Epilepsy & Behavior 37 (2014) 210–214
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Panic attack symptoms differentiate patients with epilepsy from those with psychogenic nonepileptic spells (PNES) Rick Hendrickson a,⁎, Alexandra Popescu a, Ronak Dixit b, Gena Ghearing a, Anto Bagic a a b
University of Pittsburgh, Department of Neurology, Pittsburgh, PA, USA University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
a r t i c l e
i n f o
Article history: Received 12 May 2014 Revised 20 June 2014 Accepted 22 June 2014 Available online xxxx Keywords: Psychogenic nonepileptic spells Psychogenic seizures Epilepsy Panic attack Anxiety
a b s t r a c t Psychogenic nonepileptic spells (PNES) are frequently challenging to differentiate from epileptic seizures. The experience of panic attack symptoms during an event may assist in distinguishing PNES from seizures secondary to epilepsy. A retrospective analysis of 354 patients diagnosed with PNES (N = 224) or with epilepsy (N = 130) investigated the thirteen Diagnostic and Statistical Manual—IV-Text Revision panic attack criteria endorsed by the two groups. We found a statistically higher mean number of symptoms reported by patients with PNES compared with those with epilepsy. In addition, the majority of the panic attack symptoms including heart palpitations, sweating, shortness of breath, choking feeling, chest discomfort, dizziness/unsteadiness, derealization or depersonalization, fear of dying, paresthesias, and chills or hot flashes were significantly more frequent in those with PNES. As patients with PNES frequently have poor clinical outcomes, treatment addressing the anxiety symptomatology may be beneficial. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Psychogenic nonepileptic spells (PNES) are behavioral events of psychological origin that resemble seizures caused by epilepsy but are not due to neurological or other medical disorders. It has been estimated that approximately 20 to 30% of patients referred to epilepsy centers have PNES [1–3]. Patients with PNES have variable but often poor outcomes [4–8]. The intractability of PNES is likely multifactorial, including an average of 7 years before accurate diagnosis [9], comorbid personality disorders [10,11], duration of illness [12], history of abuse [13,14], as well as frequently coexisting depression and anxiety [15]. A 2005 update on treatments for patients with PNES [16] noted that the majority of the literature consisted of class IV reports (case reports or case series) with a limited number of class III reports. Several of the more promising studies [17–19] employed cognitive–behavioral therapy (CBT) interventions. According to Goldstein et al. [17], CBT views PNES as characterized by a “vicious circle of behavioral, cognitive, affective, physiological and social factors.” What a patient experiences during PNES may include cognitions and emotions along with physiological symptoms, which could be incorporated as part of CBT treatment. As indicated by Watson and colleagues [20], there is evidence that the subjective PNES experience is different from an epileptic seizure. Yet, there is little evidence in the literature that illuminates the patients' actual experience in PNES. People with epilepsy may have prodromal ⁎ Corresponding author at: University of Pittsburgh Epilepsy Center, 810 Kaufmann Building, 3471 Fifth Avenue, Pittsburgh, PA 15213, USA. Tel.: +1 412 648 8877. E-mail address: [email protected] (R. Hendrickson).
http://dx.doi.org/10.1016/j.yebeh.2014.06.026 1525-5050/© 2014 Elsevier Inc. All rights reserved.
symptoms of fear, heart palpitations, diaphoresis, shortness of breath [21], paresthesias, nausea, chest discomfort, fear of dying [22], derealization, concerns of losing control, and tremors [23] that are characteristic of a panic attack. Similarly, patients with PNES may report symptoms reflective of a panic attack with their episodes. Vein and colleagues [24] found a group of patients with PNES who endorsed symptoms classic for a panic attack as typical of their paroxysmal event including dyspnea, palpitations, sweating, hot/cold flashes, trembling/shaking, chest pain, dizziness, abdominal distress, feeling of unreality, faintness, paresthesias, as well as fear of going crazy or doing something uncontrolled at a comparable level as another group diagnosed with panic attacks. Because of these similarities, it is not surprising that some patients with epilepsy [25,26] were initially misdiagnosed as having panic attacks. The available literature on panic symptoms in PNES is limited. One study [27] consisting of a medical review of patients with PNES found a high proportion of panic attack symptoms in adolescents but not in adults. However, this was a retrospective record review, and the patients were not specifically questioned about symptoms characteristic of a panic attack. Another study [28] assessing a select number of panic attack symptoms found that these were more common in patients with PNES compared with those with epilepsy. Our study evaluated panic attack symptomatology in patients with PNES and in those with epilepsy. The thirteen criteria for a panic attack from the Diagnostic and Statistical Manual—IV-TR (DSM-IV-TR) [29] including heart palpitations, sweating, shaking, shortness of breath, choking feeling, chest discomfort, stomach distress, feeling dizzy/ unsteady, derealization or depersonalization, fear of losing control, fear of dying, paresthesias, and chills or hot flashes were assessed for
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
each patient. It was hypothesized that patients with PNES would report an overall higher number of total panic symptoms compared with those with epilepsy. In addition, we hypothesized that individuals with PNES would endorse a greater number of the majority of the panic attack symptoms. However, it was anticipated that there would be no difference between patients with PNES and those with epilepsy for the shaking and stomach distress symptoms. Increasing our understanding of the actual PNES experience may assist in formulating an individualized treatment plan leading to better outcomes.
