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Neuropsychiatric evaluations of postictal behavioral changes
Epilepsy & Behavior 19 (2010) 134–137
Contents lists available at ScienceDirect
Epilepsy & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h
Review
Neuropsychiatric evaluations of postictal behavioral changes Masumi Ito ⁎ Department of Neuropsychiatry, Tenshi Hospital, Sapporo, Japan
a r t i c l e
i n f o
Article history: Received 17 June 2010 Accepted 17 June 2010 Available online 13 August 2010 Keywords: Epilepsy Postictal behavior Psychiatric symptom Psychosis Aggression Mood change Brief Psychiatric Rating Scale
a b s t r a c t Postictal behavioral changes (PBCs), including psychosis, aggression, and mood change, are commonly observed in patients with epilepsy. Recognition and description of the clinical manifestations of PBCs would help in understanding and treating patients. Additionally, various quantified objective scales that are widely available in clinical psychiatry could be used to assess the clinical symptoms of PBCs. There are few reports in which objective rating scales have been used to assess neuropsychiatric symptoms in patients with epilepsy. However, there have been a small number of studies on interictal psychosis and depression in which either the Brief Psychiatric Rating Scale or the Hamilton Depression Scale was used. These inventories are likely to be useful for the assessment of PBCs. Other rating scales used for schizophrenia, depression, mania, and aggressive behavior are reviewed here. The author suggests that cross-sectional and longitudinal neuropsychiatric measurement combined with other modalities, including functional neuroimaging, could provide clues to the pathophysiology of PBCs. © 2010 Elsevier Inc. All rights reserved.
1. Introduction Postictal behavioral changes (PBCs) are commonly observed in people with epilepsy. PBCs include confusion, aggression, psychosis, and mood changes. Patients with PBCs may sometimes exhibit violent and destructive behavior that bothers or scares the people around them and potentially damages their reputations, causing a decline in quality of life. On the other hand, PBCs are sometimes difficult to recognize as a seizure-related phenomenon that is essentially transient, partly because some PBCs, such as postictal psychosis, may occur after an interval of a few days without any definite clinical signs and may continue for a long period lasting up to a few weeks [1–5]. These features of PBCs may lead to the misunderstanding that these individuals have violent personality traits. It is therefore important to clarify the nature of PBCs and make it known to everyone. Recognition and description of the clinical manifestations of PBCs would help in understanding and treating patients. However, clinical characteristics of PBCs are yet to be fully evaluated, partly because of the difficulty involved in assessing the various symptoms during the very brief postictal period. Most previous studies have conducted qualitative rather than quantitative analysis of PBCs [2,5–8]. Introduction of quantitative evaluation methods would open different lines of research on PBCs. In clinical psychiatry, a number of quantitative batteries have been employed to assess the psychopathology of various psychiatric disorders. Those tests may also be applicable to the assessment of psychiatric PBCs. Administration of the tests is encouraged in future ⁎ Kita-12, Higashi-3, Higashi-ku, Sapporo 065-8611, Japan. Fax: +81 11 751 1708. E-mail address: [email protected]. 1525-5050/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2010.06.017
studies. There are two types of evaluation: one is objective scoring by clinicians through patient interviews or behavioral observation; the other is subjective self-reporting by patients. With respect to PBCs, objective rating scales may be more practical, because patients with psychosis or aggression usually lack insight into their condition, and a subjective scale may not accurately reflect their mental state. In addition, as some PBCs may be associated with impairment of consciousness and memory disturbance, it could be difficult for patients with PBCs to complete the self-rating questionnaire. In this article, several objective psychiatric rating scales used for various psychiatric disorders, including schizophrenia, aggression, depression, and mania, are introduced. Moreover, possible clinical applications of these methods to the evaluation of PBCs are proposed. 2. Neuropsychiatric test 2.1. Evaluation for psychosis Psychosis is characterized by delusions, hallucinations, or a limited number of severe abnormalities of behavior such as gross excitement, marked psychomotor retardation, and catatonic behavior [9]. Schizophrenia is the disease most representative of the psychotic state. Many widely used inventories have been developed to assess symptom severity and therapeutic effect in patients with schizophrenia. 2.1.1. Brief Psychiatric Rating Scale The Brief Psychiatric Rating Scale (BPRS) is one of the most widely used scales in psychiatric research [10]. It consists of 18 items, each of which is rated on the scale from 1 = absent to 7 = extremely severe and is administered in a semistructured interview by experienced
