Acute Concussion Symptom Severity and Delayed Symptom Resolution
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Acute Concussion Symptom Severity and Delayed Symptom Resolution WHAT’S KNOWN ON THIS SUBJECT: Children are often evaluated AUTHORS: Joseph A. Grubenhoff, MD,a,b Sara J. Deakyne, in the emergency department after a concussion. Although MPH,c Lina Brou, MPH,a,b Lalit Bajaj, MD, MPH,a,b R. Dawn prolonged symptoms are associated with higher initial symptom Comstock, PhD,a,d and Michael W. Kirkwood, PhDe severity when measured 2 to 3 weeks after injury, a similar Departments of aPediatrics, and ePhysical Medicine and association with acute symptom severity has not been Rehabilitation, University of Colorado, Aurora, Colorado; bEmergency Department, and cDepartment of Research demonstrated. Informatics, Children’s Hospital Colorado, Aurora, Colorado; and dDepartment of Epidemiology, Colorado School of Public WHAT THIS STUDY ADDS: Higher acute symptom severity is not Health, Aurora, Colorado associated with development of persistent post-concussion KEY WORDS symptoms 1 month after injury, but persistent post-concussive brain concussion, brain injury, acute, brain injury, traumatic, symptoms affect a significant number of children after post-concussion symptoms, post-concussion syndrome, concussion. Outpatient follow-up is essential to identify children emergency medicine who develop persistent symptoms. ABBREVIATIONS AUC—area under the curve CI—confidence interval DSR—delayed symptom resolution ED—emergency department GCS—Glasgow Coma Scale abstract IQR—interquartile range LOC—loss of consciousness BACKGROUND AND OBJECTIVES: Up to 30% of children who have concus- ICD-10—International Statistical Classification of Diseases and sion initially evaluated in the emergency department (ED) display delayed Related Health Problems, 10th revision OR—odds ratio symptom resolution (DSR). Greater initial symptom severity may be an PCS—post-concussion syndrome easily quantifiable predictor of DSR. We hypothesized that greater symp- RR—relative risk tom severity immediately after injury increases the risk for DSR. Dr Grubenhoff conceptualized and designed the study, designed METHODS: We conducted a prospective longitudinal cohort study of chil- the database, oversaw data collection and analysis, drafted the initial manuscript, and reviewed and revised the manuscript; Ms dren 8 to 18 years old presenting to the ED with concussion. Acute symp- Deakyne performed the primary statistical analysis, assisted tom severity was assessed using a graded symptom inventory. Presence of with study design and database design, managed study DSR was assessed 1 month later. Graded symptom inventory scores were personnel in recruitment and data acquisition, and co-authored, tested for association with DSR by sensitivity analysis. We conducted a sim- reviewed, and revised the manuscript; Ms Brou assisted with the cluster analysis and drafting and reviewed and revised the ilar analysis for post-concussion syndrome (PCS) as defined by the manuscript; Dr Bajaj assisted with study design and study International Statistical Classification of Diseases and Related Health personnel management, oversaw data analysis, and critically Problems, 10th revision. Potential symptoms characteristic of DSR were reviewed and revised the manuscript; Dr Comstock assisted explored by using hierarchical cluster analysis. with data analysis and interpretation and critically reviewed and revised the manuscript; Dr Kirkwood conceptualized and RESULTS: We enrolled 234 subjects; 179 (76%) completed follow-up. Thirty- designed the study, assisted with data instrument design, and eight subjects (21%) experienced DSR. Initial symptom severity was not co-authored, reviewed, and revised the manuscript; and all significantly associated with DSR 1 month after concussion. A total of 22 authors approved the final manuscript as submitted. subjects (12%) had PCS. Scores .10 (possible range, 0–28) were www.pediatrics.org/cgi/doi/10.1542/peds.2013-2988 associated with an increased risk for PCS (RR, 3.1; 95% confidence doi:10.1542/peds.2013-2988 interval 1.2–8.0). Three of 6 of the most characteristic symptoms of DSR Accepted for publication Apr 10, 2014 were also most characteristic of early symptom resolution. However, Address correspondence