211
Table 1 Demographic information for the 2 groups in the study. Statistically significant differences between the groups were found for sex and age at spell/seizure onset but not for level of education.
Group with PNES Group with epilepsy a b
Total
Femalea
Average education
Age at spell onsetb
224 130
167 (74.6%) 61 (46.9%)
12.4 years 12.9 years
30.6 25.7
p b 0.001. p b 0.002.
2. Methods For this study, we reviewed the medical records of 849 patients who underwent video-EEG monitoring at the University of Pittsburgh Medical Center's Epilepsy Monitoring Unit from 2006 to April 2011 and participated in either Neuropsychological or Psychological Testing as well as were interviewed for panic attack criteria. This study received approval by the University of Pittsburgh Institutional Review Board. Patients were excluded if they had an unclear diagnosis (e.g., no typical spells captured during the evaluation), episodes secondary to another physiological etiology (e.g., sleep disorder or migraines), or a diagnosis of both epilepsy and PNES. Additionally, patients were not included if English was not their first language or if they had a diagnosis of mental retardation. Many of these patients were included in an earlier study of medical comorbidities in PNES [30]. After the above exclusions, we identified 354 patients who were classified into the group with “PNES” or the group with “epilepsy” based on their video-EEG diagnosis. All patients with PNES had a typical event with an alteration in their awareness. None of those with PNES had epileptiform abnormalities during their video-EEG monitoring. We collected the following demographic variables: sex, education, and age at seizure/spell onset. As part of the clinical interview, patients were asked if they experienced each of the thirteen DSM-IV-TR panic attack symptoms: palpitations, pounding heart, or accelerated heart rate; sweating; trembling or shaking; sensations of shortness of breath; feeling of choking; chest pain or discomfort; nausea or abdominal distress; feeling dizzy, unsteady, lightheaded, or faint; derealization (e.g., feelings of unreality) or depersonalization (e.g., being detached from oneself); fear of losing control or going crazy; fear of dying; paresthesias (e.g., numbness or tingling sensations); and chills or hot flashes as part of their “seizures.” The panic attack symptoms could occur shortly before the “seizure,” during the event, or immediately afterwards. Symptoms could always or sometimes accompany their “seizures.” If symptoms happened only rarely or at other times outside their episodes, those were not included. The main emphasis was on the patients' experiences, although some individuals related being told about their symptoms after they had lost awareness (e.g., “I pass out and they say I shake”), which were included as their endorsement for this study. Face-to-face clinical interview of the panic attack symptoms was chosen as this method is presumably more accurate than self-report via tests or questionnaires. The data were coded and entered into SPSS 21. Differences between the group with PNES and the group with epilepsy were examined using either the Mann–Whitney U or the X2 analysis as appropriate. In the current study, we investigated how well each of the thirteen panic attack symptoms along with the total number of symptoms reported during a “seizure” distinguished patients with PNES from those with epilepsy. 3. Results Of the 224 patients in the group with PNES, 74.6% were female. This was a statistically significant difference (p b 0.001; Table 1) from the 130 patients in the group with epilepsy, of whom 46.9% were female. There was also a statistically significant difference (p b 0.002) for average age at “seizure” onset between 30.6 for the group with PNES and
25.7 for the group with epilepsy (Table 1). There was no statistically significant difference for education level between the group with PNES (12.4) and the group with epilepsy (12.9) (Table 1). Table 2 shows the number of each of the panic attack symptoms endorsed by both groups. Patients with PNES reported an average of 6.4 panic attack symptoms, which was significantly greater than an average of 3.4 symptoms in the group with epilepsy (p b 0.001). One hundred eighty-five (82.6%) of the individuals with PNES endorsed four or more panic attack symptoms, which were significantly greater than those of the 45 (34.6%) patients with epilepsy (p b 0.001; Table 3). The presence of four or more symptoms provided a sensitivity of 82.6% (Fig. 1) and a specificity of 65.4% (Fig. 2). Using a cutoff score of five or more also resulted in a good classification between the two groups as this was endorsed by 158 (70.5%) of the group with PNES versus 34 (26.2%) of the group with epilepsy (p b 0.001; Table 3). Using