M. Ito / Epilepsy & Behavior 19 (2010) 134–137
psychiatrists (Table 1). This scale is commonly used to evaluate psychiatric symptoms in schizophrenia including positive symptoms, such as delusion and hallucination, and negative or residual symptoms, such as blunt affect and motor retardation. It also covers nonpsychotic symptoms such as anxiety and depression. It is relatively easy to rate according to BPRS guidelines, and interrater reliability is high. The results are usually analyzed with total scores and factorial analysis. There have been very few studies on psychotic symptoms in patients with epilepsy that have employed the BPRS [11–13]. Adachi et al. [11] evaluated clinical symptoms of postictal psychosis using a modified version of the BPRS and compared these symptoms with those of interictal psychosis in patients with frontal and temporal lobe epilepsy. Patients with frontal lobe epilepsy were found to exhibit more pronounced negative symptoms, including emotional withdrawal and blunted affect, in interictal psychosis than in postictal psychosis. 2.1.2. Positive and Negative Syndrome Scale The Positive and Negative Syndrome Scale (PANSS) was developed to assess symptoms of schizophrenia and other psychotic disorders [14]. It comprises 30 items on three subscales: 7 items covering positive symptoms (hallucinations and delusions), 7 covering negative symptoms (blunted affect and social withdrawal), and 16 covering general psychopathology (somatic concern, anxiety, and depression). Each item is scored on an item-specific scale ranging from 1 to 7. The PANSS has become a standard test for assessing the efficacy of antipsychotic drugs in drug trials. A 20% reduction in PANSS total score has been employed as the criterion for response to several new antipsychotic drugs. There are only a few studies that have used the PANSS for the evaluation of psychotic symptoms in patients with epilepsy. Tadokoro et al. [15] compared the psychopathology of patients with interictal psychosis with that of patients with schizophrenia. A significant difference in the results on the negative subscales of the PANSS was noted between these patient groups. The response rate to antipsychotic drugs was also investigated based on the reduction in positive and negative scores of the PANSS. Another study [16] assessed interictal psychiatric symptoms using the PANSS in patients with temporal lobe epilepsy and found that most patients had higher scores on the negative subscale than on the positive subscale. 2.1.3. Neuropsychiatric Inventory The Neuropsychiatric Inventory (NPI) was developed to assess a wide range of behaviors encountered in patients with dementia [17]. It is a validated informant-based interview that determines the frequency and severity of behavioral changes. It has been shown to have Table 1 Items evaluated with the Brief Psychiatric Rating Scale. 1. Somatic concern 2. Anxiety 3. Emotional withdrawal 4. Conceptual disorganization 5. Guilt feelings 6. Tension 7. Mannerisms and posturing 8. Grandiosity 9. Depressive mood 10. Hostility 11. Suspiciousness 12. Hallucinatory behavior 13. Motor retardation 14. Uncooperativeness 15. Unusual thought content 16. Blunted affect 17. Excitement 18. Disorientation
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adequate test–retest and interpreter reliability and has also been used for patients with Parkinson's disease and multiple sclerosis. The NPI consists of 10 items: delusions, hallucinations, dysphoria, anxiety, euphoria, aggression, apathy, irritability, disinhibition, and aberrant motor behavior. For each item, severity is rated from 1 to 3 and frequency from 1 to 4. Recently, Krishnamoorthy and Trimble [18] used the NPI to test patients with epilepsy, and the results showed a good correlation with the BPRS. Because it has fewer questions than the BPRS, the NPI may be used to evaluate psychiatric symptoms quickly. Therefore, this scale may be a more suitable inventory for patients with difficulty in verbal communication. 