A Critical and Descriptive Approach to Interictal Behavior with the Neurobehavior Inventory (NBI)

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Epilepsy & Behavior 25 (2012) 334–340

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Epilepsy & Behavior

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A critical and descriptive approach to interictal behavior with the Neurobehavior Inventory (NBI)

Guilherme Nogueira M. de Oliveira a,b,⁎, Arthur Kummer a, Renato Luiz Marchetti c, Gerardo Maria de Araújo Filho d, João Vinícius Salgado a, Anthony S. David e, Antônio Lúcio Teixeira a

a Neuropsychiatric Unit, Neurology Division, School of Medicine, Universidade Federal de Minas Gerais, Belo Horizonte, Brazil b Epilepsy Treatment Advanced Centre (NATE), Felicio Rocho Hospital, Belo Horizonte, Brazil c Department and Institute of Psychiatry, Faculdade de Medicina da Universidade de São Paulo (FMUSP), São Paulo, Brazil d Department of Neurology and Neurosurgery, Universidade Federal de São Paulo (UNIFESP), São Paulo, Brazil e Section of Cognitive Neuropsychiatry, Institute of Psychiatry, King's College London, DeCrespigny Park, London SE5 8AF, UK

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Article history: Purpose: The purpose of this study was to test the psychometric properties of the Neurobehavior Inventory Received 23 July 2012 (NBI) in a group of temporal lobe epilepsy (TLE) patients from a tertiary care center, correlating its scores Revised 21 August 2012 with the presence of psychiatric symptoms. Accepted 23 August 2012 Methods: Clinical and sociodemographic data from ninety-six TLE outpatients were collected, and a neuro- Available online 24 October 2012 psychiatric evaluation was performed with the following instruments: Mini-Mental State Examination (MMSE), structured psychiatric interview (MINI-PLUS), Neurobehavior Inventory (NBI), and Hamilton Keywords: Depression Rating Scale (HAM-D). Temporal lobe epilepsy Interictal behavior Results: Some traits evaluated by the NBI showed adequate internal consistency (mean inter-item correlation Gastaut-Geschwind syndrome between 0.2 and 0.4) and were frequent, such as religiosity (74%) and repetitiveness (60.4%). Principal com- Neurobehavior Inventory ponent analysis showed three factors, named here as emotions (Factor 1), hyposexuality (Factor 2), and un- Psychiatric disorders usual ideas (Factor 3). Depressive symptoms on HAM-D showed a strong association with emotions and Depression hyposexuality factors. When patients with left TLE and right TLE were compared, the former exhibited more sadness (p=0.017), and the latter, a greater tendency toward sense of personal destiny (p=0.028). Conclusion: Depression inﬂuences NBI scoring, mainly emotionality and hyposexuality traits. Neurobehavior Inventory subscales can be better interpreted with an appropriate evaluation of comorbid mood and anxiety disorders. Compromise in left temporal mesial structures is associated with increased tendency toward sad affect, whereas right temporal pathology is associated with increased beliefs in personal destiny. © 2012 Elsevier Inc.Open access under the Elsevier OA license.