the presence of five or more symptoms for PNES showed a lower sensitivity of 70.5% (Fig. 1) but an increased specificity of 73.84% versus the four or more cutoff (Fig. 2). Although only 26 (20.0%) of the patients with epilepsy indicated six or more panic symptoms, this also was lower compared with 134 (59.8%) in the group with PNES (p b 0.001; Table 3). Similarly, the sensitivity for six or greater symptoms diminished to 59.8% (Fig. 1); however, the specificity increased to 80% (Fig. 2). Thus, increasing the number of panic attack symptoms from four to six sacrifices sensitivity in exchange for enhanced specificity. Fig. 3 provides a side-by-side comparison of the number of panic attack symptoms reported by the two groups, which was statistically significant for each of the above cutoff scores (p b 0.001). As mentioned in the results above, by increasing the minimum number of panic attack symptoms endorsed by patients with PNES and those with epilepsy, specificity increases, but sensitivity falls. This is best illustrated on a receiver operating characteristic (ROC) curve (Fig. 4). Each point represents a cutoff number of panic attack symptoms that a patient must have in order to be diagnosed with PNES, and each cutoff point has an associated sensitivity and specificity. The point with the highest sensitivity and specificity (i.e., the lowest 1—specificity) is considered the optimal cutoff number, and, on an ROC curve, this point lies closest to the top-left corner. In this case, both point 4 and point 5 lie near the top-left corner, but point 4 is marginally closer. Using either Table 2 Number of panic attack symptoms endorsed by each group. Number of symptoms
Group with PNES
Group with epilepsy
0 1 2 3 4 5 6 7 8 9 10 11 12 13
2 4 19 14 28 23 26 36 24 17 14 11 4 2
5 31 25 24 11 8 7 7 4 5 2 0 0 1
212
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
≥ 4 Panic Attack Symptoms Specificity
Table 3 Chi-square analysis comparing the group with PNES and the group with epilepsy showed that patients with PNES were much more likely to endorse 4 or more panic attack symptoms than those with epilepsy. ≥5 symptoms
≥6 symptoms
185 45
158 34
134 26
⁎ p b 0.001.
80 70 60
Percent
Group with PNES⁎ Group with epilepsy
≥4 symptoms
90
50 40 30
four or five as a cutoff number of symptoms results in an acceptable sensitivity (82.6% or 70.5%, respectively) and specificity (65.4% or 73.8%, respectively). Using a cutoff of six symptoms sacrifices sensitivity (59.8%) greatly, as fewer patients with PNES have six or more panic attack symptoms, and point 6 lies farthest from the top-left corner. Analysis of these data (Table 4) revealed that the group with PNES reported significantly more symptoms of heart palpitations (p b 0.001); sweating (p b 0.001); shortness of breath sensations (p b 0.001); feeling of choking (p b 0.001); chest pain or discomfort (p b 0.001); feeling dizzy, unsteady, lightheaded, or faint (p b 0.001); derealization or depersonalization (p b 0.001); fear of dying (p b 0.001); paresthesias (p b 0.001); and chills or hot flashes (p b 0.001). By contrast, there was no difference between the two groups (Table 4) for the symptoms of trembling or shaking, nausea or abdominal distress, and fear of losing control or going crazy. 4. Discussion This study has shown that the presence of panic attack symptoms can provide a useful tool in differentiating patients with PNES from those with epilepsy. Using the presence of four or more panic symptoms has a sensitivity of 82.6% and specificity of 65.4%. As the number of endorsed symptoms increases to greater than or equal to five and six, the specificity reduces to 70.5% and 59.8%, respectively, while the specificity improves to 73.8% and 80%, respectively. This suggests that using the above four or five criteria cutoff scores would provide the best combination for both high sensitivity (i.e., few false negatives) and good specificity (i.e., few false positives) to discriminate between the group with PNES and the group with epilepsy (Fig. 4). As a group, patients with PNES reported an overall higher mean number of panic attack symptoms compared with patients with epilepsy. The average number of symptoms endorsed by the group with PNES was over six, which exceeds the number of four to meet part of the criteria for a panic attack. This study did not assess the “discrete period of intense fear or discomfort” required for a diagnosis of a panic attack, although our informal observation was that this was not common. Similarly, the reported panic attack symptoms evaluated in this study could occur shortly before, during, or immediately after an event that would
20 10 0
≥ 4 Specificity
≥ 5 Specificity
≥ 6 Specificity
Fig. 2. As the number of panic attack symptoms increases from ≥4 to ≥6, specificity improves.
