WHAT’S KNOWN ON THIS SUBJECT: Although there has beenincreasing research into the effects of concussion on thedeveloping brain in recent years, little is known about theexpected duration and clinical course of individual post-concussive symptoms in children.
WHAT THIS STUDY ADDS: Children and adolescents havea significant burden of disease after concussion, with typicalpatients experiencing physical effects such as headacheimmediately after the injury, emotional symptoms later in therecovery period, and cognitive symptoms that may be presentthroughout.
abstractOBJECTIVES: To examine the incidence, duration, and clinical courseof individual post-concussive symptoms in patients presenting to apediatric emergency department (ED) with a concussion.
METHODS: We conducted secondary analysis of a prospective cohortstudy of patients 11 to 22 years old presenting to the ED of a children’shospital with an acute concussion. The main outcome measure wasduration of symptoms, assessed by the Rivermead Post-ConcussionSymptoms Questionnaire (RPSQ). Patients initially completed aquestionnaire describing mechanism of injury, associated symptoms,past medical history, and the RPSQ, then were serially administeredthe RPSQ for 3 months after the concussion or until all symptomsresolved.
RESULTS: Headache, fatigue, dizziness, and taking longer to think werethe most common symptoms encountered at presentation, whereassleep disturbance, frustration, forgetfulness, and fatigue were thesymptoms most likely to develop during the follow-up period thathad not initially been present. Median duration of symptoms wasthe longest for irritability (16 days), sleep disturbance (16 days),frustration (14 days), and poor concentration (14 days), whereasnausea, depression, dizziness, and double-vision abated mostquickly. One month after injury, nearly a quarter of children stillcomplained of headache, .20% suffered from fatigue, and nearly20% reported taking longer to think.
CONCLUSIONS: Among patients presenting to a pediatric ED after a con-cussion, physical symptoms such as headache predominate immedi-ately after the injury, emotional symptoms tend to develop later in therecovery period, and cognitive symptoms may be present throughout.Pediatrics 2014;133:999–1006
AUTHORS: Matthew A. Eisenberg, MD, William P. Meehan III,MD, and Rebekah Mannix, MD, MPH
Division of Emergency Medicine, Boston Children’s Hospital,Harvard Medical School, Boston, Massachusetts
Dr Eisenberg was responsible for study conception and design,data acquisition and analysis, and manuscript preparation;Dr Mannix was responsible for study conception, study design, dataanalysis, and manuscript preparation; Dr Meehan wasresponsible for study conception, study design, and manuscriptpreparation; and all authors approved the final manuscript assubmitted.
www.pediatrics.org/cgi/doi/10.1542/peds.2014-0158
doi:10.1542/peds.2014-0158
Accepted for publication Feb 26, 2014
Address correspondence to Matthew A. Eisenberg, MD, Division ofEmergency Medicine, Boston Children’s Hospital, 300 LongwoodAve, Boston, MA 02115. E-mail: [email protected]
FINANCIAL DISCLOSURE: The authors have indicated they haveno financial relationships relevant to this article to disclose.
FUNDING: No external funding. Expenses related to use ofresearch coordinators were paid by the Division of EmergencyMedicine, Boston Children’s Hospital.
POTENTIAL CONFLICT OF INTEREST: The authors have indicatedthey have no potential conflicts of interest to disclose.
PEDIATRICS Volume 133, Number 6, June 2014 999
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Mild traumatic brain injury (mTBI)remainsoneof themostcommonreasonschildren present for medical care in theUnited States,1–3 and concerns about itseffects on the developing brain have led toa large number of recent studies exam-ining pediatric concussion. Despite this,the expected course of individual post-concussive symptoms in children hasnot been well described. There is thuslittle evidence to help guide physicians,patients, and their families regarding in-cidence and duration of such typicalcomplaints after a head injury as fatigue,poor concentration, and irritability.