1. Introduction alternating behavior with moments of excessive religious and ethical concern and episodes of irritability and temper tantrums were also Unusual behaviors have long been described in epilepsy, especially pointed out by Kraepelin in the early twentieth century [4]. Curiously, in temporal lobe epilepsy (TLE). More than 3000 years ago, the Freud described the contradictory personality of Dostoevsky, who Babylonians reported mystical-religious states in people with epilepsy possibly had TLE [5], alternating periods of uncontrolled irritability, [1]. In the nineteenth century, psychiatrists highlighted frequent and violence with deepened guilt and attempts to follow religious irritability, anger, and rage in people with epilepsy. The concept of and moral codes [3]. “larvate epilepsy” proposed by Morel, and supported by Falret, repre- In the second half of the past century, many authors revisited the sented periodic alternations in the mental state such as aggressive, interictal behavioral changes in epilepsy. Gastaut noted that the emo- manic, and depressive states that could indicate non-convulsive tional intensity, “stickiness”, and hyposexuality were exactly opposite seizure activity [2]. Kraepelin called attention to the meticulousness, to the placidity, unfocussed attention, and hypersexuality shown by slowness, persistence, adhesion, perseveration, and mental stickiness primates following bilateral temporal lobectomy, a condition named present in patients with epilepsy that resulted in very circumstantial Klüver-Bucy syndrome [6,7]. Later, Geschwind noticed that the tenden- speech, a trait that came to be designated as viscosity [3]. The cy of patients with TLE to write extensively (hypergraphia) was associated with affective lability and preoccupation with ethical and religious issues. Thus, interictal behaviors characterized by changes in sexual ⁎ Corresponding author at: Hospital Felício Rocho, Núcleo Avançado de Tratamento behavior (usually hyposexuality), irritability, viscosity (slow thinking, das Epilepsias (NATE), Av. do Contorno, 9530. Barro Preto, 30110‐934 Belo Horizonte MG, Brazil. Fax: +55 31 3514 7294. circumstantial, and detailed speech), religiosity, hypergraphia, and fre- E-mail address: [email protected] (G.N.M. de Oliveira). quent mood swings became known as Gastaut-Geschwind syndrome