likely extend beyond the ten-minute interval to develop abruptly and reach a peak during an actual panic attack. Psychogenic nonepileptic “seizures” are classified as a conversion disorder in the DSM-IV-TR [29]. Despite some similarities, patients with PNES are distinct from those diagnosed with a panic attack with probably the most obvious feature being the marked shaking behaviors frequently observed in the former. Notably, over 84% of the group with PNES (Table 4) reported the trembling/shaking symptom. As all patients with PNES in this study had an alteration in awareness, this also is not consonant with a diagnosis of a panic attack. Prior studies of the clinical features of PNES have often focused on the physical semiology of the “seizures” [31] (for a recent review, see [32]). Although the physical manifestations of a psychogenic “seizure” are useful, as Goldstein and Mellers [33] advocated, what is of importance to the treating clinician is the patient's description of the physiological and mental processes associated with their PNES. This study provided some of that crucial missing information. As hypothesized, patients with PNES endorsed significantly more heart palpitations, sweating, breathing difficulties, choking sensation, feeling dizzy or unsteady, derealization or depersonalization, fear of dying, paresthesias, and chills or hot flashes compared with patients with epilepsy. As predicted, there was no difference between patients with PNES and those with epilepsy for the shaking and stomach distress symptoms. There was also no difference between the two groups for the fear of losing control or going crazy symptom, which was somewhat surprising given the psychological etiology of PNES. However, as documented in Table 4, this was not frequent, with less than 18% of the patients in either group reporting this symptom.
Panic Attack Symptoms Present 90
PNES*
≥ 4 Panic Attack Symptoms Sensitivity
80
Epilepsy
90 70 80 60
Percent
70
Percent
60 50 40
50 40 30
30 20 20 10
10
0
0 ≥ 4 Sensitivity
≥ 5 Sensitivity
≥ 6 Sensitivity
Fig. 1. As the number of panic attack symptoms increases from ≥4 to ≥6, sensitivity reduces.
≥4 Symptoms
≥5 Symptoms
≥ 6 Symptoms
Fig. 3. Patients with PNES endorsed significantly more panic attack symptoms than patients with epilepsy. *p b 0.001.
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
Fig. 4. The ROC curve depicts how the sensitivity and specificity of the diagnostic test are affected as the cutoff number of panic attack symptoms changes.
Based on these results, addressing anxiety-type symptoms could assist in formulating a treatment plan for the majority of patients with PNES. The most common panic attack symptoms differentially endorsed by individuals with PNES versus those with epilepsy were heart palpitations, sweating, shortness of breath, feeling dizzy/unsteady/ lightheaded, derealization/depersonalization, paresthesias, and chills or hot flashes. With the exception of dizziness, all the above symptoms were reported by 46% to 61.6% of those with PNES but only by 13.8% to 29.2% of those with epilepsy (Table 4). The dizziness symptom was noted by exactly half the patients with epilepsy but over 78% of the patients with PNES. Cognitive–behavioral psychotherapy could implement generalized strategies focusing on these numerous physiological symptoms, along with the more cognitive symptom (e.g., derealization or depersonalization). In addition, individualized psychotherapy could be developed for each patient based on their specific panic attack symptoms. Given the high number of panic attack features in this population, it is interesting to speculate if pharmacological management of these symptoms, even without self-reported anxiety during a spell or at other times, would be beneficial for at least some of these patients. These results provide further proof of the preponderance of women [34,35] but otherwise considerable heterogeneity of this population. Although the group with PNES reported an average of over six panic attack symptoms, as noted in Table 2, two subjects did not endorse any, and four subjects only reported one. Thus, not all patients with PNES experience numerous symptoms reflective of a panic attack. This variability again argues for the need of “one size does not fit all” treatment interventions [36]. Table 4 Chi-square analyses of the panic attack symptoms endorsed by each group. With the exception of three panic attack criteria, statistically significant differences between the groups exist for the remainder of the symptoms.
Heart palpitations⁎ Sweating⁎ Trembling/shaking Shortness of breath⁎ Choking feeling⁎ Chest pain or discomfort⁎ Nausea or abdominal distress Feeling dizzy, unsteady, lightheaded, or faint⁎ Derealization or depersonalization⁎ Fear of losing control/going crazy Fear of dying⁎ Paresthesias⁎ Chills or hot flashes⁎ ⁎ p b 0.001.
