms beyond 7 days (80). However, compared to adults, children and adolescents are more likely to have prolonged recovery with postconcussive symptoms reported for months (108; 122; 07; 110; 24), particularly in those with recent or multiple prior concussions (17; 28).

Chrisman and colleagues reported that after a concussion, 50% of athletes returned to school by 3 days, 50% returned to sport by 13 days, and 50% returned to a baseline level of symptoms by 3 weeks (19). Ledoux and colleagues were able to further describe how 5- to 7-year-old children had the greatest improvement in concussive symptoms in the first week, and 8 to 12 years and 13 to 18 years had the most prominent change in the first 2 weeks (65). Even further delineation, adolescent girls had predominant improvement of symptoms in the first 4 weeks, with less than half of the remaining girls reaching full recovery by 12 weeks.

The utility of symptom report alone as a measure of concussion recovery is questionable, as postconcussive symptoms are not specific to concussion and have been reported in control cohorts such as children with only orthopedic injuries (122; 103). That children without concussions also reporting persistent “postconcussive” symptoms indicates that there are likely factors beyond injury that affect outcome based exclusively on report of symptoms. Evidence also suggests potential recall bias (“the good old days” bias) in the rating of premorbid symptoms, as prospectively obtained parental ratings of their child’s premorbid symptoms decreased 80% from the time of injury to 1 month after the concussion (13). Exaggeration of symptoms may also hinder accuracy of symptom scales as the sole measure of concussion recovery, as several studies suggest a relationship between failing effort testing and increased symptom report in children with concussion (02; 56).

Stratifying risk for persistent concussion symptoms has been mostly elusive except for some studies reporting premorbid risk factors, such as school-age children (09), female gender (45), early/initial symptom burden (88; 104), and various acute and subacute symptoms (92; 54). Bernard and colleagues also mentioned that children with neuropsychological ailments such as learning disability and ADHD tend to have longer lasting symptoms (10). The influence of injury-related factors such as loss of consciousness or amnesia on outcome remains unclear (80; 89). However, early concussive symptom severity report has been linked to persistent symptoms (89; 88). Additionally, mechanism of injury may influence recovery. A study of adolescents and young adults presenting to a concussion clinic revealed that those with motor vehicle accidents had more impaired scores on a computerized cognitive battery and a longer course of recovery (106).

Within acute care settings, there are not yet clear variables or measures that can predict the course of concussive recovery. In a study of 406 children 5 to 18 years old presenting to an emergency department with concussion, 29% reported three or more symptoms rated “worse than before injury” in a telephone interview 3 months after injury. Multivariate analysis of this sample suggests that adolescent age, headache on presentation to the emergency department, and admission to the hospital were predictive of postconcussive syndrome, although premorbid factors were not evaluated in this study (04). In another study of children with concussion presenting to the emergency department, low scores on reaction time and/or cognitive flexibility obtained from a computerized cognitive battery administered in the emergency department were significantly related to persistent postconcussive symptoms at 1 month, but not to symptoms 2 or 3 months postinjury (12). On initial evaluation in a sports medicine concussion clinic, children with vestibular symptoms took significantly longer to return to both school and sports (23). It is important to gain a better understanding of variables that predict the course of recovery on acute or early evaluation as this could allow time for individualized and optimized management.

Studies also indicate the importance of preinjury child and parent factors in recovery from injury. For instance, McNally and colleagues noted that although injury-specific factors contributed to the report of concussive symptoms early, noninjury-related factors, mostly premorbid symptoms of child and parent adjustment, consistently contributed to postconcussive symptoms (86). Higher parental anxiety and higher child preinjury health-related quality of life predict persistent postconcussive symptoms between 6 and 18 months after injury (94). More significant life stressors have also been linked to persistent postconcussive symptoms in children (109). In a sports medicine concussion clinic, postconcussive symptoms were significantly related to a personal or family history of mood disorder, psychiatric disorders, or migraines (92). The complexity and variability of factors contributing to injury and recovery (premorbid child and family history, mechanism of injury, clinical evaluation and management, and postinjury factors) hinder accurate clinical prognostic ability.

