Pre- and postictal, not ictal, heart rate distinguishes complex partial and psychogenic nonepileptic seizures

doi:10.1016/j.yebeh.2011.10.008

Epilepsy & Behavior

Volume 23, Issue 1, January 2012, Pages 68-70

https://doi.org/10.1016/j.yebeh.2011.10.008 Get rights and content

Abstract

Psychogenic nonepileptic seizures (PNES) remain poorly understood neurobiologically. Previously reported work suggests that adjunct ictal heart rates (HRs) may differentiate PNES from complex partial seizures (CPS). We retrospectively reviewed and compared preictal, ictal, and postictal HR differences in patients with PNES (n = 42) and CPS controls (n = 46) electively admitted for video/EEG monitoring to further characterize PNES autonomic patterns. Statistically significant preictal HR increases (P = 0.006) and postictal (P = 0.015) HR reductions normalized to baseline were identified in subjects with PNES compared with CPS controls. Ictal HRs were not found to differentiate between PNES and CPS events. This pattern of pre-event HR increases and postevent HR decreases in patients with PNES compared with those with CPS suggests frontolimbic neural circuit dysfunction and merits further exploration.

Introduction

Psychogenic nonepileptic seizures (PNES) are the most common differential diagnosis for patients referred to the epilepsy monitoring unit (EMU) [1]. Differences between PNES and epileptic seizures (ES) include semiological and autonomic features [2], [3]. In particular, ictal heart rate (HR) increases have been reported to differentiate ES from PNES [2]. Although a distributed network of cortical (i.e., cingulate gyrus, amygdala), diencephalic (hypothalamus), and brainstem structures have been implicated in peri-ictal ES-related autonomic changes [4], patients with PNES have exhibited abnormal hypothalamic–pituitary–adrenal (HPA) axis activation [5].

Neuropsychiatric comorbid conditions diagnosed in patients with PNES, such as posttraumatic stress disorder (PTSD), are associated with abnormal, increased HR and HPA axis changes in the setting of emotional stress [6]. Patients with PNES, particularly those with a prior trauma history, exhibit increased basal cortisol levels similar to patients with PTSD [5], [7]. In this study, peri-ictal and ictal HR changes in patients with CPS and those with PNES were examined to further characterize PNES-related autonomic features. Guided by our own observations of rapid HR during PNES, we hypothesized that ictal HR would be similar in patients with PNES and those with CPS.

Section snippets

Methods

Consecutive elective admissions to the EMU between January 2008 and January 2010 were retrospectively screened for definitive CPS or PNES. Patients with any history of cardiac arrhythmia were excluded from the study. For patients with multiple captured events, only the first event was analyzed. Events with documented alteration of consciousness or bilateral motor elements without epileptiform abnormalities on the EEG were diagnosed as PNES. Events with documented alteration in awareness and

Results

Eighty-eight patients were included: 46 with CPS had 44 preictal, 46 ictal, and 44 postictal HR measurements and 42 patients with PNES had 42 preictal, 42 postictal, and 40 postictal HR measurements analyzed (Table 1). Baseline HR values (means ± SD) were 75 ± 10.7 bpm in the CPS group and 77 ± 10.0 bpm in the PNES group (P = 0.46). Peri-ictal HR measurements for patients with CPS were 104 ± 20 bpm preictally, 159 ± 43 bpm ictally, and 129 ± 34 bpm postictally, and for patients with PNES, 116 ± 21 bpm preictally, 157

Discussion

This study compared peri-ictal HRs in patients with CPS and those with PNES obtained during elective inpatient video/EEG monitoring. Maximal ictal HR increased over baseline for both CPS and PNES events, without significant differences between groups. This is in contrast to a prior report showing that rapid ictal HR strongly favored the diagnosis of epileptic seizures and could therefore reliably distinguish ES from PNES [2]. Hypermotor phenomena during clinical events in PNES with resultant

References (11)

S.R. Benbadis et al.
An estimate of the prevalence of psychogenic non-epileptic seizures
Seizure
(2000)
M. Reuber et al.
Psychogenic nonepileptic seizures: review and update
Epilepsy Behav
(2003)
V.G. Carrion et al.
Diurnal salivary cortisol in pediatric posttraumatic stress disorder
Biol Psychiatry
(2002)
C. Opherk et al.
Ictal heart rate differentiates epileptic from non-epileptic seizures
Neurology
(2002)
C. Sevcencu et al.
Autonomic alterations and cardiac changes in epilepsy
Epilepsia
(2010)

There are more references available in the full text version of this article.