2.2. Evaluation for mood disorder Mood changes, including depression during the postictal period, are commonly experienced by patients with epilepsy [19]. Kanner et al. [6] reported that 43 of 100 patients with intractable epilepsy experienced postictal depression and that 13 of these patients had suicidal ideation. A hypomanic state with excessive energy and racing thoughts was identified in 22 patients in that study. Recent studies have shown that the postictal manic state is not as rare as was previously assumed [20–22]. Additionally, it is noteworthy that mood changes, which are often mixed with manic features, are frequently observed in postictal psychosis [23]. However, subtle postictal mood changes may easily be overlooked, and close observation of these phenomena is needed to clarify their prevalence and clinical features. In contrast, although quantitative objective scales have been used less frequently than subjective self-rating scales, including the Beck Depression Inventory [24], there are numerous studies on interictal depressive symptoms in epilepsy. A combination of objective and subjective rating scales would result in further findings on postictal mood changes. 2.2.1. Hamilton Depression Scale The Hamilton Depression Scale (HAMD) is one of the most widely used depression scales in drug trials. It consists of 21 items; 11 items are rated on a 5-point scale and 10 on a 3-point scale, resulting in a total score ranging from 0 to 64 [25]. A clinician evaluates various depressive symptoms such as depressed mood, feelings of guilt, thoughts of suicide, and sleeping habits (Table 2). The guide for the structured clinical interview was developed by Williams [26]. The HAMD can be used to assess the severity of symptoms, and
Table 2 Items evaluated with the Hamilton Depression Scale. 1. Depressed mood 2. Feelings of guilt 3. Suicide 4. Insomnia, initial 5. Insomnia, middle 6. Insomnia, delayed 7. Work and interest 8. Retardation 9. Agitation 10. Anxiety, psychic 11. Anxiety, somatic 12. Somatic symptoms, gastrointestinal 13. Somatic symptoms, general 14. Genital symptoms 15. Hypochondriasis 16. Loss of weight 17. Insight 18. Diurnal variation 19. Depersonalization and derealization 20. Paranoid symptoms 21. Obsessional and compulsive symptoms
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longitudinal changes in depressive symptoms can be described and compared along certain evaluation points. The HAMD has been administered in studies assessing phenomenology [27–29] and in antidepressant drug trials [30–32] in patients with interictal depression. Moreover, a few studies have used the HAMD to assess the effects of antiepileptic drugs on depressive symptoms in patients with epilepsy [33–35]. 2.2.2. Montgomery–Asberg Depression Rating Scale The Montgomery–Asberg Depression Rating Scale (MADRS) was developed from items that were found in several studies to be sensitive to change in response to antidepressant treatment. It has become increasingly popular worldwide [36]. There is a proven correlation with the HAMD. The MADRS consists of 10 items rated on a scale from 0 to 6: apparent sadness, reported sadness, inner tension, reduced sleep, reduced appetite, concentration difficulties, lassitude, inability to feel, pessimistic thoughts, and suicidal thoughts. This scale focuses more on psychiatric symptoms including depressed mood and anhedonia than on physical symptoms. A structured interview guide has been developed and its reliability is established [37]. With the exception of a small number of studies on interictal depression, the MADRS has not been popularly employed in epilepsy research [28,34,38]. 2.2.3. Young Mania Rating Scale The Young Mania Rating Scale (YMRS) was developed as a clinical rating of manic states and is widely used to assess therapeutic effects [39]. It consists of 11 items including elevated mood and increased motor activity (Table 3). Seven items are rated 0 to 4, and 4 items regarding irritability and disruptive behavior are rated 0 to 8. The total score can range from 0 to 60. Interrater reliability is high, and the YMRS is considered to be sensitive to change in symptoms. It is an easily administered instrument for frequent longitudinal rating of manic states and would be useful in assessing postictal mania. 2.3. Evaluation for aggression It has been pointed out that PBCs often manifest as violent and aggressive behavior [40–43], usually as sudden, explosive excitement that is not always associated with delusions and hallucinations. It is also common for these symptoms not to involve mood changes such as mania. Clinical assessments using inventories for either psychosis or mood disorder may not be sufficient to evaluate the symptoms of these patients. Tools that assess abnormal behavior in various conditions may be useful for some patients with PBCs with overt aggression. 2.3.1. Social Dysfunction and Aggression Scale The Social Dysfunction and Aggression Scale (SDAS) was developed by Wistedt et al. [44] to measure aggressive and violent behavior independent of psychiatric diagnosis and is constructed as an observer scale for aggression analogs for the HAMD. It consists of nine items (SDAS-9) covering outward aggression and two items (SDAS-2) covering inward aggression such as suicidal behavior (Table 4). Each Table 3 Items evaluated with the Young Mania Rating Scale. 1. Elevated mood 2. Increased motor activity–energy 3. Sexual interest 4. Sleep 5. Irritability 6. Speech (rate and amount) 7. Language–thought disorder 8. Content 9. Disruptive–aggressive behavior 10. Appearance 11. Insight
