Continuous electroencephalography predicts delayed cerebral ischemia after subarachnoid hemorrhage: A prospective study of diagnostic accuracy.

OBJECTIVE: Delayed cerebral ischemia (DCI) is a common, disabling complication of subarachnoid hemorrhage (SAH). Preventing DCI is a key focus of neurocritical care, but interventions carry risk and cannot be applied indiscriminately. Although retrospective studies have identified continuous electroencephalographic (cEEG) measures associated with DCI, no study has characterized the accuracy of cEEG with sufficient rigor to justify using it to triage patients to interventions or clinical trials. We therefore prospectively assessed the accuracy of cEEG for predicting DCI, following the Standards for Reporting Diagnostic Accuracy Studies. METHODS: We prospectively performed cEEG in nontraumatic, high-grade SAH patients at a single institution. The index test consisted of clinical neurophysiologists prospectively reporting prespecified EEG alarms: (1) decreasing relative alpha variability, (2) decreasing alpha-delta ratio, (3) worsening focal slowing, or (4) late appearing epileptiform abnormalities. The diagnostic reference standard was DCI determined by blinded, adjudicated review. Primary outcome measures were sensitivity and specificity of cEEG for subsequent DCI, determined by multistate survival analysis, adjusted for baseline risk. RESULTS: One hundred three of 227 consecutive patients were eligible and underwent cEEG monitoring (7.7-day mean duration). EEG alarms occurred in 96.2% of patients with and 19.6% without subsequent DCI (1.9-day median latency, interquartile range = 0.9-4.1). Among alarm subtypes, late onset epileptiform abnormalities had the highest predictive value. Prespecified EEG findings predicted DCI among patients with low (91% sensitivity, 83% specificity) and high (95% sensitivity, 77% specificity) baseline risk. INTERPRETATION: cEEG accurately predicts DCI following SAH and may help target therapies to patients at highest risk of secondary brain injury. Ann Neurol 2018;83:958-969.

Early detection of consciousness in patients with acute severe traumatic brain injury.

See Schiff (doi:10.1093/awx209) for a scientific commentary on this article. Patients with acute severe traumatic brain injury may recover consciousness before self-expression. Without behavioural evidence of consciousness at the bedside, clinicians may render an inaccurate prognosis, increasing the likelihood of withholding life-sustaining therapies or denying rehabilitative services. Task-based functional magnetic resonance imaging and electroencephalography techniques have revealed covert consciousness in the chronic setting, but these techniques have not been tested in the intensive care unit. We prospectively enrolled 16 patients admitted to the intensive care unit for acute severe traumatic brain injury to test two hypotheses: (i) in patients who lack behavioural evidence of language expression and comprehension, functional magnetic resonance imaging and electroencephalography detect command-following during a motor imagery task (i.e. cognitive motor dissociation) and association cortex responses during language and music stimuli (i.e. higher-order cortex motor dissociation); and (ii) early responses to these paradigms are associated with better 6-month outcomes on the Glasgow Outcome Scale-Extended. Patients underwent functional magnetic resonance imaging on post-injury Day 9.2 ± 5.0 and electroencephalography on Day 9.8 ± 4.6. At the time of imaging, behavioural evaluation with the Coma Recovery Scale-Revised indicated coma (n = 2), vegetative state (n = 3), minimally conscious state without language (n = 3), minimally conscious state with language (n = 4) or post-traumatic confusional state (n = 4). Cognitive motor dissociation was identified in four patients, including three whose behavioural diagnosis suggested a vegetative state. Higher-order cortex motor dissociation was identified in two additional patients. Complete absence of responses to language, music and motor imagery was only observed in coma patients. In patients with behavioural evidence of language function, responses to language and music were more frequently observed than responses to motor imagery (62.5-80% versus 33.3-42.9%). Similarly, in 16 matched healthy subjects, responses to language and music were more frequently observed than responses to motor imagery (87.5-100% versus 68.8-75.0%). Except for one patient who died in the intensive care unit, all patients with cognitive motor dissociation and higher-order cortex motor dissociation recovered beyond a confusional state by 6 months. However, 6-month outcomes were not associated with early functional magnetic resonance imaging and electroencephalography responses for the entire cohort. These observations suggest that functional magnetic resonance imaging and electroencephalography can detect command-following and higher-order cortical function in patients with acute severe traumatic brain injury. Early detection of covert consciousness and cortical responses in the intensive care unit could alter time-sensitive decisions about withholding life-sustaining therapies.

