Longitudinal quantitative electroencephalographic study in mono-hemispheric stroke patients

Abstract

The identification of individual factors modulating clinical recovery after a stroke is fundamental to personalize the therapeutic intervention to enhance the final clinical outcome. In this framework, electrophysiological factors are promising since are more directly related to neuroplasticity, which supports recovery in stroke patients, than neurovascular factors. In this retrospective observational study, we investigated brain neuronal activity assessed via spectral features and Higuchi's fractal dimension (HFD) of electroencephalographic signals in acute phase (2-10 days from symptom onset, T0) and sub-acute phase (2.5 months, T1) in 24 patients affected by unilateral middle cerebral artery stroke. Longitudinal assessment of the clinical deficits was performed using the National Institutes of Health Stroke Scale (NIHSS), together with the effective recovery calculated as the ratio between difference of NIHSS at T0 and T1 over the NIHSS value at T0. We observed that delta and alpha band electroencephalographic signal power changed between the two phases in both the hemispheres ipsilateral (ILH) and contralateral (CHL) to the lesion. Moreover, at T0, bilateral higher delta band power correlated with worse clinical conditions (Spearman's r_s = 0.460, P = 0.027 for ILH and r_s = 0.508, P = 0.013 for CLH), whereas at T1 this occurred only for delta power in ILH (r_s = 0.411, P = 0.046) and not for CHL. Inter-hemispheric difference (ILH vs. CLH) of alpha power in patients was lower at T0 than at T1 (P = 0.020). HFD at T0 was lower than at T1 (P = 0.005), and at both phases, ILH HFD was lower than CLH HFD (P = 0.020). These data suggest that inter-hemispheric low band asymmetry and fractal dimension changes from the acute to the sub-acute phase are sensitive to neuroplasticity processes which subtend clinical recovery. The study protocol was approved by the Bioethical Committee of Ospedale San Giovanni Calibita Fatebenefretelli (No. 40/2011) on July 14, 2011.

Keywords: EEG; delta band; fractal dimension; inter-hemispheric asymmetries; mono-hemispheric stroke; plasticity.

Figure 1

Study flow chart. NIHSS: National Institutes of Health Stroke Scale; EEG: electroencephalogram; MRI: magnetic resonance imaging.

Figure 2

Electroencephalographic montage and power spectrum densities Up: Electrode spatial positioning of the international 10–20 system used in this study. Electrodes covering the middle cerebral artery vascular territory used for the analysis are evidenced (in red for the left, in blue for the right hemisphere). Bottom: Examples of power spectrum densities in both hemispheres of one patient (female, 86 years old, lesion with cortical involvement in the left temporal area), in both acute (T0) and sub-acute phase (T1), and a healthy control (male, 73 years old).

Figure 3

Electroencephalographic delta band power. (A) Mean (standard error) of band power values in delta band for ILH and CLH in patients in the acute and sub-acute phases. Reference values of controls are also shown. Stars indicate a significant difference in patients with respect to the corresponding value in the control group, as indicated by unpaired t-test (*P < 0.05). Horizontal bars indicate significant difference between ILH and CLH values. (B) Scatterplot of the delta band power in ILH and CLH over NIHSS scores at both acute (T0) and sub-acute phase (T1). Regression lines are displayed. (C) Left: Mean (standard error) of band power values in delta band for ILH and CLH in patients in the acute and sub-acute phases, split in two groups on the basis of the lesion site: lesion with cortical involvement, subcortical lesion. Right: Mean (standard error) of inter-hemispheric asymmetries of delta activity at both phases in both groups of patients. Stars indicate a significant difference in patients with respect to the corresponding value in the control group (*P < 0.05), as assessed by Mann-Whitney U test (Bonferroni corrected). (D) Box-plot (median, 95% confidence interval) of CLH delta power in patients at both phases (T0 and T1), stratified in accordance to effective recovery (< 75% and > 75%) and lesion site (cortical involvement, subcortical lesion). ILH: Ipsilesional hemisphere; CLH: contralesional hemisphere; NIHSS: National Institutes of Health Stroke Scale.

Figure 4

Electroencephalographic alpha band power. (A) Mean (standard error) of band power values in alpha band for ILH and CLH in patients at both acute and sub-acute phases. Reference values of controls are also shown. (B) Mean (standard error) of inter-hemispheric asymmetries of alpha activity at both phases in both groups of patients. Star indicates significant difference between acute (T0) and sub-acute phase (T1) values, as assessed by two-tailed paired samples t-test (*P < 0.05). ILH: Ipsilesional hemisphere; CLH: contralesional hemisphere.

Figure 5

Electroencephalographic fractal dimension (A) Topographies of mean values of fractal dimension in patients at T0 (acute phase, left) and T1 (sub-acute phase, center) and in healthy age-matched controls (right). Black dots indicate the position of electroencephalographic electrodes in the montage. (B) Left: mean (standard error) of global fractal dimension (average over all sensors) in patients at T0 and T1 and in healthy controls. Right: mean (standard error) of Higuchi’s fractal dimension (HFD) values in ILH and CLH of patients at both T0 and T1. Stars indicate a significant difference between groups, as assessed by two-tailed paired samples t-test (*P < 0.05). (C) In the sub-acute phase, mean and standard deviation of global fractal dimension in patients with ER lower than 75% (left) and patients with ER higher than 75%. Stars indicate a significative difference with respect to values in healthy controls. ILH: Ipsilesional hemisphere; CLH: contralesional hemisphere; ER: effective recovery [(NIHSS at T0 – NIHSS at T1)/NIHSS at T0 × 100%].