to Joseph A. Grubenhoff, MD, 13123 East cognitive symptoms were more characteristic of subjects reporting DSR. 16th Ave, B-251, Aurora, CO 80045. E-mail: joe.grubenhoff@ childrenscolorado.org CONCLUSIONS: Greater symptom severity measured at ED presentation does not predict DSR but is associated with PCS. Risk stratification there- (Continued on last page) fore depends on how the persistent symptoms are defined. Cognitive symptoms may warrant particular attention in future study. Follow-up is recommended for all patients after ED evaluation of concussion to monitor for DSR. Pediatrics 2014;134:54–62 54 GRUBENHOFF et al Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
ARTICLE There are 630 000 emergency depart- severity of acute concussion symptoms a convenience sample of children ages ment (ED) visits annually for mild trau- may be a useful indicator of overall se- 8 to 18 years who sustained con- matic brain injury (concussion) among verity, and therefore may constitute an cussions no .6 hours before present- children ages 0 to 19 years.1 The ma- easily measurable risk factor to predict ing to Children’s Hospital Colorado’s jority of those who have concussion DSR. Recent research among youth trauma center ED, which has ∼65 000 experience symptom resolution in a few athletes who have sports-related con- annual visits. Patients identified on the weeks.2 However, a notable minority cussion supports this concept.20 ED electronic track board presenting experience persistent post-concussive DSR is a defining feature of post- with complaints of head injury or symp- sequelae. concussive syndrome (PCS). However, it toms associated with concussion were When examining post-concussive se- is important to highlight that there is no screened for enrollment 16 hours per quelae with standardized performance- universally accepted definition of PCS. day, 7 days per week by professional based cognitive and behavioral tests, Indeed, whether the nonspecific symp- research assistants who enrolled sub- most prospective studies indicate that by toms typically attributed to this condition jects and administered all study proce- 2 to 3 months post-injury, deficits are no constitute a syndrome with a common dures. Subjects were contacted by longer apparent.2–6 Fewer studies have pathophysiological explanation is contro- telephone 30 days after injury to com- systematically examined outcomes using versial.21,22 Nonetheless, DSR affects chil- plete follow-up procedures. Subjects dren who have concussion, and evidence were considered lost to follow-up if they post-concussive symptom reports from suggests that the risk for experiencing failed to respond after 3 attempts. The children. However, available research persistent symptoms is modifiable.23–25 study was approved by the Colorado suggests that some pediatric patients Identifying children at increased risk for Multiple Institutional Review Board. display more persistent symptoms than might be expected if examining perfor- DSR at the time of injury would allow Subjects mance-based test results alone.7,8 The selective implementation of interventions Children were considered to have acute injury risk factors predictive of earlier in the recovery phase. concussion if they had a Glasgow Coma delayed symptom resolution (DSR) in The primary objective of this study was Scale (GCS) score of 13 or 14 or at least children are poorly understood. to determine whether greater symptom 2 of the following symptoms occurr- Traditionally, determining the severity of severity measured immediately after ing after a direct blow to or rapid concussion was predicated on the pre- injury is associated with DSR. We hy- acceleration/deceleration of the head: sence of certain signs and symptoms at pothesized that higher scores on bystander-witnessed LOC; post-traumatic the time of injury, most notably loss of a graded symptom inventory immedi- amnesia; disorientation to person, consciousness (LOC).9,10 However, LOC ately after injury would be associated place, or time; subjective feelings of occurs relatively infrequently after con- with the DSR at 1 month in a pediatric ED slowed thinking; perseveration; vomiting/ cussion and is no longer used to define cohort presenting for acute evaluation nausea; headache; diplopia/blurry vision; injury severity as it is not consistently of