[8,9]. It is worth mentioning that some features can also be observed in Descriptive analysis of categorical variables and proportions the periictal period, such as hyperreligiosity and hypergraphia, mainly were calculated and presented. Cronbach's coefficient alpha and mean associated with postictal mania and psychosis [10,11]. inter-item correlations were computed to ascertain NBI total and Though personality study concepts are relevant in the investiga- subscale internal consistency. Non-parametric correlations (Spearman's tion of long‐standing behavioral changes, the overall term “epileptic rho) were calculated between the NBI subscale scores and the HAM-D. personality” is nowadays regarded as obsolete, stigmatizing, and im- Principal component analysis was performed in order to identify precise [4,15], and we preferred the term “interictal behavior” when correlation within the set of traits. Varimax rotation was performed referring to the characteristics of Gastaut-Geschwind syndrome. The to assist interpretation of extracted factors. An adjusted score was at- issue is surrounded by controversy as some studies were unable to tributed to every factor. Each subscale had a weighted score (subscale discriminate a specific syndrome in TLE when compared with other total score multiplied by the factor correlation value). The factor ad- neurological and psychiatric control groups [12–14]. Though classi- justed score was then calculated: sum of factor subscale weighted cally described, the diagnostic hallmarks of the syndrome are not scores divided by the total number of subscales in each factor. For clearly defined and, therefore, subject to much criticism [15]. The comparison of categorical variables between groups, Fisher's exact Neuro-Behavioral Inventory (NBI) [4], an adaptation of the earlier test was performed, and continuous variables were evaluated using Bear–Fedio Inventory (BFI) [16], was introduced to evaluate such as- the Kruskal–Wallis and Mann–Whitney U tests. pects of interictal epileptic behavior (viscosity, emotions, moralism, All tests were performed using SPSS version 15.0 for Windows. A spirituality, and hyposexuality) as well as episodic states that may two-sided p value lower than 0.05 was considered significant for all have clinical relevance (mood instability, irritability, paranoia, and tests. anxiety) and has been translated and adapted to the Brazilian population [17]. The purpose of this study was to evaluate NBI performance 3. Results in a group of TLE patients and to correlate the behavioral characteristics with psychopathology and clinical variables. The sociodemographic and clinical characteristics of the ninety-six outpatients with TLE included in the study are displayed in Table 1. Most of the patients (88.5%) were on more than one antiepileptic 2. Subjects and statistical methods drug (AED). Carbamazepine (62.5%), clobazam (47.9%), lamotrigine (22.9%), clonazepam (21.9%), and topiramate (17.7%), in monotherapy A cross-sectional study was conducted with 96 TLE outpatients. All or in combination, were the most prescribed AEDs. Other AEDs used attended the Epilepsy Clinic of the Neurology Service, Hospital das were valproate (14.6%), phenytoin (14.6%), phenobarbital (12.5%), Clínicas, Universidade Federal de Minas Gerais (UFMG), which is a and oxcarbazepine (6.3%). regional referral service for refractory epilepsy. This service encom- passes around 1000 patients who are referred from general practi- tioners, general physicians, or general neurologists from the whole 3.1. Psychiatric and behavioral features state of Minas Gerais, Brazil. This study was approved by the local ethics committee in accordance with the Declaration of Helsinki. Temporal lobe epilepsy patients had a high frequency of lifetime The inclusion criteria were as follows: diagnosis of TLE according to psychiatric disorders (68.8%) (Table 2). Depression (35.4%) was the the ILAE criteria [18], age of more than 18 years, and capacity to pro- most common psychiatric disorder, while anxiety disorders, as a vide written informed consent for participation in the study. Patients group, (40.6%) were also prevalent. Panic disorder was diagnosed in were excluded if they had severe medical or neurologic diseases other 10 patients (10.4%), agoraphobia in 12 (12.5%), social phobia in 13 than epilepsy, history of previous neurosurgery, and severe cognitive (13.5%), simple phobia in 12 (12.5%), generalized anxiety disorder impairment according to MMSE performance [19]. in 22 (22.9%), and mixed anxiety-depression disorder in 1 (1%) pa- Sociodemographic (age, gender, ethnicity, marital status, employ- tient. Of note, in some patients, more than one anxiety disorder diag- ment situation, and educational level) and clinical information (age at nosis was observed. Suicide risk was present in almost a third (31.3%) onset and duration of the epilepsy, seizure type, seizure frequency, of TLE patients. One patient had epileptic (right temporal seizures) antiepileptic drug regime, MRI, and EEG findings) were collected. and psychogenic non-epileptic seizures recorded during VEEG telem- Data of epileptiform activity on interictal EEG were registered for de- etry. This patient showed no major psychiatric disorder according to scriptive purposes, as this information has limited lateralizing proper- the MINI-PLUS and exhibited only minimum depressive symptoms ties since it can represent propagation from other sites or can be (HAM-D=3 points). Curiously, he had a high NBI total score (49 normal in patients with epilepsy. As only 51 patients (53.1%) were points) and maximum scores (5 points) on persistence and repeti- assessed with VEEG telemetry, we decided to use the mesial temporal tiveness, interest in details, religious convictions, cosmic interests, sclerosis (MTS) diagnosis on MRI as a lateralizing reference. and feelings about sex subscales. He also had high scores (4 points) Psychiatric diagnosis was made according to the Mini Internation- on orderliness and sense of personal destiny subscales. al Neuropsychiatric Interview (MINI) Plus version 5.0.0. [20–22],a NBI total score showed a high Cronbach's alpha (0.9), but a low structured clinical interview that provides diagnosis according to mean inter-item correlation (0.107). Some subscales showed mean the DSM-IV criteria. Hamilton Depression Rating Scale (HAM-D) inter-item correlation lower than 0.2, such as fearfulness, sense of [23–25] was used to measure depressive symptoms. We used the personal destiny, dependency, and happiness. Seriousness showed 24-item HAM-D (total score range: 0–75), which includes helpless- mean inter-item correlation lower than 0.1. Total and subscale inter- ness, hopelessness, and low self-esteem items [25], in order to reduce nal consistencies and frequency of traits in the sample are shown in the weight of the somatic symptoms, increasing its specificity. Table 3. The Brazilian-Portuguese version of the NBI [17] was used to assess the behavioral traits of the Gastaut-Geschwind syndrome. The 3.2. Factor analysis inventory is composed of 100 true or false items (total score range: 0–100), grouped in 20 subscales (5 items in each subscale). For Neurobehavior Inventory's 20 subscales were subjected to princi- subscale scores (total score range: 0–5), 3 or more positive answers pal component analysis (PCA). Correlation values lower than 0.1 were were considered to be indicative of caseness, and a total scale score suppressed. Factorability of the correlation matrix was supported by of 20 or more determined overall caseness, as suggested by the inven- Bartlett's Test of sphericity below 0.001 and Kaiser-Meyer-Olkin Mea- tory developer [4]. sure of Sampling Adequacy of 0.869. 336 G.N.M. de Oliveira et al. / Epilepsy & Behavior 25 (2012) 334–340