Table 4 Items evaluated with the Social Dysfunction and Aggression Scale. 1. Nondirected verbal aggressiveness (general shouting, screaming, swearing) 2. Directed verbal aggressiveness (threats against defined persons) 3. Irritability (impatient, easily provoked) 4. Negativism (obstinate, uncooperative, resistant to authority) 5. Dysphoric mood (angry, quick to misinterpret) 6. Socially disturbed behavior (upsetting others, lack of feeling for situations) 7. Physical violence to personnel (kicking, beating, etc.) 8. Physical violence to others, apart from personnel (kicking, beating, etc.) 9. Self-mutilation (scratching own skin, beating himself, burn marks) 10. Physical violence to things (kicking furniture, destroying things) 11. Suicidal thoughts and impulses
item is rated on a scale from 0 to 5. The interobserver reliability of the SDAS has been found to be adequate. A single study assessed violent behavior in postictal psychosis using this scale and indicated excessively aggressive behavior in patients with postictal psychosis [12]. 3. Clinical application for evaluation of postictal behavioral changes There have been very few studies on neuropsychiatric evaluations of patients with PBCs using the quantified inventories described above, because it is difficult to assess behavior during the brief postictal period and PBCs often manifest clinically as mixed features of various psychiatric symptoms. However, cross-sectional as well as longitudinal evaluation is encouraged in certain patients as the findings may reveal clinical characteristics of PBCs, including the time course. There is a single prospective study in which the BPRS was used to assess postictal psychosis in patients with temporal lobe epilepsy [12]. The symptoms were evaluated within 1 week of the seizure and then 1 week and 1 month after the first evaluation point. The results showed that the BPRS scores decreased dramatically 1 week after the initial evaluation, with variation between cases, and the patient subsequently returned to baseline 1 month after the first evaluation. The authors pointed out that the scores did not return to their baseline until 1 month after the seizure despite the appearance of recovery from gross psychotic symptoms. This finding suggests that psychotic symptoms might linger even after apparent recovery. The postictal changes within brain functions may continue subclinically and the PBCs may be due to persistent epileptic discharges, which might explain why postictal psychosis evolves into interictal chronic psychosis in some patients [45]. This finding also indicates that more sensitive neuropsychological batteries could detect subtle behavioral changes even after the apparent disappearance of PBCs. Neuropsychiatric measurement along with various modalities, including functional neuroimaging, could provide clues for understanding the pathophysiology of PBCs. 4. Conclusions Observation of postictal behavior using quantitative evaluation methods has not yet been conducted. Assessment of PBCs with these evaluation methods would be useful for elucidation of the clinical characteristics of PBCs and the classification of some PBC patterns. Further research into the association of PBC patterns with seizure discharges could help to clarify certain neuronal networks leading to behavioral changes not only in patients with epilepsy, but also in those with other psychiatric disorders. Finally, it must be considered that scores obtained directly may not reflect the severity of the psychopathology of the patient. Diagnosis of psychiatric symptoms on the basis of scores sometimes leads to misunderstanding of the patient. The results should be compared between different evaluation periods or patients should be compared with controls. Neuropsychiatric testing becomes helpful when used with the knowledge of its significance and limitations.