Group with PNES
Group with epilepsy
103 (46.0%) 114 (50.9%) 190 (84.8%) 125 (55.8%) 51 (22.8%) 82 (36.6%) 69 (30.8%) 175 (78.1%) 138 (61.6%) 40 (17.9%) 63 (28.1%) 130 (58.0%) 119 (53.1%)
30 (23.1%) 34 (26.2%) 104 (80.0%) 18 (13.8%) 5 (03.8%) 16 (12.3%) 31 (23.8%) 65 (50.0%) 38 (29.2%) 16 (12.3%) 16 (12.3%) 30 (23.1%) 37 (28.5%)
213
There are several limitations of this study. The thirteen symptoms for a panic attack were assessed, but the clinical interview for this study did not inquire about the accompanying fear/distress and abrupt onset with ten-minute development to meet criteria for a panic attack. Those were not included as patients were asked about the symptoms over a potentially longer time span, including shortly before a “seizure,” during an event, and immediately afterwards. Thus, this study did not evaluate all necessary criteria for a diagnosis of panic attack that could have potentially been fruitful for further treatment planning. Another limitation was the focus on the physiological and mental experiences rather than on the emotions in this psychological disorder. However, as noted in an earlier study [28], physiological symptoms may occur without the associated anxiety or fear in patients with PNES. Many individuals with PNES may be similar to a subset of patients who experience panic attacks without the fear component [37]. Our study is also limited as this was a retrospective study and although the majority, but not everyone during this time interval, who participated in Neuropsychological or Psychological Testing had a panic attack interview. It is plausible that, however unlikely, those patients may have responded differently to the panic attack criteria. This study also excluded patients with a dual diagnosis of epilepsy and PNES, and, therefore, these results may not be applicable to that population. 5. Conclusion All patients in this study had an alteration of awareness during their events and thus did not have a simple partial seizure. Using a cutoff score of four or five of the thirteen DSM-IV-TR panic attack criteria provided a good combination of sensitivity and specificity in differentiating those with PNES from those with epilepsy. Our study has assisted in delineating part of what an individual experiences in PNES. Although patients with PNES are not a homogenous population, the current findings have revealed that a large proportion report panic attack symptoms during their spells. Incorporating this direct source of knowledge can increase communication between patients and health-care professionals. The details of what is actually experienced during PNES should be helpful for clinicians to develop better and more individualized treatment plans to potentially improve the frequently poor outcomes for these patients. Conflict of interest None of the authors has any conflicts of interest to disclose. References [1] Martin R, Burneo JG, Prasad A, Powell T, Faught E, Knowlton R, et al. Frequency of epilepsy in patients with psychogenic seizures monitored by video-EEG. Neurology 2003:1791–2. [2] Benbadis SR, O'Neill E, Tatum WO, Heriaud L. Outcome of prolonged video-EEG monitoring at a typical referral epilepsy center. Epilepsia 2004:1150–3. [3] Krumholz A, Hopp J. Psychogenic (nonepileptic) seizures. Semin Neurol 2006;26: 341–50. [4] Betts T, Boden S. Diagnosis, management and prognosis of a group of 128 patients with non-epileptic attack disorder. Part 1. Seizure 1992;1:19–26. [5] Lancman ME, Brotherton TA, Asconape JJ, Penry JK. Psychogenic seizures in adults: a longitudinal study. Seizure 1993;2:281–6. [6] Walczak TS, Papacostas S, Williams DT, Scheuer ML, Lebowitz N, Notarfrancesco A. Outcome after diagnosis of psychogenic nonepileptic seizures. Epilepsia 1995;36:1131–7. [7] Reuber M, Pukrop R, Bauer J, Helmstaedter C, Tessendorf N, Elger CE. Outcome in psychogenic nonepileptic seizures: 1 to 10 year follow-up in 164 patients. Ann Neurol 2003;53:305–11. [8] McKenzie P, Oto M, Russell A, Pelosi A, Duncan R. Early outcomes and predictors in 260 patients with psychogenic nonepileptic attacks. Neurology 2010;74:64–9. [9] Reuber M, Fernandez G, Bauer J, Helmstaedter C, Elger CE. Diagnostic delay in psychogenic nonepileptic seizures. Neurology 2002;58:493–5. [10] Bowman ES, Markand ON. Psychodynamics and psychiatric diagnoses of pseudoseizure subjects. Am J Psychiatry 1996;153:57–63. [11] Lacey C, Cook M, Salzberg M. The neurologist, psychogenic nonepileptic seizures and borderline personality disorder. Epilepsy Behav 2007;11:492–8. [12] Selwa LM, Geyer J, Nikakhtar N, Brown MB, Schuh LA, Drury I. Nonepileptic seizure outcome varies by type of spell and duration of illness. Epilepsia 2000;41:1330–4.