Table 1 Table 2 Sociodemographic and clinical characteristics of the study sample. Psychiatric profile in patients with temporal lobe epilepsy (note patients may have more than one diagnosis). Patients (n=96) Psychiatric disorder/symptom and suicidality Patients (n=96) n or mean Proportion (%) or (SD) median (range) n or mean Proportion (%) or (SD) median (range) Gender Male 42 43.8% Any disorder (current) 55 57.3% Female 54 56.3% Any disorder (lifetime) 66 68.8% Age, years 40.7 (10.1) 41 (21–65) Bipolar Disorder (BD) 8 8.3% Ethnic group Major depressive episode (lifetime) 34 35.4% White 47 49% Major depressive episode (current) 27 28.1% Black 10 10.4% Anxiety disorders 39 40.6% “Pardo”a 39 40.6% Obsessive–Compulsive Disorder (OCD) 8 8.3% Educational level, years of study 8.0 (3.7) 8 (0–15) Psychosis 5 5.2% Marital statusb Somatoform disorders 13 13.5% Single 39 40.6% Presence of current suicide risk 30 31.3% Married/stable union 41 42.7% HAM-D 15.2 (11.4) 12 (0–48) Divorced/separate 12 12.5% HAM-D = Hamilton Depression Rating Scale. Widowed 4 4.2% Employment situation Employed 41 42.7% subscales related to viscosity. The hyposexuality factor not only was Unemployed 18 18.8% represented by hyposexuality, anxiety symptoms (fear), seriousness, Retired (age or time of service purposes) 6 6.3% Retired (due to illness) 31 32.3% and somatic complaints, but also showed some association with emo- Seizure type tions factor (sadness and anger) subscales. By the same token, sub- Simple partial 45 46.9% scales of the hyposexuality factor (fearfulness and somatization) Complex partial 91 94.8% were associated with the emotions factor. The unusual ideas factor Partial evolving to secondarily generalized 28 29.2% Localization of epileptiform discharges was diametrically opposed to emotions and hyposexuality factors Right temporal lobe 36 37.5% and was represented mainly by subscales related to spirituality. Left temporal lobe 30 31.3% When spirituality components (religious convictions, cosmic inter- Bilateral temporal lobe 20 20.8% ests, and sense of personal destiny) were analyzed together, only No epileptiform discharges 10 10.4% 22.9% of the patients did not show any of these traits. Hypergraphia Religion b Catholic 54 56.3 showed a weak correlation ( 0.3) with all factors, but was more Protestant 33 34.4 closely related to the unusual ideas factor. Spiritism 4 4.2 Other 1 1.0 Without religion 4 4.2 3.3. Impact of depression and other psychiatric disorders on behavioral Age at onset of epilepsy, years 10.7 (9.6) 9.5 (0–49) aspects of the NBI Duration of epilepsy, years 30.0 (11.7) 29 (3–54) Seizure frequency, seizures per month 6.3 (9.6) 3 (0–60) Seizure free for 6 months or longer 8 8.3% As depression was the most frequent disorder, we analyzed the in- MRI fluence of depressive symptoms (HAM-D) on NBI traits, as depicted in WMTS 11 11.5% Fig. 1. RMTS 40 41.7% Fig. 1 stresses the strong correlation between depression LMTS 35 36.5% (HAM-D) and NBI subscales. Of note, HAM-D was associated with BMTS 10 10.4% AEDs therapy regime (%) the emotions (Factor 1) and hyposexuality (Factor 2) factor subscales, Monotherapy 11 11.5% but not with unusual ideas factor (Factor 3) subscales. Dualtherapy 58 60.4% 3 AEDs 23 24.0% 4 AEDs 4 4.1% 3.4. Psychopathology regarding laterality SD = Standard deviation; MRI = Magnetic resonance imaging; WMTS = Without MTS; RMTS = Right mesial temporal sclerosis; LMTS = Left mesial temporal sclerosis; Patients were divided in four groups regarding laterality of MTS: BMTS = Bilateral MTS; AEDs = Antiepileptic drugs. 40 patients with right MTS (RMTS), 35 with left MTS (LMTS), 10 a “ ” Pardo : mixed race or color (mulato, mestizo). with bitemporal MTS (BMTS), and 11 patients without MTS b One patient did not disclose marital status. (WMTS). Groups were statistically different according to secondary generalization of partial seizures (p=0.012), underrepresented in the RMTS group, present in 5 patients (12.5%), compared to 14 Principal component analysis revealed the presence of 3 main (40%) patients with LMTS, 5 (50%) with BMTS, and 4 (36.4%) patients components with eigenvalues over 1, explaining 35%, 10%, and 6.8% with WMTS. Also, there were differences across groups regarding du- of the variance, respectively. Varimax rotation solution is presented ration of epilepsy (p=0.011), as the WMTS group had a lower mean in Table 4. time since the onset of uncontrolled seizures, mean (SD) of 19.6 Subscales were grouped corresponding to some features of the (15.1) years, in comparison with 29.1 (9.4) years (SD) in RMTS, 33.9 Gastaut-Geschwind syndrome, described here as the following: emo- (11.5) years (SD) in LMTS, and 32 (11) years (SD) in the BMTS tions (Factor 1), hyposexuality (Factor 2), and unusual ideas (Factor group. There were no other significant differences on the 3). Emotions factor (mood, guilt, dependence, sadness, and anger) sociodemographic and clinical variables. accounted for the larger percentage (35%) of the total variance. Inter- When NBI behavioral traits were compared, there were no signif- estingly, the so-called viscosity items (orderliness, interest in details, icant differences across all four groups. However, when patients with persistence, and repetitiveness) were also grouped in the emotions LMTS and RMTS were compared separately, the LMTS group scored factor. Viscosity seems to be a prevalent subtrait in TLE as 70% of significantly higher on sadness (p=0.017) and lower on sense of per- the patients had at least 2 elevated scores in the subscales pertaining sonal destiny (p=0.028). No other significant differences were ob- to viscosity, and only 15% of the patients were negative for all 3 served in this analysis. G.N.M. de Oliveira et al. / Epilepsy & Behavior 25 (2012) 334–340 337