In an adolescent population, females were more likely to report posttraumatic headache and had a longer recovery (11). Symptom management may also contribute to persistent posttraumatic headache. An evaluation of children with chronic posttraumatic headaches revealed that 70% were medication overuse headaches and nearly 70% resolved with discontinuation of over-the-counter pain medications (44).

The most dangerous potential complication occurs in the setting of a child sustaining a second injury while not healed from an initial concussion. This second, even mild, injury may lead to “second impact syndrome” or diffuse cerebral swelling (16; 81). This proposed condition is more common in children and teenagers and has poor outcome, often death; however, at this time a majority of the literature is in the form of case series. The cerebral swelling is felt to be secondary to “second-impact dysautoregulation,” with classic features, including midline shift out of proportion to a thin subdural hematoma and extensive cerebral swelling with initial preserved grey-white differentiation (16).

Chronic traumatic encephalopathy, a potential sequelae of repetitive brain injuries, is beyond the scope of this discussion.

Clinical vignette

A healthy, athletic 14-year-old girl presented to clinic with her parents after a hit to the head during cheer practice. During a stunt, she was in position as a base holding up another smaller girl, when the smaller girl lost her balance causing her foot to land on top of this patient’s head. There was no loss of consciousness, but she had immediate onset of headache. She did not recall the actual incident, and her next memory was of walking over to the side with her hands on head. As she became more aware, her headaches increased in severity, and she developed dizziness, confusion, blurred vision, and unsteadiness. Her family was called to come pick her up. On the way home, she had emesis and, thus, was brought to a local emergency department. Her head and neck CT scans were reported to be normal. Discharge recommendations included resting and concussion clinic referral.

For the first week, she had daily headaches with trouble remembering simple tasks, difficulty concentrating, and was sleeping through large portions of the day. After being seen by her primary care provider, she was recommended to stay home and rest for 2 days. Her symptoms slowly improved with rest 10 days after her injury, she returned to school where her teachers all reported that heshe seemed “slower.” She had to take breaks during her classes due to headaches and performed poorly on a test (she is typically a straight A student). She had difficulty thinking clearly and speaking during student council meeting.

She was seen in concussion clinic 3 weeks after her concussion. At that time, she was 2 weeks behind in schoolwork, but was able to keep up with her current course load, and, though still symptomatic, she was eager to get back to sports as soon as possible. Her main complaints were headache and feeling “foggy.” Her parents also noted that she was more irritable and emotional than usual. Her general and neurologic exams were normal, except for convergence insufficiency and positive Romberg. She had normal balance testing using the Balance Error Scoring System. Neuropsychological testing Immediate Post-Concussion Assessment Cognitive Test (ImPACT) plus additional psychometric measures were average with slight worsening of symptoms after testing.

An ACE care plan ACE Care Plan was completed for school accommodations with a goal of assisting her in completing her make-up work within a reasonable time and without falling further behind. She received physical and vestibular therapy two times a week. Physical activity recommendations included gradual increase from light to moderate levels of activity as tolerated (such as walking or riding a stationary bike). This was evaluated and followed by the physical therapist. She was then transitioned to increase activity under the guidance of the school athletic trainer.

She returned for scheduled follow-up after 2 weeks. At that time, she reported that all of her symptoms had resolved, and her parents felt she was at baseline. School accommodations were removed as she had completed all make-up work. We reviewed the gradual return to play and recommended a minimum of 24 hours at each level of activity. She progressed through each stage symptom-free and was able to begin to join the cheer team in the nationals competition.

