Electrocorticography (ECoG) with a linear subdural platinum electrode strip is the current gold standard for monitoring spreading depolarizations in the clinic. The most commonly used electrode contains six platinum contacts spaced at 10mm along the strip (Wyler, 5mm diameter, Ad-Tech, Racine, WI, USA). Subdural placement on the cortical surface allows monitoring of viable tissue at risk for secondary injury. Recordings run for up to 14 days in aneurysmal subarachnoid hemorrhage (aSAH), and 7 days in other conditions.
In patients that require an open craniotomy after traumatic brain injury, intracerebral hemorrhage, or malignant hemispheric stroke, the electrode strip is placed on peri-contusional, peri-hematomal, or peri-infarct tissue, respectively. In patients that require an open craniotomy after aSAH, the electrode strip is targeted at the vascular territory of the aneurysm-carrying vessel. This area is often a predilection site for delayed cerebral ischemia because it bears the most blood clots.
These two images illustrate both correct and poor placement of subdural strip electrodes. Each of these images show a brain injury with a central contusion and surrounding penumbra. The pink line emerging from the injury indicates the hypothetical path of a spreading depolarization. Since spreading depolarizations have difficulties crossing sulci and major fissures, the strip should preferably be placed along a single gyrus so that the depolarization can contact most of the embedded electrodes. This allows the best documentation of the propagation. Increasing the distance of the strip electrode from the injury decreases the chance of detecting spreading depolarizations.
The tail of the electrode strip is tunneled subcutaneously beneath the scalp and exited 2–3 cm from the craniotomy scalp incision. It should then be coiled and sutured to the scalp to provide strain relief and guard against accidental displacement. The previously removed bone flap may be re-secured with a titanium clamp or plating system, followed by standard wound closure (paying special attention not to place any sutures around the electrode).
Electrical ground is provided by a platinum needle (Technomed Europe, Maastricht, Netherlands or Natus Neurology - Grass, Warwick, RI, USA), silver/silver chloride (Ag/AgCl) scalp electrode, or a self-adhesive Ag/AgCl patch electrode on the shoulder. For direct current (DC) referential recordings, a platinum needle or Ag/AgCl sticky electrode is placed as a reference on the mastoid or frontal apex, away from muscle attachments.
Gentle traction may not be sufficient to remove the strip after the monitoring period when it is trapped/pinched by the bone flap or the titanium fixation, or if the subcutaneous tunnel is too tight.
A cerebrospinal fluid (CSF)-fistula may develop. Therefore, the following precautions should be taken:
Not all patients require a craniotomy. Here, it is also possible to place a subdural electrode strip through a burr hole, or to monitor with an intraparenchymal electrode array (Spencer, 1.1mm diameter, Ad-Tech, Racine, WI, USA) that is placed through a burr hole or a multi-lumen bolt. This is customary practice for intracranial pressure (ICP) and tissue partial pressure of oxygen (ptiO2) monitoring.
Advantages |
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- good safety profile |
- lower risk of CSF fistula compared to a subdural strip electrode |
Disadvantages |
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- cause necrosis at insertion site |
- cause local disruption of the blood-brain barrier (upregulation of inflammatory cell types, extravasation of plasma proteins) |
- fail to detect spreading depolarizations in the wider vicinity |
- subject to spreading depolarization-triggered pH and ptiO2 changes that may influence the DC potential |
Advantages |
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- less invasive |
- permits recording of a larger cortical area |
Disadvantages |
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- risk of CSF fistula |
(- subject to spreading depolarization-triggered pH and ptiO2 changes that may influence the DC potential) |
Resistive and nonpolarizing Ag/AgCl and calomel electrodes are ideal for the recording of low-frequency potentials. Their toxicity, however, precludes an invasive use in patients. Platinum electrodes are safe to use in patients, but it has been assumed that they distort low-frequency and DC potentials due to their polarizable character. In the clinical setting, alternating current (AC) coupled amplifiers with a 0.01–0.02 Hz lower frequency limit were used until it became clear that DC coupled amplifiers could be reliably used for continuous ECoG monitoring as well. This has the great advantage that the durations of the DC shifts can be measured. Practical experience of DC recordings suggests that they are a suitable substitute for AC techniques.
Noninvasive technologies such as continuous scalp electroencephalography (EEG) are not yet sufficient to detect spreading depolarizations without simultaneous subdural ECoG monitoring. However, correlates of spreading depolarizations have previously been identified in combined scalp EEG/ECoG recordings. Scalp EEG may hold particular promise for noninvasive monitoring of spreading depolarization, if it is combined with other noninvasive technologies that measure regional cerebral blood flow (rCBF) or its surrogates.
