Depression, anxiety, and clinical history in Spanish-speaking American patients with psychogenic nonepileptic seizures (PNES) compared with Spanish-speaking American patients with epilepsy

Epilepsy & Behavior 102 (2020) 106694

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Clinical Research

Depression, anxiety, and clinical history in Spanish-speaking American patients with psychogenic nonepileptic seizures (PNES) compared with Spanish-speaking American patients with epilepsy Lorna Myers a,⁎, Robert Trobliger a, Marcela Bonafina b, Gonzalo Vazquez-Casals c, Martin Lancman a, Marcelo Lancman a a b c

Northeast Regional Epilepsy Group, United States of America Behavioral Health Department, IACH, Fort Riley, U.S. Department of Defense, United States of America Northwell Health - Glen Cove Hospital, United States of America

a r t i c l e

i n f o

Article history: Received 17 October 2019 Revised 7 November 2019 Accepted 9 November 2019 Available online xxxx Keywords: Psychogenic nonepileptic seizures Epilepsy Hispanic-American, Spanish-speaking Anxiety Depression Sexual trauma

a b s t r a c t Objective: The objective of this study was to compare Spanish-speaking American patients with epilepsy to Spanish-speaking American patients with psychogenic nonepileptic seizures (PNES) on depression, anxiety, and other clinical variables. Background: Research on Spanish-speaking American patients with epilepsy or PNES is relatively infrequent, with only a few studies on psychopathology in these two patient groups. Studies of English-speaking patients indicate that those with PNES present with greater depression and anxiety and report poorer quality of life (QOL) when compared with persons with epilepsy (PWEs). Similarly, although psychological trauma is observed in both groups, those with PNES appear to have more traumatic exposure compared with PWEs. Methods: This is a retrospective study of 74 Spanish-speaking PWEs (49 women, 31 men) and 34 Spanishspeaking patients with PNES (28 women, 4 men) (2004 to 2017). The diagnosis of epilepsy or PNES was confirmed with video-EEG. Demographic and clinical (psychological trauma, history of psychological treatment, etc.) data were collected, and Spanish versions of the Beck Depression Inventory — second edition (BDI-II) and Beck Anxiety Inventory (BAI) were completed by the patients. Results: Patients with PWEs (M = 18.19, SD = 12.89) differed significantly from those with PNES on a measure of depression (BDI-II, (M = 24.12, SD = 11.20); t (92) = − 2.22, p = 0.01). In addition, PWEs (M = 15.76, SD = 14.24) also differed significantly when compared with patients with PNES on a measure of anxiety (BAI, (M = 22.46, SD = 14.02); t (93) = − 2.05, p = 0.02). Significant differences in clinical and demographic data were also noted. Conclusions: Spanish-speaking American patients with PNES were significantly more depressed and anxious and reported greater exposure to sexual trauma as compared with PWEs. Furthermore, patients with PNES tended to report more prediagnosis utilization of mental health services than PWEs. After adjusting for potential linear effects of other predictors (e.g., gender, age, seizure frequency, and psychological trauma), only a reported history of psychological trauma had a linear relationship with a depression score while higher seizure frequency and history of mental health treatment had linear relationships with an anxiety score. © 2019 Elsevier Inc. All rights reserved.

1. Introduction Epilepsy is a disorder of the brain characterized by abnormal neuronal activity [1] with recurrent seizures. Although lifetime rates of psychiatric disorders (10–50% of depressive disorders, 10–44% of anxiety disorders, and 15–40% of personality disorders) in persons with epilepsy are lower than in persons with psychogenic nonepileptic seizures ⁎ Corresponding author at: Northeast Regional Epilepsy Group, 820 Second Avenue, Suite 6C, New York, NY 10017, United States of America. E-mail address: [email protected] (L. Myers).

https://doi.org/10.1016/j.yebeh.2019.106694 1525-5050/© 2019 Elsevier Inc. All rights reserved.