concussion. Given the lack of a uni- dizziness; or somnolence. This clinical associated with neuropsychological de- versally accepted definition of PCS, we definition of concussion has been used ficits or DSR.11,12 In contrast, research also evaluated the performance of elsewhere.28,29 Children who had open in adults who have concussion has a graded symptom inventory for iden- head injuries, intoxication with alcohol found that post-traumatic amnesia as tifying the risk for meeting clinical or controlled substances, receipt of criteria for PCS laid out in the In- narcotics for pain control, injuries re- well as higher overall symptom levels ternational Statistical Classification of sulting from child abuse, multisystem (ie, both number and severity of symp- Diseases and Related Health Problems, injuries, or underlying central nervous toms) are associated with DSR.13–17 In 10th revision (ICD-10).26 Although ICD- system abnormalities were excluded. pediatric patients, greater symptom 10 has not yet been adopted in the levels present a few weeks after injury United States for coding purposes, the Measurements are associated with a longer duration of clinical criteria for PCS have been in- post-concussive symptoms.18 Greater At the ED enrollment visit, the following vestigated in concussion research.14,27 symptom levels have also been associ- demographic and injury character- ated with objective signs of altered METHODS istics were obtained: mechanism of mental status (eg, post-traumatic am- injury; parental report of previous nesia) in pediatric ED patients immedi- Study Design concussion; GCS score as determined ately after injury.19 Taken together, these We conducted a prospective cohort study by the treating provider; and presence findings suggest that the number and from October 1, 2010 to March 31, 2013 of of abnormalities on head CT scan as PEDIATRICS Volume 134, Number 1, July 2014 55 Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
reported by a board-certified pediatric have concussion, we planned to divide were conducted by using SAS 9.3 (SAS neuroradiologist if obtained. the cohort into low and high acute Institute, Inc, Cary, NC) and hierarchical Self-reported concussion symptoms symptom groups based on a defined clustering was conducted by using were quantified by using a graded cut-off score on a graded symptom in- SPSS 22.0 (IBM SPSS Statistics, IBM concussion symptom inventory. The ventory.32 We hypothesized that DSR Corporation, Chicago, IL). symptom inventory included the 12 would be more prevalent in the high items from the Concussion Symptom symptom group. Therefore, we esti- RESULTS Inventory30 plus 2 additional items re- mated that a sample size of 202 subjects Research assistants screened 1253 garding feeling irritable and sad. Sub- would be necessary to demonstrate patients for participation; 273 met in- jects verbally rated to what degree they a 15% absolute difference in prevalence clusion criteria and 234 subjects con- were experiencing 14 symptoms com- of DSR between the low and high sented to participate in the study. Of mon to concussion. We modified the symptom group, using 90% power and those enrolled, 179 subjects (76%) instrument for our pediatric popula- 2-tailed a of 0.05. completed the 30-day follow-up call and tion from a 0 to 6 point scale to a 0 to 2 Pre-injury scores for individual symp- comprised the study cohort (Fig 1). point scale to ensure understanding toms were subtracted from both the Subjects who did not complete follow- (range, 0–28). Parents rated their initial and 30-day follow-up scores to up were similar to those who did in child’s symptom severity in the week account for the presence of these non- age, gender, initial GCS, mechanism of before injury using the same in- specific symptoms before injury. Symp- injury, and history of previous concus- strument to provide a pre-injury base- toms present before injury but absent sion. Subjects lost to follow-up had line for these nonspecific symptoms. post-injury were scored as 0 (ie, a neg- significantly lower initial graded symp- The primary outcome, DSR, was de- ative score was not assigned). De- tom inventory scores (median score, 7; fined as the presence of 3 or more scriptive statistics for demographic and interquartile range [IQR], 4–12) com- symptoms 1 month after injury