1 | Brainamp amplifier | 3 |
Laptop with software a) LabChart b) Brain Vision Recorder |
5 | Powerlab 16/SP analog/ digital converter |
2 | GT205 amplifier, 0.01–50 Hz | 4 | Integra Licox Brain Tissue Oxygen Monitoring System | 6 | Component Neuromonitoring System (CNS) Monitor |
The hallmark signature of spreading depolarization in the ECoG is a negative DC shift with sequential onset in adjacent electrodes. The raw DC can only be seen with DC-coupled amplifiers (see section above). AC-coupled amplifiers with a lower frequency limit of 0.01 or 0.02 Hz distort the cortical DC shift of spreading depolarization but a typical slow potential change is still visible. We can use the AC-recorded slow potential change to identify spreading depolarizations. However, only the unfiltered DC shift allows assessment of the local duration of spreading depolarization, and it is a true measure of tissue energy status and risk of injury. In the following section, the term DC shift also refers to the slow potential change in the AC-ECoG.
Spreading depolarization-induced spreading depression presents as a more or less rapidly developing, propagating reduction of the raw amplitude of spontaneous brain electrical activity in the 0.5-45 Hz band, or any derived measure based on amplitude. Review of the raw signal alongside a leaky integral of power of the bandpass filtered AC-ECoG most reliably shows this loss of amplitude.
1. Trace: Near-DC/AC ECoG (0.01-45 Hz) shows a spreading depolarization as a characteristic negative, slow potential change. (Negative DC shift is only seen with DC-coupled amplifiers, and is not shown here.)
2. Trace: 0.5-45 Hz bandpass-filtered ECoG shows spreading depolarization-induced spreading depression as an amplitude reduction.
Arithmetic calculation in LabChart:
bandpass(rch[No. of channel in raw recordings];0.5,45)
3. Trace: Squared 0.5-45 Hz bandpass-filtered ECoG (also called AC-ECoG power) provides better visualization of amplitude loss during spreading depression. Changes of power are less sensitive to artifacts than changes of the integral of power (see below).
Arithmetic calculation in LabChart:
bandpass(rch[No. of channel];0.5;45)^2
4. Trace: The integral of power is based on a method of computing time integrals over a sliding window according to a time decay function. This provides a smooth curve that facilitates the assessment of changes in the AC-ECoG power, i.e. the exact start and end of spreading depolarization-induced depression periods.
Arithmetic calculation in LabChart:
integrate(bandpass(rch[No. of channel];0.5;45)^2;”decay”;60)
Data analysis software such as LabChart (ADInstruments, Oxford, UK)provide various filtering and signal processing functions and allow multiple display views. DC shifts and depression durations can be observed in either monopolar (unipolar montage against a reference electrode) or bipolar recordings (each electrode subtracted from neighboring electrode). Monopolar recordings are superior to bipolar recordings when local information on individual electrodes is of interest, such as the duration of the DC shift. The bipolar montage provides more stable recordings in case of reference electrode loss due to patient movement or nursing procedures.
For the basic analysis, it is at certain points necessary and/or helpful to convert the raw ECoG signal. In the following list you will find a step-by-step tutorial for the analysis, together with the arithmetic LabChart conversion codes needed for the individual tasks.
Data post-processing provides summary measures that help to examine the relationship between recorded data and clinical events such as baseline injuries, interventions, lesion development (as assessed by neuroimaging), patient outcome, and late epilepsy. All summary measures should be normalized to the duration of valid recording.
With a bit of training, the identification of spreading depolarizations is usually straightforward and it is quite easy to distinguish the characteristic waveforms from other confounding physiologic changes or artifacts that may present as similar waves. In individual patients, spreading depolarizations often show a stereotypical pattern which means that in cases of doubt, it is useful to screen all recordings from that patient to get used to the specific spreading depolarization pattern. Once that pattern is understood, it is easier to recognize all spreading depolarizations, and to score events that would normally be missed (e.g. spreading depolarizations co-occurring with signals caused by artifacts). In addition to that, typical responses of ptiO2 or rCBF to spreading depolarization – when recorded – are also useful. If significant doubts remain, it is recommended that questionable events should not be scored as spreading depolarizations to avoid false positives. In this section, you will find some examples of frequent artifacts.
Minimal requirements to diagnose spreading depolarization
The following slide show will guide you through some of the most common troubleshooting scenarios.