High risk for seizures following subarachnoid hemorrhage regardless of referral bias.

BACKGROUND: To investigate the frequency, predictors, and clinical impact of electrographic seizures in patients with high clinical or radiologic grade non-traumatic subarachnoid hemorrhage (SAH), independent of referral bias. METHODS: We compared rates of electrographic seizures and associated clinical variables and outcomes in patients with high clinical or radiologic grade non-traumatic SAH. Rates of electrographic seizure detection before and after institution of a guideline which made continuous EEG monitoring routine in this population were compared. RESULTS: Electrographic seizures occurred in 17.6 % of patients monitored expressly because of clinically suspected subclinical seizures. In unselected patients, seizures still occurred in 9.6 % of all cases, and in 8.6 % of cases in which there was no a priori suspicion of seizures. The first seizure detected occurred 5.4 (IQR 2.9-7.3) days after onset of subarachnoid hemorrhage with three of eight patients (37.5 %) having the first recorded seizure more than 48 h following EEG initiation, and 2/8 (25 %) at more than 72 h following EEG initiation. High clinical grade was associated with poor outcome at time of hospital discharge; electrographic seizures were not associated with poor outcome. CONCLUSIONS: Electrographic seizures occur at a relatively high rate in patients with non-traumatic SAH even after accounting for referral bias. The prolonged time to the first detected seizure in this cohort may reflect dynamic clinical features unique to the SAH population.

Comparison of Head Impact Exposure Between Male and Female High School Ice Hockey Athletes.

BACKGROUND: Concussion incidence rates are higher among female than male athletes in sports played by both sexes. Biomechanical factors may play a role in observed sex-based differences in concussion incidence. PURPOSE: To compare head impact counts and magnitudes during sports participation between male and female high school ice hockey athletes. STUDY DESIGN: Cohort study; Level of evidence, 2. METHODS: Over 2 seasons, a total of 21 male and 19 female ice hockey athletes from a single high school were instrumented with impact-sensing adhesive skin patches worn over the mastoid process while participating in games and practices. The impact sensors recorded the number, magnitude (peak linear acceleration [PLA, g] and peak angular acceleration [PAA, rad/s2] of the head; Head Impact Telemetry severity profile [HITsp]), and location of impacts sustained during each instrumented session. Head impact counts, magnitudes, and locations were compared between the sexes. RESULTS: Males experienced more head impacts than females during games (mean ± SD: 7.7 ± 3.0 vs 5.3 ± 2.0, P < .001) as well as practices (4.3 ± 1.6 vs 3.8 ± 1.1, P = .002). Mean impact magnitudes were greater for females for PLA (18.8 g ± 1.7 g vs 17.1 g ± 1.6 g, P < .001) and HITsp (19.7 ± 1.5 vs 17.7 ± 1.4, P < .001), while mean PAA was greater for males (3057.6 ± 2.0 rad/s2 vs 2778.3 ± 2.7 rad/s2, P < .001). Female athletes experienced higher PLA, PAA, and HITsp magnitudes for the top 10%, 5%, and 1% of impacts (all P < .050). Males experienced more impacts to the front (34.3%) and back (31.7%) of the head, while females experienced more impacts to the side (43.1%) and top (4.1%) (χ2 = 295.70, df = 3, P < .001). CONCLUSION: While male high school ice hockey athletes experienced more head impacts than females, impact magnitudes tended to be higher for females.

Descriptive Analysis of a Baseline Concussion Battery Among U.S. Service Academy Members: Results from the Concussion Assessment, Research, and Education (CARE) Consortium.

