Seizure: European Journal of Epilepsy
Volume 19, Issue 5 , Pages 269-273, June 2010

Autonomic nervous system functions in interictal and postictal periods of nonepileptic psychogenic seizures and its comparison with epileptic seizures

Fırat (Euphrates) University, Faculty of Medicine, Department of Neurology, 23119 Elazig, Turkey

Received 23 November 2009; received in revised form 6 March 2010; accepted 1 April 2010. published online 10 May 2010.

Article Outline

Abstract 

Purpose

(1) To evaluate autonomic nervous system (ANS) functions during both interictal and postictal periods in a group of cases with nonepileptic psychogenic seizures (NEPS) and a group of epileptic patients to determine whether they have autonomic dysfunction. (2) If a significant difference can be established between epileptic and NEPS groups, to determine whether ANS tests can be used as a clinical helper in the differentiation between epileptic seizures (ES) and NEPS.

Methods

ANS functions (sympathetic skin response and R–R interval variation) were measured during both interictal and postictal periods in 25 patients who had NEPS and 30 patients who had primary generalized tonic–clonic seizures (GTCS) and partial seizures with secondary GTCS, as well as once in the healthy control group.

Results

When the patient group with NEPS both in the interictal and postictal period was compared with the control group, functions of both sympathetic and parasympathetic systems were found normal. This finding implies that patients with NEPS have normal ANS functions. A comparison of the epileptic patient group in the interictal and postictal periods with the control group revealed that the former had dysfunctions in both the sympathetic and parasympathetic systems. When patients with NEPS were compared with the ES, the measurements in sympathetic and parasympathetic nervous system functions during the interictal and postictal periods in the ES group were significantly different than those of the NEPS group.

Conclusion

This finding indicates that measurements of ANS functions may be helpful in differentiating between ES and NEPS.

Keywords: Autonomic nervous system, Epileptic seizures, Nonepileptic psychogenic seizures

 

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1. Introduction 

Nonepileptic seizures which result from emotional or psychological disorders and resemble epileptic seizures (ES) due to their abnormal motor, sensory, autonomic and behavioral properties, but are not accompanied by abnormal electrical discharges in the brain and electroencephalography (EEG) disturbances are called nonepileptic psychogenic seizures (NEPS).1, 2, 3, 4 The incidence of NEPS has been reported as 1.4 per 100,000,5 or 3 per 100,000 per year.6 NEPS may be identified more commonly in specialized clinical settings. For instance, 24% of patients with refractory seizures referred to a typical U.S. epilepsy center for video/EEG monitoring7 and up to 50% of patients with refractory “status” have been diagnosed with NEPS rather than epilepsy.8 The clinical features of NEPS can vary among different patients. Some studies have identified three principal symptom clusters. Cluster 1 patients have unresponsiveness associated with major motor symptoms, such as violent, diffuse, and highly disorganized activity. Cluster 2 patients have unresponsiveness accompanied by minor motor or trembling-like activity. Cluster 3 patients manifest with paroxysms of purely sensory or experiential/subjective symptoms during which full consciousness is preserved.4 NEPS are associated with high levels of psychiatric co morbidity. Patients most commonly fulfill the diagnostic criteria for other somatoform (22–84%), other dissociative (22–91%), posttraumatic stress (35–49%), depressive (57–85%), or anxiety disorders (11–50%). The degree of psychopathology correlates positively with the severity of the NEPS disorder.4 In the daily clinical practice, there may sometimes be problems in differentiating between ES and NEPS. Although clinical characteristics, video-EEG, imaging methods such as magnetic resonance imaging (MRI) and single photon emission computed tomography (SPECT), as well as quantification of serum levels of some hormones (like prolactin) are used in their differentiation. There have been some observations and data suggesting that dysfunction develops in the autonomic nervous system (ANS) in the course of some ES.9, 10, 11, 12, 13, 14, 15, 16, 17, 18 It has been recently established that ANS dysfunction may occur during the interictal period in epileptic patients.19, 20, 21, 22, 23, 24, 25 There are some studies demonstrating that there may be autonomic dysfunctions in some psychiatric disorders.26, 27, 28, 29, 30, 31, 32 The patients in the concerned studies do not have NEPS group. Only one recent study has reported an autonomic dysfunction in NEPS cases.33 However, ANS functions during the interictal and postictal periods of patients with NEPS have not been examined yet.

