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2009 40: 168Clin EEG NeurosciL.C. Fonseca, G.M.A.S. Tedrus, G.H. Letro and A.S. Bossoni

Dementia, Mild Cognitive Impairment and Quantitative EEG in Patients with Parkinson's Disease  

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CLINICAL EEG and NEUROSCIENCE 02009 VOL. 40 NO 3

Dementia, Mild Cognitive Impairment and Quantitative EEG in Patients With Parkinson's Disease

L.C. Fonseca, G.M.A.S. Tedrus, G.H. Letro and A.S. Bossoni

Key Words

Dementia Electroencephalography Mild Cognitive Impairment Parkinson's Disease

ABSTRACT The objective of this study was to evaluate relationships between

quantitative EEG (qEEG) changes and cognitive disturbance (mild cognitive impairment or dementia) and the motor disturbance stage in Parkinson's disease (PD).

Thirty-two PD patients (age=67.2*10.0) and 26 normal subjects (age=68.4?4.7) were assessed using a neurological evaluation, modified Hoehn and Yahr (HY) scale for PD, a Portuguese version of the CERAD neuropsychological battery (consortium to establish a registry for Alzheimer's disease) incorporating the Mini-mental Status Examination, Clinical Dementia Rating and an EEG analysis of absolute and relative band amplitude at rest. Four groups were compared: three with PD (7 patients with dementia, 10 with mild cognitive impairment and 15 with no cognitive disturbances) and the control group.

The qEEG showed no significant differences between the control group and PD patients without cognitive disturbance. Abnormalities on the qEEG were essentially associated with the occurrence of mild cognitive impairment or dementia in patients with PD. There was an increase in the absolute and relative posterior theta amplitude in the groups with mild cognitive impairment or dementia and of the posterior absolute and relative delta amplitude in the group with dementia

This study suggested qEEG as a possible physiological tool in the assessment of cognitive aspects in PD. INTRODUCTION

Parkinson's disease (PD) was initially characterized as a movement disorder, although in recent decades frequent cognitive impairments have been reported in PD patients.' The electroencephalogram (EEG) could contribute to an understanding of the physiopathological mechanisms of cognitive impairment in PD.2-7 Initial evaluations in patients with PD using the EEG showed a slowing of the basal rhythm in the posterior regions, associated with an increase in diffuse theta activity, or even slow, intermittent focal waves.89 An increase in slow activities was also reported using the quantitative EEG (qEEG).46 lo

These alterations in the EEG and qEEG only occurred in PD patients with associated den~entia.~

Recently, alterations in the relative powers on the qEEG were observed in PD patients, not only associated with dementia but also with the presence of mild cognitive impairment.' Analyses, such as those of the absolute and relative powers by qEEG have been shown to be useful in showing differences between various cognitive groups4.' 11.12 and can provide predictive models for cognitive impairment.l3

The objective of the present study was to consider the differences in qEEG between different cognitive states of PD, as compared to a healthy control group, using an analysis of the absolute and relative amplitudes. MATERIALS AND METHODS

Thirty-two patients (16 male) selected from the neurological outpatients department of the Celso Pierro Hospital (PUC-Campinas), with an average age of 67.2 (? 10.0) years, and a diagnosis of PD according to the criteria of Calne et aI.,l4 were included in this study. Information on the clinical data was obtained from the medical file of the patients and from their relatives. All the patients included in the study used dopamine and were evaluated in the on phase. Patients using anti-psychotic or benzodiazepine medication were not included. A control group (CG) contained 26 individuals with no history of cognitive impairment or neuropsychiatric disability, and with similar ages and educational levels to those in the PD groups

The following procedures were used: a neurological examination, CERAD neuropsychological battery (Consortium lo Establish a Registry forAlzheirners Disease), Clinical Dementia Rating - CDR, the Hoehn and Yahr scale and the qEEG. CERAD is composed of the Mini- mental Status Examination (MMSE), semantic verbal fluency, modified Boston naming, word list memory, constructional praxis, word recall, word recognition, and the praxis 1eca11.l~ Its applicability to the Brazilian population has been verified.I6 Motor disability was graded by the modified Hoehn and Yahr staging scale."

The EEG was recorded with a resolution of 12 bits, 0.5 and 35 Hz filters and 200 samples per second, using the Braintech 3.0 equipment (EMSA Equipamentos Medicos). Impedance was maintained below 10 K . The electrodes were placed according to the International 10-20 System, with the use of an additional two electrodes placed 1 cm below (left side) and above (right side) the external angle of the eyelid, with the objective of evaluating eye movements. The inter-connected ear lobe electrodes served as the reference. The data were recorded during approximately 12 minutes, alternating resting periods with the eyes closed with awake periods when the eyes were open, each period lasting 2 minutes.

