Elsevier

Clinical Neurophysiology

Volume 115, Issue 12, December 2004, Pages 2699-2710
Clinical Neurophysiology

Quantitative continuous EEG for detecting delayed cerebral ischemia in patients with poor-grade subarachnoid hemorrhage

https://doi.org/10.1016/j.clinph.2004.06.017Get rights and content

Abstract

Objective

Delayed cerebral ischemia (DCI) due to vasospasm is often undetected by clinical exam in patients with poor-grade subarachnoid hemorrhage (SAH). The purpose of this study was to identify quantitative EEG (qEEG) parameters that are most sensitive and specific for the detection of DCI in stuporous or comatose SAH patients.

Methods

Of 78 consecutive Hunt–Hess grade 4 or 5 SAH patients admitted to our Neuro-ICU over a 2-year period, 48 were eligible for participation and 34 were enrolled. Continuous EEG monitoring was performed from post-operative day 2 to post-SAH day 14. In each patient, 20 artifact-free, 1 min EEG-clips following an alerting stimulus were analyzed: 10 clips were obtained on monitoring day 1 (baseline), and 10 on days 4–6 (follow-up). In DCI patients, follow-up clips were obtained after the onset of deterioration and before infarction had occurred. Twelve qEEG parameters were calculated using fast Fourier transformation; generalized estimating equations were used to compare ratios of change in qEEG parameters in patients with and without DCI.

Results

Nine of 34 patients (26%) developed DCI. The alpha/delta ratio (alpha power/delta power; ADR) demonstrated the strongest association with DCI. The median decrease of ADR for patients with DCI was 24%, compared to an increase of 3% for patients without DCI (Z=4.0, P<0.0001). Clinically useful cut-offs included 6 consecutive recordings with a >10% decrease in ADR from baseline (sensitivity 100%, specificity 76%) and any single measurement with a >50% decrease (sensitivity 89%, specificity 84%).

Conclusions

A decrease in the ADR may be a sensitive method of detecting DCI, with reasonable specificity. This post-stimulation qEEG parameter may supplement the clinical exam in poor-grade SAH patients and may prove useful for the detection of DCI.

Significance

Following ADRs may allow earlier detection of DCI and initiation of interventions at a reversible stage, thus preventing infarction and neurological morbidity.

Introduction

Delayed cerebral ischemia (DCI) from vasospasm is an important cause of morbidity and mortality after subarachnoid hemorrhage (SAH) (Kassell et al., 1982, Mayberg, 1998). Angiographic vasospasm is detected in 50–70% of patients with SAH (Weir et al., 1978) and DCI occurs in 19–46% of SAH patients (Hijdra et al., 1988, Murayama et al., 1997, Charpentier et al., 1999, Hop et al., 1999, Qureshi et al., 2000, Claassen et al., 2001) and 54% of poor-grade SAH patients (Kirmani et al., 2002). One of the greatest challenges for the acute management of poor-grade SAH patients remains the early detection of clinically relevant DCI due to vasospasm. In these poor-grade patients, deterioration is often missed and silent infarction occurs in 21% (Kirmani et al., 2002). Silent infarction accounts for approximately one fourth of patients with DCI (Claassen et al., 2001, Shimoda et al., 2001) and is associated with poor clinical grade and poor outcome (Claassen et al., 2001, Kirmani et al., 2002).

EEG monitoring provides continuous information about cerebral function and may allow early detection of focal ischemia (Labar et al., 1991, Vespa et al., 1997, Vespa et al., 1999). EEG changes due to energy and ion pump failure occur when cerebral blood flow (CBF) falls below 25–30 ml/100 g per min, at a time when therapeutic interventions might prevent permanent brain damage as infarction does not occur until CBF falls below 18 ml/100 g per min (Astrup et al., 1981, Baron, 2001, Sundt et al., 1981). Cerebral infarction may result in polymorphic delta, and attenuation of fast activity, including sleep spindles (Cohn et al., 1948, Niedermeyer, 1999, Nuwer et al., 1987). These EEG findings reflect abnormal CBF and disrupted metabolism (cerebral metabolic rate of oxygen) as seen with positron emission tomography (Nagata et al., 1989) and Xenon-CT-CBF studies (Tolonen and Sulg, 1981, Ingvar et al., 1976). The sensitivity of EEG to detect reversible ischemia was clinically first applied to intraoperative monitoring, specifically to monitor CBF during carotid endarterectomy (Sharbrough et al., 1973, Zampella et al., 1991).