The objectives of the present study are

1.To evaluate ANS functions during both interictal and postictal periods in a group of cases with NEPS and to determine whether they have autonomic dysfunction.

2.To evaluate ANS functions separately during interictal and postictal periods in a group of epileptic patients and to determine whether they have autonomic dysfunction.

3.If a significant difference can be established between epileptic and NEPS groups, to determine whether ANS tests can be used as a clinical tool in the differentiation between ES and NEPS.

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2. Materials and methods 

This study registered 25 patients who did not have any organic disease or epileptic seizures (ES), but nonepileptic psychogenic seizures (NEPS), associated with pure conversion disorder or depressive disorder and 30 patients with primary generalized epilepsy or partial epilepsy (21 cases with primary generalized tonic–clonic seizures and 9 cases with partial seizures with secondary generalized tonic–clonic seizures), who presented at Neurology and Psychiatry Clinics of Fırat University Hospital for examination and treatment purposes from January 2007 to May 2008, as well as a control group consisting of 20 healthy volunteers, who were age- and sex-matched with patients diagnosed as epilepsy and NEPS. These patients were randomly selected from among the 112 patients who were clinically evaluated, treated and followed by Neurology Clinic Epilepsy Unit and Psychiatrics Clinic. 57 patients which have both epileptic seizures and nonepileptic psychogenic seizures were excluded from study. Written consents of all the cases in both the study and control groups were taken before the study.

Diagnostic stages for nonepileptic psychogenic seizures include the following:

(I)Clinical evaluation:


1.Medical history: Obtaining detailed information from the patient and/or relatives about the currently present seizures and other symptoms.

2.The background history: Investigating about the history of other physical symptoms or illnesses, operations and psychiatric treatments.

3.Exclusion of organic illnesses by systemic and neurological examination, routine blood analyses and cranial MRI.

4.Psychiatric evaluation (examination by a psychiatrist and perform of required tests).


(II)Evaluation of seizures:


1.Examination of home video or photo camera recordings, if there are any, of the patient's seizures.

2.Observation of the seizures by an expert neurologist.


(a)Observation of the seizures in the polyclinic for outpatients and in the service for inpatients.

(b)Observation of at least two or more seizures and recording of their characteristics.

(c)Gathering information from the patient's relatives about whether the observed seizures are similar to other habitual seizures.


(3)Recording of seizures by EEG:


(a)Routine EEG examination (including hyperventilation and photo stimulation).In case the patient does not have a seizure during recording,

(b)seizure induction by verbal suggestion during EEG recording.In case the patient does not have a seizure during the abovementioned procedure or if the clinical signs are doubtful,

(c)Performing a long-term video-EEG monitoring procedure.

Seven patients were referred to the video-EEG monitorization unit. Psychiatric diagnosis of the patients with NEPS was given by the psychiatry clinic of our hospital in accordance with the diagnosis of conversion disorder, with seizures and convulsions subtype, as stated in the DSM-IV.34 Cases included in the study in this group had not received any drug treatment for at least the last two weeks. Disease duration in the group ranged between 1 and 5 years, with a mean disease duration of 3.2 years.

2.1. Group of epilepsy 

Anamneses of all patients were taken, physical and neurological examinations were performed, necessary routine blood analyses were conducted, and EEG, cranial computed tomography (CCT) or cranial MRI examinations were carried out. The cases that have normal CCT or MRI were admitted to the study. The patients with mixed seizures that have both ES and NEPS did not admit to the study. Epilepsy diagnosis was given by the neurology clinic according to the Classification of the International League Against Epilepsy (1981).35 Six patients who have doubtful findings were referred to the video-EEG monitorization unit. Of the patients in the epileptic patient group, 22 were on monotherapy (valproate, phenytoin or carbamazepine) and 8 were on polytherapy (paired use of valproate, carbamazepine, lamotrigine or levetiracetam). Disease duration in the patients ranged between 1 and 10 years, with a mean disease duration of 5.4 years.