Table 3 Frequency of personality traits and internal consistency of the Neurobehavior Inventory.

Domains (items) Cronbach's alpha Caseness (%) Mean (SD) Median Mean inter-item (range) correlation

Total score 0.925 97.9 52.29 (16.228) 54 (16–85) 0.107 Writing tendency (6,18,53,62,98) 0.527 38.5 2.25 (1.392) 2 (0–5) 0.181 Sense of law and order (19,41,49,75,83) 0.494 74 3.24 (1.288) 3.5 (0–5) 0.170 Religious convictions (13,24,48,94,99) 0.595 74 3.35 (1.361) 4 (0–5) 0.238 Anger and temper (20,25,36,43,91) 0.741 44.8 2.22 (1.736) 2 (0–5) 0.364 Orderliness (5,14,21,42,71) 0.481 63.5 2.78 (1.363) 3 (0–5) 0.161 Feelings about sex (7,10,52,77,84) 0.672 49 2.67 (1.639) 2 (0–5) 0.290 Fearfulness (16,40,57,64,86) 0.465 49 2.59 (1.342) 2 (0–5) 0.150 Feelings of guilt (4,55,61,70,80) 0.537 60.4 2.74 (1.416) 3 (0–5) 0.193 Seriousness (29,45,66,88,100) 0.323 76 3.45 (1.123) 3 (1–5) 0.072 Sadness (33,38,73,85,92) 0.739 38.5 2.01 (1.645) 2 (0–5) 0.363 Emotions (9,23,54,69,89) 0.598 55.2 2.79 (1.514) 3 (0–5) 0.225 Suspicion (12,17,22,34,63) 0.689 41.7 2.09 (1.610) 2 (0–5) 0.307 Interest in details (26,50,58,67,81) 0.532 75 3.43 (1.351) 4 (1–5) 0.169 Cosmic interests (37,46,51,72,76) 0.555 52.1 2.58 (1.491) 3 (0–5) 0.200 Sense of personal destiny (1,11,27,32,97) 0.438 63.5 2.91 (1.290) 3 (0–5) 0.131 Persistence and repetitiveness (35,44,60,78,90) 0.698 60.4 2.90 (1.651) 3 (0–5) 0.316 Hatred and revenge (56,68,82,87,96) 0.668 24 1.49 (1.436) 1 (0–5) 0.291 Dependency (3,15,28,39,93) 0.514 40.6 2.31 (1.300) 2 (0–5) 0.145 Happiness (2,31,59,65,79) 0.475 29.2 1.89 (1.280) 2 (0–5) 0.154 Physical well-being (8,30,47,74,95) 0.601 55.2 2.60 (1.483) 3 (0–5) 0.225

