Sex differences in white matter alterations following repetitive subconcussive head impacts in collegiate ice hockey players

Sollmann, Nico; Echlin, Paul S.; Schultz, Vivian; Viher, Petra; Lyall, Amanda E.; Tripodis, Yorghos; Kaufmann, David; Härtl, Elisabeth; Kinzel, Philipp; Forwell, Lorie; Johnson, Andrew M.; Skopelja, Elaine N.; Lepage, Christian; Bouix, Sylvain; Pasternak, Ofer; Lin, Alexander P.; Shenton, Martha E.; Koerte, Inga K.

doi:10.1016/j.nicl.2017.11.020

Cited by 68 publications

(50 citation statements)

References 58 publications

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“…Relation to previous investigations. A variety of previous investigations into the effects of sports participation, repetitive head impacts and white matter tissue properties of athletes have used the diffusion tensor (DTI) model (Bahrami et al, 2016;Basser et al, 1994;Bazarian et al, 2014;Burzynska et al, 2016;Chang et al, 2015;Chun et al, 2015;Churchill et al, 2017aChurchill et al, , 2017bDavenport et al, 2016aDavenport et al, , 2016bDavenport et al, , 2014Deng et al, 2018;Duru and Balcioglu, 2018;Gajawelli et al, 2013;Hänggi et al, 2015Hänggi et al, , 2010Jäncke et al, 2009;Koerte et al, 2012;Kuzminski et al, 2018;Lao et al, 2015;Marchi et al, 2013;Mayinger et al, 2018;McAllister et al, 2014;Merchant-Borna et al, 2016;Myer et al, 2018Myer et al, , 2016aMyer et al, , 2016bPark et al, 2015;Saghafi et al, 2018;Schlaffke et al, 2014;Schranz et al, 2018;Sollmann et al, 2018;Stamm et al, 2015;Yuan et al, 2018) . The studies investigating the effects of elite sports participation commonly report lower fractional anisotropy (FA) and higher mean diffusivity (MD) between athletes and non-athletes.…”

Section: Discussionmentioning

confidence: 99%

“…amygdala, hippocampus, basal ganglia) white matter. A paucity of articles have studied differences in either major (Bahrami et al, 2016;Bazarian et al, 2014;Churchill et al, 2017aChurchill et al, , 2017bDavenport et al, 2016aDavenport et al, , 2016bKoerte et al, 2012;Kuzminski et al, 2018;Mayinger et al, 2018;McAllister et al, 2014;Merchant-Borna et al, 2016;Saghafi et al, 2018;Sollmann et al, 2018;Stamm et al, 2015;Yuan et al, 2018) or cortical and subcortical (Mayer et al, 2017) white matter between collision sport participants and controls (i.e., non-athletes, non-collision sport athletes, within-subject longitudinal), but few have looked at all three to fully characterize the effects of sports participation.…”

Section: Introductionmentioning

confidence: 99%

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Advanced mapping of the human white matter microstructure better separates elite sports participation

Caron¹,

Bullock²,

Kitchell³

et al. 2020

Preprint

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Collision-sport athletes, especially football players, are exposed to a higher number of repetitive head impacts. Little is known, however, regarding the effects of long-term exposure to repetitive head impacts on brain tissue structure and the locations (i.e. superficial or deep tissue structures) affected. On top of this, little is known about the effects of highly competitive athletics on brain tissue structure. We investigated this relationship, including the baseline effect of collegiate athletic participation, by mapping measures of microstructure to cortical and subcortical white matter parcels and major white matter tracts of varsity IU football players, cross-country runners, and non-athlete students using advanced microstructural mapping techniques and machine-learning. We tested a series of hypotheses on the differences between the subject groups. To do so, we implemented an innovative approach to statistical hypothesis testing combining advanced white matter tissue properties and machine-learning classifiers. We used cross-validation to select the best subject group model and best machine-learning classifier. Wide-spread differences in brain tissue microstructure across cortical, subcortical, and major white matter structures were documented. The tissue properties of the major white matter tracts were found to best predict collision-sport participation and sports participation in general, however, cortical and subcortical white matter parcels were also found to predict collision-sports participation. The biggest differences in brain tissue microstructure is between the athletes (football and cross country combined) and the non-athletes students. The rewards and risks of playing competitive sports at the highest collegiate level may account for the differences in brain microstructure. This was the first investigation into the effects of repetitive head impacts to use an open-source data processing platform brainlife.io. The data and code for these analyses are available via brainlife.io.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Advanced mapping of the human white matter microstructure better separates elite sports participation