(PNES), such disorders are higher than in the general population [2]. Depression and anxiety are the two conditions most frequently reported as psychiatric comorbidities in epilepsy [3]. Psychogenic nonepileptic seizures are paroxysmal events that resemble epileptic seizures in appearance but lack electrophysiological correlates or clinical evidence for epilepsy. Instead, psychological antecedents (e.g., life adversities) and psychiatric comorbidities are typically observed in those with PNES. Elevated rates of depressive disorders (57–85%), anxiety disorders (11–50%), posttraumatic stress disorder (PTSD) (35–49%), somatic symptoms, and related disorders including pain syndromes (22–84%), dissociative disorders (22–91%), and

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L. Myers et al. / Epilepsy & Behavior 102 (2020) 106694

personality disorders (10–86%) have been identified as comorbidities in PNES [2]. While epilepsy and PNES are clearly different in etiology, they do share some similarities including the secondary effects of living with seizures (e.g., concerns about unexpected seizures, loss of driving privileges, and independence) which can evidently contribute to a perceived lower quality of life (QOL) in both groups (although, surprisingly, those with epilepsy tend to report somewhat higher QOL scores) [4]. Additionally, psychological trauma and other life adversities have been identified both in PNES [5,6] and epilepsy [7], although those with PNES appear to have greater traumatic exposure [8] and, specifically, more commonly have experienced some form of sexual trauma. The Hispanic population of the United States is estimated to be 59.9 million [9]. Hispanics in the US, regardless of their immigration status, have been identified as a high-risk group for depression and other mental illnesses [10]. When Spanish-speaking Hispanic persons with epilepsy (PWEs) were compared with American-born English-speaking PWEs, the former reported greater depression and a lower QOL on seizure worry [11]. Furthermore, the prevalence of serious psychological distress (SPD) in Hispanic PWEs has been reported to be higher than in non-Hispanic white adults and non-Hispanic black adults [12]. To the best of our knowledge, the present study is the first to compare Spanish-speaking American PWEs to Spanish-speaking American patients with PNES on depression, anxiety, and other clinical factors. We hypothesized that both samples would demonstrate elevations on clinical variables (e.g., depression, anxiety) but that persons with PNES might present with higher rates of depression, anxiety, and exposure to psychological trauma. 2. Method This is a retrospective study of 74 (46 women, 28 men) consecutive “Spanish speaking” patients diagnosed as having epilepsy (2004 to 2017) and 34 (29 women, 5 men) consecutive “Spanish speaking” patients diagnosed as having PNES (2004 to 2017) who underwent neuropsychological testing. All patients required formal testing in Spanish conducted by a bilingual Spanish-speaking neuropsychologist (GV, MB, LM) using a validated Spanish language battery of tests because they were not fluent in English and therefore testing them in that language would have produced equivocal results. These patients were evaluated at the Northeast Regional Epilepsy Group, an epilepsy program that serves New York and New Jersey with 15 hospital epilepsy monitoring units. The diagnosis of epilepsy or PNES was confirmed using video-EEG that was interpreted by a fellowship-trained epileptologist. Neuropsychological testing was requested when the referring physician was seeking to further characterize the patients' cognitive or diagnostic condition or when a patient reported concerns about his/her cognitive functioning. Patients were excluded from this study if their intellectual quotient (IQ) was less than 70 because this would result in difficulties understanding the self-report measures being administered and if they were dually diagnosed as having epilepsy and PNES. Consequently, the initial number of 121 patients with epilepsy was reduced to 74 because 38 earned an IQ of less than 70 and 9 were dually diagnosed as having epilepsy and PNES. As for patients with PNES, the initial number of 37 was reduced to 34 because 3 earned an IQ of less than 70. Demographics (age, education, country of origin) and clinical data (age of onset; trauma (yes/no) and trauma type: sexual, physical or other; age of first trauma; seizure frequency; and number of current antiepileptic drugs being taken) were included. Seizure frequency was calculated as “seizures per day”. For example, one seizure per week would translate into 1/7 (0.14), one seizure per month would translate into 1/30 (0.03), and 3 seizures per week would translate into 3/7 (0.43). Patients' psychiatric histories and other personal and clinical data were initially obtained from an intake form that patients were asked to fill out prior to meeting with the neuropsychologist. These responses were further

