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White Matter Abnormalities Associated With Prolonged Recovery in Adolescents Following Concussion.

ABSTRACT: Background: Concussion symptoms in adolescents typically resolve within 4 weeks. However, 20 - 30% of adolescents experience a prolonged recovery. Abnormalities in tracts implicated in visuospatial attention and emotional regulation (i.e., inferior longitudinal fasciculus, ILF; inferior fronto-occipital fasciculus, IFOF; uncinate fasciculus; UF) have been consistently reported in concussion; yet, to date, there are no objective markers of prolonged recovery in adolescents. Here, we evaluated the utility of diffusion MRI in outcome prediction. Forty-two adolescents (12.1 - 17.9 years; female: 44.0%) underwent a diffusion Magnetic Resonance Imaging (dMRI) protocol within the first 10 days of concussion. Based on days of injury until medical clearance, adolescents were then categorized into SHORT (<28 days; N = 21) or LONG (>28 days; N = 21) recovery time. Fractional anisotropy (FA) in the ILF, IFOF, UF, and/or concussion symptoms were used as predictors of recovery time (SHORT, LONG). Forty-two age- and sex-matched healthy controls served as reference. Higher FA in the ILF (left: adjusted odds ratio; AOR = 0.36, 95% CI = 0.15 - 0.91, P = 0.030; right: AOR = 0.28, 95% CI = 0.10 - 0.83, P = 0.021), IFOF (left: AOR = 0.21, 95% CI = 0.07 - 0.66, P = 0.008; right: AOR = 0.30, 95% CI = 0.11 - 0.83, P = 0.020), and UF (left: AOR = 0.26, 95% CI = 0.09 - 0.74, P = 0.011; right: AOR = 0.28, 95% CI = 0.10 - 0.73, P = 0.010) was associated with SHORT recovery. In additional analyses, while adolescents with SHORT recovery did not differ from HC, those with LONG recovery showed lower FA in the ILF and IFOF (P < 0.014). Notably, inclusion of dMRI findings increased the sensitivity and specificity (AUC = 0.93) of a prediction model including clinical variables only (AUC = 0.75). Our findings indicate that higher FA in long associative tracts (especially ILF) might inform a more objective and accurate prognosis for recovery time in adolescents following concussion.

SUBMITTER: Lima Santos JP

PROVIDER: S-EPMC8264142 | biostudies-literature | 2021

REPOSITORIES: biostudies-literature

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White Matter Abnormalities Associated With Prolonged Recovery in Adolescents Following Concussion.

Lima Santos João Paulo JP Kontos Anthony P AP Mailliard Sarrah S Eagle Shawn R SR Holland Cynthia L CL Suss Stephen J SJ Abdul-Waalee Halimah H Stiffler Richelle S RS Bitzer Hannah B HB Blaney Nicholas A NA Colorito Adam T AT Santucci Christopher G CG Brown Allison A Kim Tae T Iyengar Satish S Skeba Alexander A Diler Rasim S RS Ladouceur Cecile D CD Phillips Mary L ML Brent David D Collins Michael W MW Versace Amelia A

Frontiers in neurology 20210624

<b>Background:</b> Concussion symptoms in adolescents typically resolve within 4 weeks. However, 20 - 30% of adolescents experience a prolonged recovery. Abnormalities in tracts implicated in visuospatial attention and emotional regulation (i.e., inferior longitudinal fasciculus, ILF; inferior fronto-occipital fasciculus, IFOF; uncinate fasciculus; UF) have been consistently reported in concussion; yet, to date, there are no objective markers of prolonged recovery in adolescents. Here, we evalua ...[more]

