Peri-ictal Psychiatric Phenomena: Clinical Characteristics and Implications of Past and Future Psychiatric Disorders



Peri-ictal Psychiatric Phenomena: Clinical Characteristics and Implications of Past and Future Psychiatric Disorders


Andres M. Kanner



Introduction

Patients with epilepsy may experience psychiatric and cognitive symptoms preceding the seizure (preictal), following the seizure (postictal), independently of seizure occurrence (interictal), or as an expression of the seizure (ictal). The practicality of classifying psychiatric and cognitive symptomatology according to their temporal relation to seizure occurrence has been recognized since the times of Gowers (1) and Hughlings Jackson (2) in the nineteenth century and of Kraepelin (3) in the early twentieth century. Paradoxically, among all psychiatric phenomena, preictal, ictal, and postictal psychiatric symptoms (PPSs) are the least recognized by clinicians and the least investigated in systematic research studies. From a theoretical standpoint, such paucity of data is surprising given that ictal and peri-ictal psychiatric symptoms are the clinical expression of the close relationship between epilepsy and the major psychiatric disorders, such as mood and anxiety disorders, and psychotic and attention deficit disorders. The impact of postictal psychiatric symptomatology is illustrated by Fisher and Schachter’s writings: “Some of the disability deriving from epilepsy derives from the postictal state. The postictal state may be complicated by impaired cognition, headache, injuries, or secondary medical conditions. Postictal depression is common, postictal psychosis relatively rare, but both add to the morbidity of seizures” (4).

Peri-ictal psychiatric episodes usually consist of cluster of symptoms of short duration ranging from a few minutes up to 3 days, although postictal episodes can at times last up to 4 weeks in duration. Ictal psychiatric phenomena are usually the expression of simple partial seizures (auras), although on occasion they may be the clinical manifestation of complex partial status or absence stupor. The purpose of this chapter is to review the available data on preictal, ictal, and postictal psychiatric phenomena and their implications with respect to the patient’s interictal psychiatric disorders and epileptic syndrome.


Preictal Psychiatric Symptoms

The existence of preictal symptoms was described in the early nineteenth century by Burrows who described symptoms of irritability and depression, and grandiose
delusions (5). In the twentieth century, Blanchet and Frommer investigated the presence of preictal psychiatric symptoms in 27 consecutive patients who were asked to rate their mood on a daily basis for a period of 1 month (6). Thirteen patients recorded at least one seizure during this period. Rating scales identified the presence of dysphoric symptoms, consisting of irritability and mood changes, approximately 3 days before the seizures. These symptoms worsened in severity closer to the time of the seizure and remitted approximately 1 day after the seizure, although in some cases the symptoms persisted for up to 3 days after the seizure. It is not uncommon, therefore, for parents or family members of the patients to be able to predict the occurrence of seizures. In the case of children, they typically become more irritable, and display motor hyperactivity, impulsive behavior, and poor frustration tolerance.


Ictal Symptoms

As stated in the preceding text, psychiatric ictal symptomatology and episodes are the clinical expression of simple partial seizures, most of which are of mesial temporal origin, although epileptogenic zones in orbitofrontal, cingulate gyrus, and insula can also be identified in psychiatric ictal events. Jackson described a “dreamy state” in seizures originating in mesial temporal structures, consisting of vivid memory–like hallucinations, and/or the sense of having previously lived through exactly the same situation (déja vu) (7). It has been estimated that psychiatric symptoms occur in 25% of “auras,” 60% of these presenting as fear or panic, and 20% as symptoms of depression (8), whereas less frequent psychiatric symptoms include pleasurable experiences (feelings of ecstasy), and visual and auditory hallucinations (see subsequent text).