Exclusion criteria for both epilepsy and psychogenic nonepileptic seizure patients were smoking, use of alcohol, diabetes mellitus, other polyneuropathies, pulmonary diseases, and use of drugs could compromise ANS functions. ANS functions in ES and NEPS groups were measured in both interictal and postictal periods. The criterion for the interictal period was set as a lapse of at least one week or longer since the last seizure. Postictal period was accepted after 2h which was considered as the earliest time the patients could adjust to the tests after seizure. ANS functions in the healthy individuals forming the control group were measured once.

In order to evaluate ANS functions, sympathetic skin responses (SSR) and R–R interval variation (RRIV) were measured using Dantec Keypoint brand 4-channel EMG equipment in electromyography (EMG) laboratory of our clinic. The electrophysiological tests were performed in a semi-darkened silent room. The recordings were made in the afternoon, 3h after lunch with empty bladder and bowel. The subjects were asked to avoid activities that would affect blood pressure (like running, jumping, etc.) for 2h before the tests. The patients and controls were admitted 20min earlier in order to stabilize skin temperature at 25°C room temperature. When measuring SSR, Ag/AgCl disk electrodes and two-channel active electrodes were placed on the palm of the hands and sole of the feet, while reference electrodes were placed on the dorsum of the hands and feet, and the ground electrode on the wrist. A single supramaximal electrical stimulus was given to the median nerve opposite the recorded side. The band pass was 0.1–1000Hz, the sensitivity was 0.5–2mV/division and the sweep speed was 1–5s/division. The duration of the stimulus was between 0.1 and 0.2ms and the stimulus intensity ranged from 10 to 40mA. Five responses were recorded and the averages of the potentials were taken into consideration. To avoid any habituation effect, stimulation was made at randomized intervals with different intensities and the interval between two stimuli was kept longer than 20s. The latency was measured from the onset of the stimulus artifact to the first deflection of the potential from baseline. The amplitude was measured from peak to peak.36 When recording RRIV, active electrode was placed on the apex of the heart, reference electrode was placed on the clavicle, and the ground electrode on the wrist after a period of 30min supine rest and deep breathing (6breaths/min). Twenty recordings were done at rest and during deep breathing. The band pass was 20–100Hz, the sensitivity 384 and the sweep speed was 1.5mV/division and 2s/division, respectively. For RRIV calculation the formula of RRIV=a/b×100 was used. “a” was described as the difference between earliest and latest R waves and “b” was the mean of R–R intervals. RRIV recorded at rest was termed R% and the one recorded during hyperventilation was termed as DR%.36, 37

Independent sample test, paired sample test and ANOVAs tests were used in the comparisons between groups. All values obtained in the study are presented as mean±standard deviation.

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3. Results 

Age and sex distributions of ES and NEPS groups, as well as the control group, are presented in Table 1. In terms of gender between ES and NEPS groups, there is a statistically significant difference.

Table 1. Demographic characteristics of patient and control groups included in the study.
Male number (%)Female number (%)Age (year)
MinMaxMean±SD
ES group14 (%46.6)16 (%53.3)176231.6±12.1
NEPS group6 (%24)19 (%76)135030.2±10.1
Control group10 (%50)10 (%50)154431.1±8.8

ES: epileptic seizures. NEPS: nonepileptic psychogenic seizures.

When deep breath R–R interval variation (DB-RRIV) levels of epileptic seizures (ES) group in the interictal period (21.4±8.74) were compared with those of the control group (23.17±8.59), they were found significantly lower in the ES group in the interictal period (p<0.05).

A comparison of the DB-RRIV levels in ES group in the postictal period (18.49±7.12) and those of the control group (23.17±8.19) showed that the former was statistically significantly lower (p<0.05).