214
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
[13] Bowman ES. Etiology and clinical course of pseudoseizures. Relationship to trauma, depression, and dissociation. Psychosomatics 1993;4:333–42. [14] Baslet G, Roiko A, Prensky E. Heterogeneity in psychogenic nonepileptic seizures: understanding the role of psychiatric and neurological factors. Epilepsy Behav 2010;17:236–41. [15] Kuyk J, Siffels MC, Bakvis P, Swinkels WAM. Psychological treatment of patients with psychogenic non-epileptic seizures: an outcome study. Seizure 2008;17:595–603. [16] LaFrance WC, Barry JJ. Update on treatments of psychological nonepileptic seizures. Epilepsy Behav 2005;7:364–74. [17] Goldstein LH, Deale AC, Mitchell-O'Malley SJ, Toone BK, Mellers JDC. An evaluation of cognitive behavioral therapy as treatment for dissociative seizures. A pilot study. Cogn Behav Neurol 2004;17:41–9. [18] LaFrance WC, Miller IW, Ryan CE, Blum AS, Solomon DA, Kelley JE, et al. Cognitive behavioral therapy for psychogenic nonepileptic seizures. Epilepsy Behav 2009;14: 591–6. [19] Goldstein LH, Chalder T, Chigwedere C, Khondoker MR, Moriarty J, Toone BK, et al. Cognitive–behavioral therapy for psychogenic nonepileptic seizures. A pilot RCT. Neurology 2010;74:1986–94. [20] Watson NF, Doherty MJ, Dodrill CB, Farrell D, Miller JW. The experience of earthquakes by patients with epileptic and psychogenic nonepileptic seizures. Epilepsia 2002:317–20. [21] Weilburg JB, Bear DM, Sachs G. Three patients with concomitant panic disorders and seizure disorder: possible clues to the neurology of anxiety. Am J Psychiatry 1987;144:1053–6. [22] Thompson SA, Duncan JS, Smith SJM. Partial seizures presenting as panic attacks. BMJ 2000;321:1002–3. [23] Bernik MA, Corregiari FM, Braun IM. Panic attacks in the differential diagnosis and treatment of resistant epilepsy. Depress Anxiety 2002;15:190–2. [24] Vein AM, Djukova G, Vorobieva OV. Is panic attack a mask of psychogenic seizures?— A comparative analysis of phenomenology of psychogenic seizures and panic attacks. Funct Neurol 1994;9:153–9.
[25] Young GB, Chandarana PC, Blume WT, McLachlan RS, Munoz DG, Girvin JP. Mesial temporal lobe seizures presenting as anxiety disorders. J Neuropsychiatry Clin Neurosci 1995;3:352–7. [26] Plotnik AN, Carney P, Schweder P, O'Brien TJ, Velakoulis D, Drummond KJ. Seizures initially misdiagnosed as panic attacks: case series. Aust N Z J Psychiatry 2009;9: 878–82. [27] Witgert ME, Wheless JW, Breier JI. Frequency of panic symptoms in psychogenic nonepileptic seizures. Epilepsy Behav 2005;6:174–8. [28] Goldstein LH, Mellers JDC. Ictal symptoms of anxiety, avoidance behavior, and dissociation in patients with dissociative seizures. J Neurol Neurosurg Psychiatry 2006;77:616–21. [29] American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders—4th Edition-Text Revision. Washington, DC: American Psychiatric Association; 2000. [30] Dixit R, Popescu A, Bagic A, Ghearing G, Hendrickson R. Medical comorbidities in patients with psychogenic nonepileptic spells (PNES) referred for video-EEG monitoring. Epilepsy Behav 2013;28:137–40. [31] Seneviratne U, Reutens D, D'Souza W. Stereotypy of psychogenic nonepileptic seizures: insights from video-EEG monitoring. Epilepsia 2010;51:1159–68. [32] Mostacci B, Bisulli F, Alvisi L, Licchetta L, Baruzzi A, Tinuper P. Ictal characteristics of psychogenic nonepileptic seizures: what we learned from video/EEG recordings—a literature review. Epilepsy Behav 2011;22:144–53. [33] Goldstein LH, Mellers JD. Recent developments in our understanding of the semiology and treatment of psychogenic nonepileptic seizures. Curr Neurol Neurosci Rep 2012;12:436–44. [34] Lesser RP. Psychogenic seizures. Neurology 1996;46:1499–507. [35] Rosenbaum M. Psychogenic seizures—why women? Psychosomatics 2000;41:147–9. [36] LaFrance WC. Treating patients with functional disorders: one size does not fit all. J Psychosom Res 2007;63:633–5. [37] Russell JL, Kushner MG, Beitman BD, Bartels KM. Nonfearful panic disorder in neurology patients validated by lactate challenge. Am J Psychiatry 1991;148:361–4.
