Long-Term Cognitive and Neuropsychiatric Consequences of Repetitive Concussion and Head-Impact Exposure

Initially, interest in sport-related concussion arose from the premise that the study of athletes engaged in sports associated with high rates of concussion could provide insight into the mechanisms, phenomenology, and recovery from mild traumatic brain injury. Over the last decade, concerns have focused on the possibility that, for some athletes, repetitive concussions may raise the long-term risk for cognitive decline, neurobehavioral changes, and neurodegenerative disease. First conceptualized as a discrete event with variable recovery trajectories, concussion is now viewed by some as a trigger of neurobiological events that may influence neurobehavioral function over the course of the life span. Furthermore, advances in technology now permit us to gain a detailed understanding of the frequency and intensity of repetitive head impacts associated with contact sports (eg, football, ice hockey). Helmet-based sensors can be used to characterize the kinematic features of concussive impacts, as well as the profiles of typical head-impact exposures experienced by athletes in routine sport participation. Many large-magnitude impacts are not associated with diagnosed concussions, whereas many diagnosed concussions are associated with more modest impacts. Therefore, a full understanding of this topic requires attention to not only the effects of repetitive concussions but also overall exposure to repetitive head impacts. This article is a review of the current state of the science on the long-term neurocognitive and neurobehavioral effects of repetitive concussion and head-impact exposure in contact sports.

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Head Kinematics by Contact Scenarios in Youth Ice Hockey

Neurology ◽

10.1212/wnl.0000000000011045 ◽

2020 ◽

Vol 95 (20 Supplement 1) ◽

pp. S1.1-S1

Author(s):

Abigail Swenson ◽

Logan Miller ◽

Jillian Urban ◽

Joel Stitzel

Keyword(s):

Rotational Velocity ◽

Angular Acceleration ◽

Linear Acceleration ◽

Head Impact ◽

Ice Hockey ◽

Contact Sports ◽

Head Impacts ◽

Rigorous Study ◽

Improving Accuracy ◽

Impact Events

ObjectiveThe objective of this pilot study was to characterize head impact exposure in a sample of youth boys' ice hockey using a novel instrumented mouthpiece, improving accuracy.BackgroundFrom 2010 to 2018 youth ice hockey saw a 15% increase in participation, despite growing concerns for concussion risk in contact sports. While contact sports with similar rates of concussion have been subjected to rigorous study, head impact exposure in youth ice hockey has been largely underexplored. Existing youth studies have utilized helmet-mounted sensors, which are associated with error due to poor coupling with the skull.Design/MethodsCustom mouthpieces containing a tri-axial accelerometer and gyroscope were fit to seven enrolled athletes, and monitored during practices and games throughout the season. Linear acceleration and rotational velocity of the head were recorded for 60 ms when 5 g was exceeded on any axis for at least 3 ms. Time-synchronized film was reviewed to identify the contact scenario and head contact. Summary statistics of kinematics were calculated by scenario and presence of head contact.ResultsA total of 465 events were recorded over 25 weeks. Of these events 25% involved head contact; 92% of all contact scenarios were board checks, falls, or ice checks. Events involving head contact (i.e., head impacts) had median [95th percentile] peak linear acceleration, rotational velocity, and angular acceleration of 8.1 [30.9] g, 7.9 [20.2] rad/s, and 614 [2673] rad/s2, respectively. Events not involving head contact had median [95th percentile] peak linear acceleration, rotational velocity, and angular acceleration of 6.6 [43.8] g, 6.5 [17.5] rad/s, and 455 [4115] rad/s2, respectively.ConclusionsThe majority of the recorded events could be classified as board checks, falls, or ice checks. Median peak kinematics were higher for head impacts than non-head impact events. In contrast, 95th percentile linear and angular accelerations were greater for impacts not involving head contact.