that acute injury data were calculated as pared with subjects completing the were absent or less severe in the week proportions or medians with inter- study (median score, 10; IQR, 7–13; before injury reflective of findings in quartile ranges and compared by using P = .01). similar cohorts.18 a x 2 test and Wilcoxon rank sum as Thirty-eight children (21%) from the ICD-10 criteria for PCS require the appropriate. Because there is no de- study cohort met the study definition for presence of 3 or more of the following 8 fined point separating low from high DSR. The pre-injury baseline symptom symptoms 1 month after injury: head- symptoms, a sensitivity analysis was score differed significantly in both ache, dizziness, fatigue, irritability, dif- performed by using the x2 statistic to groups, but the scores were low for both ficulty in concentration or performing determine the best cut-point for initial groups (Table 1). Two subjects in the mental tasks, impairment of memory, symptom severity scores to divide the early symptom resolution (ESR) group insomnia, and reduced tolerance to low and high groups using DSR as the and 1 in the DSR group experienced stress, emotional excitement, or alco- outcome. After sensitivity analysis, the a subsequent concussion in the follow- hol.31 The criteria do not adjust for best cut-point score was used for mul- up period. Forty subjects underwent symptoms present before injury as our tiple logistic regression, adjusting for head CT scan with only 5 abnormal clinical definition did. Patients were gender and age, as symptom report findings, all found in the ESR group considered to have PCS if they reported may vary by both age and gender.32–34 (Table 2). 3 or more symptoms on the Concussion The same methods were used The results of sensitivity analysis of Symptom Inventory that aligned with substituting our clinical definition of initial symptom inventory scores rang- PCS diagnostic criteria. There is no DSR with the PCS criteria. Results of x 2 ing from 8 to 14 are shown in Table 3. corollary for “reduced tolerance to analysis were considered significant if P The receiver-operator characteristic stress, emotional excitement, or alco- , .05. Relative risk and odds ratios (OR) curve is shown in Fig 2 (area under the hol” on the Concussion Symptom In- were considered significant if the 95% curve [AUC], 0.508; 95% CI, 0.475–0.683; ventory, so that symptom was excluded confidence interval (CI) did not include P = .14, rounded). The best cut point during analysis. 1. Lastly, we conducted hierarchical was a score of 11 with a sensitivity of clustering with average linkage analysis 63% and a specificity of 50% for DSR. Statistical Analysis to determine if certain symptoms were However, a score of 11 was not signif- Based on a previous study examining more characteristic of delayed versus icantly associated with DSR (P = .46). In symptom severity in ED patients who early symptom resolution.35 Analyses multivariate analysis, adjusting for age 56 GRUBENHOFF et al Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
ARTICLE PCS in the high symptom versus low symptom group was 3.7 (95% CI, 1.3– 10.6). Figures 3 and 4 show the results of cluster analysis. Three of the 6 most characteristic initial symptoms in the DSR and ESR groups (those in which the relative linkage distance on the x-axis are shortest) were similar (pho- nophobia, photophobia, blurred, or dou- ble vision). However, cognitive symptoms (difficulty remembering, difficulty con- centrating, or “feeling foggy”) were more characteristic of the DSR group. DISCUSSION Our study of children 8 to 18 years old presenting to an ED ,6 hours after FIGURE 1 concussion demonstrated that initial Study Participant Flow Diagram. symptom severity is not associated with DSR. This is an important finding given and gender, a score of 11 was still not in Fig 2 (AUC, 0.629; 95% CI, 0.509–0.748; evolving knowledge of concussion symp- associated with DSR (OR, 1.4; 95% CI, P = .03). The best cut point was 10 with tom resolution. In 1988, Lishman pro- 0.7–2.8). a sensitivity of 77% and specificity of posed that symptoms appearing shortly Twenty-two subjects (12%) met criteria 51% for PCS (P = .02). The relative risk after a concussion were primarily the for PCS. Sensitivity analysis for initial for PCS in subjects who