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Panic attack symptoms differentiate patients with epilepsy from those with psychogenic nonepileptic spells (PNES) Rick Hendrickson a,⁎, Alexandra Popescu a, Ronak Dixit b, Gena Ghearing a, Anto Bagic a a b
University of Pittsburgh, Department of Neurology, Pittsburgh, PA, USA University of Pittsburgh School of Medicine, Pittsburgh, PA, USA
a r t i c l e
i n f o
Article history: Received 12 May 2014 Revised 20 June 2014 Accepted 22 June 2014 Available online xxxx Keywords: Psychogenic nonepileptic spells Psychogenic seizures Epilepsy Panic attack Anxiety
a b s t r a c t Psychogenic nonepileptic spells (PNES) are frequently challenging to differentiate from epileptic seizures. The experience of panic attack symptoms during an event may assist in distinguishing PNES from seizures secondary to epilepsy. A retrospective analysis of 354 patients diagnosed with PNES (N = 224) or with epilepsy (N = 130) investigated the thirteen Diagnostic and Statistical Manual—IV-Text Revision panic attack criteria endorsed by the two groups. We found a statistically higher mean number of symptoms reported by patients with PNES compared with those with epilepsy. In addition, the majority of the panic attack symptoms including heart palpitations, sweating, shortness of breath, choking feeling, chest discomfort, dizziness/unsteadiness, derealization or depersonalization, fear of dying, paresthesias, and chills or hot flashes were significantly more frequent in those with PNES. As patients with PNES frequently have poor clinical outcomes, treatment addressing the anxiety symptomatology may be beneficial. © 2014 Elsevier Inc. All rights reserved.
1. Introduction Psychogenic nonepileptic spells (PNES) are behavioral events of psychological origin that resemble seizures caused by epilepsy but are not due to neurological or other medical disorders. It has been estimated that approximately 20 to 30% of patients referred to epilepsy centers have PNES [1–3]. Patients with PNES have variable but often poor outcomes [4–8]. The intractability of PNES is likely multifactorial, including an average of 7 years before accurate diagnosis [9], comorbid personality disorders [10,11], duration of illness [12], history of abuse [13,14], as well as frequently coexisting depression and anxiety [15]. A 2005 update on treatments for patients with PNES [16] noted that the majority of the literature consisted of class IV reports (case reports or case series) with a limited number of class III reports. Several of the more promising studies [17–19] employed cognitive–behavioral therapy (CBT) interventions. According to Goldstein et al. [17], CBT views PNES as characterized by a “vicious circle of behavioral, cognitive, affective, physiological and social factors.” What a patient experiences during PNES may include cognitions and emotions along with physiological symptoms, which could be incorporated as part of CBT treatment. As indicated by Watson and colleagues [20], there is evidence that the subjective PNES experience is different from an epileptic seizure. Yet, there is little evidence in the literature that illuminates the patients' actual experience in PNES. People with epilepsy may have prodromal ⁎ Corresponding author at: University of Pittsburgh Epilepsy Center, 810 Kaufmann Building, 3471 Fifth Avenue, Pittsburgh, PA 15213, USA. Tel.: +1 412 648 8877. E-mail address: [email protected] (R. Hendrickson).
http://dx.doi.org/10.1016/j.yebeh.2014.06.026 1525-5050/© 2014 Elsevier Inc. All rights reserved.
symptoms of fear, heart palpitations, diaphoresis, shortness of breath [21], paresthesias, nausea, chest discomfort, fear of dying [22], derealization, concerns of losing control, and tremors [23] that are characteristic of a panic attack. Similarly, patients with PNES may report symptoms reflective of a panic attack with their episodes. Vein and colleagues [24] found a group of patients with PNES who endorsed symptoms classic for a panic attack as typical of their paroxysmal event including dyspnea, palpitations, sweating, hot/cold flashes, trembling/shaking, chest pain, dizziness, abdominal distress, feeling of unreality, faintness, paresthesias, as well as fear of going crazy or doing something uncontrolled at a comparable level as another group diagnosed with panic attacks. Because of these similarities, it is not surprising that some patients with epilepsy [25,26] were initially misdiagnosed as having panic attacks. The available literature on panic symptoms in PNES is limited. One study [27] consisting of a medical review of patients with PNES found a high proportion of panic attack symptoms in adolescents but not in adults. However, this was a retrospective record review, and the patients were not specifically questioned about symptoms characteristic of a panic attack. Another study [28] assessing a select number of panic attack symptoms found that these were more common in patients with PNES compared with those with epilepsy. Our study evaluated panic attack symptomatology in patients with PNES and in those with epilepsy. The thirteen criteria for a panic attack from the Diagnostic and Statistical Manual—IV-TR (DSM-IV-TR) [29] including heart palpitations, sweating, shaking, shortness of breath, choking feeling, chest discomfort, stomach distress, feeling dizzy/ unsteady, derealization or depersonalization, fear of losing control, fear of dying, paresthesias, and chills or hot flashes were assessed for
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
each patient. It was hypothesized that patients with PNES would report an overall higher number of total panic symptoms compared with those with epilepsy. In addition, we hypothesized that individuals with PNES would endorse a greater number of the majority of the panic attack symptoms. However, it was anticipated that there would be no difference between patients with PNES and those with epilepsy for the shaking and stomach distress symptoms. Increasing our understanding of the actual PNES experience may assist in formulating an individualized treatment plan leading to better outcomes.
211
Table 1 Demographic information for the 2 groups in the study. Statistically significant differences between the groups were found for sex and age at spell/seizure onset but not for level of education.