Eighteen to 26 epochs were selected for the qEEG while awake and resting (eyes closed), each lasting 2.56s. Epochs with more than 100 pV on the electro-oculogram were excluded from the means. After applying the Fast Fourier Transform, the absolute and relative

From the School of Medicine, Pontificia Universidade Catolica de Campinas (PUC-

Presented at the 13th European Congress of Clinical Neurophysiology, 2008, Istanbul Address requests for reprints to Dr Lineu C. Fonseca. Rua Sebastitio de Souza 205. CJ.

Email: lineu fonseca@uol com.br Received. December 5. 2008; accepted: April 6, 2009

Campinas), Campinas. SP, Brazil.

122, CEP 13 013.173, Campinas. S ~ O Paulo, Brazil.

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CLINICAL EEG and NEUROSCIENCE 02009 VOL 40 NO 3

Table 1 Clinical features of the control group and of the subgroups with Parkinson's Disease, subdivided according to cognitive aspects

CG P D-N LCOg PD-MCI PD-Dem Degrees of freedom F-value ANOVA p Subjects 26 15 10 7 Age (yr) 68.3 (4.72) 63.5 (9.58) 70.3 70.6 (9.1) Between groups 3 2.184 0.101 Education (yr) 6.1 (4.9) 5.9 (5.4) 2.3 (1.6) 1.7 (1.7) Within groups 54 3.146 0.032'

Mini-mental Status Z score -0.103 (2.04) 0.208 (1.18) -0.577 (1.53) -3.008 (1.37) 6.405 0.001' Duration of PD (yr) - -6.8 (3.93) 6.0 (2.36) 8.7 (8.6) Between groups 2 0.409 0.537

1.87 (0.72) 2.0 (0.58) 2.57 (0.45) Within groups 29 1.979 0.062 Hoehn and Yahr scale -

*ANOVA, p<0.05

Total 57

Total 31

amplitudes of 17 electrodes were studied (Fp2, Fp l and Oz were not included) in the following frequency bands: delta (0.8 to 3.9 Hz), theta (4.29 to 7.8 Hz), alpha 1 (8.2 to 9.8 Hz), alpha 2 (10.1 to 12.5 Hz) and beta (12.8 to 19.9 Hz). To obtain the normal distribution, the values for absolute amplitude were substituted by their logarithms, and the relative amplitude values transformed by Logit.'*

The absolute and relative amplitudes were analyzed for the various bands at all the individual electrode positions. The averages were also calculated for the regional position sets, that is "frontotemporal" for F8, F7, F4, F3, Fz, C4, C3, Cz, T4 and T3, and "posterioi' for P4, P3, Pz, T6, T5, 0 2 and 01. A global value, derived from all evaluated 17 electrodes, was also studied. Data analysis

The patients with PD were divided into 3 subgroups according to their performance in the cognitive evaluation.

1 - PD with normal cognition (PD-NLCog) - without evident cognitive deficits.

2 - PD with mild cognitive impairment (PD-MCI) -corresponding to cognitive complaints from the patients or their families; the reporting of a relative decline in cognitive functioning during the past year by a patient or informant; cognitive disorders as evidenced by a clinical evaluation; absence of major repercussions on daily life; and absence of dementia.13

3 - PD with dementia (PD-Dem) - dementia according to the criteria of (DSMIV)20 starting at least 1 year after installation of Parkinson's Disease, and without the characteristics of dementia with Lewy bodies.

The Statistical Packages for Social Sciences (SPSS 10.0.1) statistical program was used and the level of significance considered was p<0.05. Group differences (PD-Dem, PD-MCI, PD-NLCog and control group) were investigated with the one-way ANOVAfor the delta, theta, alpha and beta relative and absolute amplitude for the individual, regional and global electrode positions. When a significant result was observed in the one-way ANOVA, the significance of the intergroup differences was confirmed with the Tukey's post hoc test. Ethical aspects

The Ethics Commission for Research with Human Beings of PUC- Campinas approved the project, and subjects signed informed consent.

RESULTS Table 1 shows the distribution of the individuals in the study groups

and the control and also their clinical features. There was no statistical difference between the groups with respect to age, or between the subgroups with PD with respect to the duration of the disease or

grading on the Hoehn and Yahr scale, but a difference was shown in the MMSE between the PD-Dem and the other groups (ANOVA, Tukey HSD, p<0.05). Adifference was found between the groups with respect to scholastic level (ANOVA, p=0.032), but was not found to be significant between the pairs of groups in the Tukey HSD analysis.