had an initial result of physiologic derangements di- graded symptom scores ranging from 8 symptom score .10 was 3.1 (95% CI, rectly related to the injury, whereas to 14 is shown in Table 4. The receiver- 1.2–8.0). In multivariate analysis, ad- protracted symptoms were more likely operator characteristic curve is shown justing for age and gender, the OR for related to latent psychological factors.36 Two decades later, accumulated research suggests that “physiogenic” and “psy- TABLE 1 Demographic and Injury Characteristics for Early and Delayed Symptom Resolution chogenic” factors contribute to the con- Groups stellation of symptoms present both ESR (n = 141) DSR (n = 38) Pa immediately after injury as well as Demographics throughout recovery.37 Mean age, years (SD) 12.6 (2.5) 13.4 (2.2) .79 Male, % 70 66 .69 Intuitively, it is reasonable to assume History of previous concussion, % 24 29 .53 that more severe acute physiologic in- Injury characteristics jury will manifest as more severe Mechanism, % — — .79 Sport 48 53 — symptomatology and likely require Fall 43 34 — a longer recovery period. Recent re- Assault 3 5 — search supports this assumption. A Motor vehicle collision 1 3 — Other 5 5 — prospective cohort study of youth ath- LOC, % 26 29 0.68 letes evaluated in sports concussion Post-traumatic amnesia, % 26 34 0.42 clinics in the first 3 weeks after a con- Received head CT scan in ED, % 21 26 0.52 Abnormal head CT scan results, % 4 0 0.02 cussion demonstrated that increasing Initial GCS, medianb 15 15 0.99 initial graded symptom inventory Preinjury graded symptom score, median (IQR) 1 (0–2) 2 (1–4) 0.002 scores were associated with increased Initial ED graded symptom score, median (IQR) 9 (6–13) 10.5 (7–15) 0.14 odds of symptom resolution occurring a x 2 was used to compare proportions and Wilcoxon rank sum to compare medians. x2 analysis compared the overall difference among mechanism for the ESR and DSR groups and only this single p-value is provided. beyond 28 days.20 Similarly, pediatric b IQR for GCS was 15–15 for both groups. ED patients who had high symptom PEDIATRICS Volume 134, Number 1, July 2014 57 Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
TABLE 2 Characteristics of Subjects Who Had Abnormal Head CT Scans but our results differed from these Age (y) Gender GCS LOC (+/2) Injuries previous reports. This suggests that 10.8 F 15 – Cerebral contusion acute symptom report alone is not an 10.0 M 14 – Subarachnoid and epidural hematoma, skull fracture accurate reflection of the physiologic 14.0 M 15 + Subdural hematoma 9.4 M 14 – Subarachnoid hematoma, skull fracture and psychological factors that ulti- 10.1 M 15 + Subarachnoid hematoma mately lead to DSR. We defined DSR in terms relevant to TABLE 3 Sensitivity Analysis of Graded Symptom Inventory Scores for Identifying Delayed clinical practice. Specifically, we de- Symptom Resolution veloped a definition that would likely Cut Point Sensitivity, % Specificity, % NPV, % PPV, % P prompt a primary care provider to refer 8 73 33 79 26 .66 a child for specialist evaluation (at least 9 71 33 81 22 .45 3 symptoms that are worse 1 month 10 71 35 82 23 .14 after injury than they were before in- 11 63 50 84 26 .46 12 53 55 81 24 .13 jury). Although the clinical criteria for 13 47 66 82 27 .19 PCS also require the presence of at least 14 37 74 81 27 .10 3 symptoms 1 month after concussion, the diagnostic accuracy of this defini- levels measured in the early weeks tation of concussion symptoms, there is tion is a topic of scientific debate as it is after a concussion had significantly some evidence that the acute injury both subjective and imprecise.39–41 higher odds of symptoms persisting factors are stronger determinants of There is also significant controversy as for up to 1 year.18 In both studies, initial symptom reports early in recovery, to whether the term “syndrome” is symptom inventories were obtained an whereas non-injury factors contribute appropriate, given that common con- average of 11 days after concussion. more to persistent symptoms.38 A cussion symptoms are also found in Although both physiologic and psycho- strength of our study is that we en- patients who do not have concussion.42 logical factors contribute to manifes- rolled subjects within 6 hours of injury, Regardless of these shortcomings, PCS FIGURE 2 ROC curves displaying sensitivity analysis of concussion symptom inventory scores for identifying delayed symptom resolution or post-concussive syndrome. Optimal scores (closest to upper left of graph) for each outcome are shown along with the AUC and associated P value for each curve. 58 GRUBENHOFF et al Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