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Association Between Antemortem FLAIR White Matter Hyperintensities and Neuropathology in Brain Donors Exposed to Repetitive Head Impacts

Neurology ◽

10.1212/wnl.0000000000013012 ◽

2021 ◽

pp. 10.1212/WNL.0000000000013012

Author(s):

Madeline Uretsky ◽

Sylvain Bouix ◽

Ronald J. Killiany ◽

Yorghos Tripodis ◽

Brett Martin ◽

...

Keyword(s):

White Matter ◽

White Matter Hyperintensities ◽

Microvascular Disease ◽

Head Impact ◽

American Football ◽

Football Players ◽

Head Impacts ◽

Repetitive Head Impacts ◽

Pathological Correlation ◽

Daily Function

Background and Objectives:Late neuropathologies of repetitive head impacts from contact sports can include chronic traumatic encephalopathy (CTE) and white matter degeneration. White matter hyperintensities (WMH) on fluid attenuated inversion recovery (FLAIR) MRI scans are often viewed as microvascular disease from vascular risk, but might have unique underlying pathologies and risk factors in the setting of repetitive head impacts. We investigated the neuropathological correlates of antemortem WMH in brain donors exposed to repetitive head impacts. The association between WMH, and repetitive head impact exposure and informant-reported cognitive and daily function were tested.Methods:This imaging-pathological correlation study included symptomatic deceased men exposed to repetitive head impacts. Donors had antemortem FLAIR scans from medical records and were without evidence of CNS neoplasm, large vessel infarcts, hemorrhage, and/or encephalomalacia. WMH were quantified using log-transformed values for total lesion volume (TLV), calculated using the lesion prediction algorithm from the Lesion Segmentation Toolbox. Neuropathological assessments included semi-quantitative ratings of white matter rarefaction, cerebrovascular disease, p-tau severity (CTE stage, dorsolateral frontal cortex), and Aβ. Among football players, years of play was a proxy for repetitive head impact exposure. Retrospective informant-reported cognitive and daily function were assessed using the Cognitive Difficulties Scale (CDS) and Functional Activities Questionnaire (FAQ). Regression models controlled for demographics, diabetes, hypertension, and MRI resolution. Statistical significance was defined as p<0.05.Results:The sample included 75 donors: 67 football players and 8 non-football contact sport athletes and/or military veterans. Dementia was the most common MRI indication (64%). Fifty-three (70.7%) had CTE at autopsy. Log-TLV was associated with white matter rarefaction (OR=2.32, 95% CI=1.03,5.24, p=0.04), arteriolosclerosis (OR=2.38, 95% CI=1.02,5.52, p=0.04), CTE stage (OR=2.58, 95% CI=1.17,5.71, p=0.02), and dorsolateral frontal p-tau severity (OR=3.03, 95% CI=1.32,6.97, p=0.01). There was no association with Aβ. More years of football play was associated with log-TLV (b=0.04, 95% CI=0.01,0.06, p=0.01). Greater log-TLV correlated with higher FAQ (unstandardized beta=4.94, 95% CI=0.42,8.57, p=0.03) and CDS scores (unstandardized beta=15.35, 95% CI=-0.27,30.97, p=0.05).Discussion:WMH might capture long-term white matter pathologies from repetitive head impacts, including those from white matter rarefaction and p-tau, in addition to microvascular disease. Prospective imaging-pathological correlation studies are needed.Classification of Evidence:This study provides Class IV evidence of associations between FLAIR white matter hyperintensities, and neuropathological changes (white matter rarefaction, arteriolosclerosis, p-tau accumulation), years of American football play, and reported cognitive symptoms in symptomatic brain donors exposed to repetitive head impacts.

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Spectrum of acute clinical characteristics of diagnosed concussions in college athletes wearing instrumented helmets

Journal of Neurosurgery ◽

10.3171/2012.8.jns112298 ◽

2012 ◽

Vol 117 (6) ◽

pp. 1092-1099 ◽

Cited By ~ 82

Author(s):

Ann-Christine Duhaime ◽

Jonathan G. Beckwith ◽

Arthur C. Maerlender ◽

Thomas W. McAllister ◽

Joseph J. Crisco ◽

...