explored during the neuropsychological intake and testing. Neuropsychological testing was conducted on an outpatient basis. The following measures were administered as part of the standard Northeast Regional Epilepsy Group neuropsychological battery: the Spanish language versions of the Beck Depression Inventory — second edition (BDI-II) [13,14] and the Beck Anxiety Inventory (BAI) [15]. The BDI-II is a 21-item self-report multiple-choice measure that is used to evaluate depressive symptomatology in individuals ranging in age from 13 to 80 years. Scores are interpreted in the following manner: Minimal, 0–13; Mild, 14–19; Moderate, 20–28; and Severe, 29–63. The BAI is a self-report measure of anxiety [15]. This inventory is a 21-question self-report multiple-choice inventory used to assess anxiety the day of and up to 7 days prior to being answered. The BAI scores are interpreted in the following manner: Minimal, 0–7; Mild, 8–15; Moderate, 16–25; and Severe, 26–63. Institutional review board approval for an anonymous archival record review was obtained with removal of nonrelevant PHI (Copernicus IRB NRE1-11-155). 3. Analysis A chi-square test of independence was performed on the relation between diagnosis (epilepsy or PNES) and the presence of trauma histories (sexual or nonsexual) and participation in psychiatric/psychological treatment. An independent-samples t-test was conducted to compare the total raw scores from the BDI-II and BAI in patients with PNES and in those with epilepsy. In order to determine if any variability in anxiety (BAI) and depression (BDI-II) scores could be explained by the variability in any of the following factors: conditions (epilepsy/PNES), gender (female/male), reported exposure to psychological trauma (yes/no), psychological treatment (yes/no), age, years of education, age of onset, duration, antiepileptic drugs (yes/no), and seizure frequency, the steps described below were taken. A test of the normality of estimated residuals via Kolmogorov– Smirnov and Shapiro–Wilk tests was used and revealed slight deviations from normality. As a result, the decision was made to use bootstrap based on 1000 independent bootstrap samples whenever determining statistical significance of the predictors in a given linear model. Next, in order to develop the “optimal” linear model for the dependent variable, we adopted a forward stepwise selection. Forward stepwise selection starts with the intercept only and then adds the most statistically significant predictor to the next model only if there are any statistically significant predictors left. Once the “optimal” linear model was finalized, it was used for inference. Throughout the analysis, the significance level of 5% was used. 4. Results In the epilepsy sample, mean age was 51.95 ± 15.68 years and years of education was 11.83 ± 2.69. Mean age of epilepsy onset was 21.74 ± 17.41 years. In the PNES sample, mean age was 54.29 ± 12.29 years and years of education was 10.38 ± 4.00. Mean age of PNES onset was 32.93 ± 15.72 years. There was no significant difference between samples on age at the time of assessment, but there were significant differences on duration of seizure disorder, age of onset, and education. Mean duration of epilepsy (M = 28.14, SD = 15.9 years) was greater than in those with PNES (M = 20.15, SD = 13.9 years; t (95) = 65, p = 0.00). Mean age of epilepsy onset (M = 21.74, SD = 1.41) was younger than for those with PNES (M = 32.93, SD = 15.72; t (94) = 70, p = 0.00). Mean education of PWEs (M = 11.9, SD = 2.69) was greater than in those with PNES (M = 10.38, SD = 3.94; t (95) = 16, p = 0.01). Patients with epilepsy (M = 0.13, SD = 0.41) and those with PNES (M = 0.17, SD = 0.31) did not differ significantly on seizure frequency

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Table 1 Demographic and clinical data for two samples of Spanish-speaking American (with epilepsy and with PNES) patients.

Age Education Mental health treatment (yes/no) Sexual trauma (yes/no) Nonsexual trauma (yes/no) Age of first trauma Duration of seizure disorder Seizure frequency AEDs (lifetime) BDI-II BAI

Patients with epilepsy (n = 74) Mean (SD)

Patients with PNES (n = 34) Mean (SD)

Significance p b 0.05

51.95 (15.68) 11.83 (2.69) 27/47 5/69 23/51 16.3 (12.63) 28.14 (15.9) 0.13 (0.41) 3.32 (2.3) 18.19 (12.89) 15.76 (14.24)

54.29 (12.29) 10.38 (4.00) 23/11 10/24 14/20 9.67 (7.72) 20.15 (13.9) 0.17 (0.31) 2.24 (2.03) 24.12 (11.20) 22.46 (14.02)

0.4 0.01⁎ 0.002⁎ 0.00⁎ 0.30 0.03⁎ 0.00⁎ 0.32 0.01⁎ 0.01⁎ 0.02⁎

Antiepileptic drugs (AEDs). ⁎ = p b 0.05.

