Cardiovascular regulation in epilepsy with emphasis on the interictal state

Hanna Ansakorpi

Department of Neurology, University of Oulu
Department of Clinical Neurophysiology, University of Oulu

Abstract

Epilepsy is associated with changes in autonomic cardioregulatory function. Ictally, autonomic disturbances may be evident with significant changes in heart rate (HR), blood pressure (BP) and respiration. However, interictal dysfunction of autonomic cardiovascular system may be subtle and it may be recognized only by delicate tools designed for that purpose. The aim of this study was to evaluate the function of the cardiovascular autonomic regulatory system in patients with epilepsy.

Cardiovascular reflex tests were performed on patients with partial or idiopathic generalized epilepsies. Special attention was paid to temporal lobe epilepsy (TLE). An association of refractory and well controlled TLE and hippocampal sclerosis with altered cardioregulation was evaluated by using cardiovascular reflex tests and an analysis of spectral and non-linear analysis of heart rate variation (HRV).

Cardiovascular reflexes were altered both in patients with partial and idiopathic generalized epilepsies who had been treated for epilepsy with antiepileptic drugs (AEDs), whereas patients with newly, untreated epilepsy did not differ from the control subjects. Diminished cardiovascular reflexes also seemed to be associated with carbamazepine (CBZ) treatment. Various parameters of cardiovascular reflex tests and analysis of spectral and dynamic measures of HRV were diminished in patients with TLE compared to the control subejcts.

These results indicate that epilepsy, especially TLE, is associated with interictal changes of autonomic cardioregulation. Although these changes seem to be evident in patients with severe form of TLE, patients with well controlled TLE and patients without hippocampal sclerosis also have altered autonomic cardioregulatory function. These results suggest that dysfunction of the cardioregulatory system is rather associated with functional than structural changes of the inner temporal lobe in patients with TLE.

Dedication

Disce aliquid. Nam cum subito Fortuna recessit,

ars remanet vitamque hominis non deserit umquam.

Marcius Porcius Cato

To my teachers

Table of Contents

Acknowledgements

Abbreviations

List of original papers

1. Introduction

2. Review of the literature

2.1. General aspects of epilepsy

2.1.1. Definition
2.1.2. Epidemiology
2.1.3. Etiology
2.1.4. Classification
2.1.5. Diagnosis
2.1.6. Prognosis

2.2. Temporal lobe epilepsy

2.2.1. General aspects
2.2.2. Focal structural lesions in temporal lobe
2.2.3. MRI-findings in temporal lobe epilepsy

2.3. Treatment of epilepsy

2.3.1. General aspects
2.3.2. Antiepileptic medication
2.3.3. Surgery
2.3.4. Vagal nerve stimulator

2.4. Autonomic nervous system

2.4.1. General aspects
2.4.2. Central autonomic network
2.4.3. The physiology of cardiovascular regulation

2.5. Evaluation of autonomic nervous system function

2.5.1. General aspects
2.5.2. Cardiovascular autonomic reflexes
2.5.3. Ambulatory ECG and analysis of heart rate variability

2.6. Epilepsy and autonomic nervous system

2.6.1. General aspects
2.6.2. Ictal autonomic dysfunction
2.6.3. Long-term autonomic dysfunction
2.6.4. Sudden unexpected death in epilepsy (SUDEP)

3. Aims of the research

4. Subjects and methods

4.1. Subjects

4.2. Methods

4.2.1. Clinical evaluation
4.2.2. Cardiovascular autonomic reflex tests
4.2.3. Heart rate variability analysis
4.2.4. Magnetic resonance imaging
4.2.5. Statistical analysis

5.1. Clinical findings
5.2. Cardiovascular reflex tests (Studies I-II and IV)
5.3. Heart rate variability analysis (Studies III - IV)
5.4. Correlation of cardiovascular autonomic reflex tests and heart rate variability analysis (Study IV)
5.5. MRI findings (Study IV)

6. Discussion

6.1. General aspects

6.2. Clinical findings

6.3. Cardiovascular regulation

6.3.1. Untreated patients
6.3.2. Patients with idiopathic generalized epilepsies
6.3.3. Patients with partial epilepsies
6.3.4. The effects of different AEDs

6.4. Cardiovascular reflexes and heart rate variation

6.5. Hippocampal sclerosis and cardiovascular regulation

6.6. Magnetic resonance imaging

7. Conclusions

List of Tables
1. Distribution of seizure types in an epileptic population in Kuopio, Finland (Keränen et al. 1988).
2. Proportion of incidence cases of epilepsy by etiology, Rochester, Minnesota, 1935-1984 (Hauser 1997).
3. International classification of epilepsies and epileptic syndromes (Commission on Classification and Terminology (ILAE, 1989).
4. The recommendations of antiepileptic medications for various types of epilepsy in their alphabethical order in each epilepsy type (modified after Keränen et al 1997, Kälviäinen 2001, Leppik 2001).
5. The methods used to study autonomic failure (Bannister & Mathias 1999).
6. The demographics of the study patients and the control subjects.
7. The antiepileptic medication of the study patients
8. Number of patients epilepsy participating in various examinations in different substudies.
9. The heart rate and blood pressure responses in patients with partial and primary generalized epilepsy compared to the control subjects.
10. The heart rate and blood pressure responses in patients with untreated epilepsy and in epilepsy patients with carbamazepine medication compared to the control subjects.
11. The heart rate responses in patients with refractory and well controlled temporal lobe epilepsy and in temporal lobe epilepsy patients with CBZ medication compared to the control subjects.
12. The heart rate responses in temporal lobe epilepsy patients with and without hippocampal sclerosis and the control subjects.
13. Analysis of heart rate variation in patients with refractory and well controlled temporal lobe epilepsy and the control subjects.
14. Analysis of heart rate variation in temporal lobe epilepsy patients with and without hippocampal sclerosis and the control subjects.
15. The correlation of cardiovascular reflex tests and heart rate variability analysis in patients with temporal lobe epilepsy.
16. The mean (± SD) volumes of the hippocampus and amygdalas in TLE patients with and without hippocampal sclerosis.

List of Figures
1. The peripheral divisions of autonomic sympathetic and parasympathetic nervous systems.
2. Schematic diagram of the main neural components participating in the vagal control of the heart rate. The arrowheads indicate stimulation and the diamondheads inhibition of the cardiovagal motoneurons (Modified after Benarroch 1997c).
3. Schematic diagram of the sympathetic control of the heart rate.
4. Schematic diagram of the components regulating arterial blood pressure (Modified after Benarroch 1997e). AVP, natriuretic peptide; R-A-A, renin-angiotensin system.
5. Spectral analysis of HRV in a healthy subject (A) and in a TLE patient (B). The area from 0.005 to 0.04 Hz represents VLF power, the area from 0.04 to 0.15 Hz LF power, and the area from 0.15 to 0.4 Hz HF power (data from Study III).
6. Poincaré plot from a healthy subject (A) and a TLE patient (B). SD1 indicates SD of instantaneous RR interval variability measured from axis 1, and SD2 indicates SD of long-term continuous RR interval variability measured from axis 2 (data from Study III).
7. Slopes of power-law relation of a healthy subject (A) and a TLE patient (B) (data from Study III).

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