Estimates as to duration of post-concussive symptoms in children rangewidely, with reports showing as few as10% of patients symptomatic 7 days aftersport-related concussion4 to as many as43% still with symptoms 3 months afterbeing hospitalized for mTBI.5 One cohortstudy conducted in the emergency de-partment (ED) setting showed 29.3% ofchildren aged 5 to 18 years still symp-tomatic 3 months after sustaining aconcussion, with the most commonsymptoms being headache, fatigue,and frustration.6 Another study of chil-dren 18 years and younger demonstratedthat 11% of patients who had a concus-sion were symptomatic at the 3-monthmark, with fatigue, emotional lability, andirritability being the most common en-during symptoms.7 In a smaller group ofadolescents hospitalized for mTBI, sleepissues, difficulty concentrating, and feel-ing “slower” were the most commonsymptoms reported at a 2- to 3-weekfollow-up visit.5
To our knowledge, only 1 study hasattempted to delineate the course ofspecific post-concussive symptoms inchildren. This prospective cohort studyof patients aged 5 to 17 years who hadmTBI focused exclusively on headaches,finding the prevalence of this symptomwas 43% 3 months after injury and41% a full 12 months later.8 For con-cussed children, their families, and their
physicians, an understanding of thetime course over which specific symp-toms resolve after a head injury isimportant to optimally manage and setexpectations for recovery. In a pre-vious study of children and adolescentspresenting to a pediatric ED after anacute concussion, we sought to identifydemographic and injury factors thatwould predict a prolonged recoveryperiod. Our previous results showedthat themedian time to resolution fromall post-concussive symptoms was 13days, with .30% of patients stillsymptomatic 4 weeks after injury.9 Inthis study, we performed a secondaryanalysis of this same cohort, to exam-ine individual post-concussive symp-toms and better define their incidence,duration, and clinical course.
METHODS
Study Design and Population
We conducted secondary analysis ofa prospective cohort study of consec-utive patients aged 11 to 22 years whopresented to the ED of a tertiary carechildren’s hospital within 72 hours ofa concussion from September 1, 2011to August 31, 2012.
Definition
Concussion was defined as a blunt in-jury to the head or to the body withimpulsive force transmitted to the headthat resulted in either (1) alteration ofmental status, or (2)anyof the followingsymptoms that started after the injuryand were not present before the injury:headache, nausea, vomiting, dizziness/balance problems, fatigue, drowsiness,blurred vision, memory difficulty, ordifficulty concentrating, without evi-dence of intracranial hemorrhage. Wechose this broad definition to includeboth those who had alteration of con-sciousness and those who presentedwith typical post-concussive symptomsfollowing a head injury.10–12
Patients were excluded from the studyif any of the following were present:(1) Glasgow Coma Score (GCS),13 onarrival to the ED, (2) coexisting frac-ture of skull or long-bone, (3) coex-isting injury to intra-abdominal orintrathoracic organ or spinal cord, (4)cognitive or developmental disabilitypreventing patient from completing thequestionnaire, or (5) involvement ofeither law enforcement or ED socialworkers for victims of an assault.These criteria were designed to dis-tinguish post-concussive symptomsfrom symptoms related to other inju-ries or psychological stresses relatedto major trauma or assault.
Outcomes
The primary outcome was time courseof recovery of individual post-concussivesymptoms assessed via the RivermeadPost-Concussion Symptoms Ques-tionnaire (RPSQ). The RPSQ is a 16-item concussion symptom inventorychecklist that has been used exten-sively in both adult and pediatricstudies of mTBI,7,13,14 has shown a highdegree of inter-rater and test-retestreliability,15,16 and is valid and unbi-ased in young children.14,17 The ques-tionnaire was available to studyparticipants in both English and Span-ish. Symptom duration was defined asthe amount of time between the datethat the patient first reported thesymptom present at greater than pre-injury baseline (score of 2 or higher onthe symptom inventory) and the datethat the patient first reported that thesymptom was no longer present orwas back to pre-injury level (score of0 or 1 on the symptom inventory). Onfollow-up questionnaires, patients ad-ditionally were asked to report theiramount of cognitive and athletic activityon a 5-point scale ranging from full restto full participation, and to comparecurrent school and athletic perfor-mance to their pre-injury performance.
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Enrollment and Consent
Study participants were enrolled dur-ing their ED visit by trained researchcoordinators after informed consent(and assent for patients age ,18years) was obtained. Eligible patientswho were not contacted during theirED visit were offered enrollment afterED discharge via phone if they were stillwithin 72 hours of the injury. Onenrollment, patients completed anelectronic questionnaire asking fordemographic information, mechanismof injury, associated symptoms, pastmedical history, and the RPSQ. Dataregarding patient medical history wasculled from this self-report anda questionnaire filled out by the EDprovider, with selective chart reviewperformed to clarify discrepancies.
