Spreading depolarization may represent a novel mechanism for delayed fluctuating neurological deficit after chronic subdural hematoma evacuation

Abstract

<jats:sec><jats:title>OBJECTIVE</jats:title><jats:p>Most patients with chronic subdural hematoma (cSDH) recover after surgical evacuation with a straightforward course. There is a subset of patients who develop transient and fluctuating deficits not explained by seizures, stroke, or mass effect after evacuation. The objective of this study was to investigate whether these postoperative neurological deficits may be related to temporary brain dysfunction caused by cortical spreading depolarizations (SDs).</jats:p></jats:sec><jats:sec><jats:title>METHODS</jats:title><jats:p>The authors conducted a prospective observational study of 40 patients who underwent cSDH evacuation. At the time of surgery, a 1 × 6 subdural electrode strip was placed on the cortex parallel to the subdural drain. Clinical outcomes were assessed utilizing the Markwalder Grading Scale, need for clinical EEG for new deficit, and presence of new deficits.</jats:p></jats:sec><jats:sec><jats:title>RESULTS</jats:title><jats:p>Definitive SD was detected in 6 (15%) of 40 patients. Baseline and cSDH characteristics did not differ between patients with and without SD. More patients experienced postoperative neurological deterioration if they had SD (50%) compared to those without SD (8.8%; p = 0.03). Only 2 patients in the entire cohort demonstrated early neurological deterioration, both of whom had SD. One of these cases demonstrated a time-locked new focal neurological deficit (aphasia) at the start of a series of multiple clusters of SD.</jats:p></jats:sec><jats:sec><jats:title>CONCLUSIONS</jats:title><jats:p>This is the first observation of SD occurring after cSDH evacuation. SD occurred at a rate of 15% and was associated with neurological deterioration. This may represent a novel mechanism for otherwise unexplained fluctuating neurological deficit after cSDH evacuation. This could provide a new therapeutic target, and SD-targeted therapies should be evaluated in prospective clinical trials.</jats:p></jats:sec>

Oxygen-Induced and pH-Induced Direct Current Artifacts on Invasive Platinum/Iridium Electrodes for Electrocorticography

“…Accordingly, SD is observed as a large negative direct current (DC) shift, two-photon microscopy shows neuronal swelling with a beaded morphology of neuronal dendrites during SD [2], and magnetic resonance imaging shows a propagating wave of diffusion restriction [3][4][5]. SDs occur during a plethora of clinical conditions, including migraine aura [6,7], ischemic stroke [8,9], traumatic brain injury [10,11], aneurysmal subarachnoid hemorrhage (aSAH) and delayed ischemic stroke [12][13][14], spontaneous intracerebral hemorrhage [15], subdural hematoma [16], development of brain death [17,18], and dying from circulatory arrest [19]. The SD continuum describes the spectrum from transient events of intermediate duration to short duration in less ischemic or adequately supplied tissue to terminal SDs in severely ischemic tissue characterized by the transition of the neurons from the state of injury to cell death [20,21].…”

Cortical Spreading Depolarization in Chronic Subdural Hematoma: Bridging the Gap

“…Interestingly, the presence of CSD in patients with SDH proved to be a marker for worse prognostic outcome, 39 while the presence of NESIS, believed to be a marker of CSD, was associated with favorable outcome in two distinct studies. 7,10 Although the different study design limits the possibility for direct comparisons, such discrepancies could be related to the different population studied.…”

“…A recent study using ECoG in 40 patients with chronic SDH post-surgical evacuation revealed the presence of definite CSD in 15% of patients post-surgical evacuation (independent of the presence or absence of TNS). 39 One of the cases demonstrated a time-lock focal neurological deterioration at the onset of CSD clusters with no alternative causal explanation on MRI or EEG supporting that his TNS may have been directly caused by the CSD. The presence of CSD proved to be of prognostic significance and was associated with postoperative neurological deterioration in 50% compared to 8.8% in the subgroup without evidence of CSD.…”

Spreading Depolarizations and Neurological Deterioration in Patients with Subdural Hematoma: Putting a Name to a Face?

“…SDs are pathologic waves in cerebral gray matter defined by the near-complete breakdown of electrochemical membrane gradients, with consequent silencing of electrical activity (spreading depression) [5]. The hypothesis that SDs underlie some of these syndromes is supported by the known role of SDs in delayed neurological injury [5], including in patients with cSDH [6].In this issue of Neurocritical Care, Meadows et al[7] expand on prior work by examining the clinical characteristics and significance of definite and "probable" SDs in postoperative patients with cSDH. The authors combined two cohorts for this study: one cohort consisted of prospectively enrolled patients with cSDH with strip electrodes, whereas a second and larger cohort consisted of postoperative patients with cSDH who underwent usual care without a strip electrode.…”

“…SDs are pathologic waves in cerebral gray matter defined by the near-complete breakdown of electrochemical membrane gradients, with consequent silencing of electrical activity (spreading depression) [5]. The hypothesis that SDs underlie some of these syndromes is supported by the known role of SDs in delayed neurological injury [5], including in patients with cSDH [6].…”