Objective: To test the hypothesis that a history of concussion (HOC) causes greater disturbances in cerebral blood flow (CBF) and white matter microstructure of midline brain structures after subsequent concussions, during the acute and chronic phases of recovery.

Methods: In this longitudinal magnetic resonance imaging (MRI) study, 61 athletes with uncomplicated concussion (36 with HOC) were imaged at the acute phase of injury (1 to 7 days post-injury), the subacute phase (8 to 14 days), medical clearance to return to play (RTP), one month post-RTP and one year post-RTP. A normative group of 167 controls (73 with HOC) were also imaged. Each session assessed CBF of the cingulate cortex, along with fractional anisotropy (FA) and mean diffusivity (MD) of the corpus callosum. Linear mixed models tested for interactions of HOC with time post-injury. The sport concussion assessment tool (SCAT) was also used to evaluate effects of HOC on symptoms, cognition and balance.

Results: Athletes with HOC had greater declines in midcingulate CBF subacutely (z=-3.29, p=0.002) and greater declines in posterior cingulate CBF at one year post-RTP (z=-2.42, p=0.007). No significant effects of HOC were seen for FA, whereas athletes with HOC had higher MD of the splenium at RTP (z=2.54, p=0.008). These effects were seen in the absence of differences in SCAT domains (|z|<1.14, p>0.256) or time to RTP (z=0.23, p=0.818).

Conclusions: Results indicate subacute and chronic effects of HOC on cingulate CBF and callosal microstructure, in the absence of differences in clinical indices. These findings provide new insights into physiological brain recovery after concussion, with cumulative effects of repeated injury detected among young, healthy athletes.