In an attempt to estimate the syndrome frequency, factor adjusted on the translation of the NBI into Brazilian-Portuguese that was ap- scores extracted from PCA were categorized with a split on the medi- plied to 15 patients [17], showing the stability of the scale across an (caseness was defined if factor score was over the median). In this this population. sense, twenty-one patients (21.9%) were negative for all factors, Nowadays, personality experts seem to be more interested on sin- whereas eighteen (18.8%) patients were positive for all 3 factors, gle psychological constructs of limited domain rather than on the de- thirty-five (36.5%) for 2 factors, and twenty-two (22.9%) patients for velopment of global measures of personality. Personality studies 1 factor. None of the patients fulfilled the 20 positive traits, median usually focus on the assessment of the variation across individuals. (range) of 11 (0–19) elevated subscales per patient. Therefore, measures of relationship (correlation coefficients) are used instead of mean differences (analysis of variance). When a 4. Discussion large number of characteristics are measured, it is important to specify accurately each trait separately in groups of highly inter- In our sample, the majority of patients had high scores on the NBI correlated items [26]. According to Briggs and Cheek [26], an optimal (97% had scores over 20 points). The present findings suggest that the level of homogeneity is reached when the mean inter-item correla- syndrome with all 20 traits evaluated by the NBI is rare, as none of the tion is within the 0.2 to 0.4 range. If inter-item correlation is lower patients were positive for all subscales. When the traits were grouped than 0.1, it is unlikely that the total score represents the items' com- in PCA, the presence of all three factors in the same patient was ob- plexity, and if it is higher than 0.5, the items on the scale tend to be served in a minority of the patients, around 20%. An important finding redundant. From this point of view, it is appropriate to suggest that is that the frequency of many traits was similar to the ones reported future research may revise some items with low internal consistency, such as seriousness. Based on the assumption that a “single scale ought to measure a ” “ Table 4 single construct , it is important to take into account that any test Principal component analysis of the 20 subscales from the Neurobehavior Inventory. that measures more than one common factor to a substantial degree yields scores that are psychologically ambiguous and very difficult Subscale Component to interpret” [26]. Thus, the mean pairwise correlation among the 123100 items of 0.107 (range from −0.369 to 0.626) leads to the conclu- Suspicion .760 .103 sion that there is a weak correlation among items, as many presented Emotions .756 .112 .149 a negative correlation. An alpha of 0.93 indicates that this sample of Feelings of guilt .733 .181 items probably correlates around 93% with another sample of items Dependency .726 .186 .107 Sadness .716 .426 −.140 drawn from the same population. However, a mean inter-item corre- Persistence and repetitiveness .710 .125 lation of 0.107 indicates that the items are very disparate. The Anger and temper .698 .392 .188 Neurobehavior Inventory probably measures a construct that is Orderliness .665 .107 broad and polymorphous. One argument supporting this hypothesis Sense of law and order .646 .173 is that there are 20 subscales within the NBI. This would imply that Hatred and revenge .626 .156 Interest in details .521 .193 .253 the NBI total score has limited value. Feelings about sex .107 .712 It is suggested that the characteristics of the Gastaut-Geschwind Seriousness .230 .621 .255 syndrome are manifested primarily in patients with TLE. Bear et al. Fearfulness .452 .563 reported higher sadness, emotionality (emotional intensity), and reli- Physical well-being .487 .523 Religious convictions −.172 .189 .815 gious and philosophical interests in 10 patients with TLE compared to Cosmic interests .302 .703 10 patients with generalized and focal non-temporal epilepsy [27]. Sense of personal destiny .144 −.129 .656 Recently, a study using the BFI stressed that the only different trait Happiness .171 −.443 .492 between TLE patients subjects with psychogenic non-epileptic sei- Writing tendency .153 .267 zures (PNES) was hypergraphia, which was more frequent in TLE 338 G.N.M. de Oliveira et al. / Epilepsy & Behavior 25 (2012) 334–340

