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Simulation of spreading depolarization trajectories in cerebral cortex: Correlation of velocity and susceptibility in patients with aneurysmal subarachnoid hemorrhage

: Milakara, Denny; Grozea, Cristian; Dahlem, Markus; Major, Sebastian; Winkler, Maren K.L.; Lückl, Janos; Scheel, Michael; Kola, Vasilis; Schoknecht, Karl; Lublinsky, Svetlana; Friedman, Alon; Martus, Peter; Hartings, Jed A.; Woitzik, Johannes; Dreier, Jens P.

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NeuroImage: Clinical. Online journal 16 (2017), S.524-538
ISSN: 2213-1582
Zeitschriftenaufsatz, Elektronische Publikation
Fraunhofer FOKUS ()
3D, three dimensional; alternating current (AC); apparent diffusion coefficient (ADC); co-operative studies on brain injury depolarization (COSBID); computed tomography (CT); cytotoxic edema; direct current (DC); diffusion-weighted imaging (DWI); electrode; electrocorticography (ECoG); fluid-attenuated inversion recovery (FLAIR); hounsfield unit; intracerebral hemorrhage (ICH); intrinsic optical signal (IOS); Ischemia; middle cerebral artery (MCA); malignant hemispheric stroke (MHS); magnetization prepared rapid gradient echo (MPRAGE); magnetic resonance imaging (MRI); nitric oxide (NO); peak total SD-induced depression duration of a recording day (PTDDD); radius difference; subarachnoid hemorrhage (SAH); spreading depolarization (SD); slow potential change (SPC); spreading depression; stroke; subarachnoid hemorrhage; traumatic brain injury (TBI); time-of-SD-arrival-difference (TOAD); velocity difference; World Federation of Neurosurgical Society (WFNS); aneurysmal subarachnoid hemorrhage (aSAH)

In many cerebral grey matter structures including the neocortex, spreading depolarization (SD) is the principal mechanism of the near-complete breakdown of the transcellular ion gradients with abrupt water influx into neurons. Accordingly, SDs are abundantly recorded in patients with traumatic brain injury, spontaneous intracerebral hemorrhage, aneurysmal subarachnoid hemorrhage (aSAH) and malignant hemispheric stroke using subdural electrode strips. SD is observed as a large slow potential change, spreading in the cortex at velocities between 2 and 9 mm/min. Velocity and SD susceptibility typically correlate positively in various animal models. In patients monitored in neurocritical care, the Co-Operative Studies on Brain Injury Depolarizations (COSBID) recommends several variables to quantify SD occurrence and susceptibility, although accurate measures of SD velocity have not been possible. Therefore, we developed an algorithm to estimate SD velocities based on reconstructing SD trajectories of the wave-front's curvature center from magnetic resonance imaging scans and time-of-SD-arrival-differences between subdural electrode pairs. We then correlated variables indicating SD susceptibility with algorithm-estimated SD velocities in twelve aSAH patients. Highly significant correlations supported the algorithm's validity. The trajectory search failed significantly more often for SDs recorded directly over emerging focal brain lesions suggesting in humans similar to animals that the complexity of SD propagation paths increase in tissue undergoing injury.