Follow-Up
An online follow-up questionnaire con-tainingtheRPSQwassentelectronically topatients or their parent, depending onfamilypreference,1,2,4,6,8,and12weeksafter theirEDvisitoruntil theymetcriteriafor symptom resolution, defined as allindices of the RPSQ scored a 0 or 1. Studyparticipation terminated with the week-12 questionnaire. Instructions requestedthat the patient fill out the surveywith theassistance of the parents as needed.Patients who reported resolution ofsymptoms were prompted to provide thelast date on which any symptoms oc-curred. Patients who had incomplete orinconsistent data were called to resolvethese issues. Patients who failed over2 consecutive intervals to fill out thequestionnaire were considered lost tofollow-up. Study data were collected andmanaged by using REDCap (ResearchElectronic Data Capture, Nashville, TN)electronic data capture tools hosted atBoston Children’s Hospital.18
Statistical Analysis
Statistical analysis was performed byusing PASW Statistics 18 (SPSS, Inc,
Chicago, IL). Continuous data were ana-lyzed by Student’s t test orWilcoxon RankSum test as appropriate. Mediansymptom duration was assessed asa continuous variable from 0 to 90 daysusing Kaplan-Meier analysis, a measurethat takes into account expected dura-tion of symptoms for censored patients(those who were either lost to follow-upor still symptomatic at the end of thestudy period). Percent of patients symp-tomatic at each time point was cal-culated by dividing the number ofpatients reporting the symptom at thespecified time by the number of patientswho either met criteria for symptomresolution or were still actively beingfollowed at that time point. Values wereconsidered statistically significant ifP # .05. The Boston Children’s HospitalInstitutional ReviewBoard approved thisstudy before onset of data collection.
RESULTS
Study Population
Of 302 patients approached for thestudy, 280 (93%) were enrolled; 235(84%) of these patients completed atleast 1 follow-up questionnaire, and 45(16%) were lost to follow-up. Sixty-sixpercent were enrolled on the calen-dar day their concussion occurred,24.7% thenext calendarday, 7.2%2dayslater, and 1.7% 3 days later. Demographicsand characteristics of patients whowere included in the study and thosewhowere lost to follow-up are shown inTable 1.
Course of Symptoms
Although headache, fatigue, dizziness,and taking longer to think were themost common symptoms encounteredat presentation, sleep disturbance,frustration, forgetfulness, and fatiguewere the symptoms most likely to de-velop during the follow-up period thathad not been present initially after theinjury (Table 2).
Duration of Symptoms
Irritability, sleep disturbance, frustra-tion, and poor concentration persistedthe longest, whereas nausea, de-pression, dizziness, and double visionabated the most quickly (Table 2). Onemonth after injury, nearly one-quarterof children still complained of head-ache,.20% suffered from fatigue, andnearly 20% reported taking longer tothink (Figs 1 and 2).
Cognitive Rest, School, and AthleticPerformance
One week after the injury, 197 subjectscompleted the questionnaire regardingcognitive and sports activity and schooland athletic performance. Fifty-sevenpercent of patients reported at leastmoderately limiting cognitive activity,whereas15.2% limitedcognitiveactivityonly minimally and 27.4% had notlimited cognitive activity at all. Eighteenpercent of patients reported worseschool performance than before theirconcussion, whereas 48.2% reportedno decline in school work (the remain-der had not attended school or doneany school work in the interim). Only8.2% of patients had returned to fullathletic activity, with the majority(63.8%) reporting no athletic activity atall except for walking.
DISCUSSION
To our knowledge, this is thefirst reportto describe the precise duration of in-dividual symptoms after pediatricconcussion. Previous studies havedemonstrated that post-concussivesymptoms can be broadly categorizedinto physical, emotional, and cognitiveclusters, with a high degree of overlapbetween them,19–22 but neither the in-cidence of these symptoms nor theirrelative burden throughout the re-covery period have been well de-scribed in children.23,24 Here we showthat although the majority of chil-dren initially present to care after
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a concussion with symptoms of head-ache, dizziness, and fatigue, new symp-toms often develop during the recoverycourse, particularly those that havea substantial emotional component.Whether this secondary symptom de-velopment is attributable to the un-derlying pathophysiology of mTBI orthe psychosocial consequences of theconcussion and the restrictions placedon children during their recovery is notknown. Understanding the recoverycourse for children after concussionis important for caregivers and fami-lies who will be managing symptoms,as well as for academic and athleticaccommodations.
