HJAR Jul/Aug 2024
HEALTHCARE JOURNAL OF ARKANSAS I JUL / AUG 2024 13 INTRODUCTION Asingle football possesses the extraordi- nary ability to foster unity among individu- als spanning diverse ages, races and eth- nicities, and socioeconomic backgrounds. 1 However, this unifying force comes at a cost, with repetitive subconcussive head impacts often stemming from tackling, posing a risk of triggering neurodegenerative disorders. 2 This issue is particularly pertinent to young athletes, as a recent study 3 has reported cases of chronic traumatic encephalopa- thy among young adults with a history of head impact exposure. Numerous neuroimaging studies have delved into the neurological correlates of sports-related brain injuries. For example, former athletes engaged in collision sports (eg, football, soccer, boxing) exhibit reduced cortical thickness across widespread brain regions compared with their nonathlete counterparts. 4-6 A large-scale pediatric mild traumatic brain injury (mTBI) study revealed significant cortical thinning in frontal and occipital regions among male patients with persistent symptoms beyond 3 months compared with those without per- sistent symptoms. 7 Likewise, current high school and college football players showed greater brain volume reduction and cor- tical thinning in frontotemporal regions after a single 8 and also several seasons, 9 compared with control athletes (eg, volley- ball). Furthermore, resting-state (RS) func- tional magnetic resonance imaging (fMRI) functional connectivity has revealed neuro- physiological changes due to repetitive head impacts. For instance, decreased connectiv- ity was pronounced in frontal and cingulate regions, whereas increased connectivity was identified in posterior brain regions (eg, pre- cuneus, supramarginal gyrus) after a rugby game 10 and a season in collision sports. 11-13 However, limitations in prior studies, such as small sample sizes from a single high school program and narrow panels of imag- ing, hinder the broad implications of these findings. Addressing these limitations, multipa- rameter morphometric techniques, encom- passing volumetric analysis (cortical thick- ness) and geometric analysis (gyrification and sulcal depth), provide valuable insights into the neurobiological underpinnings of maturation, aging, injury, and degenera- tive conditions. 14,15 The cortical thickness informs changes in gray matter volumes, whereas the gyrification and sulcal depth examine the complexity and depth of corti- cal folding, respectively. 16 In addition, a cor- tical surface-based fMRI analysis 17 offers a novel approach to examine not only the RS functional connectivity (FC) but also the amplitude of low-frequency fluctuation (ALFF) and regional homogeneity (ReHo) on the cortical surface. 18 ALFF estimates the ABSTRACT Importance Recurring exposure to head impacts in American football has garnered public and scientific attention, yet neurobiological associations in adolescent football players remain unclear. Objective To examine cortical structure and neurophysiological characteristics in adolescent football players. Design, Setting, and Participants This cohort study included adolescent football players and control athletes (swimming, cross country, and tennis) from 5 high school athletic programs, who were matched with age, sex (male), and school. Neuroimaging assessments were conducted May to July of the 2021 and 2022 seasons. Data were analyzed from February to November 2023. Exposure Playing tackle football or noncontact sports. Main Outcomes and Measures Structural magnetic resonance imaging (MRI) data were analyzed for cortical thickness, sulcal depth, and gyrification, and cortical surface-based resting state (RS)–functional MRI analyses examined the amplitude of low-frequency fluctuation (ALFF), regional homogeneity (ReHo), and RS-functional connectivity (RS-FC). Results Two-hundred seventy-five male participants (205 football players; mean [SD] age, 15.8 [1.2] years; 5 Asian [2.4%], 8 Black or African American [3.9%], and 189White [92.2%]; 70 control participants; mean [SD] age 15.8 [1.2] years, 4 Asian [5.7], 1 Black or African American [1.4%], and 64White [91.5%]) were included in this study. Relative to the control group, the football group showed significant cortical thinning, especially in fronto-occipital regions (eg, right precentral gyrus: t =−2.24; P =.01; left superior frontal gyrus: −2.42; P =.002). Elevated cortical thickness in football players was observed in the anterior and posterior cingulate cortex (eg, left posterior cingulate cortex: t =2.28; P =.01; right caudal anterior cingulate cortex 3.01; P =.001). The football group had greater and deeper sulcal depth than the control groups in the cingulate cortex, precuneus, and precentral gyrus (eg, right inferior parietal lobule: t =2.20; P =.004; right caudal anterior cingulate cortex: 4.30; P <.001). Significantly lower ALFFwas detected in the frontal lobe and cingulate cortex of the football group ( t =−3.66 to −4.92; P <.01), whereas elevated ALFF was observed in the occipital regions (calcarine and lingual gyrus, t =3.20; P <.01). Similar to ALFF, football players exhibited lower ReHo in the precentral gyrus and medial aspects of the brain, such as precuneus, insula, and cingulum, whereas elevated ReHo was clustered in the occipitotemporal regions ( t =3.17; P <.001; to 4.32; P <.01). There was no group difference in RS-FC measures. Conclusions and Relevance In this study of adolescent athletes, there was evidence of discernible structural and physiological differences in the brains of adolescent football players compared with their noncontact controls. Many of the affected brain regions were associated with mental health well-being. Cerebral Cortical Surface Structure and Neural Activation Pattern Among Adolescent Football Players Zuidema TR, Hou J, Kercher KA, et al. Cerebral Cortical Surface Structure and Neural Activation Pattern Among Adolescent Football Players. Originally published in JAMA Network Open 7, No. 2 (Feb. 1, 2024): e2354235. doi:10.1001/jamanetworkopen.2023.54235 © 2024 LLS. Printed with permission. https://creativecommons.org/licenses/by/4.0/ JAMA NETWORK OPEN ORIGINAL INVESTIGATION / PEDIATRICS
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