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Heart rate and autonomic biomarkers distinguish convulsive epileptic vs. functional or dissociative seizures
2023, Seizure
20–40% of individuals whose seizures are not controlled by anti-seizure medications exhibit manifestations comparable to epileptic seizures (ES), but there are no EEG correlates. These events are called functional or dissociative seizures (FDS). Due to limited access to EEG-monitoring and inconclusive results, we aimed to develop an alternative diagnostic tool that distinguishes ES vs. FDS. We evaluated the temporal evolution of ECG-based measures of autonomic function (heart rate variability, HRV) to determine whether they distinguish ES vs. FDS.
The prospective study includes patients admitted to the University of Rochester Epilepsy Monitoring Unit. Participants are 18–65 years old, without therapies or co-morbidities associated with altered autonomics. A habitual ES or FDS is recorded during admission. HRV analysis is performed to evaluate the temporal changes in autonomic function during the peri‑ictal period (150-minutes each pre-/post-ictal). We determined if autonomic measures distinguish ES vs. FDS.
The study includes 53 ES and 46 FDS. Temporal evolution of HR and autonomics significantly differ surrounding ES vs. FDS. The pre-to-post-ictal change (delta) in HR differs surrounding ES vs. FDS, stratified for convulsive and non-convulsive events. Post-ictal HR, total autonomic (SDNN & Total Power), vagal (RMSSD & HF), and baroreflex (LF) function differ for convulsive ES vs. convulsive FDS. HR distinguishes non-convulsive ES vs. non-convulsive FDS with ROC>0.7, sensitivity>70%, but specificity<50%. HR-delta and post-ictal HR, SDNN, RMSSD, LF, HF, and Total Power each distinguish convulsive ES vs. convulsive FDS (ROC, 0.83–0.98). Models with HR-delta and post-ictal HR provide the highest diagnostic accuracy for convulsive ES vs. convulsive FDS: 92% sensitivity, 94% specificity, ROC 0.99).
HR and HRV measures accurately distinguish convulsive, but not non-convulsive, events (ES vs. FDS). Results establish the framework for future studies to apply this diagnostic tool to more heterogeneous populations, and on out-of-hospital recordings, particularly for populations without access to epilepsy monitoring units.
Epilepsy & Behavior: At the forefront of functional (dissociative) seizures
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Psychogenic non-epileptic seizures in children – psychophysiology & dissociative characteristics
2020, Psychiatry Research
The purpose of this study was to determine psychophysiology and dissociative characteristics of psychogenic non-epileptic seizures (PNES) in a clinical pediatric setting. A retrospective chart review was conducted over a 5-year period that included children meeting criteria for probable, clinically established or documented PNES. Of these, 33 patients (81%) underwent psychophysiology assessment as part of standardized care and were selected for study inclusion. Ages ranged from 10 to 17 years inclusive (70% female). The majority of patients were found to have some form of autonomic decompensation at baseline (82%) and lack of autonomic recovery from a cognitive stressor (58%). Inhibition of electrodermal skin response to laboratory stressor was associated with significantly longer duration of PNES illness (t=2.65, p=.013), while elevated heart rate (above 90^th percentile) was associated with significantly higher frequency of PNES events in the month preceding diagnosis (t=3.1, p=.004). High levels of dissociation and hyperventilation symptoms were self-reported by adolescent patients (n=19) with a moderate degree of positive association (r=0.35, p=.038). The majority of patients (n= 25, 89%) were taught to correct respiratory CO₂ levels during a single biofeedback training session. Conclusions: Child PNES populations appear to be characterized by chronic autonomic hyperarousal reflecting severity of their symptoms, which can feasibly be targeted for behavioral treatment.
Can seizure-related heart rate differentiate epileptic from psychogenic nonepileptic seizures?
2020, Epilepsy and Behavior
Citation Excerpt :
This finding is supported by previous studies of smaller sample size comparing convulsive ES with convulsive PNES specifically [4,6,8] indicating that postictal HR normalizes quickly to baseline in PNES despite rigorous motor activity during the event, as opposed to convulsive ES. It has been postulated that there is a relative autonomic hypoactivity post-PNES event because of dysfunction of the hypothalamic–pituitary–adrenal axis in patients with PNES [7]. This provides an alternative explanation to the proposed mechanisms of sympathetic overdrive in ES secondary to epileptic disruption of central autonomic network or the increased plasma catecholamines after tonic–clonic ES [27,28] leading to higher HR after ES.
We aimed to (1) determine if seizure-related heart rate (HR) differentiates epileptic seizures (ES) from psychogenic nonepileptic seizures (PNES); (2) define the most useful point of the following HR measurements: preictal, ictal-onset, maximal-ictal, or postictal; and (3) delineate the optimal HR cutoff points (absolute HR and relative HR increase) to differentiate ES from PNES.
