Reproducibility and clinical relevance of quantitative EEG parameters in cerebral ischemia: A basic approach

https://doi.org/10.1016/j.clinph.2009.02.171Get rights and content

Abstract

Objective

To investigate reproducibility and clinical relevance of quantitative EEG parameters in ischemic cerebrovascular disease.

Methods

EEG was recorded in 31 patients suffering from subacute ischemic cerebrovascular disease. Ten age-matched control subjects were included as a reference group. Intra-recording, intrarater and interrater reproducibility was calculated for standard EEG measures and for a pair wise derived Brain Symmetry Index (pdBSI). Correlations between EEG parameters, clinical status and volume of ischemia on diffusion weighted imaging (DWI) were calculated.

Results

pdBSI was sensitive to asymmetry in the amplitude and frequency domain in a random white noise model and in a simulated sinusoidal model. Minimal Cronbach alpha for intra-recording, intra- and inter-rater reproducibility ranged between 0.95 and 0.99 for standard spectral parameters and between 0.96 and 0.99 for pdBSI. We found a significant difference in pdBSI between stroke patients and control or TIA (p = 0.0003). pdBSI correlated significantly with NIH stroke scale at admission and DWI volume across different levels of stroke probability (Spearman’s ρ = 0.64–0.70 and 0.79–0.84, respectively, p < 0.00001 for both).

Conclusions

pdBSI displays high multilevel reproducibility and reliably discriminates between stroke and TIA patients or control subjects, and correlates significantly with clinical and radiological status.

Significance

Based on this methodological analysis, reliable EEG parameters can be evaluated in a general stroke population for clinically relevant state and outcome measures.

Introduction

The progression from ischemia to infarction is a dynamic, rapidly evolving process with irreversible changes occurring within a few minutes to a few hours. EEG may reflect changes in cerebral blood flow and metabolism within seconds as these are directly reflected in the neuronal rhythms. Although the spatial resolution of the EEG is low compared to structural imaging modalities, the high temporal resolution of the EEG may permit a rapid, inexpensive and sensitive evaluation of instantaneous brain functioning (Niedermeyer, 1993, Jordan, 2004). Moreover, quantitative EEG from a standard number of electrodes could assist in outcome prediction (Finnigan et al., 2007, Cuspineda et al., 2007, de Vos et al., 2008). Cuspineda et al. (2007) found absolute power of alpha and theta band for short-term outcome and absolute power of delta band for long-term outcome to be highly reliable in 28 patients with subacute ischemic stroke. Delta/alpha power ratio and relative alpha power were significantly correlated with 30-day NIHSS score in 13 patients with subacute ischemic stroke (Finnigan et al., 2007). Poststroke EEG delta activity was shown to be significantly reduced after thrombolysis with consequent reperfusion of cerebral tissue prior to any significant improvement in clinical symptoms (Finnigan et al., 2006). Moreover, using sLORETA (Pascual-Marqui et al., 2002), sources of pre-thrombolysis delta activity were shown to be co-localized with ischemic brain regions, particularly those which were shown to be reperfused after thrombolysis as indicated by perfusion weighted MR imaging (Finnigan et al., 2006). de Vos et al. (2008) demonstrated that the change in EEG brain symmetry as quantified with the revised Brain Symmetry Index during intravenous thrombolysis correlated significantly with the change in NIHSS score.

Clinical sensitivity and specificity of quantitative EEG (qEEG) are related to the stability and reliability of qEEG upon repeat testing (Thatcher, 2006). qEEG is reported to be highly reliable and reproducible in healthy controls and in young patients with psychiatric disorders (Hughes and John, 1999, Lund et al., 1995, Hamilton-Bruce et al., 1991, Salinsky et al., 1991, Pollock et al., 1991). However, reproducibility measures for qEEG in patients with ischemic cerebrovascular conditions have not been reported so far. A basic issue that needs to be addressed is the reproducibility of visual artifact rejection on the raw EEG selected for quantitative analysis.

Furthermore, persons labeled as normal, healthy controls do not necessarily exhibit EEG signals containing normative data 3 (Guggenheim and Karbowski, 1979, Logar et al., 1993).

This raises the question which EEG segment is representative of the underlying condition for which correlative EEG measures are determined. The aim of this study was to examine intra-record, intra-rater and inter-rater reproducibility and clinical relevance of EEG power and asymmetry in patients with ischemic cerebrovascular disease – i.e. TIA or stroke – during a single recording in routine clinical setting. We included a control group consisting of age-matched subjects who were free of clinically overt central neurologic dysfunction.

Section snippets

Study population

The study is part of the Middelheim’s Interdisciplinary Stroke Study (MISS), which is a project on the clinical, biochemical, neuroimaging, neuropsychological and electrophysiological evaluation of patients with ischemic stroke or transient ischemic attack (TIA) at ZNA Middelheim hospital, Antwerp. EEG was recorded in 41 patients. Ten patients, aged 55 years or more, with subjective memory complaints without evidence of cognitive decline on formal neuropsychological evaluation, normal brain MRI

Results

Fig. 1 illustrates the sensitivity of pdBSI based on the ratio of spectral power density of homologous channel pairs as a function of the amplitude ratio in a typical range of interest of 2.

As the left/right – amplitude ratio increases, pdBSI increases reflecting its sensitivity to lateralized asymmetry in the amplitude domain.

Fig. 2 illustrates the sensitivity of pdBSI as a function of varying frequency at one channel compared to its contralateral homologous channel in a typical range of

Discussion

Recent reports indicate a promising diagnostic and/or predictive value of qEEG parameters in acute ischemic stroke (Finnigan et al., 2004, Finnigan et al., 2007, van Putten and Tavy, 2004, Burghaus et al., 2007, Cuspineda et al., 2007, de Vos et al., 2008). Sensitivity and specificity of qEEG parameters are related to the reproducibility of qEEG upon repeat testing (Thatcher, 2006). Visual reading of the raw EEG by a trained electroencephalographer is considered a crucial and indispensable

Conclusions

In addition to the previously described BSI (van Putten and Tavy, 2004) and rsBSI (van Putten, 2007) which measure global hemispheric asymmetry, we now propose the pdBSI, which measures asymmetry between homologous channels. As we have shown, pdBSI allows a reliable analysis of brain symmetry changes in acute ischemic stroke after visual artifact rejection.

Based on this exploratory methodological analysis, reliable EEG parameters with discriminatory features, obtained in a naturalistic setting,

Conflict of interest

None.

Acknowledgements

We thank the anonymous reviewers for their valuable comments.

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