Introduction: The prevalence and possible long-term consequences of concussion remain an increasing concern to the U.S. military, particularly as it pertains to maintaining a medically ready force. Baseline testing is being used both in the civilian and military domains to assess concussion injury and recovery. Accurate interpretation of these baseline assessments requires one to consider other influencing factors not related to concussion. To date, there is limited understanding, especially within the military, of what factors influence normative test performance. Given the significant physical and mental demands placed on service academy members (SAM), and their relatively high risk for concussion, it is important to describe demographics and normative profile of SAMs. Furthermore, the absence of available baseline normative data on female and non-varsity SAMs makes interpretation of post-injury assessments challenging. Understanding how individuals perform at baseline, given their unique individual characteristics (e.g., concussion history, sex, competition level), will inform post-concussion assessment and management. Thus, the primary aim of this manuscript is to characterize the SAM population and determine normative values on a concussion baseline testing battery. Materials and Methods: All data were collected as part of the Concussion Assessment, Research and Education (CARE) Consortium. The baseline test battery included a post-concussion symptom checklist (Sport Concussion Assessment Tool (SCAT), psychological health screening inventory (Brief Symptom Inventory (BSI-18) and neurocognitive evaluation (ImPACT), Balance Error Scoring System (BESS), and Standardized Assessment of Concussion (SAC). Linear regression models were used to examine differences across sexes, competition levels, and varsity contact levels while controlling for academy, freshman status, race, and previous concussion. Zero inflated negative binomial models estimated symptom scores due to the high frequency of zero scores. Results: Significant, but small, sex effects were observed on the ImPACT visual memory task. While, females performed worse than males (p < 0.0001, pη2 = 0.01), these differences were small and not larger than the effects of the covariates. A similar pattern was observed for competition level on the SAC. There was a small, but significant difference across competition level. SAMs participating in varsity athletics did significantly worse on the SAC compared to SAMs participating in club or intramural athletics (all p's < 0.001, η2 = 0.01). When examining symptom reporting, males were more than two times as likely to report zero symptoms on the SCAT or BSI-18. Intramural SAMs had the highest number of symptoms and severity compared to varsity SAMs (p < 0.0001, Cohen's d < 0.2). Contact level was not associated with SCAT or BSI-18 symptoms among varsity SAMs. Notably, the significant differences across competition level on SCAT and BSI-18 were sub-clinical and had small effect sizes. Conclusion: The current analyses provide the first baseline concussion battery normative data among SAMs. While statistically significant differences may be observed on baseline tests, the effect sizes for competition and contact levels are very small, indicating that differences are likely not clinically meaningful at baseline. Identifying baseline differences and significant covariates is important for future concussion-related analyses to inform concussion evaluations for all athlete levels.

Individual Impact Magnitude vs. Cumulative Magnitude for Estimating Concussion Odds.

Helmeted impact devices have allowed researchers to investigate the biomechanics of head impacts in vivo. While increased impact magnitude has been associated with greater concussion risk, a definitive concussive threshold has not been established. It is likely that concussion risk is not determined by a single impact itself, but a host of predisposing factors. These factors may include genetics, fatigue, and/or prior head impact exposure. The objective of the current paper is to investigate the association between cumulative head impact magnitude and concussion risk. It is hypothesized that increased cumulative magnitudes will be associated with greater concussion risk. This retrospective analysis included participants that were recruited from regional high-schools in Illinois and Michigan from 2007 to 2014 as part of an ongoing study on concussion biomechanics. Across seven seasons, 185 high school football athletes were instrumented with the Head Impact Telemetry system. Out of 185 athletes, 31 (17%) sustained a concussion, with two athletes sustaining two concussions over the study period, yielding 33 concussive events. The system recorded 78,204 impacts for all concussed players. Linear acceleration, rotational acceleration, and head impact telemetry severity profile (HITsp) magnitudes were summed within five timeframes: the day of injury, three days prior to injury, seven days prior to injury, 30 days prior to injury, and prior in-season exposure. Logistic regressions were modeled to explain concussive events based on the singular linear acceleration, rotational acceleration, and HITsp event along with the calculated summations over time. Linear acceleration, rotational acceleration, and HITsp all produced significant models estimating concussion (p < 0.05). The strongest estimators of a concussive impact were the linear acceleration (OR = 1.040, p < 0.05), rotational acceleration (OR = 1.001, p < 0.05), and HITsp (OR = 1.003, p < 0.05) for the singular impact rather than any of the cumulative magnitude calculations. Moreover, no cumulative count measure was significant for linear or rotational acceleration. Results from this investigation support the growing literature indicating cumulative magnitude is not related to concussion likelihood. Cumulative magnitude is a simplistic measure of the total exposure sustained by a player over a given period. However, this measure is limited as it assumes the brain is a static structure unable to undergo self-repair. Future research should consider how biological recovery between impacts may influence concussion risk.

Head Impact Density: A Model To Explain the Elusive Concussion Threshold.