PMID: 34248824

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Project description:Objectives: To examine the association between concussion duration and two calcium channel, voltage-dependent, R type, alpha 1E subunit (CACNA1E) single nucleotide polymorphisms (i.e., rs35737760 and rs704326). A secondary purpose was to examine the association between CACNA1E single nucleotide polymorphisms (SNPs) and three acute concussion severity scores (i.e., vestibule-ocular reflex test, balance error scoring scale, and Immediate Post-Concussion Assessment and Cognitive Testing). Methods: Forty athletes with a diagnosed concussion from a hospital concussion program completed a standardized initial evaluation. Concussion injury characteristics, acute signs and symptoms followed by an objective screening (i.e., vestibular ocular assessments, balance error scoring system test, and Immediate Post-Concussion Assessment and Cognitive Testing exam) were assessed. Enrolled participants provided salivary samples for isolation of DNA. Two exon SNPs rs35737760 and rs704326 within CACNA1E were genotyped. Results: There was a significant difference found between acute balance deficits and prolonged recovery group (X2 = 5.66, p = 0.017). There was an association found between the dominant model GG genotype (X2 = 5.41, p = 0.027) within the rs704326 SNP and prolonged recovery group. Significant differences were identified for the rs704326 SNP within the dominant model GG genotype (p = 0.030) for VOR scores by recovery. A significant difference was found between the rs704326 SNP codominant model AA (p = 0.042) and visual memory. There was an association between acute balance deficits and prolonged recovery (X2 = 5.66, p = 0.017) for the rs35737760 SNP. No significant associations between concussion severity and genotype for rs35737760 SNP. Conclusion: Athletes carrying the CACNA1E rs704326 homozygous genotype GG are at a greater risk of a prolonged recovery. Athletes that reported balance deficits at the time of injury were more likely to have prolonged recovery. These polymorphisms within CACNA1E could alter the CACNA1E protein and allow for an increase of calcium leading to deficits to the granule cells within the brain.

Project description:ImportancePediatric concussion affects millions and results in heterogeneous outcomes and recovery trajectories. Given favorable outcome for most children, it is useful to understand characteristics of positive outcome to promote full recovery in all children.ObjectiveTo document the timeframe of recovery to optimal functioning, defined comprehensively across motor-physical, cognitive, socioemotional, and resilience-support domains, after concussion among children ages 8 to 16 years.Design, setting, and participantsFor this prospective cohort study, children ages 8 to 16.99 years with a concussion or orthopedic injury (OI) were recruited between September 2016 and July 2019 from 5 Pediatric Emergency Research Canada emergency departments and assessed approximately 10 days, 3 months, and 6 months after their injury. Data were analyzed from January 29, 2024, to January 11, 2025.ExposureConcussion.Main outcomes and measuresParticipants completed self-report and direct assessment measures of postconcussive symptoms, physical activity and function, balance, cognitive function, quality of life, resilience, and social support. The main outcome was optimal functioning, which was derived from 11 variables and criteria indicative of absence of impairment and average or above functioning in each domain (overall score, 0-11; higher score indicates better function). A longitudinal, multivariable, cumulative probability ordinal regression model was fitted to examine factors associated with optimal functioning.ResultsA total of 967 children (median [IQR] age, 12.3 [10.5-14.3] years; 562 [58.1%] male) were enrolled, including 633 children with a concussion and 334 children with an OI. The median (IQR) optimal functioning scores for the OI group were 6.0 (4.0-8.0) at 10 days, 7.0 (5.0-9.0) at 3 months, and 7 (5.0-9.0) at 6 months, compared with 4.0 (2.0-6.0) at 10 days, 6.0 (4.0-9.0) at 3 months, and 7.0 (4.0-9.0) at 6 months in the concussion group. The 3 main variables (time, sex, and group) were significantly associated with optimal functioning, as were all 2-way interactions. Time was the strongest factor associated with optimal functioning (Wald χ258 = 485.11; P < .001), followed by group (Wald χ26 = 95.10; P < .001), and sex (Wald χ26 = 23.19; P < .001). At the 10-day follow-up, concussion was associated with lower optimal functioning than OI among females (odds ratio [OR], 0.24 [95% CI, 0.16-0.36]) and males (OR, 0.37 [95% CI, 0.26-0.53]). This difference persisted for females at 3 months (OR, 0.57 [95% CI, 0.35-0.93]) but not for males. Optimal functioning was comparable at 6 months.Conclusions and relevanceIn this prospective cohort study of children with concussion, achieving optimal functioning levels across physical, cognitive, socioemotional, and resilience domains took 3 months or more, especially for girls with concussion. Multiple domains of outcome need to be taken into account when considering full recovery and optimal function after pediatric concussion.