Ictal fear or ictal panic may present as a simple partial seizure or can be an aura followed by a complex partial seizure in temporal lobe epilepsy (TLE) (8,9,10). Frequently, patients fail to recognize and report associated symptoms (such as transient confusion or subtle automatisms) indicative of an ictal event, which often results in its misdiagnosis and treatment as a panic disorder, and the correct diagnosis is reached only after the patient has experienced a secondary generalized tonic-clonic seizure. Yet, a careful history can help distinguish a panic disorder occurring interictally from an ictal panic. Indeed, ictal panic is typically brief (<30 seconds in duration), is stereotypical, occurs out of context to concurrent events, and is associated with other ictal phenomena, such as periods of confusion of variable duration and subtle or overt automatisms (11). The intensity of the sensation of fear is mild to moderate and rarely reaches the intensity of a panic attack. On the other hand, interictal panic attacks consist of episodes of 5 to 20 minutes’ duration which at times may persist for several hours during which the feeling of fear or panic is very intense (“feeling of impending doom”) and associated with a variety of autonomic symptoms, including tachycardia, diffuse diaphoresis, and shortness of breath. Patients may become completely absorbed by the panicky experience to the point where they may not be able to report what is going on around them; however, there is no confusion or loss of consciousness as in complex partial seizures. It is not infrequent for patients to become extremely apprehensive about experiencing another panic attack that may then lead to the development of a full-blown agoraphobia. The misdiagnosis of ictal fear as a panic disorder may be compounded by the failure to identify an electrographic ictal pattern in simple partial seizures of mesial temporal origin, above all when the seizure focus is in the amygdala. In such cases, electroencephalographic (EEG) recordings with sphenoidal electrodes placed under fluoroscopic guidance may be necessary to demonstrate the epileptiform activity (12). Finally, patients with ictal panic may also have interictal panic attacks and other types of anxiety disorders (13).

Ictal fear may be easily missed in children; this is illustrated in the following example of a 7-year-old child who experienced recurrent nocturnal and occasional
daytime attacks consisting of intense fear and complex visual hallucinations (14). He was thought to have panic disorder, pavor nocturnus, and nightmares. Furthermore, because the attacks appeared after the divorce of his parents, an adjustment disorder was suspected, and he received psychotherapy for more than 2 years, without an effect on the attacks. Routine EEG and magnetic resonance imaging (MRI) studies had been reported to be normal, but because of persistent attacks, he underwent a prolonged video electroencephalography (VEEG) monitoring study in which two typical attacks were recorded displaying a left temporal ictal pattern. He was successfully treated with antiepileptic medication. A high-resolution MRI revealed a cortical dysplasia extending from the left anteromedial temporal lobe to the amygdala with a suspected origin of seizures in the amygdala.

Ictal symptoms of depression rank second in frequency after ictal fear (8,9,10). Such mood changes are typically brief, stereotypical, occur out of context, and are associated with other ictal phenomena. The most frequent symptoms include feelings of anhedonia, guilt, and suicidal ideation. More typically, however, ictal symptoms of depression are followed by alteration of consciousness as the ictus evolves from a simple to a complex partial seizure.

Ictal hallucinations include visual and, less frequently, auditory hallucinations. In contrast to “psychotic hallucinations,” patients are able to realize that the hallucinations reflect unreal phenomena. Ictal hallucinations of insular origin are usually associated with autonomic symptoms. For example, Insard and Mauguiere reported six patients in whom seizures were recorded with intracranial electrodes from the insula, consisting of an initial sensation of laryngeal constriction followed by paresthesia that were often unpleasant affecting large cutaneous territories and were eventually followed by dysarthric speech and/or elementary auditory hallucinations (15).

Ictal psychiatric phenomena may also consist of pleasurable experiences. For example, among 11 consecutive patients reported by Hansen and Brodtkorb, 8 experienced sensory hallucinations, 4 erotic sensations, 5 described “a religious/spiritual experience,” and several had symptoms that were felt to have no counterpart in human experience (16). The ictal onset could be localized to the temporal lobe only in four patients. Eight patients voiced their wish to experience seizures; five could induce them, and four were noncompliant with their antiepileptic drugs (AEDs).

Ictal auras can also include autoscopic phenomena, which consist of a hallucination of seeing one’s double and out-of-body experiences. Devinsky et al. reported ten patients with such ictal phenomena (17); these authors found a 6.3% incidence of ictal autoscopic phenomena in the consecutive patients they interviewed in their clinic. Among 21 patients in whom the seizure focus could be identified, seizures originated in the temporal lobe in 18 (86%) with no clear lateralization.