(t (94), p = 0.32). As could be expected, patients with epilepsy (M = 3.32, SD = 2.3) differed significantly from those with PNES on the number of AEDs prescribed (M = 2.24, SD = 2.03; t (104) = 9.81, p = 0.01) (Table 1). Regarding country of origin, the epilepsy sample originated from a total of 14 countries (plus Puerto Rico), and the PNES sample originated from a total of 9 countries (plus Puerto Rico) Table 2. Patients in both samples reported experiencing traumatic events, including sexual and nonsexual trauma. However, histories of sexual trauma were significantly more frequent in patients with PNES than in PWEs (χ2 (32df, N = 108) = 9.99, p b 0.002). No significant differences were found with regard to nonsexual trauma between the groups (χ 2 (32df, N = 108) = 1.05, p b 0.30). The reported age of the first experienced psychological trauma was much younger in those with PNES (M = 9.67, SD = 7.72) than in PWEs (M = 16.3, SD = 12.63; t (39) = 1.99, p = 0.03). Patients with PNES (27/74) differed significantly from PWEs (23/34) on participation in mental health treatment (χ2 (1df, N = 108) = 9.09, p b 0.002) with the first group, not surprisingly, reporting much higher rates of psychological/psychiatric treatment (Table 1). On psychological measures, there was a significant difference on the depression scores (BDI-II) between PWEs (M = 18.19, SD = 12.89) and those with PNES (M = 24.12, SD = 11.20; t (92) = −2.22, p = 0.01). Patients with epilepsy (M = 15.76, SD = 14.24) also differed significantly when compared with patients with PNES (M = 22.46, SD = 14.02; t (93) = −2.05, p = 0.02) on a measure of anxiety (Table 1). After adjusting for potential linear effects of other predictors, only psychological treatment and seizure frequency had a linear relationship with the BAI score and could partially explain the variability in the BAI.

Therefore, after adjusting for the potential effects of other predictors, patients who reported being in psychological treatment at some time and those with more frequent seizures tended to have higher BAI scores. The estimated model exhibited satisfactory predictive ability explaining 30.4% of variability in BAI scores on a new, independent data set (adjusted R-square = 0.304) (Table 3). Subsequently, after adjusting for potential linear effects of other predictors, a reported history of psychological trauma was the only one that had linear relationship with the BDI-II score. After adjusting for potential effects of other predictors, patients who reported psychological trauma in their life tended to have higher BDI-II scores. However, the estimated model exhibited very low predictive ability as it only explained 7.7% of BDI-II variability in a new, independent data set (adjusted R-square = 0.077) (Table 4).

5. Discussion To the best of our knowledge, this is the first study that compares Spanish-speaking American PWEs to Spanish-speaking American persons with PNES on measures of depression, anxiety, and other clinical factors. Cross-cultural studies can potentially contribute useful information regarding the universality and particularity of mental health and clinical variables in disorders such as PNES or epilepsy.

Table 3 Bootstraps for coefficients (BAI). Model

B

Bootstrap Bias

Std. error

p-Value (2-tailed)

Lower

Upper

10.173 15.430

−0.086 −0.173

1.881 2.931

0.001 0.001

6.691 9.515

14.265 20.929

7.796

1.089

4.864

0.032

1.201

21.869

Table 2 Country of origin for the epilepsy and PNES samples.

Argentina Bolivia Chile Colombia Costa Rica Cuba Dominican Republic Ecuador El Salvador Guatemala Mexico Panama Paraguay Peru Puerto Rico Venezuela Missing Total

Epilepsy

PNES

1 1 1 12 1 3 12 16 1 1 3 1 0 3 13 1 4 70

0 0 0 4 1 0 9 4 1 1 2 0 2 0 7 2 1 33

1

(Constant) Psychological treatment Seizure frequency

95% confidence interval

Table 4 Bootstraps for coefficients (BDI-II). Model

1

(Constant) Trauma

B

17.073 7.517

Bootstrap Bias

Std. error

p-Value (2-tailed)