Biological basis

Etiology and pathogenesis

Concussion is induced by a force to the head, resulting in a neurometabolic cascade relating to the physical symptoms associated with injury (36). Dr. Choe described the pathophysiology as the mechanical injury from the force to the head causing a “disruption of cellular membranes resulting in efflux of intracellular potassium… causing neuronal depolarization” (18). This then stimulates neurotransmitters, specifically glutamate, to be excessively released and bind to N-methyl-D-aspartate (NMDA)-receptors. This action opens K+/Ca2+ channels, causing released extracellular Ca2+ to cause cellular damage (18).

Although sports-related concussions have received a great deal of media attention, from professional athletes to little league sports, it is important to remember that falls, motor vehicle accidents, recreational activities, and other accidental events are among the multitude of other causes of concussions.

One study reviewing pediatric concussions in the emergency department reported that 41% of concussions in 11- to 19-year-old children were “sports-related,” whereas only 8% of concussions in children younger than 11 years old were related to sports (87). Haarbauer-Krupa and associates found similar demographics with their pediatric cohort, with 70% of concussions being sports-related, whereas the age group 0 to 4 years had 18% of their concussions that were sports-related, increasing the proportion with age (41). They even noted that those non-sport related concussions were mostly due to falls, being struck by an object, MVC, and assaults. There is no current evidence to suggest a difference in the pathophysiology, recovery, or management of sports-related concussions and concussions from other mechanisms. However, comparison of cognitive measures in college athletes suggests reduced learning, memory, and speed in those athletes participating in contact sports compared to noncontact sports (77).

The stature and nervous system of children are thought to lead to unique vulnerabilities to concussive injury. Karlin summarizes that children have an immature developing nervous system, larger head-body ratio, thinner cranial bones, larger subarachnoid space, different cerebral blood volume/regulation, weaker neck musculature, and incomplete myelination, and increased skull vault elasticity (51). These factors all likely contribute to the differences in concussion injury and recovery specific to the pediatric population.

Monitoring neural response in a mouse model of mTBI, impact induces a neurometabolic cascade, including immediate glutamate release, activation of excitatory receptors, and ionic fluxes leading to hypermetabolism despite reduced cerebral blood flow and reduced glucose supply (35). This results in cellular energy crisis and is followed by reduced cerebral metabolism. Calcium remains increased, further disrupting neural connectivity and mitochondrial function, and triggering cell apoptosis. The measured neurochemical changes normalize over 10 days in experimental models (34). Similar animal models revealed altered long-term potentiation 8 weeks after injury (105).

Using MRI to compare 12 children with sports-related concussion to controls, cerebral blood flow was significantly altered out to 30 days postinjury (75), which is consistent with prior data of cerebral blood flow dysregulation after brain injury. Magnetic resonance spectroscopy (MRS) imaging revealed altered N-acetylaspartate levels normalizing over 30 days following concussion in adolescent and young adult athletes (115). Furthermore, multiple concussions have been related to alterations in MRS findings (49). SPECT imaging revealed medial temporal hypoperfusion, which significantly correlated with persistent postconcussion syndrome 3 months after injury (01).

Diffusion tensor imaging detected significant white matter tract injuries (suggesting cytotoxic edema) that correlated with postconcussive symptoms (119). Another small sample of adolescent athletes revealed alterations in white matter that could be predicted by the SCAT 2, a sideline concussion screen (117). In a small sample of children with concussion, diffusion abnormalities were able to classify pediatric concussion with 90% accuracy, and diffusion abnormalities persisted at least 4 months after injury (76). Early white matter diffusion alterations were reported in youth with concussion who underwent neuroimaging within 96 hours of injury; however, these changes were not related to acute postconcussive symptoms (05). These studies of postconcussive white matter restricted diffusion suggest cytotoxic edema (such as from axonal swelling) following concussion in children. Furthermore, swine models of mTBI also indicate diffuse axonal injury, the extent of which varied by the plane of induced rotational injury (15).

Compared to a control population, changes in fMRI signal in adolescents with concussion has been related to specific task performance as well as cognitive function and symptom report (43; 52).