ARTICLE TABLE 4 Sensitivity Analysis of Graded Symptom Inventory Scores for Identifying ICD-10 Post- different criteria for PCS showed that Concussion Syndrome a subset of 6 symptoms common to all 3 Cut Point Sensitivity, % Specificity, % NPV, % PPV, % P criteria was specific to PCS owing to 8 77 33 91 14 .46 concussion among adults.44 In contrast, 9 77 36 92 14 .34 10 77 51 94 18 .02 other work calls into question whether 11 64 55 92 17 .11 the symptoms included in various di- 12 55 66 91 18 .10 agnostic criteria are specific to con- 13 41 73 90 18 .21 cussion. Our results resemble those of 14 36 80 90 21 .10 McCauley, Boake, and colleagues, who found wide variations in the prevalence has been studied as an outcome mea- .10 was associated with a threefold of PCS, depending on the criteria sure in studies of persistent symp- increased risk for PCS in our cohort, employed as well as a lack of specificity, toms.27,43,44 Therefore, we repeated our whereas there was no association with because many adult patients who did analysis using PCS as the outcome our clinical definition. not have head trauma also met PCS rather than our clinical definition of One may conclude from these findings criteria.45,46 Additionally, although the DSR. We noted 2 important findings. that the smaller subset of symptoms PCS ROC curve showed a statistically First, we found a 43% relative decrease that meet criteria for PCS are more significant association (P = .034) be- in prevalence in the outcome (9% ab- representative of a specific clinical entity tween an initial symptom severity score solute difference) when applying this characterized by persistent symptoms of 10 and PCS, the absolute AUC of 0.629 alternate definition. Second, we showed than those found on broader symptom suggests no more than a modest re- that a graded symptom inventory score inventories. An analysis comparing 3 lationship. Therefore, concluding that FIGURE 3 Hierarchical cluster analysis for participants who had early symptom resolution. Shorter relative cluster linkage distances on the x-axis indicate symptoms (y-axis) that are more characteristic of the group, whereas longer distances indicate symptoms that are less characteristic. PEDIATRICS Volume 134, Number 1, July 2014 59 Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
FIGURE 4 Hierarchical cluster analysis for participants who had delayed symptom resolution. Shorter relative cluster linkage distances on the x-axis indicate symptoms (y-axis) that are more characteristic of the group, whereas longer distances indicate symptoms that are less characteristic. PCS criteria are more representative of specific symptoms are more closely fying children who, at the time of their a unique clinical syndrome is difficult to associated.14,48 The exploratory na- concussion, are at risk for DSR. We did justify and suggests that accurate risk ture of cluster analysis prevents not perform serial assessments to stratification is heavily dependent on drawing firm conclusions regarding determine the precise day of symptom how the outcome is defined. the ability of these symptoms to pre- resolution or the range of symptom Hierarchical cluster analysis is an ex- dict DSR. However, cognitive symp- duration. It is possible that some sub- ploratory method that aims to dem- toms may warrant particular scrutiny jects in the DSR group had resolution of onstrate which features are most when present. symptoms shortly after their 30-day characteristic of a group. Three of the 6 We experienced a lost-to-follow-up rate follow-up call and were misclassified. most characteristic symptoms for both of 24%. The subjects lost to follow-up However, the prevalence of DSR in this the DSR and ESR groups were identical in had a significantly lower median ini- study was 21% compared with studies our cohort, suggesting that these symp- tial symptom score than the final study in other US pediatric ED cohorts 3 toms (phonophobia, photophobia, blur- cohort. It