Postictal Psychiatric Phenomena

PPSs have been recognized for a long time, but in general, remain poorly understood, particularly with respect to their prevalence, clinical characteristics, and pathogenic mechanisms. They may present as individual symptoms or as a cluster of symptoms, mimicking any type of psychiatric disorder, that is, anxiety, depression, and psychosis. The vast majority of articles on PPSs have revolved around postictal psychotic symptoms and episodes that have been encountered in the course of VEEG.


Postictal Psychiatric Symptoms

The only systematic investigation of the prevalence and clinical characteristics of PPSs published to date was carried out by Kanner et al. and hence will be reviewed in some detail. This study was conducted at the Rush Epilepsy Center with 100 consecutive patients who had pharmacoresistent partial epilepsy (18). Every patient was asked
to complete a 42-item questionnaire (The Rush Postictal Psychiatric Questionnaire— see Appendix) designed to identify the frequency of 26 PPSs and 5 cognitive symptoms during a 3-month period. These included symptoms of depression and of various anxiety disorders (i.e., general anxiety, panic attacks, agoraphobia, obsessions, and compulsions), hypomanic and psychotic symptoms, and neurovegetative and physical symptoms. These latter two types of symptoms are common in seizures and in depressive and anxiety disorders. Accordingly, they were recorded as separate symptom categories, so as not to erroneously increase the number of postictal symptoms of depression and anxiety. The postictal period was defined as the 72 hours that followed a seizure. The questionnaire was also developed to discriminate between interictal and postictal symptoms and to identify interictal symptoms that worsen in severity during the postictal period. Each question inquired about the frequency of the symptom and only those that were identified after more than 50% of seizures were included in this study, so as to reflect a “habitual” phenomenon.

Among the 100 patients, the authors identified a lifetime prevalence of psychiatric disorders in 54 patients, which consisted of mood disorders in 33; anxiety disorder in 16, 12 of whom also had a mood disorder; and attention-deficit hyperactivity disorder in 5. No patient had a history of a psychotic disorder. Eleven patients reported one or more hospitalizations for psychiatric disorders.

A median of eight postictal symptoms was identified (range 0 to 25) corresponding to a median of three cognitive symptoms (range 0 to 5) and five PPSs (range 0 to 22); 74 patients experienced at least one type of PPS—68 reported PPSs and cognitive symptoms, and 6 reported only PPSs. An additional 14 patients experienced only postictal cognitive symptoms, whereas 12 did not report any postictal symptoms. The prevalence of the different types of PPSs and their median duration appear in the Table 19.1.

Among the 74 patients with PPSs, 60 (81%) experienced PPSs of more than one psychiatric disorder. The most frequent combination included postictal symptoms of anxiety and depression, and neurovegetative symptoms. Notably, the existence of PPSs had been investigated in only seven patients before this study and only one was offered treatment specifically directed to the remission of habitual postictal symptoms of depression.


Clinical Characteristics of Postictal Psychiatric Symptoms and Relation to Past Psychiatric History



  • Postictal Symptoms of Depression: Forty-three patients reported a median of five postictal symptoms of depression (range 2 to 9). The median duration of each symptom was 24 hours (0.1 to 240 hours) with the exception of postictal crying which had a median duration of 6 hours (0.1 to 108 hours). Thirty-two patients experienced postictal symptoms of depression of at least 24 hours’ duration (18 experienced a minimum of six symptoms lasting 24 hours or longer), five reported symptoms of 1 to 23 hours’ duration and only three patients had symptoms lasting less than 1 hour. Thirteen patients reported habitual postictal suicidal ideation; eight experienced passive and active suicidal thoughts, whereas only five reported passive suicidal ideation. No patient ever acted on these symptoms. As shown in Table 19.1, postictal symptoms of depression always occurred in combination with other PPS categories, although correlations were identified only with postictal symptoms of anxiety (r = 0.556, p <0.0001), psychotic symptoms (r = 0.3, p = 0.002), and neurovegetative symptoms (r = 0.37, p <0.0001).