Toledo and colleagues thoroughly summarized the current literature on neuroimaging and pathophysiology specific to the developing brain (114).

Serum astrocytic protein S100B and autoantibodies were positively correlated with increased numbers of subconcussive events, indicating disruption of the blood-brain barrier in college football players; furthermore, S100B autoantibody levels correlated with diffusion tensor imaging abnormalities and cognitive changes (74). GFAP is another potential biomarker, with evidence suggesting a correlation between GFAP levels at the time of concussive injury and symptoms reported at injury and after 1 month (72). However, symptom severity has not been correlated with acute changes in biomarkers (03). However, symptom severity has not been correlated with acute changes in biomarkers (03).

In a juvenile rat model of repeated traumatic brain injury, a second injury 24 hours after initial injury led to increased axonal injury, astrocyte reactivity, and increased memory impairment on a novel object recognition task (99).

Genetic and other metabolic biomarkers from serum, salivary, cerebrospinal fluid as well as neuroimaging and electrophysiological measures are still experimental.

Epidemiology

The CDC reports 2.8 million traumatic brain injuries annually, 75% of which are mild traumatic brain injury or concussion (112). However, an accurate estimate is difficult to obtain as many concussions are not diagnosed, occur across a wide range of activities, and may be evaluated/diagnosed in multiple locations, including the emergency room or in outpatient settings such as the pediatrician, a sports medicine physician, a pediatric neurologist, or an athletic trainer. Across the spectrum of traumatic brain injury-related injuries, very young children aged 0 to 4 years old had the highest rate of traumatic brain injury-related emergency department visits followed by older adolescents aged 15 to 19 years of age. In 2019, Yaramothu and colleagues reported that pediatric patients who were in organized sport accounted for 53.3% of concussions (121). Within the school setting, soccer has the highest incidence of concussion at 16.5%. The traumatic brain injury rate is higher overall for males of all age ranges; however, in gender-comparable high school sports, a study indicated girls have a higher rate of concussions (73).

It is estimated that concussion is diagnosed in one of every 160 pediatric patients seen in the emergency department, with 60% having head CT and nearly half receiving medical intervention including pain management or intravenous fluids (21). A review of pediatric concussions in organized team sports noted that the number of emergency department visits had doubled for children 8 to 13 years old and increased by more than 200% for 14- to 19-year-old athletes (06).

Evaluating 20 high school sports, the overall concussion rate was 2.5 per 10,000 athletic exposures; the majority of concussions occurred in football, girls’ soccer, wrestling, and basketball (73). Concussion occurred as the largest percentage of injuries sustained within ice hockey. The risk of sustaining a concussion was higher in competition than in practice, with the majority missing more than 1 week of sports due to the concussion. Incidence rate of concussions in 8- to 12-year-olds playing youth football was reported as 1.76 concussions per 1000 athletic exposures; additionally, the risk of concussion was higher in games, compared to practice, and in the 11- to 12-year-old age group compared to 8- to 10-year-old children (57).

In 2019, Kerr and colleagues reported that The National Federation of State High School Associations had indicated a steady rise in high school sports participation overall (a 3.5% increase from 2012–2013 to 2017–2018) (53). When evaluating 20 high school sports, they also reported the overall concussion rate was 4.17 per 10,000 athletic exposures—the majority in boys’ football, followed by girls’ soccer and boys’ ice hockey. The risk of sustaining a concussion was higher in competition than practice. When examining concussion incidence in practice, the highest rates were observed in boys’ football, followed by cheerleading and boys’ wrestling.

In a prospective cohort study conducted from 2016 to 2017 in a youth football league (ages 5–14), Chrisman and colleagues found an athlete-level incidence of 5.1% per season with two-thirds of the concussions occurring during games. This is slightly higher than previously reported in 2013 by Kontos and colleagues, but may be due to more surveillance at games. Youth with a history of concussion had a 2-fold increased risk for sustaining an incident concussion, and youth with depression had a 5-fold increased risk of concussion.