Digital EEG can be transformed into power spectra by fast Fourier transformation (FFT), compressing long periods of raw EEG into quantitative EEG (qEEG) parameters. These can be displayed as graphs and may reveal subtle changes in the EEG earlier than any other monitoring technique. These graphs can be used to monitor depth of sedation, intraoperative brain function (effects of sedation or brain injury), detect seizures, and possibly detect DCI due to vasospasm after SAH (Labar et al., 1991, Vespa et al., 1997).

Two prior studies have related quantitative analysis of continuous EEG (cEEG) data with vasospasm in SAH patients. They found the trend analysis of total power (1–30 Hz) (Labar et al., 1991), and the variability of relative alpha (6–14/1–20 Hz) (Vespa et al., 1997) to be most predictive. Both these studies were almost entirely limited to non-comatose, good-grade patients (Hunt–Hess grades 1–3). However, awake patients are easily monitored with serial clinical exams. In this context, the utility of cEEG may still exist, as one prior report demonstrated qEEG changes preceding the clinical deterioration by a mean of 2.9 days (Vespa et al., 1997). It is unclear if this technique may also be useful in poor-grade SAH patients, who often have severely abnormal EEG findings, which are more pronounced with increasing impairment of consciousness (Daly and Markand, 1990).

The purpose of this study was to identify EEG parameters with a high sensitivity for DCI in poor-grade patients in order to alert the treating neurologist so that more definitive diagnostic tests and therapeutic interventions may be initiated. We also intended to determine the feasibility of this monitoring technique in these often medically unstable patients that require frequent in-hospital transportation and procedures.

Section snippets

Subjects

All SAH patients admitted to the Neurological Intensive Care Unit (NICU) of Columbia-Presbyterian Medical Center between January 2000 and January 2002 were offered enrollment in the study. Eligibility criteria included: (1) Hunt–Hess grade 4 or 5 (stupor or coma) on admission or within 24 h of NICU admission but prior to aneurysm treatment; (2) aneurysm treated with surgery or Guglielmi Detachable Coils; (3) alive on post-operative day 1; (4) EEG hook-up possible within 7 days of SAH onset; and

Study cohort

Of 78 consecutive Hunt–Hess grade 4 or 5, SAH patients admitted to the Columbia Neuro-ICU between 1/2000 and 1/2002, 48 were eligible for enrollment in the study protocol, and cEEG was performed in 34 (Fig. 1). Six eligible patients were not included because they were medically unstable, and 8 because of technical or logistical difficulties. Among the 30 non-eligible Hunt–Hess grade 4 or 5 SAH patients, 17 died prior to surgery, 11 had documented vasospasm on their initial angiogram, and 2 were

Discussion

We studied the ability of qEEG parameters to detect DCI from vasospasm in poor-grade SAH patients. The post-stimulation ADR (PSADR) detected patients with DCI with good sensitivity and specificity. In poor-grade stuporous or comatose patients, the earliest stages of DCI often go undetected. Alternative methods of continuous brain monitoring are limited by lack of sensitivity (e.g. clinical exam, CT, TCD), high false positive rates (e.g. TCD), and no standardized criteria for abnormality (e.g.

Acknowledgements

We would like to thank the ICU fellows, residents, and nurses of New York Presbyterian Hospital at Columbia University for their overall support of this project. This paper was supported by a Grant-in-Aid to Stephan A. Mayer, MD from the American Heart Association (#9750432N).

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