    Among these 43 patients, 25 had a history of a mood disorder and 11 had an anxiety disorder. There was significant association between a history of depression and the postictal symptoms of self-deprecation and guilt, whereas a significant association with a history of anxiety and postictal guilt was identified. Furthermore, the number of postictal symptoms of depression was higher in

    patients with a prior history of depression and anxiety. Notably, 10 of the 13 (77%) patients with postictal suicidal ideation had a history of either major depression or bipolar disorder. Also, postictal suicidal ideation was an indicator of previous severe psychiatric disorders as it was significantly associated with previous hospitalization for psychiatric disorders.








    TABLE 19.1 Prevalence and Median Duration of Postictal Psychiatric and Cognitive Symptoms in 100 Patients with Intractable Partial Epilepsy


























































































































































































    Postictal Symptom Prevalence Median Duration in Hours (Range)
    Symptoms of depression, total 43  
      Irritability 30 24 (0.5–108)
      Poor frustration tolerance 36 24 (0.1–108)
      Anhedonia 32 24 (0.1–148)
      Hopelessness 25 24 (1.0–108)
      Helplessness 31 24 (1.0–108)
      Crying bouts 26 6 (0.1–108)
      Suicide ideation 13 24 (1.0–240)
        Active suicidal thoughts 8  
        Passive suicidal thoughts 13  
      Feelings of self–deprecation 27 24 (1.0–120)
      Feelings of guilt 23 24 (0.1–240)
    Neurovegetative symptoms, total 62  
      Early night insomnia 11
      Middle night awakening 13
      Early morning awakening 11
      Excessive somnolence 43 24 (2–72)
      Loss of appetite 36 24 (2–148)
      Excessive appetite 10 15 (0.5–48)
      Loss of sexual interest (not related to fatigue) 26 39 (6–148)
    Symptoms of anxiety, total 45  
      Constant worrying 33 24 (0.5–108)
      Panicky feelings 10 6 (0.1–148)
      Agoraphobic symptoms 29 24 (0.5–296)
        Due to fear of seizure recurrence 20
      Compulsions 10 15 (0.1–72)
      Self consciousness 26 6 (0.05–108)
    Psychotic symptoms, total 7  
      Referential thinking 5 15 (0.1–108)
      Auditory hallucinations 2 6.0 (0.1–108)
      Paranoid delusions 4 0.2 (0.1–0.25)
      Religious delusions 3 6.0 (0.1–108)
      Visual hallucinations 1 36 (6–48)
    Hypomanic symptoms, total 22  
      Excessive energy 9 2 (0.15–48)
      Thought racing 15 2 (0.1–24)
      Fatigue 37 24 (0.1–108)
    Cognitive symptoms, total 82  
      Difficulty in concentration 71 6 (0.1–108)
      Problems with memory 66 6 (0.1–108)
      Confusion 65 2 (0.1–72)
      Disorientation 46 1 (0.05–24)
      Thought blockage 42 9 (0.1–98)
        Only cognitive symptoms 14
        No postictal symptoms 12


  • Postictal Symptoms of Anxiety: Forty-five patients reported a median of 2 (range 1 to 5) postictal symptoms of anxiety. The median duration of individual symptoms ranged from 6 to 24 hours (0.1 to 296 hours). In 30 patients, at least one symptom lasted 24 hours or longer (15 patients [33%] reported a cluster of four postictal symptoms of anxiety of at least 24 hours); 10 patients reported at least one symptom of 1 to 23 hours’ duration; and 5 patients had symptoms lasting less than 1 hour. Twenty-nine patients experienced symptoms of postictal agoraphobia; 18 (62%) attributed these symptoms to the fear of seizure recurrence. Nevertheless, the presence of this fear was not related to the actual occurrence of seizures in clusters. A prior history of anxiety disorder was identified in 15 patients (33%). There was an association between a history of anxiety disorder and the occurrence of postictal symptoms of constant worrying and panicky feelings.


  • Postictal Psychotic Symptoms: Seven patients experienced a median of two postictal psychotic symptoms (range 1 to 5). Five patients reported referential thinking (people are staring and talking about me), two reported auditory hallucinations, four paranoid delusions, three religious delusions, and one visual hallucinations. The duration of individual symptoms ranged from 0.2 to 36 hours (0.1 to 108 hours). In four of these patients, at least one psychotic symptom lasted for a minimum of 24 hours, two patients experienced symptoms lasting between 1 and 23 hours, and one reported symptoms of less than 1-hour duration. These seven patients also experienced postictal symptoms of anxiety and depression and five patients reported postictal hypomanic symptoms. No
    patient had experienced a history of interictal psychosis. A history of psychiatric disorder was not significantly associated with the development of postictal psychotic symptoms but a history of anxiety disorder was associated with a greater number of psychotic symptoms.