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[22] Barczak P, Edmunds E, Betts T. Hypomania following complex partial seizures: a report of three cases. Br J Psychiatry 1988;152:137–9. [23] Kanemoto K, Kawasaki J, Mori E. Violence and epilepsy: a close relation between violence and postictal psychosis. Epilepsia 1999;40:107–9. [24] Beck AT, Steer RA, Carbin MG. Psychometric properties of the Beck Depression Inventory: twenty-five years of evaluation. Clin Psychol Rev 1988;8:77–100. [25] Hamilton M. A rating scale for depression. J Neurol Neurosurg Psychiatry 1960;23: 56–62. [26] Williams BW. A structured interview guide for Hamilton Depression Rating Scale. Arch Gen Psychiatry 1978;45:742–7. [27] Ito M. Epilepsy and affective disorders. In: Matsuura M, Inoue Y, editors. Neuropsychiatric issues in epilepsy. Montrouge: John Libbey Eurotext; 2010. p. 129–36. [28] Robertson MM, Trimble MR, Townsend HRA. Phenomenology of depression in epilepsy. Epilepsia 1987;28:364–72. [29] Grabowska-Grzyb A, Jędrzejczak J, Nagańska E, Fiszer U. Risk factors for depression in patients with epilepsy. Epilepsy Behav 2006;8:411–7. [30] Hovorka J, Herman E, Nemcova I. Treatment of interictal depression with citalopram in patients with epilepsy. Epilepsy Behav 2000;1:444–7. [31] Robertson MM, Trimble MR. The treatment of depression in patients with epilepsy: a double-blind trial. J Affect Disord 1985;9:127–36. [32] Kühn K, Quednow BB, Thiel M, Falkai P, Maier W, Elger CE. Antidepressive treatment in patients with temporal lobe epilepsy and major depression: a prospective study with three different antidepressants. Epilepsy Behav 2003;4:674–9. [33] Harden CL, Lazar LM, Pick LH, et al. A beneficial effect on mood in partial epilepsy patients treated with gabapentin. Epilepsia 1999;40:1129–34. [34] Mazza M, Della Marca G, Di Nicola M, et al. Oxcarbazepine improves mood in patients with epilepsy. Epilepsy Behav 2007;10:397–401. [35] Mazza M, Martini A, Scoppetta M, Mazza S. Effect of levetiracetam on depression and anxiety in adult epileptic patients. Prog Neuropsychopharmacol Biol Psychiatry 2008;32:539–43. [36] Montgomery SA, Asberg M. A new depression scale designed to be sensitive to change. Br J Psychiatry 1979;134:382–9. [37] Williams JB, Kobak KA. Development and reliability of a structured interview guide for the Montgomery–Asberg Depression Rating Scale (SIGMA). Br J Psychiatry 2008;192:52–8. [38] Kalogjera-Sackellares D, Sackellares JC. Improvement in depression associated with partial epilepsy in patients treated with lamotrigine. Epilepsy Behav 2002;3:510–6. [39] Young RC, Biggs JT, Ziegler VE, Meyer DA. A rating scale for mania: reliability, validity and sensitivity. Br J Psychiatry 1978;133:429–35. [40] Gerard ME, Spitz MC, Towbin JA, Shantz D. Subacute postictal aggression. Neurology 1998;50:384–8. [41] Ito M, Okazaki M, Takahashi S, Muramatsu R, Kato M, Onuma T. Subacute postictal aggression in patients with epilepsy. Epilepsy Behav 2007;10:611–4. [42] Mendez MF. Postictal violence and epilepsy. Psychosomatics 1998;39:478–80. [43] Yankovsky AE, Veilleux M, Dubeau F, Andermann F. Post-ictal rage and aggression: a video-EEG study. Epileptic Disord 2005;7:143–7. [44] Wistedt B, Rasmussen A, Pedersen L, et al. The development of an observer-scale for measuring social dysfunction and aggression. Pharmacopsychiatry 1990;23:249–52. [45] Adachi N, Matsuura M, Hara T, et al. Psychoses and epilepsy: are interictal and postictal psychoses distinct clinical entities? Epilepsia 2002;43:1574–82.
Contents lists available at ScienceDirect
Epilepsy & Behavior j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / ye b e h
Review
Neuropsychiatric evaluations of postictal behavioral changes Masumi Ito ⁎ Department of Neuropsychiatry, Tenshi Hospital, Sapporo, Japan
a r t i c l e
i n f o
Article history: Received 17 June 2010 Accepted 17 June 2010 Available online 13 August 2010 Keywords: Epilepsy Postictal behavior Psychiatric symptom Psychosis Aggression Mood change Brief Psychiatric Rating Scale
a b s t r a c t Postictal behavioral changes (PBCs), including psychosis, aggression, and mood change, are commonly observed in patients with epilepsy. Recognition and description of the clinical manifestations of PBCs would help in understanding and treating patients. Additionally, various quantified objective scales that are widely available in clinical psychiatry could be used to assess the clinical symptoms of PBCs. There are few reports in which objective rating scales have been used to assess neuropsychiatric symptoms in patients with epilepsy. However, there have been a small number of studies on interictal psychosis and depression in which either the Brief Psychiatric Rating Scale or the Hamilton Depression Scale was used. These inventories are likely to be useful for the assessment of PBCs. Other rating scales used for schizophrenia, depression, mania, and aggressive behavior are reviewed here. The author suggests that cross-sectional and longitudinal neuropsychiatric measurement combined with other modalities, including functional neuroimaging, could provide clues to the pathophysiology of PBCs. © 2010 Elsevier Inc. All rights reserved.
