Development and Evaluation of a Method for Automated Detection of Spreading Depolarizations in the Injured Human Brain

Jewell, Sharon; Hobson, Stephen; Brewer, Grant; Rogers, Michelle; Hartings, Jed A.; Foreman, Brandon; Lavrador, José-Pedro; Sole, Michael J.; Pahl, Clemens; Boutelle, Martyn G.; Strong, Anthony J.

doi:10.1007/s12028-021-01228-x

Cited by 5 publications

(25 citation statements)

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“…Besides movement artifacts, there is at least one other type of DC artifact that is significantly more complex and specifically related to Pt electrodes. Thus, it was previously noted in two clinical cases that the interference of tissue partial pressure of oxygen (p ti O 2 ) with subdural platinum electrodes produces DC artifacts [19,41]. These artifacts are particularly impressive when nurses or intensivists increase blood oxygenation by increasing the fraction of inspired oxygen (FiO 2 ) on the ventilator (Figs.…”

Section: Introductionmentioning

confidence: 96%

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

et al. 2021

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Background Spreading depolarization (SD) and the initial, still reversible phase of neuronal cytotoxic edema in the cerebral gray matter are two modalities of the same process. SD may thus serve as a real-time mechanistic biomarker for impending parenchyma damage in patients during neurocritical care. Using subdural platinum/iridium (Pt/Ir) electrodes, SD is observed as a large negative direct current (DC) shift. Besides SD, there are other causes of DC shifts that are not to be confused with SD. Here, we systematically analyzed DC artifacts in ventilated patients by observing changes in the fraction of inspired oxygen. For the same change in blood oxygenation, we found that negative and positive DC shifts can simultaneously occur at adjacent Pt/Ir electrodes. Methods Nurses and intensivists typically increase blood oxygenation by increasing the fraction of inspired oxygen at the ventilator before performing manipulations on the patient. We retrospectively identified 20 such episodes in six patients via tissue partial pressure of oxygen (ptiO2) measurements with an intracortical O2 sensor and analyzed the associated DC shifts. In vitro, we compared Pt/Ir with silver/silver chloride (Ag/AgCl) to assess DC responses to changes in pO2, pH, or 5-min square voltage pulses and investigated the effect of electrode polarization on pO2-induced DC artifacts. Results Hyperoxygenation episodes started from a ptiO2 of 37 (30–40) mmHg (median and interquartile range) reaching 71 (50–97) mmHg. During a total of 20 episodes on each of six subdural Pt/Ir electrodes in six patients, we observed 95 predominantly negative responses in six patients, 25 predominantly positive responses in four patients, and no brain activity changes. Adjacent electrodes could show positive and negative responses simultaneously. In vitro, Pt/Ir in contrast with Ag/AgCl responded to changes in either pO2 or pH with large DC shifts. In response to square voltage pulses, Pt/Ir falsely showed smaller DC shifts than Ag/AgCl, with the worst performance under anoxia. In response to pO2 increase, Pt/Ir showed DC positivity when positively polarized and DC negativity when negatively polarized. Conclusions The magnitude of pO2-induced subdural DC shifts by approximately 6 mV was similar to that of SDs, but they did not show a sequential onset at adjacent recording sites, could be either predominantly negative or positive in contrast with the always negative DC shifts of SD, and were not accompanied by brain activity depression. Opposing polarities of pO2-induced DC artifacts may result from differences in baseline electrode polarization or subdural ptiO2 inhomogeneities relative to subdermal ptiO2 at the quasi-reference.

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Section: Introductionmentioning

confidence: 96%

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

et al. 2021

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“…In this section, we explore the performance of our method in prediction of the number of SDs from the total minutes of detected SD events. This analysis is inspired by the recent work of Jewell et al [10], where a linear regression was used for estimation of the number of SDs in 24-hour time windows. The frequency of occurrence of SDs could help clinicians make an informed decision on the type of medications and/or invasive procedures.…”

Section: Performance Of Wavefront In Prediction Of Sd Frequencymentioning

confidence: 99%

“…Increasing evidence shows that SDs are associated with poor clinical outcomes in traumatic brain injuries (TBIs), stroke, and hemorrhages [4][5][6][7][8][9]. Experts believe that this association is causal, such that the neurophysiological sequelae of SDs directly worsen secondary brain injury [9][10][11][12][13][14][15]. Recent studies have explored the potential of SD as a therapeutic target in subarachnoid hemorrhage (SAH) [9,[16][17][18] and TBI [19,20].…”

Section: Introductionmentioning

confidence: 99%

“…In [10], towards automating ECoG-based SD detection, Jewell et al developed a technique for real-time SD detection using ECoG signals, by combining features from low-frequency bands (e.g., slow potential changes in 0.005-0.5 Hz) and highfrequency bands (e.g., reduction of envelope amplitude in 0.5-45 Hz). They reported a detection rate of ∼ 79%, with a 0.9% false alarm rate 2 , in 18 acute brain injuries patients with DHC.…”