With respect to medication, all the patients were taking levodopalbenserazida, 8 were taking pramipexol, 4 selegiline, 2 biperiden and 1 entacapone. There was no significant difference between the subgroups PD-Dem, PD-MCI, PD-NLCog with respect to the type and dose of antiparkinsonian drugs.

Complaints of "depression" were observed in 11 (34%) patients with PD. There was no relationship between these complaints and either the PD subgroups or variations on the qEEG. Comparison between the 3 subgroups with PD and the control group based upon the qEEG parameters

The absolute and relative amplitudes in the theta range increased from the control and PD-NLCog groups to the PDI-MCI and PD-Dem groups, for all the 17 electrode positions studied, with values of p<O.O1 (ANOVA). For the amplitudes in the delta range, the differences were significant in the same way except for positions F8 and F7 for absolute amplitude, and F8, F7, F4, F3, C3,Cz, T4 and T3 for relative amplitude (p<0.05). For the alpha and beta absolute amplitudes the differences between the groups were not significant.

Considering that the alterations on the qEEG for the PD groups extended to various electrodes, and that for the relative amplitudes of the delta and alpha bands, the frontotemporal electrode positions showed activities that were somewhat different statistically from those in the posterior positions, the means for the amplitudes in the two groups (frontotemporal and posterior) were calculated.

Table 2 shows the results for the analysis of variance between the PD subgroups and the control group with respect to the posterior and frontotemporal relative EEG amplitude and posterior absolute amplitude. It can be seen in Table 2 that the posterior absolute amplitude and the posterior and frontotemporal relative amplitude in the delta and theta ranges were progressively greater in the PD-MCI and PD-Dem groups, and that the reverse occurred with respect to the alpha and beta relative amplitude. With the exception of the frontotemporal delta and alpha relative amplitude, statistical significance was attained in these analyses (ANOVA, p<0.05).

In the post-hoc pairwise multiple comparisons, applied after the variance analysis (Table 3), there was a difference in the posterior relative amplitude between the control group and the PD-Dem group for all the frequency ranges, while in the comparison between the control group and PD-MCI, differences were only found in the theta

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CLINICAL EEG and NEUROSCIENCE 02009 VOL. 40 NO. 3

Table 2 Means (SD) for the posterior and frontotemporal relative amplitudes and posterior absolute amplitude

for the 3 subgroups with Parkinson's Disease and the control group. Results for the ANOVA between the groups EEG amplitude CG PD-NLCOg PD-MCI PD-Dem F Anova p

Posterior relative Delta 0.139 (0.052) 0.167 (0.073) 0.156 (0.036) 0.270 (0.136) 6.435 0.001* Theta 0.206 (0.144) 0.221 (0.088) 0.370 (0.181) 0.395 (0.034) 6.559 0.001' Alpha 0.330 (0.133) 0.310 (0.116) 0.252 (0.143) 0.154 (0.091) 3.981 0.012'

relative Theta 0.198 (0,090) 0.202 (0.791) 0.331 (0.149) 0.339 (0.097) 7.143 0.000"

Posterior absolute Delta 57.46 (18.48) 65.91 (33.17) 63.7 (17.20) 119.1 (54.62) 8.662 0.000*'

Beta 0.162 (0.076) 0.130 (0.053) 0.094 (0.054) 0.061 (0.056) 4.343 0.008* Frontotemporal Delta 0.182 (0.055) 0.182 (0.077) 0.177 (0.048) 0.256 (0.128) 2.235 0.095

Alpha 0.272 (0.107) 0.254 (0.126) 0.209 (0.107) 0.142 (0.069) 2.977 0.050 Beta 0.147 (0.653) 0.126 (0.052) 0.093 (0.050) 0.082 (0.051) 3.577 0.039'

Theta 76.13 (50.31) 80.07 (11.29) 97.30 (33.42) 156.21 (68.87) 5.277 0.003* Anova: distribution F - 3.54 (degrees of freedom; 3 and 54); 'p<0.05; "p<O.OOI

Table 3 Post hoc pairwise multiple comparisons (Tukey method): values for p in the comparison between posterior and global

relative amplitude and posterior absolute amplitude in the various frequency bands, between the 3 groups with PD and the control group CG CG CG PD-NLCog PD-NLCog PD-MCI

EEG amplitude X X X X X X

PD-NLCOg PD-MCI PD-Dem PD-MCI PD-Dem PD-Dem Posterior relative Delta 0.618 0.917 0.000" 0.981 0.012* 0.009"

Theta 0.995 0.009*' 0.009" 0.033* 0.026' 0.983 Alpha 0.959 0.358 0.010* 0.683 0.046' 0.402 Beta 0.458 0.035' 0.027' 0.521 0.980 0.980