Keyword(s):

Collegiate Athletes ◽

Head Impact ◽

Ice Hockey ◽

Future Research ◽

Impact Event ◽

Head Impacts ◽

Presenting Symptoms ◽

Wide Range ◽

Impact Events ◽

Specific Impact

Object Concussive head injuries have received much attention in the medical and public arenas, as concerns have been raised about the potential short- and long-term consequences of injuries sustained in sports and other activities. While many student athletes have required evaluation after concussion, the exact definition of concussion has varied among disciplines and over time. The authors used data gathered as part of a multiinstitutional longitudinal study of the biomechanics of head impacts in helmeted collegiate athletes to characterize what signs, symptoms, and clinical histories were used to designate players as having sustained concussions. Methods Players on 3 college football teams and 4 ice hockey teams (male and female) wore helmets instrumented with Head Impact Telemetry (HIT) technology during practices and games over 2–4 seasons of play. Preseason clinical screening batteries assessed baseline cognition and reported symptoms. If a concussion was diagnosed by the team medical staff, basic descriptive information was collected at presentation, and concussed players were reevaluated serially. The specific symptoms or findings associated with the diagnosis of acute concussion, relation to specific impact events, timing of symptom onset and diagnosis, and recorded biomechanical parameters were analyzed. Results Data were collected from 450 athletes with 486,594 recorded head impacts. Forty-eight separate concussions were diagnosed in 44 individual players. Mental clouding, headache, and dizziness were the most common presenting symptoms. Thirty-one diagnosed cases were associated with an identified impact event; in 17 cases no specific impact event was identified. Onset of symptoms was immediate in 24 players, delayed in 11, and unspecified in 13. In 8 cases the diagnosis was made immediately after a head impact, but in most cases the diagnosis was delayed (median 17 hours). One diagnosed concussion involved a 30-second loss of consciousness; all other players retained alertness. Most diagnoses were based on self-reported symptoms. The mean peak angular and rotational acceleration values for those cases associated with a specific identified impact were 86.1 ± 42.6g (range 16.5–177.9g) and 3620 ± 2166 rad/sec2 (range 183–7589 rad/sec2), respectively. Conclusions Approximately two-thirds of diagnosed concussions were associated with a specific contact event. Half of all players diagnosed with concussions had delayed or unclear timing of onset of symptoms. Most had no externally observed findings. Diagnosis was usually based on a range of self-reported symptoms after a variable delay. Accelerations clustered in the higher percentiles for all impact events, but encompassed a wide range. These data highlight the heterogeneity of criteria for concussion diagnosis, and in this sports context, its heavy reliance on self-reported symptoms. More specific and standardized definitions of clinical and objective correlates of a “concussion spectrum” may be needed in future research efforts, as well as in the clinical diagnostic arena.

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Head Impact Kinematics do not Predict In-Season Concussion or Lower Extremity Injury in Ice Hockey

Neurology ◽

10.1212/01.wnl.0000581128.49893.c3 ◽

2019 ◽

Vol 93 (14 Supplement 1) ◽

pp. S30.2-S31

Author(s):

Melissa DiFabio ◽

Katherine Breedlove ◽

Thomas Buckley

Keyword(s):