1. Introduction Postictal behavioral changes (PBCs) are commonly observed in people with epilepsy. PBCs include confusion, aggression, psychosis, and mood changes. Patients with PBCs may sometimes exhibit violent and destructive behavior that bothers or scares the people around them and potentially damages their reputations, causing a decline in quality of life. On the other hand, PBCs are sometimes difficult to recognize as a seizure-related phenomenon that is essentially transient, partly because some PBCs, such as postictal psychosis, may occur after an interval of a few days without any definite clinical signs and may continue for a long period lasting up to a few weeks [1–5]. These features of PBCs may lead to the misunderstanding that these individuals have violent personality traits. It is therefore important to clarify the nature of PBCs and make it known to everyone. Recognition and description of the clinical manifestations of PBCs would help in understanding and treating patients. However, clinical characteristics of PBCs are yet to be fully evaluated, partly because of the difficulty involved in assessing the various symptoms during the very brief postictal period. Most previous studies have conducted qualitative rather than quantitative analysis of PBCs [2,5–8]. Introduction of quantitative evaluation methods would open different lines of research on PBCs. In clinical psychiatry, a number of quantitative batteries have been employed to assess the psychopathology of various psychiatric disorders. Those tests may also be applicable to the assessment of psychiatric PBCs. Administration of the tests is encouraged in future ⁎ Kita-12, Higashi-3, Higashi-ku, Sapporo 065-8611, Japan. Fax: +81 11 751 1708. E-mail address: [email protected]. 1525-5050/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2010.06.017
studies. There are two types of evaluation: one is objective scoring by clinicians through patient interviews or behavioral observation; the other is subjective self-reporting by patients. With respect to PBCs, objective rating scales may be more practical, because patients with psychosis or aggression usually lack insight into their condition, and a subjective scale may not accurately reflect their mental state. In addition, as some PBCs may be associated with impairment of consciousness and memory disturbance, it could be difficult for patients with PBCs to complete the self-rating questionnaire. In this article, several objective psychiatric rating scales used for various psychiatric disorders, including schizophrenia, aggression, depression, and mania, are introduced. Moreover, possible clinical applications of these methods to the evaluation of PBCs are proposed. 2. Neuropsychiatric test 2.1. Evaluation for psychosis Psychosis is characterized by delusions, hallucinations, or a limited number of severe abnormalities of behavior such as gross excitement, marked psychomotor retardation, and catatonic behavior [9]. Schizophrenia is the disease most representative of the psychotic state. Many widely used inventories have been developed to assess symptom severity and therapeutic effect in patients with schizophrenia. 2.1.1. Brief Psychiatric Rating Scale The Brief Psychiatric Rating Scale (BPRS) is one of the most widely used scales in psychiatric research [10]. It consists of 18 items, each of which is rated on the scale from 1 = absent to 7 = extremely severe and is administered in a semistructured interview by experienced
M. Ito / Epilepsy & Behavior 19 (2010) 134–137
psychiatrists (Table 1). This scale is commonly used to evaluate psychiatric symptoms in schizophrenia including positive symptoms, such as delusion and hallucination, and negative or residual symptoms, such as blunt affect and motor retardation. It also covers nonpsychotic symptoms such as anxiety and depression. It is relatively easy to rate according to BPRS guidelines, and interrater reliability is high. The results are usually analyzed with total scores and factorial analysis. There have been very few studies on psychotic symptoms in patients with epilepsy that have employed the BPRS [11–13]. Adachi et al. [11] evaluated clinical symptoms of postictal psychosis using a modified version of the BPRS and compared these symptoms with those of interictal psychosis in patients with frontal and temporal lobe epilepsy. Patients with frontal lobe epilepsy were found to exhibit more pronounced negative symptoms, including emotional withdrawal and blunted affect, in interictal psychosis than in postictal psychosis. 2.1.2. Positive and Negative Syndrome Scale The Positive and Negative Syndrome Scale (PANSS) was developed to assess symptoms of schizophrenia and other psychotic disorders [14]. It comprises 30 items on three subscales: 7 items covering positive symptoms (hallucinations and delusions), 7 covering negative symptoms (blunted affect and social withdrawal), and 16 covering general psychopathology (somatic concern, anxiety, and depression). Each item is scored on an item-specific scale ranging from 1 to 7. The PANSS has become a standard test for assessing the efficacy of antipsychotic drugs in drug trials. A 20% reduction in PANSS total score has been employed as the criterion for response to several new antipsychotic drugs. There are only a few studies that have used the PANSS for the evaluation of psychotic symptoms in patients with epilepsy. Tadokoro et al. [15] compared the psychopathology of patients with interictal psychosis with that of patients with schizophrenia. A significant difference in the results on the negative subscales of the PANSS was noted between these patient groups. The response rate to antipsychotic drugs was also investigated based on the reduction in positive and negative scores of the PANSS. Another study [16] assessed interictal psychiatric symptoms using the PANSS in patients with temporal lobe epilepsy and found that most patients had higher scores on the negative subscale than on the positive subscale. 