Caron¹,

Bullock²,

Kitchell³

et al. 2020

Preprint

View full text Add to dashboard Cite

show abstract

“…AD represents the magnitude of diffusion along the direction of axons, and an AD reduction is often interpreted as a reflection of compromised axonal membrane integrity or axonal injury. 25,26 Although there are some opposing data, 27,28 studies have shown that contact-sport athletes had significantly lower MD in the corpus callosum than noncontact-sport athletes at preseason baseline. 29 Previous studies further reported that significant preseason to postseason decreases in MD and AD were observed in widespread white matter areas in high school football players, [30][31][32] and that the similar reduction in AD was found in youth football players at postseason.…”

Section: Discussionmentioning

confidence: 99%

“…Three serum samples in the football group were not assessed for biomarkers due to hemolysis, and a boxplot analysis identified 1 data point for Tau and NfL in the crosscountry group to be an unexplainable outlier, which was excluded from the analysis. As a result, 28 imaging data (n=20 football, n=8 cross-country) and 30 blood biomarker data (n=22 football, n=7 cross-country) were valid for the group difference analysis. We used 24 completed sets of the imaging-blood biomarker data (n=17 football, n=7 cross-country) for the association analysis.…”

Section: Demographicsmentioning

confidence: 95%

Association between proteomic blood biomarkers and DTI/NODDI metrics in adolescent football players

Kawata

Steinfeldt

Huibregtse

et al. 2020

Preprint

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250/250 words]The objective of the study was to examine the association between diffusion MRI techniques [diffusion tensor imaging (DTI) and neurite orientation/dispersion density imaging (NODDI)] and brain-injury blood biomarker levels [Tau, neurofilament-light (NfL), glialfibrillary-acidic-protein (GFAP)] in high-school football and cross-country runners at their baseline, aiming to detect cumulative neuronal damage from prior seasons. Twenty-five football players and 8 cross-country runners underwent MRI and blood biomarker measures during preseason data collection. The whole-brain, tract-based spatial statistics was conducted for six diffusion metrics: fractional anisotropy (FA), mean diffusivity (MD), axial/radial diffusivity (AD, RD), neurite density index (NDI), and orientation dispersion index (ODI). Diffusion metrics and blood biomarker levels were compared between groups and associated within each group. The football group showed lower AD and MD than the cross-country group in various axonal tracts of the right hemisphere. Elevated ODI was observed in the football group in the right hemisphere of the corticospinal tract. Blood biomarker levels were consistent between groups except for elevated Tau levels in the cross-country group. Tau level was positively associated with MD and negatively associated with NDI in the corpus callosum of football players, but not in crosscountry runners. Our data suggest that football players may develop axonal microstructural abnormality. Levels of MD and NDI in the corpus callosum were associated with serum Tau levels, highlighting the vulnerability of the corpus callosum against cumulative head impacts.Despite observing multimodal associations in some brain areas, neuroimaging and blood biomarkers may not strongly correlate to reflect the severity of brain damage.

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“…Though neuroimaging (e.g., functional MRI, DTI) can identify functional impairments and changes in white matter microstructure, we do not understand the clinical implications of these measures. [11][12][13][14][15] Moreover, on-field RHI exposure varies greatly in terms of magnitude, timing, type, and location of impact. [3][4][5][6] Variability in RHI exposure likely contributes to conflicting results across studies.…”

Section: Introductionmentioning

confidence: 99%

Repetitive subconcussive head impacts and changes in sensory processing for balance control

Santos

Anson

et al. 2019

Preprint

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Background: Repetitive subconcussive head impacts (RHI) may be associated with current and future detrimental neurological effects. However, the effects of RHI on sensory processing for balance control is unknown and may have significant clinical implications if athletes are still participating in sport despite impairments. Research Question: Are there changes in sensory processing for balance control during standing and walking following RHI? Methods: Thirty healthy, adult, amateur soccer players (15 males, 15 females, 21.8±2.8 years, 69.9±11.5 kg, 171.4±8.2 cm) volunteered for the standing balance Significance: Although the cumulative effects of RHI may result in later-life cognitive, behavioral, and mood impairments, a single episode of repeated soccer headers does not appear to be associated with acute impairments in sensory processing for balance control.

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Sex differences in white matter alterations following repetitive subconcussive head impacts in collegiate ice hockey players

Cited by 68 publications

References 58 publications

Advanced mapping of the human white matter microstructure better separates elite sports participation

Advanced mapping of the human white matter microstructure better separates elite sports participation

Association between proteomic blood biomarkers and DTI/NODDI metrics in adolescent football players

Repetitive subconcussive head impacts and changes in sensory processing for balance control

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