0.8 Lesions in the non-dominant temporal lobe were associated with Factor 2 depression initially by Flor-Henry [37]. Subsequently, other studies 0.6 have been devoted to this issue, and linked depression to an epileptic Factor 3 focus on the right hemisphere, while others do not show this association (30–32). For instance, Victoroff et al. found that left temporal 0.4 hypometabolism was associated with depression in patients with partial seizures. However, patients with hypometabolism in the right Factor 1 0.2 temporal lobe also had a history of depression. These authors state that the onset of seizures in the left temporal lobe and the degree of (Spearman's rho) (Spearman's hypometabolism in the temporal lobes were independent risk factors

Correlation with HAM-D 0.0 of depression [38]. Inactivation of the left hemisphere by injection of amobarbital to the left carotid artery can induce crying, pessimistic -0.2 statements, guilt, complaints, and worries about the future [39]. Bear and Fedio [16] also pointed out that patients with right TLE minimized depressive complaints on self-reports, while patients with left TLE Guilt** Destiny Cosmic Anger** Details* tended to exaggerate them. Altshuler et al. described that patients Hatred** Sadness** Religiosity Happiness with left TLE scored higher on self-ratings for depression [40]. Van Emotions** Suspicion** Orderliness** Fearfulness** Hypergraphia Elst et al. investigated the characteristics of the Geschwind syndrome Dependency** Seriousness** Somatization** Law and Order* and Law Hyposexuality** Repetitiveness** with NBI in a group of nine patients with TLE and bilateral hippocam- NBI Total Score** Total NBI pal atrophy in comparison to a group of 14 patients with TLE but with Fig. 1. Correlation of behavioral traits with depressive symptoms according to the normal hippocampal volumes [41]. The group with bilateral hippo- Hamilton Depression Rating Scale (HAM-D). Subscales are displayed in the sequence campal atrophy showed significant reduction in the left amygdala presented in factor analysis (*pb0.05; **pb0.001). (pb0.01), which may explain the tendency of this group to show emotionality, fear, guilt, and sadness. Hence, the findings of the present [12]. Mungas argues that a large percentage of the variation of traits study are in line with the studies that link damage to the left temporal evaluated by the BFI could be explained by the presence of mental dis- lobe to negative thoughts and feelings such as sadness, an important orders and general psychopathology. Hence, the inventory would be symptom of depressive disorder. nonspecific and unable to distinguish TLE patients with the proposed Bear and Fedio described 27 outpatients with TLE (15 with a right syndrome from psychiatric patients [13]. In view of this, the present focus and 12 with left focus) that showed differences on behavioral study highlights the major impact of depression on various features profile according to the laterality of epileptic focus and also when of the Gastaut-Geschwind syndrome, especially the “episodic traits”, compared with patients with neurological disease and asymptomatic such as anger and sadness. For example, sexual interests were controls [42]. These authors described a double dissociation at the influenced by depression, and the analysis of hyposexuality must principal component factor analysis in which the first factor was char- consider the high frequency of depression among these patients. Also, acterized by traits of emotionality (anger, aggression, and sadness), more stable traits, such as viscosity subscales, were associated with most frequently found in patients with right TLE, and an ideational/ depression. Circumstantiality and obsessionalism are characteristics ruminative factor (religion, seriousness, and personal destiny), more observed in some patients without epilepsy in a mood disorders clinic common in left TLE [42]. Our data go on the opposite direction of [28], and we could hypothesize that bidirectional mechanisms the Bear and Fedio study regarding sense of personal destiny, which increase the vulnerability to mood disorders and viscosity, especially was associated with RMTS in the present study [16]. It must be in TLE. Some of these symptoms may be better described by standard highlighted that our study was based