−0.050 0.232

1.534 2.581

0.001 0.004

95% confidence interval Lower

Upper

14.157 2.667

20.019 12.840

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L. Myers et al. / Epilepsy & Behavior 102 (2020) 106694

An examination of the samples' reported countries of origin revealed they were generally comparable with a diverse representation from South and Central America and the Caribbean in both groups. The relative similarity in both samples is significant because inhabitants of diverse Latin American countries can differ notably in culture, race, ethnicity, and even dialects. Both samples were also similar with regard to age. There was, however, a significant difference in education with the PWE sample having completed more years of education on average. Since nearly 50% of PWEs experienced the onset of their seizure disorder during school year ages and only 18% of persons with PNES experienced their seizure onset in school year ages, it is unlikely that the seizure disorder itself resulted in these differences. It might be speculated that psychiatric comorbidities and other life adversities in those with PNES contributed to this finding, but determining this extends past the scope of this project. As for seizure characteristics, the samples did not differ in terms of seizure frequency, but the PWE sample did present with much younger onset ages as compared with the PNES sample. Comparisons of Englishspeaking PNES and epilepsy samples have resulted in similar findings regarding equivalent seizure frequency yet differing ages of onset [8]. Furthermore, a recent Colombian study also reported later onset in a PNES-alone sample as compared with a dually diagnosed PNES/epilepsy sample [16]. As for utilization of psychological or psychiatric treatments, the samples differed significantly, with the PNES sample reporting much higher utilization rates of mental health services, a finding that is not surprising considering that this disorder is often accompanied by other psychiatric ailments. Also, not unexpectedly, the epilepsy sample had been prescribed a significantly higher number of AEDs in their lifetime as compared with the PNES sample. For the most part, higher numbers of psychological traumatic events have been reported in PNES samples than in PWE samples, although trauma in epilepsy is not an uncommon finding. Alper et al. [17] first reported a notable frequency of childhood sexual abuse in patients with PNES compared with that in patients with complex partial epilepsy. Along similar lines, Duncan and Oto [18] found that nearly 25% of patients with PNES presented with a history of sexual abuse and that 32% of subjects reported experiencing either sexual abuse, physical abuse, or combined types of abuse. However, although Arnold and Privitera [19] found that the experience of psychological trauma was an important factor in the development of PNES, they did not find that sexual trauma alone was significantly associated with the development of PNES. Moreover, after Brown and Reuber [20] reviewed over 100 studies, they too could not definitively confirm the significance of psychological trauma in the development of PNES. Despite the still uncertain link between psychological trauma and the development of PNES, most PNES samples tend to present with a considerable history of traumatic or adverse experiences [21]. Furthermore, a review on diverse types of functional neurological disorders (FND) identified an association between life adversities and childhood or adult abuse with an increase in the risk of FNDs [22]. With regard to a Hispanic sample, in a recent Argentinian long-term study of PNES, nearly all respondents reported experiencing some form of psychologically traumatic and/or adverse life event, including sexual and nonsexual abuse and trauma [23]. Therefore, it is not all that surprising that patients in the two HispanicAmerican samples of this current study reported experiencing sexual and nonsexual traumatic events. However, reports of sexual trauma were clearly more frequent in the PNES sample than in the epilepsy one. In addition, the age when the first traumatic event occurred was significantly younger for the PNES sample. These differing rates in psychological trauma have also been reported in studies with Englishspeaking and French-speaking samples comparing adults with PNES with PWEs [8,24]. Although the exact role that sexual trauma plays in PNES is still unclear, research continues to indicate that there are