Project description:BackgroundSleep problems are common after concussion; yet, to date, no study has evaluated the relationship between sleep, white matter integrity, and post-concussion symptoms in adolescents. Using self-reported quality of sleep measures within the first 10 days of injury, we aimed to determine if quality of sleep exerts a main effect on white matter integrity in major tracts, as measured by diffusion Magnetic Resonance Imaging (dMRI), and further examine whether this effect can help explain the variance in post-concussion symptom severity in 12- to 17.9-year-old adolescents.MethodsdMRI data were collected in 57 concussed adolescents (mean age[SD] = 15.4[1.5] years; 41.2 % female) with no history of major psychiatric diagnoses. Severity of post-concussion symptoms was assessed at study entry (mean days[SD] = 3.7[2.5] days since injury). Using the Pittsburgh Sleep Quality Index (PSQI), concussed adolescents were divided into two groups based on their quality of sleep in the days between injury and scan: good sleepers (PSQI global score ≤ 5; N = 33) and poor sleepers (PSQI global score > 5; N = 24). Neurite Orientation Dispersion and Dispersion Index (NODDI), specifically the Neurite Density Index (NDI), was used to quantify microstructural properties in major tracts, including 18 bilateral and one interhemispheric tract, and identify whether dMRI differences existed in good vs poor sleepers. Since the interval between concussion and neuroimaging acquisition varied among concussed adolescents, this interval was included in the analysis along with an interaction term with sleep groups. Regularized regression was used to identify if quality of sleep-related dMRI measures correlated with post-concussion symptom severity. Due to higher reported concussion symptom severity in females, interaction terms between dMRI and sex were included in the regularized regression model. Data collected in 33 sex- and age-matched non-concussed controls (mean age[SD] = 15.2[1.5]; 45.5 % female) served as healthy reference and sex and age were covariates in all analyses.ResultsRelative to good sleepers, poor sleepers demonstrated widespread lower NDI (18 of the 19 tracts; FDR corrected P < 0.048). This group effect was only significant with at least seven days between concussion and neuroimaging acquisition. Post-concussion symptoms severity was negatively correlated with NDI in four of these tracts: cingulum bundle, optic radiation, striato-fronto-orbital tract, and superior longitudinal fasciculus I. The multiple linear regression model combining sex and NDI of these four tracts was able to explain 33.2 % of the variability in symptom severity (F[7,49] = 4.9, P < 0.001, Adjusted R2 = 0.332). Relative to non-concussed controls, poor sleepers demonstrated lower NDI in the cingulum bundle, optic radiation, and superior longitudinal fasciculus I (FDR corrected P < 0.040).ConclusionsPoor quality of sleep following concussion is associated with widespread lower integrity of major white matter tracts, that in turn helped to explain post-concussion symptom severity in 12-17.9-year-old adolescents. The effect of sleep on white matter integrity following concussion was significant after one week, suggesting that acute sleep interventions may need this time to begin to take effect. Our findings may suggest an important relationship between good quality of sleep in the days following concussion and integrity of major white matter tracts. Moving forward, researchers should evaluate the effectiveness of sleep interventions on white matter integrity and clinical outcomes following concussion.

Dataset Information

White Matter Abnormalities Associated With Prolonged Recovery in Adolescents Following Concussion.

Publications

White Matter Abnormalities Associated With Prolonged Recovery in Adolescents Following Concussion.

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