When the patient group with ES both in the interictal and postictal period DB-RRIV levels (respectively, 21.4±8.74, 18.49±7.12) was compared with NEPS (respectively, 25.04±8.02, 23.09±7.87) group, there were statistically significant differences between groups (p<0.05).

When the patient group with NEPS both in the interictal and postictal period DB-RRIV levels (respectively, 25.04±8.02, 23.09±7.87) was compared with control group (23.17±8.59), there was no statistically significant difference.

A comparison of the upper extremity latencies-sympathetic skin responses (UEL-SSR) levels of the ES group in the interictal period (1.11±0.22msn) and those of the control group (1.06±0.25msn) demonstrated that latency in the former was prolonged and was significant in statistical terms (p<0.05).

When UEL-SSR levels of the ES group in the postictal period (1.19±0.30msn) were compared with those of the control group (1.06±0.25msn), the former group was found to have prolonged latency, which was significant in statistical terms (p<0.05).

When the patient group with ES both in the interictal and postictal period UEL-SSR levels (respectively, 1.11±0.22msn, 1.19±0.30msn) was compared with NEPS group, there were differences between groups statistically significant (p<0.05).

Although there were differences between groups in terms of the other parameters measured, these were not statistically significant. The data related to the measurements in the patient and control groups were presented in Table 2.

Table 2. RRIV and SSR levels of all patient and control groups.
NB-RRIV (%)DB-RRIV (%)UEL-SSR (ms)LEL-SSR (ms)
ES group-interictal period17.84±6.3021.40±8.74*,†1.11±0.22*,†1.96±0.39
ES group-postictal period16.97±6.4018.49±7.12*,§1.19±0.30*,§2.03±047
NEPS group-interictal period18.33±8.4625.04±8.021.02±0.231.86±049
NEPS group-postictal period18.28±6.3823.09±7.871.03±0.171.89±0.35
Control18.07±6.7123.17±8.591.06±0.251.91±0.43

ES: epileptic seizures; NEPS: nonepileptic psychogenic seizures; NB-RRIV: normal breath R–R interval variation; DB-RRIV: deep breath R–R interval variation; UEL-SSR: upper extremity latencies-sympathetic skin responses; LEL-SSR: lower extremity latencies-sympathetic skin responses.

*p<0.05; when compared with control group.

†p<0.05; when compared with NEPS group in the interictal group.

§p<0.05; when compared with NEPS group in the postictal group.

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4. Discussion 

It was established in our study that patient group with nonepileptic psychogenic seizures (NEPS) had normal sympathetic and parasympathetic system functions during both the interictal and postictal period, in comparison to the control group. This finding suggests that patients with NEPS have normal autonomic nervous system (ANS) functions. A small part of NEPS patients may show signs of autonomic origin like urinary incontinence, fecal incontinence and sinus tachycardia in the ictal period.4 There are also some studies demonstrating that there may be autonomic dysfunctions in some psychiatric disorders.26, 27, 28, 29, 30, 31, 32 The patients in the concerned studies do not have NEPS. Only one recent study has reported an autonomic dysfunction in NEPS cases.33 Our patients, on the other hand, had normal ANS functions both in the interictal and postictal period. Our literature review did not produce any study evaluating the autonomic functions during both interictal and postictal periods in the same patient group. When we compared the epileptic patient group in the interictal period with the control group, we established dysfunctions in both the sympathetic and parasympathetic systems. Similarly, we found dysfunctions in the postictal period of this group as well. The dysfunctions in the sympathetic and parasympathetic systems of the epileptic patient group during the postictal period were more marked than those in the interictal period. There is a host of studies evaluating the functions of the ANS during the ictal or interictal periods in epileptic patients.9, 10, 11, 12, 13, 14, 15, 16, 17, 18, 20, 21, 22, 23, 24, 25 Although contradictory results have been obtained in these studies, most of them found ANS dysfunctions during either ictal or interictal periods. Likewise, in our one study, we evaluated functions of the ANS during the interictal period in epilepsy patients, and found sympathetic dysfunction in patients with partial epilepsy and parasympathetic dysfunction in patients with primary generalized seizures.19 An experimental study assessing autonomic functions during preictal and postictal periods established a slight, but significant impairment in autonomic functions during the postictal period, relative to the preictal period.38 However, in a clinical study no difference was found in autonomic functions before or after seizures in complex partial seizure patients, while a difference was found in generalized seizures.39 It was suggested that autonomic dysfunction established during both ictal or interictal periods in patients with epileptic seizures was associated with the effect of epileptic discharges on limbic structures, and amygdala and periamygdaloid piriform cortex in particular.10, 11, 40 It was accepted that each seizure caused a sudden and temporary impairment in the autonomic functions. Additionally, it was concluded that repetition of seizures led to long-term abnormalities in the autonomic systems.38 By the same token, that autonomic dysfunction becomes more marked during the postictal period suggests that repetition of seizures exacerbates the present autonomic dysfunction.38 Similarly, in this study we found the dysfunctions in the sympathetic and parasympathetic systems of epileptic patient group during the postictal period were more marked than those in the interictal period.