A study also showed that children with ADHD are significantly more likely to report a history of concussion compared to children without ADHD (48).

Prevention

Despite increasing knowledge about the risks of concussion unique to children, there is not specific equipment that can prevent a concussion. In fact, evidence suggests the incidence of sports-related concussion was not related to the brand or helmet worn by high school athletes (08; 84). It is important to use safety equipment, from seatbelts in cars to helmets when skiing or biking to protective gear in athletics. There has been discussion about other measures to further protect children in sports, such as a limit on the amount of contact in football practice or the number of “headings” in soccer (similar to a pitch count in baseball). Impact monitoring systems in football helmets have not yet been proven to be clinically efficacious as current studies have not supported the reliability and clinical usefulness of head impact telemetry systems (39; 40). Although not correlated clinically, impact monitoring in youth football reveals an average of 247 notable impacts per season and indicated limiting contact in practice may reduce these exposures (20). Proper technique of high-risk activities, such as tackling, should be taught and emphasized. For sports-related concussions, it is even recommended that athletic trainers use socioecological framework to develop strategies to help mitigate risk for their athletes, which would go beyond watching educational videos or reading handouts (102).

Most importantly, however, is to remove any child displaying symptoms of a concussion from play for more thorough, concussion-specific evaluation. It is important to have children seen and cleared by professionals trained in management of concussion as this should help prevent risk of repeated injury while still recovering from an initial injury.

Differential diagnosis

Acutely, it is important to consider if the child’s presentation could be indicative of a more severe brain injury. Consider the following factors, which could indicate greater severity of injury.

• Severe mechanism of injury • Time to follow commands is more than 15 minutes, • Loss of consciousness is greater than 30 minutes • Duration of posttraumatic amnesia is longer than 1 hour (eg, is the child repeating the same question?) • Trauma-related findings on neuroimaging • Extreme or exaggerated symptoms • Focal neurologic findings on exam • Seizure-like activity

Other confounding factors that would warrant further work up to rule out severe brain injury would be a child less than 2 years of age, any drug/alcohol intoxication, and hypocoagulability.

Diagnostic workup

The latest International Consensus Statement on Concussion in Sport provided updated framework for acute sport-related concussion evaluations within the first 72 hours and up to 1 week after the injury by using Concussion Recognition Tool-6 (CRT6), Sport Concussion Assessment Tool-6 (SCAT6), and Child SCAT6 (95). A systematic review stated that utilizing a combination of computerized cognitive testing and use of the Post-Concussion Symptoms Scale distinguished high school athletes with mild traumatic brain injury from those without traumatic brain injury within the first 4 days of injury, and the Graded Symptom Checklist was found useful in distinguishing children 6 years and older with mild traumatic brain injury from those without within the first 2 days post-injury (68). Additional measures available for immediate assessment of concussion include the Standardized Assessment of Concussion (SAC), King-Devick Test, and balance testing such as the Balance Error Scoring System. There are multiple “apps” on concussion that can be used at the sideline. Independent of the sideline test results, if a child is complaining of symptoms of concussion after an injury, the child should not return to play that day and should be further evaluated.

Many children are brought to the emergency department for evaluation after concussive injury, leading to critical evaluation of clinical indications to obtain a head CT balanced with the risk of radiation exposure. Over a 5-year period, the rate of head CT use in the evaluation of patients diagnosed with concussion increased nearly 40% despite an overall decrease in head injury severity (124). One hospital found that creating and implementing a “minor head injury guideline” led to a reduced number of head CTs (37). In an effort to avoid unnecessary head CTs, the Pediatric Emergency Care Applied Research Network (PECARN) derived and validated two age-based prediction rules to identify children at very low risk of clinically-important traumatic brain injuries who do not typically require CT scans (59). Up to 7.5% of children seen in the emergency department with mild traumatic brain injury will have an intracranial injury. It is recommended that health care professionals should not routinely obtain head CT for diagnostic purposes in mild traumatic brain injury. They should, however, identify risk factors that may indicate a more severe form of traumatic brain injury and, thus, warrant neuroimaging. These include age younger than 2 years, vomiting, loss of consciousness, severe mechanism of injury, severe or worsening headache, amnesia, nonfrontal scalp hematoma, GSC lower than 15, and clinical suspicion for a skull fracture (68).