All video-electroencephalography (VEEG) recorded at an Australian tertiary hospital from May 2009 to November 2015 were retrospectively reviewed. Baseline (during rest and wakefulness), 1-min preictal, ictal-onset, maximal-ictal, and 1-min postictal HR were measured for each ES and PNES event. Events lasting < 10 s or with uninterpretable electrocardiogram (ECG) due to artifacts were excluded. Receiver operating characteristic curve analysis was performed to assess the diagnostic accuracy of HR reflected by the area under the curve (AUC).
Video-electroencephalography of 341 ES and 265 PNES from 130 patients were analyzed. The AUC for preictal, ictal-onset, maximal-ictal, and postictal HR were found to have poor differentiation between all types of ES and PNES. However, comparing bilateral tonic–clonic ES and PNES, AUC for absolute maximal-ictal HR was 0.84 (95% confidence interval [CI]: 0.73–0.95) and for absolute postictal HR was 0.90 (95% CI: 0.81–1.00) indicating good diagnostic discrimination. Using Youden's index to diagnose tonic–clonic ES, the optimal cutoff point for absolute maximal-ictal HR was 114 bpm (sensitivity: 84%, specificity: 82%) and for absolute postictal HR was 90 bpm (sensitivity: 91%, specificity: 82%).
These findings suggest that seizure-related HR is useful in differentiating bilateral tonic–clonic ES from PNES. Based on the AUC, the best diagnostic measurements are maximal-ictal and postictal HR.
Preictal autonomic dynamics in psychogenic nonepileptic seizures
2019, Epilepsy and Behavior
Citation Excerpt :
However, there was a significant difference, in the group with PNES, of HR from 1 min to event onset. Interestingly, our values of absolute mean HR measured around these two time points were similar to previous reports (Reinsberger – PNES: 89 ± 18 bpm; complex partial seizures (CPS): 78 ± 14 bpm at 30 s before seizure onset [10]; Opherk & Hirsch – PNES: 84 ± 14 bpm; ES: 71 ± 13 bpm during the first 10 s of the ictus [16]) and thus was not a novel finding. Two possible reasons for this rise in HR are there is an acute increase in panic or anxiety in patients with PNES right before event occurrence.
Psychogenic nonepileptic seizures (PNES) resemble seizures but are psychological in origin. The etiology of PNES remains poorly understood, yet several theories argue for the importance of autonomic dysregulation in its pathophysiology. We therefore conducted a retrospective study to investigate autonomic dynamics leading up to a seizure to inform their mechanistic relevance.
One hundred one patients with PNES and 45 patients with epileptic seizure (ES) were analyzed for preictal heart rate (HR) and respiratory rate (RR) at baseline and at minute intervals from 5 min to onset.
Patients with PNES showed rising HR (p < 0.001, repeated-measures analysis of variance (ANOVA)) and rising RR (p = 0.012, repeated-measures ANOVA) from baseline to the onset of their seizures. Patients with ES did not exhibit significant preictal HR or RR increase. Patients with PNES had nonsignificantly higher preictal HR and RR than patients with ES.
Patients with PNES exhibit increasing autonomic arousal prior to seizure events unlike patients with epilepsy. This may reflect increasing levels of preictal anxiety, and future studies could study patients' subjective experiences of the preictal period, and more definitive measures of ventilation to see if this supported a model of PNES as “panic without panic”.
The role of the anterior and midcingulate cortex in the neurobiology of functional neurologic disorder
2019, Handbook of Clinical Neurology
Functional neurologic disorder (FND)/conversion disorder is a prevalent and disabling condition at the intersection of neurology and psychiatry. Clinicians often report feeling ill-equipped treating patients with FND, perpetuated by a historically limited understanding of neurobiologic disease mechanisms. In this review, we summarize the neuroimaging literature across the spectrum of sensorimotor FND, including functional imaging studies during rest, sensorimotor performance, and emotional-processing tasks as well as structural magnetic resonance imaging findings. Particular attention is given to studies implicating the anterior and middle cingulate cortex and related salience network structures (insula, amygdala, and periaqueductal gray) in the neurobiology of FND. Neuroimaging studies identify cingulo-insular functional alterations during rest, motor performance, and emotion processing in FND populations. The literature also supports that patients with FND exhibit heightened amygdalar and periaqueductal gray reactivity to emotionally valenced stimuli, enhanced coupling between amygdalar and motor control areas, and increased amygdalar volumes. The structural neuroimaging literature also implicates cingulo-insular areas in the pathophysiology of FND, though these findings require replication and clarification. While more research is needed to fully elucidate the pathophysiology of FND, salience network alterations appear present in some FND populations and can be contextualized using biopsychosocial models for FND.

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Brief CommunicationPre- and postictal, not ictal, heart rate distinguishes complex partial and psychogenic nonepileptic seizures

Abstract

Introduction

Section snippets

Methods

Results

Discussion

Seizure

Epilepsy Behav

Biol Psychiatry

Ictal heart rate differentiates epileptic from non-epileptic seizures

Neurology

Autonomic alterations and cardiac changes in epilepsy

Epilepsia

Brief Communication
Pre- and postictal, not ictal, heart rate distinguishes complex partial and psychogenic nonepileptic seizures