on self-rating profiles, whereas psychiatric evaluation, including assessment with instruments as the in the Bear and Fedio study, this difference was observed on rater re- BDI, Brief Psychiatric Rating Scale, or even specific mood instruments ports. Other explanations for this difference may be based on meth- such as the Interictal Dysphoric Disorder Inventory [29–31] or the Neu- odological issues; we used MTS on MRI to determine laterality, rological Disorders Depression Inventory for Epilepsy [32,33].Thus,an while Bear and Fedio used interictal EEG. Another difference is the alternative explanation for so many traits in BFI and NBI is that some number of patients used in each study [16]. Cultural differences of these traits are ‘artifacts’ of underecognized and undertreated de- across countries may have also played a role, and the fact that sense pression and anxiety in TLE. One message for clinicians is that treatment of personal destiny subscale had a low internal consistency (mean for mood/anxiety disorders should be optimal before behaviors are con- inter-item correlation of 0.131) can indicate that this is a fragile considered to be due to enduring personality changes. struct. Regardless of these methodological distinctions, other studies A possible explanation for the dichotomy between the unusual showed the involvement of the right temporal lobe in religious expe- ideas factor (linked with spirituality) and emotions factor (and also riences. Smaller right hippocampus volume was observed in patients hyposexuality factor) may lie on the secondary association with de- with epilepsy with high religiosity on the NBI [43]. Accordingly, a re- pression in the latter group. Consequently, the lack of association of cent study showed a possible lateralizing value of a manual automa- the unusual ideas factor with depressive symptoms can be explained tism usually made by a group of Christians, the Sign of the Cross, by the fact that strong spiritual and religious beliefs may be protective which was present in the ictal period of four patients, all with unilat- against depression [34]. In addition, hypergraphia was associated with eral right mesial TLE [44]. Some authors also report ictal religious ex- the unusual ideas factor, pointing to a possible correlation with spiri- periences linked to epileptic focus in the non-dominant hemisphere tuality. Curiously, many reports point out the religious themes written [45–47]. As personal destiny was associated with spirituality factor by many hypergraphic people with epilepsy [5,10,35]. It is also and more frequent in RMTS in the present study, we can hypothesize plausible that hypergraphia is an isolated component of the syn- that this supports the involvement of right temporal structures in drome, observed only in a few patients. Gastaut-Geschwind syndrome subjective spiritual perception. characteristics are difficult to measure, and some traits are really dif- One important limitation of this study is the absence of a caregiver ferent from pure depression/anxiety and could be better explained rating evaluation. Many patients came from the countryside without by impairment in language function, theory of mind, self-awareness, a close relative (or the relative had a low level of education) which and environmental monitoring related to damage and decreased func- impaired the rating evaluation. The next of kin impressions are need- tional connectivity of mesial temporal structures [36]. ed as individuals with cognitive impairment or even some degree of G.N.M. de Oliveira et al. / Epilepsy & Behavior 25 (2012) 334–340 339 psychopathology have impairment in insight [4]. However, self-rating Acknowledgments instruments have benefits as many caregivers are unaware of the spiritual and religious beliefs of the patients [4]. The conclusion that We are thankful to Mery Natali Silva Abreu for her statistical depression influences NBI scoring is limited by the transversal design support. of the present study, which limits causal relationships. It is possible that some patients with behavioral changes may emphasize negative References aspects of behavior, increasing self‐reports of depressive symptoms. However, considering the high frequency of depression in TLE, as [1] Reynolds EH, Wilson JVK. 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