The effect of antiepileptic drugs on ANS is unclear. We previously investigated the pre- and post-treatment ANS functions in partial epileptic patients.19 We found pre-treatment sympathetic system dysfunction to improve after three months of antiepileptic treatment.19 This supports the beneficial effect of antiepileptic drugs on ANS dysfunction. However, the mechanism is still obscure.19 Therefore, we do not think that antiepileptic drugs might negatively affect the ANS functions of ES group in this study. When we compared the patient group with NEPS and the epileptic patient group, the measurements in sympathetic and parasympathetic nervous system functions during the interictal and postictal periods in the ES group were significantly different than those of the NEPS group. This finding indicates that measurements of ANS functions may be helpful in differentiating between ES and NEPS. For this purpose, however, it would be helpful to determine the cut-off ratios for DB-RRIV and SSR in the EMG laboratories in the great patient populations.

A limitation of the present study is the lack of ictal video-EEG recordings of all participating patients, making the diagnosis of NEPS maximally reliable. The diagnosis of NEPS is based on the combination of history, seizure observation, and ictal EEG recordings. Video-EEG monitoring is the gold standard for diagnosis of NEPS, and is indicated in all patients who continue to have frequent seizures despite medication.41 When undertaken as a brief outpatient test, video/EEG monitoring captures NEPS in about 50% of patients. The likelihood of a seizure rises to at least two-thirds if photo stimulation and hyperventilation are combined with verbal suggestion.4 Long-term video-EEG monitoring allows the diagnosis of NEPS to be made with near certainty.41 Long-term video-EEG monitoring is both a cumbersome and costly procedure. It is not necessary to apply this procedure to each and every patient in daily medical practice. Therefore, in the present study we used the protocol which we explained in the material and method part in detail.

Accurate differentiation between ES and NEPS is pivotal for correct diagnosis, and thus, for correct treatment. It is reported in the literature that patients with NEPS are followed with epilepsy diagnosis for an average period of 7.2 years42 and that three-quarters of them receive unnecessary treatment.43 Besides being exposed to the iatrogenic side effects of drugs during this period,44, 45, 46 patients with NEPS may be driven to suicide,47, 48 if the underlying psychiatric problem goes unnoticed. Therefore, correct differential diagnosis of ES and NEPS shall reduce morbidity and mortality. Although clinical characteristics, video-EEG, imaging methods such as MRI and SPECT, as well as quantification of serum levels of some hormones (like prolactin) are used in their differentiation, they may sometimes remain inadequate for distinction. Novel, easily usable and noninvasive methods are required to differentiate between ES and NEPS.

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Conflict of interest 

None.

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PII: S1059-1311(10)00073-7

doi:10.1016/j.seizure.2010.04.002

Seizure: European Journal of Epilepsy
Volume 19, Issue 5 , Pages 269-273, June 2010

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