Lower Extremity ◽

Linear Acceleration ◽

Mean Value ◽

Small Sample ◽

Head Impact ◽

Ice Hockey ◽

Lower Extremity Injury ◽

Extremity Injury ◽

Head Impacts ◽

Increased Risk

ObjectiveTo examine if head impact kinematics (HIK) predict in-season concussion or acute lower extremity injury (LEI) in collegiate ice hockey.BackgroundSustaining head impacts in sport regularly may be damaging to long-term neurological health. Individuals who sustain higher head impact loads may be at increased risk for concussion, and furthermore, individuals who sustain a concussion are more likely to sustain a subsequent LEI than those without a history of concussion.Design/MethodsTwenty-nine collegiate club male ice hockey players (age: 20.2 ± 1.4) over the 2015-2018 seasons completed a survey at the conclusion of their season of LEI and concussion in-season. HIK (number of impacts, and mean, peak, and cumulative linear acceleration) were recorded via tri-axial accelerometers (Triax, Nowalk, CT) that each player wore for games/practices with a 10g impact threshold. Two binary logistic regressions were performed to determine if either sustaining a concussion or LEI was predicted by HIK.ResultsThere was no relationship between LEI or concussion with number of impacts (β:-0.018, p = 0.711, 95% CI:-0.12-0.84; β:-0.039, p = 0.55, 95% CI: -0.21-0.08, respectively), or mean (β:0.041, p = 0.79, 95% CI: -0.26-0.38; β:-0.040, p = 0.81, 95% CI: -0.37-0.32), peak (β:-0.065, p = 0.14, 95% CI: -0.16-0.01; β:0.0007, p = 0.99, 95% CI: -0.09-0.09), or cumulative acceleration (β:0.001, p = 0.42, 95% CI: -0.001-0.004; β:0.001, p = 0.55, 95% CI:-0.002-0.005). 7/29 players sustained a LEI and 6/29 sustained a concussion. Mean value for number of impacts was 59.7 ± 49.1 (range:3-171); mean acceleration: 33.9 ± 5.3g (range:22.0-42.22), peak: 71.8 ± 19.0g (range: 30.8-108.4); cumulative: 2,108.5 ± 1,793.8g (range 71.8-6517.2).ConclusionsThe main finding of this study is that greater HIK do not predict whether individuals sustained either an acute LEI or concussion during the season, albeit from a small sample. As HIK load is related to concussion incidence, it is possible HIK load may also be related to LEI, however, these results suggest HIK alone is not related to either in an ice hockey cohort.

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Head-Impact–Measurement Devices: A Systematic Review

Journal of Athletic Training ◽

10.4085/1062-6050.52.2.05 ◽

2017 ◽

Vol 52 (3) ◽

pp. 206-227 ◽

Cited By ~ 48

Author(s):

Kathryn L. O'Connor ◽

Steven Rowson ◽

Stefan M. Duma ◽

Steven P. Broglio

Keyword(s):

Clinical Utility ◽

Female Athletes ◽

Error Rates ◽

Head Impact ◽

Ice Hockey ◽

Diagnostic Methods ◽

Biomechanical Analysis ◽

Targeted Prevention ◽

Head Impacts ◽

Google Search

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.

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Long‐term effects of repetitive head impacts on gray matter cortical thickness

Alzheimer s & Dementia ◽

10.1002/alz.052875 ◽

2021 ◽

Vol 17 (S6) ◽

Author(s):

Bailee Brekke ◽

Renee DeVivo ◽

Ann C. McKee ◽

Thor D. Stein ◽

Yorghos Tripodis ◽

...

Keyword(s):

Cortical Thickness ◽

Gray Matter ◽

Long Term Effects ◽

Head Impacts ◽

Repetitive Head Impacts

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Relationships between Head Impacts, Competitive Aggression, and Risk-taking Behavior in Collegiate Ice Hockey Players

Archives of Clinical Neuropsychology ◽

10.1093/arclin/acz026.50 ◽

2019 ◽

Vol 34 (5) ◽

pp. 780-780

Author(s):

M S DiFabio ◽

T A Buckley

Keyword(s):