significantly higher rates of this kind of trauma in patients with PNES than in the general population and in those with epilepsy. Reports consistently show that rates of comorbid psychiatric conditions in PNES are especially elevated. Depressive disorders (57–85%) and anxiety disorders including panic disorder (11–50%) are frequently observed in patients who are diagnosed as having PNES [2]. A review by Kanner et al. [25] estimated a prevalence of depression in PNES somewhere between 21% and 60%. However, existing reports [3,26,27] also suggest an increased prevalence of depression and anxiety in PWEs as compared with healthy controls. Despite this, it has been reported that rates of psychiatric disorders in epilepsy are lower than in PNES [4,28–31]. With respect to psychiatric comorbidities in a Hispanic sample, an Argentinian study compared a PNES sample with a drugresistant epilepsy sample on psychiatric comorbidities. It was reported that the first group had higher rates of anxiety [32]. In our present study, our Spanish-speaking PNES sample also exhibited significantly higher scores on a self-report inventory of anxiety as compared with the epilepsy sample. In fact, 68% of the respondents with PNES scored in the moderate to severe range of anxiety while 47% of the respondents with epilepsy scored in the same range. Additionally, patients who reported being in psychological treatment prior to the assessment and those with more frequent seizures tended to have higher BAI scores. A higher frequency of seizures could increase anxiety or vice versa since the experience of heightened anxiety could lead to more seizures. On the other hand, it is also possible that anxiety predated the initiation of psychotherapy and has continued or even increased as a result of this new disruptive health condition. Unfortunately, neither of these issues can be definitively answered by this manuscript as it extends beyond the scope of the study. Consistent with the research discussed above, in our present study, the Spanish-speaking PNES sample also exhibited significantly higher scores on a self-report inventory of depression as compared with a Spanish-speaking epilepsy sample. In fact, 65% of the respondents with PNES scored in the moderate to severe range of depression while 36% of the respondents with epilepsy fell in the same range. These results are consistent with results from other studies, including ones that have reported the prevalence rates of depressive disorders in adults with PNES ranging from 21 to 60% [33,34]. Additionally, patients reporting a history of psychological trauma tended to have higher scores on a measure of depression. Associations between retrospective reports of sexual or physical childhood abuse and comorbid mood and posttraumatic disorders have been described [35,36]; the sample in this study would appear to be consistent with those reports. As with all studies, there are some limitations to note in this particular study. Primarily, this study did not include a measure of acculturation that could have revealed important differences between both samples of Spanish-speaking, Hispanic-Americans. However, considering that language is a major factor in acculturation, that all patients required neuropsychological testing in Spanish suggests that, as a whole, they were comparable in sharing a lower level of acculturation. Future studies might be improved by including a formal assessment of acculturation, documentation status, and social economic status. Also, because the participants in our sample are from a tertiary epilepsy program, this could result in our PNES sample not being fully representative of patients with PNES who never reach a tertiary setting. In those patients, a lack of chronicity might produce differences on measures of anxiety and depression. Another important limitation is that this study relied on self-report inventories as well as on self-report of historical data. Walsh and Reuber [37] reviewed 34 studies that reported on separate adult epilepsy and PNES samples that used a validated measure of depression. They found that patients with PNES demonstrated a higher prevalence of depression than patients with epilepsy. However, the difference between both patient groups was more pronounced when the study used a self-report measure, such as the ones used in this present study, than when an independent clinical diagnosis was made by a professional. With this in mind, there is the obvious concern

L. Myers et al. / Epilepsy & Behavior 102 (2020) 106694

for potential recall bias and under- or overreporting of symptomatology. Future studies might use prospective data collection from more than one source and also evaluate other variables that could impact mental health (e.g., socioeconomic status and immigration status). Moreover, the inclusion of measures of the presence and severity of PTSD, dissociation, and selected personality variables or styles could potentially shed additional clarification about the role of trauma in the production and perpetuation of depressive and anxiety symptoms. In conclusion, the present study examined two samples of Spanishspeaking Hispanic-American patients: one with PNES and the other with epilepsy. Significant differences were identified between the two, with those with PNES exhibiting greater rates of sexual trauma, depression, anxiety, and utilization of mental health services. As for the PWE sample, a significantly longer duration of the seizure disorder and higher lifetime rates of AEDs were noted. These findings are consistent with existing studies that have examined English-speaking PNES and epilepsy samples. Similarly, these are also consistent in some respects with research findings in Latin American PNES samples. This type of ethnic study helps elucidate characteristics found in Hispanic-American (immigrant) patients with PNES as compared with those in PWEs which can assist in identifying the particular versus the universal features in this disorder and in epilepsy.

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Declaration of competing interest [24]

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Relevant ethical guidelines regulating research involving human participants were followed throughout the project. All data collection, storage, and processing were done in compliance with the Helsinki Declaration. The authors have no disclosures that could be interpreted as conflicts of interest.

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