Concussion is a heterogeneous injury occurring throughout a range of impact magnitudes. Consequently, research focusing on a single or set of variables at the time of injury to understand concussive biomechanics has been thwarted by low injury prediction sensitivity. The current study examined the role of Impact Density in estimating concussive injury risk. Head impact data were collected across seven high school football seasons with the Head Impact Telemetry System (HIT System). Over the study period, 29 concussions were included for data analysis. The linear acceleration of the concussive impact was matched to a Control athlete, along with impacts in the 24 h before. Linear and rotational acceleration for the 19 impacts leading into the final event and the cumulative accelerations over time were evaluated. Analyses indicated no difference in impact counts within the final 24 h, or impact magnitudes for linear and rotational acceleration among the final 20 impacts (p > 0.05). A novel metric, Impact Density, was calculated from the final 20 impacts by summing the acceleration magnitude divided by time from the previous impact. Analyses indicated the Concussed athletes incurred a significantly higher linear (concussed: 255.4g/sec (standard error of the mean [SEM] = 40.1), controls:145.4g/sec (SEM = 23.8), p = 0.016), and rotational (Concussed:10311.3 rad/s/s/s (SEM = 1883.7), Controls: 6083.8 rad/s/s/s (SEM = 1115.9), p = 0.029) Impact Density than the Control athletes. Similar to other investigations, there was no difference in individual linear or rotational impact magnitude in the 20 impacts before and including the injury. The measure of Impact Density, however, revealed differences between the Concussed and Control athletes. These data suggest that the biomechanical threshold for concussion fluctuates downwardly with a greater impact magnitude and number with a return to pre-impact levels with time, suggesting physiological vulnerability to repeated head impacts. The current results highlight that time between impacts, not just impact magnitude, influences risk for concussion.

Head-Impact-Measurement Devices: A Systematic Review.

CONTEXT: With an estimated 3.8 million sport- and recreation-related concussions occurring annually, targeted prevention and diagnostic methods are needed. Biomechanical analysis of head impacts may provide quantitative information that can inform both prevention and diagnostic strategies. OBJECTIVE: To assess available head-impact devices and their clinical utility. DATA SOURCES: We performed a systematic search of the electronic database PubMed for peer-reviewed publications, using the following phrases: accelerometer and concussion, head impact telemetry, head impacts and concussion and sensor, head impacts and sensor, impact sensor and concussion, linear acceleration and concussion, rotational acceleration and concussion, and xpatch concussion. In addition to the literature review, a Google search for head impact monitor and concussion monitor yielded 15 more devices. STUDY SELECTION: Included studies were performed in vivo, used commercially available devices, and focused on sport-related concussion. DATA EXTRACTION: One author reviewed the title and abstract of each study for inclusion and exclusion criteria and then reviewed each full-text article to confirm inclusion criteria. Controversial articles were reviewed by all authors to reach consensus. DATA SYNTHESIS: In total, 61 peer-reviewed articles involving 4 head-impact devices were included. Participants in boxing, football, ice hockey, soccer, or snow sports ranged in age from 6 to 24 years; 18% (n = 11) of the studies included female athletes. The Head Impact Telemetry System was the most widely used device (n = 53). Fourteen additional commercially available devices were presented. CONCLUSIONS: Measurements collected by impact monitors provided real-time data to estimate player exposure but did not have the requisite sensitivity to concussion. Proper interpretation of previously reported head-impact kinematics across age, sport, and position may inform future research and enable staff clinicians working on the sidelines to monitor athletes. However, head-impact-monitoring systems have limited clinical utility due to error rates, designs, and low specificity in predicting concussive injury.

Epidemiology of Sport-Related Concussions in High School Athletes: National Athletic Treatment, Injury and Outcomes Network (NATION), 2011-2012 Through 2013-2014.