Risk Taking ◽

Sensation Seeking ◽

Linear Acceleration ◽

Head Impact ◽

Ice Hockey ◽

Impact Loads ◽

Head Impacts ◽

Hockey Players ◽

Risk Taking Behavior ◽

Sensation Seeking Scale

Abstract Purpose To examine relationships between head impact kinematics sustained over a season and competitive aggression and self-reported risk-taking behavior in collegiate club ice-hockey athletes. Methods Twenty male ice-hockey players (19.9±1.2 y.o, 1.8±0.06 m, 78.5±5.7 kg) completed the Competitive Anger and Aggression Scale (CAAS, Range:0-84) and the Brief Sensation Seeking Scale (BSSS, Range:8-40) during the preseason as measures of competitive aggression and risk-taking behavior with higher/lower reflecting higher/lower aggression and risk taking. Penalty minutes (PM) and games played (GP) were taken from official game records. Head impact kinematics (number of impacts, linear mean, peak, cumulative acceleration) were recorded by tri-axial accelerometers worn during games/practices. Spearman correlation was performed to examine relationships between variables. Results The mean number of impacts was 76.6±54.9 (range: 6–171); mean and cumulative acceleration were 36.3±4.2g (range:27.8–42.2g) and 2829.4±2024.9g (range:198.4–6527.2g), respectively. Neither CAAS (mean: 48.7±10.9, range: 24–64) nor BSSS scores (mean: 25.3±4.4, range:15–32) were significantly related to impact kinematics. GP was significantly correlated with number of impacts (r=.63, p=.003) and cumulative linear acceleration (r=.61, p=.004). PM was significantly correlated with number of impacts (r=.52, p=.20) and cumulative linear acceleration (r=.55, p=.13). Conclusion There were no relationships between the head impact kinematics and self-reported aggressiveness or risk taking behavior, but more PM was strongly related to higher head impact loads. Considering PM may be useful in aiding to identify athletes who may sustain higher head impact loads, however, self-reports of behavior may not be.

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The long-term consequences of repetitive head impacts: Chronic traumatic encephalopathy

Handbook of Clinical Neurology - Geriatric Neurology ◽

10.1016/b978-0-12-804766-8.00018-2 ◽

2019 ◽

pp. 337-355 ◽

Cited By ~ 1

Author(s):

Michael L. Alosco ◽

Robert A. Stern

Keyword(s):

Chronic Traumatic Encephalopathy ◽

Head Impacts ◽

Repetitive Head Impacts ◽

Long Term Consequences

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High-frequency head impact causes chronic synaptic adaptation and long-term cognitive impairment in mice

Nature Communications ◽

10.1038/s41467-021-22744-6 ◽

2021 ◽

Vol 12 (1) ◽

Author(s):

Stephanie S. Sloley ◽

Bevan S. Main ◽

Charisse N. Winston ◽

Alex C. Harvey ◽

Alice Kaganovich ◽

...

Keyword(s):

Cognitive Impairment ◽

High Frequency ◽

Chronic Traumatic Encephalopathy ◽

Glutamate Release ◽

Head Impact ◽

Physiological Adaptation ◽

Head Impacts ◽

Behavioral Impairments ◽

Human And Mouse

AbstractRepeated head impact exposure can cause memory and behavioral impairments. Here, we report that exposure to non-damaging, but high frequency, head impacts can alter brain function in mice through synaptic adaptation. High frequency head impact mice develop chronic cognitive impairments in the absence of traditional brain trauma pathology, and transcriptomic profiling of mouse and human chronic traumatic encephalopathy brain reveal that synapses are strongly affected by head impact. Electrophysiological analysis shows that high frequency head impacts cause chronic modification of the AMPA/NMDA ratio in neurons that underlie the changes to cognition. To demonstrate that synaptic adaptation is caused by head impact-induced glutamate release, we pretreated mice with memantine prior to head impact. Memantine prevents the development of the key transcriptomic and electrophysiological signatures of high frequency head impact, and averts cognitive dysfunction. These data reveal synapses as a target of high frequency head impact in human and mouse brain, and that this physiological adaptation in response to head impact is sufficient to induce chronic cognitive impairment in mice.

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