2.1.3. Neuropsychiatric Inventory The Neuropsychiatric Inventory (NPI) was developed to assess a wide range of behaviors encountered in patients with dementia [17]. It is a validated informant-based interview that determines the frequency and severity of behavioral changes. It has been shown to have Table 1 Items evaluated with the Brief Psychiatric Rating Scale. 1. Somatic concern 2. Anxiety 3. Emotional withdrawal 4. Conceptual disorganization 5. Guilt feelings 6. Tension 7. Mannerisms and posturing 8. Grandiosity 9. Depressive mood 10. Hostility 11. Suspiciousness 12. Hallucinatory behavior 13. Motor retardation 14. Uncooperativeness 15. Unusual thought content 16. Blunted affect 17. Excitement 18. Disorientation
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adequate test–retest and interpreter reliability and has also been used for patients with Parkinson's disease and multiple sclerosis. The NPI consists of 10 items: delusions, hallucinations, dysphoria, anxiety, euphoria, aggression, apathy, irritability, disinhibition, and aberrant motor behavior. For each item, severity is rated from 1 to 3 and frequency from 1 to 4. Recently, Krishnamoorthy and Trimble [18] used the NPI to test patients with epilepsy, and the results showed a good correlation with the BPRS. Because it has fewer questions than the BPRS, the NPI may be used to evaluate psychiatric symptoms quickly. Therefore, this scale may be a more suitable inventory for patients with difficulty in verbal communication. 2.2. Evaluation for mood disorder Mood changes, including depression during the postictal period, are commonly experienced by patients with epilepsy [19]. Kanner et al. [6] reported that 43 of 100 patients with intractable epilepsy experienced postictal depression and that 13 of these patients had suicidal ideation. A hypomanic state with excessive energy and racing thoughts was identified in 22 patients in that study. Recent studies have shown that the postictal manic state is not as rare as was previously assumed [20–22]. Additionally, it is noteworthy that mood changes, which are often mixed with manic features, are frequently observed in postictal psychosis [23]. However, subtle postictal mood changes may easily be overlooked, and close observation of these phenomena is needed to clarify their prevalence and clinical features. In contrast, although quantitative objective scales have been used less frequently than subjective self-rating scales, including the Beck Depression Inventory [24], there are numerous studies on interictal depressive symptoms in epilepsy. A combination of objective and subjective rating scales would result in further findings on postictal mood changes. 2.2.1. Hamilton Depression Scale The Hamilton Depression Scale (HAMD) is one of the most widely used depression scales in drug trials. It consists of 21 items; 11 items are rated on a 5-point scale and 10 on a 3-point scale, resulting in a total score ranging from 0 to 64 [25]. A clinician evaluates various depressive symptoms such as depressed mood, feelings of guilt, thoughts of suicide, and sleeping habits (Table 2). The guide for the structured clinical interview was developed by Williams [26]. The HAMD can be used to assess the severity of symptoms, and
Table 2 Items evaluated with the Hamilton Depression Scale. 1. Depressed mood 2. Feelings of guilt 3. Suicide 4. Insomnia, initial 5. Insomnia, middle 6. Insomnia, delayed 7. Work and interest 8. Retardation 9. Agitation 10. Anxiety, psychic 11. Anxiety, somatic 12. Somatic symptoms, gastrointestinal 13. Somatic symptoms, general 14. Genital symptoms 15. Hypochondriasis 16. Loss of weight 17. Insight 18. Diurnal variation 19. Depersonalization and derealization 20. Paranoid symptoms 21. Obsessional and compulsive symptoms
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longitudinal changes in depressive symptoms can be described and compared along certain evaluation points. The HAMD has been administered in studies assessing phenomenology [27–29] and in antidepressant drug trials [30–32] in patients with interictal depression. Moreover, a few studies have used the HAMD to assess the effects of antiepileptic drugs on depressive symptoms in patients with epilepsy [33–35]. 2.2.2. Montgomery–Asberg Depression Rating Scale The Montgomery–Asberg Depression Rating Scale (MADRS) was developed from items that were found in several studies to be sensitive to change in response to antidepressant treatment. It has become increasingly popular worldwide [36]. There is a proven correlation with the HAMD. The MADRS consists of 10 items rated on a scale from 0 to 6: apparent sadness, reported sadness, inner tension, reduced sleep, reduced appetite, concentration difficulties, lassitude, inability to feel, pessimistic thoughts, and suicidal thoughts. This scale focuses more on psychiatric symptoms including depressed mood and anhedonia than on physical symptoms. A structured interview guide has been developed and its reliability is established [37]. With the exception of a small number of studies on interictal depression, the MADRS has not been popularly employed in epilepsy research [28,34,38]. 