Theta 0.995 0.651 0.002" 0.823 0.080 0.080 Posterior absolute Delta 0.801 0.936 0.000" 0.998 0.001" 0.001**

'p<0.05; **p<O.Ol

and beta ranges and between PD-NLCog and PD-Dem in the theta and alpha ranges. Differences were only noted between PD-MCI and PD-Dem for the delta and theta posterior absolute amplitudes. No significant differences were found on the qEEG between the control group and PD-NLCog. Relationship between qEEG and the Hoehn and Yahr staging score

In the evaluation of the correlation between the qEEG results and the Hoehn and Yahr staging score," significant correlations were only found for the posterior, frontotemporal and global alpha 2 relative amplitude (Spearman's correlation coefficient, p<0.05).

DISCUSSION In the present PD study, the finding of cognitive changes in 53% of

the cases, of which 22% of the individuals had dementia and 31% mild cognitive impairment, was within the ranges of prevalence found in the literature.221 The PD patients showed greater slowing down on the qEEG as compared to healthy individuals in a way similar to other

and an association was shown between this increase in amplitudes in the slow ranges and the occurrence of d e r n e ~ ~ t i a . ~ ~ ~ . ~ ~

Caviness et al.' in their study with PD patients made the first report using qEEG for individuals with mild cognitive impairment, and on comparing these results with those of patients with normal cognition or dementia. Those authors found significant differences that placed these patients in an intermediate position between the other 2 subgroups with respect to the qEEG. The occurrence of impaired cognition and its effect on the qEEG of the 3 PD subgroups was similar in this study.

In an original approach, the present study included a comparison of the 3 PD subgroups with a healthy group, and no differences were found between the control group and the PD-NLCog group. There was, therefore, a dissociation between motor alterations in PD and cognitive alterations and the corresponding qEEG data.

On the other hand, the comparison of the control group with the PD-MCI and PD-Dem groups, showed differences in the qEEG findings. An analysis of the differences between the groups showed an increase in the absolute amplitude in the delta and theta ranges causing increases in the respective relative amplitudes, without the occurrence of modifications in the absolute beta and alpha ranges.

With respect to the positions of the electrodes involved, ANOVA showed significant differences between the study groups in all the ranges for the "posterior" set of electrodes, which did not occur to a significant degree for the delta and alpha bands in the "frontotemporal" electrode set, thus suggesting a regional difference in the EEG.

For the PD-MCI group, the posterior relative theta activity was greater than for the control group or the PD-NLCog group. Since there was no increase in the absolute beta amplitude, the increase in the relative beta amplitude of this group must be secondary to the increase in theta.

In the PD-Dem group there was an increase in the relative delta and theta amplitudes and a decrease in the relative alpha and beta ranges when compared to the control group, and in theta and alpha when compared with the PD-NLCog group. In other words, the difference compared with PD-MCI was the increase in the absolute

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CLINICAL EEG and NEUROSCIENCE 02009 VOL. 40 NO. 3

theta and delta amplitudes, which did not express themselves by differences in the relative amplitudes.

It is evident from these results that a study of both the absolute and relative amplitudes allows for a more complete assessment of the qEEG data in patients with PD. Other studies reported in the literature did not reveal mild cognitive impairment and were carried out with limited quantitative analyses regarding the positions of the electrode^.^'^

The association of posterior slowing with cognitive decline was indicated by Neufeld et aL3 from a visual analysis of the EEG. Soikkeli et aL4 carried out a quantitative analysis of a derivation (T6-02) and observed that patients with dementia presented greater delta and theta amplitude, and that the PD group without dementia presented greater theta amplitude than the control group. Sinanovic et aL6 found focal or diffuse alterations associated with dementia. Caviness et al.' evaluated the dominant posterior background rhythm frequency and relative global measurements including all the electrodes, and concluded that these variables were more important qEEG data for cognitive aspects of PD. In this study, both the relative and absolute amplitudes, focal, regional or global, were evaluated, and it was shown that although the alterations found were global, they were accentuated in the posterior regions, and more related to cognitive impairment in PD.

A relationship between motor deterioration and worsening cognition was noted in the analysis of the relationship between the various cognitive subgroups in PD, but it was not statistically significant. The relationship between the motor and cognitive aspects has been pointed out by various author^.^' The cognitive deficit in PD patients may depend on multiple pathological changes due to relatively restricted involvement of the subcorticalcortical projections along with associated subcortical and cortical lesions (comparable with Alzheimer's disease and Lewy

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DISCLOSURE AND CONFLICT OF INTEREST

no conflicts of interest in relation to this article. L.C. Fonseca, G.M.A.S. Tedrus, G.H. Letro and A.S. Bossoni have

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