is plausible that most of these months after concussion, which ranged red or double vision) may not be useful in subjects would have fallen into the ESR from 15% to 29%, so this limitation is identifying those at risk for DSR. However, group but did not complete the study unlikely to have had a significant impact we found it interesting that cognitive owing to resolution of symptoms.49 If on our results.50,51 symptoms were more characteristic of true, the absence of these patients Finally, we did not include a control subjects who had DSR. Although some from analysis would tend to bias our group who had injuries to body regions authorshavefoundastrongerassociation results toward the null hypothesis. other than the head. Although children between the number of initial symptoms Our follow-up period was limited to 30 who have concussion tend to report and DSR,17,47 others have shown that days, as we were interested in identi- more post-concussive symptoms than 60 GRUBENHOFF et al Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
ARTICLE children with orthopedic injuries, there specificity further emphasizes the need sequelae and that accounts for the is considerable overlap in symptom re- for more accurate definitions related to contribution of both physiologic and port, highlighting the non-specific na- sequelae after concussion. psychological processes. Given the in- ture of post-concussive symptoms.29 We ability to predict the resolution of post- are therefore unable to evaluate what CONCLUSIONS concussive symptoms at the time of proportion of symptoms is simply at- Greater symptom severity at the time of injury, outpatient follow-up and serial tributable to injury in general and what injury does not predict DSR among symptom assessment should be a cor- proportion is attributable to concus- children presenting to the ED for eval- nerstone of concussion management sion specifically. 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Copyright © 2014 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose. FUNDING: Funding for the conduct of this study was provided by a Thrasher Research Fund Early Career Award to Dr Grubenhoff. Use of REDCap Database was supported by NIH/NCATS Colorado CTSI grant UL1 TR000154. Contents are the authors’ sole responsibility and do not necessarily represent official NIH or Thrasher Research Fund views. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose. 62 GRUBENHOFF et al Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
Acute Concussion Symptom Severity and Delayed Symptom Resolution Joseph A. Grubenhoff, Sara J. Deakyne, Lina Brou, Lalit Bajaj, R. Dawn Comstock and Michael W. Kirkwood Pediatrics 2014;134;54; originally published online June 23, 2014; DOI: 10.1542/peds.2013-2988 Updated Information & including high resolution figures, can be found at: Services http://pediatrics.aappublications.org/content/134/1/54.full.ht ml References This article cites 48 articles, 13 of which can be accessed free at: http://pediatrics.aappublications.org/content/134/1/54.full.ht ml#ref-list-1 Citations This article has been cited by 2 HighWire-hosted articles: http://pediatrics.aappublications.org/content/134/1/54.full.ht ml#related-urls Permissions & Licensing Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://pediatrics.aappublications.org/site/misc/Permissions.xh tml Reprints Information about ordering reprints can be found online: http://pediatrics.aappublications.org/site/misc/reprints.xhtml PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2014 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275. Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
Acute Concussion Symptom Severity and Delayed Symptom Resolution Joseph A. Grubenhoff, Sara J. Deakyne, Lina Brou, Lalit Bajaj, R. Dawn Comstock and Michael W. Kirkwood Pediatrics 2014;134;54; originally published online June 23, 2014; DOI: 10.1542/peds.2013-2988 The online version of this article, along with updated information and services, is located on the World Wide Web at: http://pediatrics.aappublications.org/content/134/1/54.full.html PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2014 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275. Downloaded from pediatrics.aappublications.org by guest on May 23, 2015
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