CONTEXT: Sports participation is one of the leading causes of concussions among nearly 8 million US high school student-athletes. OBJECTIVE: To describe the epidemiology of sport-related concussion (SRC) in 27 high school sports during the 2011-2012 through 2013-2014 academic years. DESIGN: Descriptive epidemiology study. SETTING: Aggregate injury and exposure data from 27 sports in 147 high schools in the National Athletic Treatment, Injury and Outcomes Network (NATION). PATIENTS OR OTHER PARTICIPANTS: Boy and girl high school athletes during the 2011-2012 through 2013-2014 academic years. MAIN OUTCOME MEASURE(S): Sport-related concussion counts, percentages, rates per 10 000 athlete-exposures (AEs), rate ratios (RRs), and injury proportion ratios (IPRs) were reported with 95% confidence intervals (CIs). Rate ratios and IPRs with 95% CIs not containing 1.0 were considered significant. RESULTS: Overall, 2004 SRCs were reported among 27 high school sports, for a rate of 3.89 per 10 000 AEs. Football had the highest SRC rate (9.21/10 000 AEs), followed by boys' lacrosse (6.65/10 000 AEs) and girls' soccer (6.11/10 000 AEs). The SRC rate was higher in competition than in practice (RR = 3.30; 95% CI = 3.02, 3.60). Among sex-comparable sports, the SRC rate was higher in girls than in boys (RR = 1.56; 95% CI = 1.34, 1.81); however, the proportion of SRCs due to player-to-player contact was higher in boys than in girls (IPR = 1.48; 95% CI = 1.27, 1.73). Common symptoms reported among all athletes with SRCs were headache (94.7%), dizziness (74.8%), and difficulty concentrating (61.0%). Only 0.8% of players with SRCs returned to play within 24 hours. The majority of athletes with SRCs (65.8%) returned to play between 7 and 28 days. More players had symptoms resolve after 7 days (48.8%) than less than a week (40.7%). CONCLUSIONS: Our findings provide updated high school SRC incidence estimates and further evidence of sex differences in reported SRCs. Few athletes with SRCs returned to play within 24 hours or a week. Most injured players returned after 7 days, despite a smaller proportion having symptoms resolve within a week.

Head Impact Measurement Devices.

CONTEXT: Concussive injuries are at the forefront of sports medicine research. Recently, researchers have used a variety of head- and helmet-based impact-monitoring devices to quantify impacts sustained during contact sport participation. This review provides an up-to-date collection of head accelerometer use at the youth, high school, and collegiate levels. EVIDENCE ACQUISITION: PubMed was searched for articles published between 1980 and 2015 using the terms accelerometer and concussion, impact sensor and concussion, head impact telemetry system, head impact telemetry, and linear acceleration and concussion. An additional Google search was performed to capture devices without publications. STUDY DESIGN: Clinical review. LEVEL OF EVIDENCE: Level 4. RESULTS: Twenty-four products track and/or record head impact for clinical or research use. Ten of these head impact devices have publications supporting their utility. CONCLUSION: Head impact measuring devices can describe athlete exposure in terms of magnitude and/or frequency, highlighting their utility within a multimodal approach for concussion assessment and diagnosis.

Football Players' Head-Impact Exposure After Limiting of Full-Contact Practices.

CONTEXT: Sporting organizations limit full-contact football practices to reduce concussion risk and based on speculation that repeated head impacts may result in long-term neurodegeneration. OBJECTIVE: To directly compare head-impact exposure in high school football players before and after a statewide restriction on full-contact practices. DESIGN: Cross-sectional study. SETTING: High school football field. PATIENTS OR OTHER PARTICIPANTS: Participants were varsity football athletes from a single high school. Before the rule change, 26 athletes (age = 16.2 ± 0.8 years, height = 179.6 ± 6.4 cm, weight = 81.9 ± 13.1 kg) participated. After the rule change, 24 athletes (age = 15.9 ± 0.8 years, height = 178.3 ± 6.5 cm, weight = 76.2 ± 11.6 kg) participated. Nine athletes participated in both years of the investigation. MAIN OUTCOME MEASURE(S): Head-impact exposure was monitored using the Head Impact Telemetry System while the athletes participated in football games and practices in the seasons before and after the rule change. Head-impact frequency, location, and magnitude (ie, linear acceleration, rotational acceleration, and Head Impact Telemetry severity profile [HITsp], respectively) were measured. RESULTS: A total of 15 398 impacts (592 impacts per player per season) were captured before the rule change and 8269 impacts (345 impacts per player per season) after the change. An average 42% decline in impact exposure occurred across all players, with practice-exposure declines occurring among linemen (46% decline); receivers, cornerbacks, and safeties (41% decline); and tight ends, running backs (including fullbacks), and linebackers (39% decline). Impact magnitudes remained largely unchanged between the years. CONCLUSIONS: A rule change limiting full-contact high school football practices appears to have been effective in reducing head-impact exposure across all players, with the largest reduction occurring among linemen. This finding is likely associated with the rule modification, particularly because the coaching staff and offensive scheme remained consistent, yet how this reduction influences concussion risk and long-term cognitive health remains unknown.