Section: Introductionmentioning

confidence: 99%

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Noninvasive, automated and reliable detection of spreading depolarizations in severe traumatic brain injury using scalp EEG

Chamanzar

Elmer

Shutter

et al. 2022

Preprint

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Background: Noninvasive detection of spreading depolarizations (SD), as a potentially treatable mechanism of worsening brain injuries after traumatic brain injuries (TBI), has remained elusive. Current methods to detect SDs are based on intracranial recording, an invasive method with limited spatial coverage. Less invasive methods to diagnose SD are needed to improve generalizability and application of this emerging science and to guide worsening brain injury treatments. Here, we demonstrate, for the first time, a signal processing paradigm that can enable automated detection of SDs using noninvasive electroencephalography (EEG). Methods: Building on our previously developed WAVEFRONT algorithm, we have designed a novel automated SD detection method. This algorithm, with learnable parameters and improved velocity estimation, extracts and tracks propagating power depressions, as well as near-DC shifts using low-density EEG. This modified WAVEFRONT is robust to the amplitude outliers and non-propagating depressions on the scalp. We show the feasibility of detecting SD events (700 total SDs) in continuous, low-density scalp EEG recording (95±42.2 hours with 19 electrodes) acquired from 12 severe TBI patients who underwent decompressive hemicraniectomy (DHC) and intracranial EEG that could be used as a ground truth for event detection. We quantify the performance of WAVEFRONT in terms of SD detection accuracy, including true positive rate (TPR) and false positive rate (FPR), as well as the accuracy of estimating the frequency of SDs. Results: WAVEFRONT achieves the best average validation accuracy of 74% TPR (with 95% confidence interval of 70.8%-76.7%), with less than 1.5% FPR using Delta band EEG. Preliminary evidence suggests that WAVEFRONT can achieve a very good performance (regression with R2 ≃ 0.71) in the estimation of SD frequencies. Conclusions: We demonstrate feasibility and quantify the performance of noninvasive SD detection after severe TBI using an automated algorithm. WAVEFRONT can potentially be used for diagnosis and monitoring of worsening brain injuries to guide treatments by providing a measure of SD frequency. Extension of these results to patients with intact skulls requires further study.

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“…Depolarization of neural tissue is an inciting event that starts the clock on cell death machinery, and work in anoxic brain injury highlights the importance of SD and their potential as a diagnostic or therapeutic target in patients suffering cardiac arrest (Han et al [unpublished]). Finally, practical efforts to reliably detect SD in the intensive care unit setting are represented through exciting new tools that can be used at the bedside [18].…”

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confidence: 99%

Introduction to Spreading Depolarizations: Special Edition of Neurocritical Care

Balu

Foreman

2021

Neurocrit Care

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Spreading depolarization (SD) of brain tissue is one of the most common, dramatic, and mysterious physiologic events in the central nervous system [1,2]. Seemingly all at once, the charge polarization of neuronal and glial cell membranes completely dissipates, silencing normal brain electrical activity and creating widespread changes in volume, flow, and metabolism. These massive depolarizations are akin to a dam bursting open, and they propagate across the cerebral cortex like tsunamis at speeds of approximately 3 mm/min. The dissipation of charge within neural tissues during SDs flattens electroencephalographic signals and sparks a scramble of adenosine-triphosphate (ATP)-dependent activity aimed at restoring normal membrane gradients in their wake. First described in the 1940s, SDs were viewed for decades as a physiological curiosity. However, a multitude of studies since Leao's initial description [3] have linked SDs to the pathophysiology of some of the most prevalent neurological diseases, including migraine, stroke, anoxic brain injury, and traumatic brain injury. Nearly 60 years after their initial description in the laboratory, the first confirmation of the occurrence of SDs in the injured human neocortex was reported in patients undergoing subdural electrocorticography [4], cementing their clinical relevance and ushering a new era of translational SD research.Much foundational translational work has been done under the leadership and inspiration of the Co-Operative Studies on Brain Injury Depolarizations (http:// www. cosbid. org/) consortium. Co-Operative Studies on Brain Injury Depolarizations studies have convincingly demonstrated that SDs occur with high frequency in nearly all

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Development and Evaluation of a Method for Automated Detection of Spreading Depolarizations in the Injured Human Brain

Cited by 5 publications

References 33 publications

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

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

Noninvasive, automated and reliable detection of spreading depolarizations in severe traumatic brain injury using scalp EEG

Introduction to Spreading Depolarizations: Special Edition of Neurocritical Care

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