Current recommendation is that biomarkers should not be used outside of research setting to diagnose mild traumatic brain injury in children (68). The U.S. Food and Drug Administration have approved the use of blood testing Ubiquitin C-terminal Hydrolase L1 (UCH-L1) and Glial Fibrillary Acidic Protein (GFAP) in patients 18 years and older with suspected concussion. There are computerized tools available for assessment of cognitive function after an injury. These computerized tools, such as ImPACT, are increasingly being used in athletics to collect baseline data, although the clinical utility of baseline testing has not been fully established. Evidence indicates that the validity of computerized tests used for baseline (preinjury) documentation may be affected by multiple factors including age, test setting, and recent sleep (66; 78). The lower age limit of ImPACT is 12 years old, and a pediatric version of ImpACT is also now available for 5 to 11 years of age. Taylor provides a summary and critical assessment of neuropsychological measures used in pediatric concussion (111).

More research is needed to validate all of the acute and computerized testing in the pediatric concussion population. All of these tests may also be influenced by premorbid factors such as underlying ADHD as well as use of stimulants; thus, interpretation is often appropriately deferred to a pediatric neuropsychologist. In fact, emerging evidence indicates the confounding effects of ADHD and learning disability on current concussion testing and supports evaluation of different baseline/normalized scores for those with premorbid learning and attention disorders (30). Additional “pencil and paper” tests or other tools may be appropriately used by neuropsychologists when evaluating children with concussion.

Graded exercise testing, vestibular-ocular motor screening, and dual task balance testing are some of the additional methods being explored to aid the assessment of concussion (47; 63; 93).

Management

Other than symptom management and supportive care, there is little to suggest specific acute medical interventions following a concussion. A study suggests a potential benefit from hypertonic saline, with children with closed head injury reporting less pain 2 to 3 days after hypertonic saline compared to those that received normal saline following concussion (67). However, hypertonic saline should not be administered outside of a research setting (68). More evidence is needed regarding potential acute interventions before changes are expected in the management shortly after concussion. However, for those seeking emergent or urgent care, concussion education and discharge instructions are critical. Patients and families should be counseled that most (70% to 80%) of children with mild traumatic brain injury do not show significant difficulties that last more than 1 to 3 months and that each injury is unique and follows its own healing trajectory. It Is important to recognize premorbid conditions that will assist in anticipatory guidance for prognosis as well. These include a previous history of concussions, lower cognitive ability, neurologic or psychological disorders, learning disabilities, increased pre-injury symptoms, and family or social stressors (68).

An analysis of concussion in one pediatric emergency department indicated that most children with concussion were discharged without a concussion diagnosis or instructions and restrictions (26). A survey of pediatric emergency care providers revealed that 81% of providers report using a published concussion guideline for clinical management and 91% reported using medications to treat concussive symptoms, most often acetaminophen and nonsteroidal antiinflammatory treatment (55).

Early education on concussion symptoms, expected course of recovery, and management/coping strategies may notably improve recovery. One study found that parents and children seen in clinic within 1 week from injury and given a basic concussion information booklet demonstrated recovery within 3 months compared to the control group of children with concussion (not given the pamphlet and seen at 3 months) who reported more symptoms and increased stress 3 months after injury (98).

Hallmarks in the management of pediatric concussion include immediate removal from the game at onset of concussive symptoms and NO same day return to play. Physical and cognitive rest is recommended while actively symptomatic in the acute period; however, neither evidence nor guidelines exist to clarify the definition or extent of either. Silverberg and Iverson provide a thoughtful analysis of the current concussion management recommendations for physical and cognitive rest (107).