For themajority of patients in our study,symptoms resolved within 2 weeks ofthe injury. During that recovery period,however, patients experienced a largesymptomburdenandsignificant impacton subjective functioning. One weekafter the injury, more than two-thirds of
the patients still had a headache;a majority complained of poor con-centration, dizziness, fatigue, and tak-ing longer to think; and.40% struggledwith forgetfulness, light sensitivity, andnoise sensitivity. Few patients hadreturned to full cognitive activity orsports participation 1 week after theinjury, although we cannot say whetherthese limitations were attributable tosymptoms or to clinician advice to rest.Taken together, these findings showthat although concussion symptomsoften resolve quickly, they can be de-bilitating in the short term for manypatients.
Our study adds to previous inves-tigations that have demonstrated thatheadache is themost commonly reportedpost-concussive symptom,5,6,8,25–28 pres-ent in 85.1% of children in our cohorton presentation to the ED and in 88.9%of patients at any point during thefollow-up period. We found that the
median duration of headache was 13days, with 5.3% still having headache at3 months, notably less than the 43%reported by Blume and colleagues ina previous pediatric mTBI cohort.8 Webelieve differing survey methodologyexplains these discrepant findings, asparticipants in Dr Blume’s study wereasked to rate their pain on a scale of0 to 10, with any score $1 consideredpositive for presence of headache. Inour study, on the other hand, we con-sidered a patient to have ongoingheadache only if they indicated thattheir pain was greater than their pre-injury baseline on the RPSQ.
After headache, fatigue was the secondmost common presenting symptom inour study, reported by 64.2%of patientson initial evaluation. Notably, an addi-tional 15.4% of children who did notinitially report fatigue subsequentlydeveloped this symptom. A substantialnumber of children (21.6%) also de-veloped sleep disturbance after theirinitial evaluation. This finding suggeststhat children who have a concussionshould be warned about the possibilityof developing fatigue and sleep issues,and these symptoms should be spe-cifically assessed during follow-upevaluation. Moreover, despite beingcharacterized as somatic symptoms,both sleep issues and fatigue may havea significant emotional component, socareful attention should be paid to co-incident emotional symptoms in chil-dren who have these complaints.21
The emotional symptoms of concussion(frustration, depression, irritability,and restlessness) were not commonlyreported on presentation, but did de-velop in large numbers of patientsduring follow-up and were among thesymptoms that lasted the longest. Anexception to thiswas depression, whichdeveloped in only 8.6% of patients whodid not report it initially. It is unclearwhether this reflects the fact that de-pression itself did not develop as
TABLE 1 Patient Demographics
Included in Study (N = 235) Lost to Follow-up (N = 45) P Value
All data are presented as percentages unless otherwise noted. ADHD, attention-deficit/hyperactivity disorder; CT, computedtomography; GCS, Glasgow Coma Scale; LD, learning disability; LOC, loss of consciousness; PMH, previous medical history.
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frequently as other complaints, or thatpatients were reticent to endorse de-pression owing to the stigma associ-ated with this symptom. Pediatriciansand specialists in concussion careshould continue to carefully evaluatepatients for the emotional symptoms ofconcussions attributable to both thephysical injury and the psychosocialsequelae that often follow these headinjuries.
Cognitive symptoms were particularlyburdensome inourcohort, as theywerepresent in substantial percentagesinitially, still went on to develop inmanyadditional patients, and had greaterthan average duration of symptoms,with the exception of forgetfulness,which resolved on average within 11days. These findings support the im-portanceofacademicaccommodationsfor children after concussion.
Allowing for overlap between domainsand some notable exceptions outlinedabove, our study shows that the phys-ical symptoms of concussion presentearly and resolve early after the injury,emotional symptomsdevelop later thanthe other domains, and cognitive
symptoms impair many patients bothimmediately after their head traumaand long into the recovery period. Un-derstanding this expected progressionof symptoms has several potentialbenefits. For patients, it may help tonormalize the experience of recoveryfrom concussion, preventing the addi-tional stress that comes from worryingthat symptoms are unusual or exces-sive. For families and school personnel,this knowledge may help them betterprepare the home and school envi-ronment for expected obstacles to re-covery and return to normal academicand athletic participation. For healthcare providers, it may help reduceunnecessary testing and referrals ow-ing to concern that a patient’s course isatypical, better target post-concussiveevaluations to expected symptoms, andbetter inform the anticipatory guid-ance given to patients and their fami-lies.