2.2.3. Young Mania Rating Scale The Young Mania Rating Scale (YMRS) was developed as a clinical rating of manic states and is widely used to assess therapeutic effects [39]. It consists of 11 items including elevated mood and increased motor activity (Table 3). Seven items are rated 0 to 4, and 4 items regarding irritability and disruptive behavior are rated 0 to 8. The total score can range from 0 to 60. Interrater reliability is high, and the YMRS is considered to be sensitive to change in symptoms. It is an easily administered instrument for frequent longitudinal rating of manic states and would be useful in assessing postictal mania. 2.3. Evaluation for aggression It has been pointed out that PBCs often manifest as violent and aggressive behavior [40–43], usually as sudden, explosive excitement that is not always associated with delusions and hallucinations. It is also common for these symptoms not to involve mood changes such as mania. Clinical assessments using inventories for either psychosis or mood disorder may not be sufficient to evaluate the symptoms of these patients. Tools that assess abnormal behavior in various conditions may be useful for some patients with PBCs with overt aggression. 2.3.1. Social Dysfunction and Aggression Scale The Social Dysfunction and Aggression Scale (SDAS) was developed by Wistedt et al. [44] to measure aggressive and violent behavior independent of psychiatric diagnosis and is constructed as an observer scale for aggression analogs for the HAMD. It consists of nine items (SDAS-9) covering outward aggression and two items (SDAS-2) covering inward aggression such as suicidal behavior (Table 4). Each Table 3 Items evaluated with the Young Mania Rating Scale. 1. Elevated mood 2. Increased motor activity–energy 3. Sexual interest 4. Sleep 5. Irritability 6. Speech (rate and amount) 7. Language–thought disorder 8. Content 9. Disruptive–aggressive behavior 10. Appearance 11. Insight
Table 4 Items evaluated with the Social Dysfunction and Aggression Scale. 1. Nondirected verbal aggressiveness (general shouting, screaming, swearing) 2. Directed verbal aggressiveness (threats against defined persons) 3. Irritability (impatient, easily provoked) 4. Negativism (obstinate, uncooperative, resistant to authority) 5. Dysphoric mood (angry, quick to misinterpret) 6. Socially disturbed behavior (upsetting others, lack of feeling for situations) 7. Physical violence to personnel (kicking, beating, etc.) 8. Physical violence to others, apart from personnel (kicking, beating, etc.) 9. Self-mutilation (scratching own skin, beating himself, burn marks) 10. Physical violence to things (kicking furniture, destroying things) 11. Suicidal thoughts and impulses
item is rated on a scale from 0 to 5. The interobserver reliability of the SDAS has been found to be adequate. A single study assessed violent behavior in postictal psychosis using this scale and indicated excessively aggressive behavior in patients with postictal psychosis [12]. 3. Clinical application for evaluation of postictal behavioral changes There have been very few studies on neuropsychiatric evaluations of patients with PBCs using the quantified inventories described above, because it is difficult to assess behavior during the brief postictal period and PBCs often manifest clinically as mixed features of various psychiatric symptoms. However, cross-sectional as well as longitudinal evaluation is encouraged in certain patients as the findings may reveal clinical characteristics of PBCs, including the time course. There is a single prospective study in which the BPRS was used to assess postictal psychosis in patients with temporal lobe epilepsy [12]. The symptoms were evaluated within 1 week of the seizure and then 1 week and 1 month after the first evaluation point. The results showed that the BPRS scores decreased dramatically 1 week after the initial evaluation, with variation between cases, and the patient subsequently returned to baseline 1 month after the first evaluation. The authors pointed out that the scores did not return to their baseline until 1 month after the seizure despite the appearance of recovery from gross psychotic symptoms. This finding suggests that psychotic symptoms might linger even after apparent recovery. The postictal changes within brain functions may continue subclinically and the PBCs may be due to persistent epileptic discharges, which might explain why postictal psychosis evolves into interictal chronic psychosis in some patients [45]. This finding also indicates that more sensitive neuropsychological batteries could detect subtle behavioral changes even after the apparent disappearance of PBCs. Neuropsychiatric measurement along with various modalities, including functional neuroimaging, could provide clues for understanding the pathophysiology of PBCs. 4. Conclusions Observation of postictal behavior using quantitative evaluation methods has not yet been conducted. Assessment of PBCs with these evaluation methods would be useful for elucidation of the clinical characteristics of PBCs and the classification of some PBC patterns. Further research into the association of PBC patterns with seizure discharges could help to clarify certain neuronal networks leading to behavioral changes not only in patients with epilepsy, but also in those with other psychiatric disorders. Finally, it must be considered that scores obtained directly may not reflect the severity of the psychopathology of the patient. Diagnosis of psychiatric symptoms on the basis of scores sometimes leads to misunderstanding of the patient. The results should be compared between different evaluation periods or patients should be compared with controls. Neuropsychiatric testing becomes helpful when used with the knowledge of its significance and limitations.
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