  • Postictal Hypomanic Symptoms: Postictal hypomanic symptoms include excessive energy and racing thoughts, which were identified in 22 patients: 15 patients reported racing thoughts and 9 reported increased energy, but only 2 reported both symptoms. The median duration of both symptoms was 2 hours (0.1 to 48 hours). Six patients experienced hypomanic symptoms lasting 24 hours or longer. There was no significant association between a history of psychiatric disorder and the development of hypomanic symptoms.


  • Postictal Neurovegetative Symptoms: Postictal neurovegetative symptoms are among the most commonly reported postictal symptoms, above all postictal somnolence and loss of appetite. Sixty-two patients experienced a median of two symptoms (range 1 to 5) and in 12 patients they were the only PPS category reported. In addition, early night insomnia was reported by 11% of patients, middle night awakening by 13%, early morning awakening by 11%, and excessive appetite by 10%. These are four symptoms not typically associated with the postictal state. The median duration of individual symptoms ranged from 15 to 39 hours (0.5 to 148 hours). A history of psychiatric disorder did not worsen or act as a risk factor of these postictal symptoms.


  • Postictal Fatigue: Thirty-seven patients reported postictal fatigue with a median duration of 24 hours (0.1 to 108 hours).


Relation between Postictal Cognitive and Psychiatric Symptoms

Eighty-two patients experienced a median of four postictal cognitive symptoms (range 1 to 5). Fourteen patients reported only postictal cognitive symptoms, whereas the other 68 experienced postictal cognitive and psychiatric symptoms. The median duration of individual cognitive symptoms ranged from 1 to 9 hours (0.05 to 108 hours). In general, the “estimated” duration of PPSs was significantly longer than that of cognitive symptoms. The presence of postictal symptoms of depression was associated with worst postictal cognitive disturbances, as evidenced by a greater number of postictal cognitive symptoms.


Interictal Psychiatric Symptoms with Postictal Exacerbation

Thirty-eight patients experienced a median of 3 (range 1 to 15) psychiatric symptoms during the interictal period, 34 of whom had symptoms of depression (n = 24), anxiety (n = 3), or mixed, anxiety/depression (n = 6), and 4 had only neurovegetative symptoms. Thirty-six of these 38 patients (94%) experienced interictal symptoms as well with postictal exacerbation in severity and in 19 patients all interictal recorded symptoms were only coded as such. Furthermore, among these 36 patients, 30 (83%) also experienced de novo PPSs. Among 20 patients with interictal fatigue, 18 reported significant worsening during the postictal period. Finally, 37 patients reported interictal cognitive symptoms that worsened postictally; all of these patients also experienced de novo postictal cognitive symptoms.

Thirteen patients were taking antidepressant medications at the time of the study, ten for the treatment of an interictal depressive disorder, two for an anxiety disorder, and one for the treatment of irritability. Being on antidepressant, however, did not prevent the development of postictal symptoms (n = 3) or the postictal exacerbation of interictal symptoms of depression and/or anxiety (n = 10), despite a significant improvement of the interictal disorder.

There was no significant association between the development of PPS and the location of the seizure focus, type of seizures, or the occurrence of seizures in clusters. On the other hand, taking AEDs with negative psychotropic properties (barbiturates and benzodiazepines) yielded a trend toward a
greater likelihood of developing postictal psychotic symptoms.

Clearly, these data illustrate the relatively high prevalence of PPS and the very close relationship between interictal and postictal symptomatology and between a history of prior psychiatric disorders and the development of PPS. Without doubt, recognition of PPS is the essence in the understanding of psychiatric symptomatology in patients with epilepsy, including (as it pertains to) the interpretation of its response to treatment.

Aug 28, 2016 | Posted by in PSYCHIATRY | Comments Off on Peri-ictal Psychiatric Phenomena: Clinical Characteristics and Implications of Past and Future Psychiatric Disorders

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