There are several limitations to ourstudy. We did not include a controlgroup, so we cannot conclude withcertainty that the symptoms experi-enced by patients in our cohort are
attributable to the head injury and notpart of the recovery from injury ingeneral, the psychosocial conse-quences of illness, or malingering. Awide body of literature, however, hasestablished that post-concussive symp-toms are more frequent in mTBI patientsthan in other injured patients, and thatpost-concussion syndrome should berecognized as a unique and valid di-agnosis apart from other forms of re-covery from trauma.7,29–31
An additional limitation is that westudied only self-reported symptoms,and patient reports may have beeninfluenced by a desire to either ex-pedite or, conversely, avoid returnto school or sports. Furthermore,although we surveyed patients fre-quently during the study period, ourprimary focus was on pinpointing thedate on which all symptoms resolved,not individual symptoms. As a result, wedefined the duration of a symptom asthe time from which a patient firstreported the symptom until the timethat the patient first reported that thesymptom was no longer present. Thisnumber may have been shorter or
TABLE 2 Time to Resolution of Individual Post-Concussive Symptoms
CI, 95% confidence interval; n/a, not applicable.a Number of patients in the study minus patients censored before given time interval.
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longer than the actual symptom dura-tion, depending on the timing of thequestionnaire being filled out. However,
because we surveyed patients fre-quently during the follow-up period,we believe these estimates are likely
to more closely approximate symp-tom duration than a single follow-up questionnaire administered at 1
FIGURE 1Percent of patients reporting individual physical symptoms during study period. Bars represent 95% CI.
FIGURE 2Percent of patients reporting individual cognitive and emotional symptoms during study period. Bars represent 95% CI.
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given time point after the injury.Another limitation may come from thesmall number of patients who wereenrolled after their ED visit, and whoseinitial questionnaire may therefore re-flect the symptomspresent in the hoursto days after the initial injury, ratherthan those present at the time of theirED evaluation. Given the small numberof patients in this category and theshort time window in which they wererequired to fill out the questionnaireafter thehead injury,we think this effectis likely to be small.
There were differences between ourstudy population and the group thatwas lost to follow-up in terms of race,ethnicity, and presence of attention-deficit/hyperactivity disorder, althoughthere were no differences in otherfactors that have been shown to in-fluence concussion outcome, such asage, gender, loss of consciousness,previous concussion, or initial symp-tom burden. Finally, our study pop-ulation consisted of children and
adolescents referred to a tertiary carepediatric ED. This group likely repre-sents amore severely injured subset ofconcussion patients than those whoare treated on the field, in an outpatientclinic, or in a community ED, as patientsmay be treated initially in these lattersettings and then be referred to a pe-diatric ED owing to severity of symp-toms or need for imaging, subspecialtyconsultation, or admission. As a result,these results may not be generalizableto all children and adolescents aftera concussion.
Despite these limitations, our study hadseveral strengths, including a largesample size and prospective method-ology. We enrolled a high percentage ofeligible patients and a majority ofpatients continued participation untilsymptom resolution. Finally, unlikeprevious studies that focused on par-ticular subgroups of patients, such asparticipants in a particular sport, ourstudyexaminedall eligiblepatientswhopresented to a tertiary care ED.
CONCLUSIONS
Among children and adolescents pre-senting to a pediatric ED after a con-cussion, there is a significant burden ofdisease, particularly during the first 2weeks after injury. The typical patientwill see physical effects such as head-ache immediately after the injury,emotional symptoms that develop laterin the recovery period, and cognitivesymptoms may be present throughout.
ACKNOWLEDGMENTSMichael Monutaeux, ScD, provided sta-tistical guidance and support. MarkBerry, MA, provided programming andadministrative support. Mark Neuman,MD, and Lise Nigrovic, MD, assistedwithmanuscript review. The research coor-dinator team (John Andrea, BS, ElizabethPaulsen, BS, Lucy Abernethy, BA, KaitlinMorris, BA, Hillary Chu, BA, and JessicaLeSage, BS) enrolled and followed upwith patients and provided administra-tive support.
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DOI: 10.1542/peds.2014-0158 originally published online May 12, 2014; 2014;133;999Pediatrics
Matthew A. Eisenberg, William P. Meehan III and Rebekah MannixDuration and Course of Post-Concussive Symptoms
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