Sub-acute Changes on MRI Measures of Cerebral Blood Flow and Venous Oxygen Saturation in Concussed Australian Rules Footballers

Abstract

Background: Sports-related concussion (SRC) is common in collision sport athletes. There is growing evidence that repetitive SRC can have serious neurological consequences, particularly when the repetitive injuries occur when the brain has yet to fully recover from the initial injury. Hence, there is a need to identify biomarkers that are capable of determining SRC recovery so that they can guide clinical decisions pertaining to return-to-play. Cerebral venous oxygen saturation (SvO₂) and cerebral blood flow (CBF) can be measured using magnetic resonance imaging (MRI) and may provide insights into changing energy demands and recovery following SRC.

Results: In this study we therefore investigated SvO₂ and CBF in a cohort of concussed amateur Australian Football athletes (i.e., Australia's most participated collision sport). Male and female Australian footballers (n = 13) underwent MRI after being cleared to return to play following a mandatory 13-day recovery period and were compared to a group of control Australian footballers (n = 16) with no recent history of SRC (i.e., > 3 months since last SRC). Despite the concussed Australian footballers being cleared to return to play at the time of MRI, we found evidence of significantly increased susceptibility in the global white matter (p = 0.020) and a trend (F_5,21 = 2.404, p = 0.071) for reduced relative CBF (relCBF) compared to the control group. Further, there was evidence of an interaction between sex and injury in straight sinus susceptibility values (F_1,25 = 3.858, p = 0.061) which were decreased in female SRC athletes (p = 0.053). Of note, there were significant negative correlations between straight sinus susceptibility and relCBF suggesting impaired metabolic function after SRC.

Conclusions: These findings support the use of quantitative susceptibility mapping (QSM) and relCBF as sensitive indicators of SRC, and raise further concerns related to SRC guidelines that allow for return-to-play in less than two weeks.

Keywords: Hypometabolism; Mild traumatic brain injury; Neuroimaging; Quantitative susceptibility mapping; Return-to-play.

Fig. 1

Decreased relative cerebral blood flow (relCBF) 14 days after SRC. A Representative relCBF images from one male control (mCon), female control (fCon), male SRC (mSRC), and female SRC (fSRC) athlete. Four slices are shown for each representative athlete. Colorbar shows relCBF values and ‘L’ indicates left side of brain. B Representative relCBF image overlaid with co-registered Harvard–Oxford Subcortical Structural Atlas. C Median relCBF values plotted for 5 ROIs. Two-way MANOVA revealed a significant main effect of injury with concussed athletes having significantly decreased relCBF (p = 0.039). relCBF = relative cerebral blood flow, SRC = sports related concussion

Fig. 2

Analysis of global white and gray matter susceptibility values. A Mean control QSM image in study template space. Colorbar indicates susceptibility values in ppm. B Map of coefficient of variability. C Masks of global white (red, χ < − 0.03 ppm) and gray (orange, χ > 0.05 ppm) matter were generated by thresholding reliable QSM values (i.e. those voxels with coefficient of variability < 0.8) from the mean control image. D Two-way MANOVA revealed a significant effect of injury (p = 0.044, *) with post-hoc comparisons showing that SRC athletes had significantly increased susceptibility in the global white matter (Bonferroni corrected p = 0.020). QSM = quantitative susceptibility mapping, SRC = sports related concussion

Fig. 3

Straight sinus susceptibility as a measure of SvO₂. A Representative maximum intensity projection (MIP) image for one participant with the straight sinus manually delineated in magenta. B Mean susceptibility values for the straight sinus for all participants. Statistical testing with 2-way ANOVA revealed a trend towards a main effect of injury (p = 0.061). SvO₂ = Cerebral venous oxygen saturation

Fig. 4

Straight sinus susceptibility values correlated with relCBF in the left hemisphere. Across all participants relCBF in the left A grey and B white matter correlated negatively with susceptibility values in the straight sinus—a measure of SvO₂. C Although not reaching significance, an analysis of the SRC athletes also revealed an inverse relationship between straight sinus susceptibility and relCBF in the basal ganglia. relCBF = relative cerebral blood flow, SRC = sports related concussion, SvO₂ = Cerebral venous oxygen saturation