Based on the neurometabolic case in mouse models of mTBI, the occurrence of diffuse brain edema following a second injury before recovery from an initial concussion, and a window of neurometabolic vulnerability between concussions noted in MRS studies (116) and mouse models (90), there seems to be a period where the brain is uniquely susceptible. Thus, “rest” is a reasonable recommendation after concussion. At this time, the precise timing of vulnerability in children with concussion has not been further detailed. Additionally, the meaning of “rest” is unclear, though certainly avoiding a second injury during the acute phase is critical.

Clinical treatment plans often include extending “rest” until the patient is fully asymptomatic. However, De Luigi and colleagues reviewed a compilation of studies that compared and contrasted rest, exercise, rehabilitation, and return to activity in actively symptomatic pediatric concussion patients, and it was found that there was strong evidence to suggest sub-symptom threshold aerobic exercise (such as walking or stationary bike) was beneficial for adolescent patients regarding their concussion symptoms (25). The term “relative rest” is more appropriate in regard to recommendations for continuing activities of daily living and reduced screen time in the first 48 hours (95).

“Cognitive rest” was previously recommended in the acute (days) period after injury; however, it is important to recognize the benefits of returning to school quickly and providing proper academic accommodations (100). A retrospective review of children with concussion indicated that the clinical recommendation of cognitive rest did not affect time to symptom resolution; only the number of acute symptoms predicted prolonged recovery (33). Furthermore, a study of school aged children and young adults with concussion suggests that those undergoing 5 days of “strict rest” reported more postconcussive symptoms and had a longer time to symptom resolution compared to the cohort of children taking only 1 to 2 days of strict rest followed by gradual return to activity (113). However, another study found that both total symptom burden and cognitive activity days were related to symptom duration, suggesting that children reporting more days of greater cognitive activity had a longer time to resolution of symptoms (14). A study looked more specifically at the academic effects of concussion in both children and adolescents, noting that concussion can adversely affect learning and school performance, especially in children who had not yet recovered from concussion (101). With returning to learn, it has been shown that the limiting of use of screen time is best used in the first 48 hours after injury, but otherwise, it may not be effective beyond that (69). The Concussion in Sport Group published guidelines on “Return to Learn” strategy (95; 91).

Physical rest is equally nuanced. It is currently recommended to return to activities of daily living as soon as possible with only mild and brief exacerbations of symptoms should be encouraged provided that symptoms are no more than mildly and briefly increased (95). Emerging evidence supports graded exercise within the subacute period (31; 62), which may promote recovery to cerebral blood flow alterations (61). Furthermore, a symptom-free waiting period (withholding the child from activity for several days after symptom resolution) did not appear to alter recovery of high school and college athletes compared to those without a period of waiting (79). In a sample of 364 children and young adults presenting to a sports medicine clinic, the reported level of daily physical activity following injury was not related to postconcussion symptoms, and in adolescents, higher reported levels of physical activity were associated with shorter symptom duration (46). Therefore, resuming some degree of physical exertion may not be detrimental and may even be beneficial to concussion recovery. An individually tailored rehabilitation program, utilizing the submaximal threshold of a patient with sports-related concussion, with graded aerobic treadmill testing may be helpful in the assessment and treatment of concussion as reported by Cordingley and colleagues (22).

Given the high potential for prolonged symptoms, clinical providers may also notice deconditioning or mood effects (often leading to a late increase in symptoms) if a child is withheld from all physical activity until asymptomatic. One small resting state–fMRI indicated altered connections present only after physical exertion 10 days after injury (50), and another study of adolescent athletes demonstrated decline in memory testing and speed on ImPACT after physical exertion (83). Thus, the specific timing, duration, and intensity of gradual exercise represent another area in need of evidence.

Gradual return to play is recommended under the guidance of a trainer, coach, physician, or other provider skilled in managing concussions. A child should complete each level of activity for a minimum of 24 hours before advancing; thus, it should take a minimum of 6 days before returning to full contact sports. The American Academy of Pediatrics report on sports-related concussion in adolescents and children provides another sample of the stepwise approach to resuming physical activity (42). It is important to assure a child has resumed and is tolerating their full school load (the “job” of a child) prior to complete clearance for sports. The CDC and Concussion in Sport Group have published guidelines on “Return to Sport” strategy (95).

The following are Gradual Return to Play guidelines as per the ACE Care Plan:

	1. No physical activity.
	2. Low levels of physical activity. This includes walking, light jogging, light stationary biking, and light weightlifting (lower weight, higher reps, no bench, no squat).
	3. Moderate levels of physical activity with body or head movement. This includes moderate jogging, brief running, moderate-intensity stationary biking, moderate-intensity weightlifting (reduced time or reduced weight from the typical routine).
	4. Heavy noncontact physical activity. This includes sprinting or running, high-intensity stationary biking, regular weightlifting routine, noncontact sport-specific drills (in three planes of movement).
	5. Full contact in controlled practice.
	6. Full contact in game play.

Accommodations involve communication with the school guidance counselor, administrator, nurse, and/or athletic trainer, if available. The ACE Care Plan provided by the CDC includes a template for both school and physical accommodations. It is also important to assess tolerance/symptom exacerbation and remove/adjust supports as needed. The treatment plan should be individualized to each specific child.

Posttraumatic headache was reported in almost 8% of children 3 months after having sustained a concussion, with 82% having past or family medical history of migraines (58). Larsen and colleagues performed a systematic review of pharmacologic treatment of acute and persistent posttraumatic headaches, and they concluded that there is minimal evidence with an increased need for randomized control trials to draw better conclusions (60). Regarding which medications are typically used, there was a survey of 95 child neurologists who manage posttraumatic headache. Amitriptyline/nortriptyline was chosen as a first-line agent 94% of the time, followed by topiramate at 72% and vitamins/supplements at 59%. Nonsteroidal anti-inflammatory medications were most recommended as abortive treatment (97). Caution should be taken to avoid medication overuse headaches, especially with nonsteroidal anti-inflammatory medications. Proper nutrition, adequate hydration, and rest are strongly encouraged. Docosahexaenoic acid is felt to be beneficial for overall brain health, and there is emerging evidence of the protective role of docosahexaenoic acid in injured brain (120); however, effective or treatment doses specific to children have not been clearly established.

It is important to consider a multidisciplinary approach for children. Early evidence suggests that an active rehabilitation program can promote recovery with reduced symptoms, decreased fatigue, and improved mood for adolescents slow to recover from a sports-related concussion (32).

Physical therapy can provide endurance training and encourage return to physical activity for children who remain persistently inactive. There was a case control study that evaluated benign paroxysmal positional vertigo in concussed pediatric patients occurring in about one third of their patients. All of their patients with benign paroxysmal positional vertigo were able to be treated with repositioning maneuvers (118). This further stresses the need of physical therapy for patients, even in the acute period.

Screening for concomitant mental health concerns or other stressors are important. Behavioral psychology can work on headache management techniques or cognitive behavior therapy in certain circumstances.

Outcomes

Most evidence indicates gradual recovery from symptoms within days to weeks of injury. Compared to adults, children and adolescents are more likely to have prolonged recovery with postconcussive symptoms reported for months in only a minority (108; 122; 07; 110; 24).

Patients and families should be counseled that most (70% to 80%) of children with mild traumatic brain injury do not show significant difficulties that last more than 1 to 3 months and that each injury is unique and follows its own healing trajectory (68). Chrisman and colleagues reported that after a concussion, 50% of athletes returned to school by 3 days, 50% returned to sport by 13 days, and 50% returned to a baseline level of symptoms by 3 weeks (19).