Group with PNES Group with epilepsy a b
Total
Femalea
Average education
Age at spell onsetb
224 130
167 (74.6%) 61 (46.9%)
12.4 years 12.9 years
30.6 25.7
p b 0.001. p b 0.002.
2. Methods For this study, we reviewed the medical records of 849 patients who underwent video-EEG monitoring at the University of Pittsburgh Medical Center's Epilepsy Monitoring Unit from 2006 to April 2011 and participated in either Neuropsychological or Psychological Testing as well as were interviewed for panic attack criteria. This study received approval by the University of Pittsburgh Institutional Review Board. Patients were excluded if they had an unclear diagnosis (e.g., no typical spells captured during the evaluation), episodes secondary to another physiological etiology (e.g., sleep disorder or migraines), or a diagnosis of both epilepsy and PNES. Additionally, patients were not included if English was not their first language or if they had a diagnosis of mental retardation. Many of these patients were included in an earlier study of medical comorbidities in PNES [30]. After the above exclusions, we identified 354 patients who were classified into the group with “PNES” or the group with “epilepsy” based on their video-EEG diagnosis. All patients with PNES had a typical event with an alteration in their awareness. None of those with PNES had epileptiform abnormalities during their video-EEG monitoring. We collected the following demographic variables: sex, education, and age at seizure/spell onset. As part of the clinical interview, patients were asked if they experienced each of the thirteen DSM-IV-TR panic attack symptoms: palpitations, pounding heart, or accelerated heart rate; sweating; trembling or shaking; sensations of shortness of breath; feeling of choking; chest pain or discomfort; nausea or abdominal distress; feeling dizzy, unsteady, lightheaded, or faint; derealization (e.g., feelings of unreality) or depersonalization (e.g., being detached from oneself); fear of losing control or going crazy; fear of dying; paresthesias (e.g., numbness or tingling sensations); and chills or hot flashes as part of their “seizures.” The panic attack symptoms could occur shortly before the “seizure,” during the event, or immediately afterwards. Symptoms could always or sometimes accompany their “seizures.” If symptoms happened only rarely or at other times outside their episodes, those were not included. The main emphasis was on the patients' experiences, although some individuals related being told about their symptoms after they had lost awareness (e.g., “I pass out and they say I shake”), which were included as their endorsement for this study. Face-to-face clinical interview of the panic attack symptoms was chosen as this method is presumably more accurate than self-report via tests or questionnaires. The data were coded and entered into SPSS 21. Differences between the group with PNES and the group with epilepsy were examined using either the Mann–Whitney U or the X2 analysis as appropriate. In the current study, we investigated how well each of the thirteen panic attack symptoms along with the total number of symptoms reported during a “seizure” distinguished patients with PNES from those with epilepsy. 3. Results Of the 224 patients in the group with PNES, 74.6% were female. This was a statistically significant difference (p b 0.001; Table 1) from the 130 patients in the group with epilepsy, of whom 46.9% were female. There was also a statistically significant difference (p b 0.002) for average age at “seizure” onset between 30.6 for the group with PNES and
25.7 for the group with epilepsy (Table 1). There was no statistically significant difference for education level between the group with PNES (12.4) and the group with epilepsy (12.9) (Table 1). Table 2 shows the number of each of the panic attack symptoms endorsed by both groups. Patients with PNES reported an average of 6.4 panic attack symptoms, which was significantly greater than an average of 3.4 symptoms in the group with epilepsy (p b 0.001). One hundred eighty-five (82.6%) of the individuals with PNES endorsed four or more panic attack symptoms, which were significantly greater than those of the 45 (34.6%) patients with epilepsy (p b 0.001; Table 3). The presence of four or more symptoms provided a sensitivity of 82.6% (Fig. 1) and a specificity of 65.4% (Fig. 2). Using a cutoff score of five or more also resulted in a good classification between the two groups as this was endorsed by 158 (70.5%) of the group with PNES versus 34 (26.2%) of the group with epilepsy (p b 0.001; Table 3). Using the presence of five or more symptoms for PNES showed a lower sensitivity of 70.5% (Fig. 1) but an increased specificity of 73.84% versus the four or more cutoff (Fig. 2). Although only 26 (20.0%) of the patients with epilepsy indicated six or more panic symptoms, this also was lower compared with 134 (59.8%) in the group with PNES (p b 0.001; Table 3). Similarly, the sensitivity for six or greater symptoms diminished to 59.8% (Fig. 1); however, the specificity increased to 80% (Fig. 2). Thus, increasing the number of panic attack symptoms from four to six sacrifices sensitivity in exchange for enhanced specificity. Fig. 3 provides a side-by-side comparison of the number of panic attack symptoms reported by the two groups, which was statistically significant for each of the above cutoff scores (p b 0.001). As mentioned in the results above, by increasing the minimum number of panic attack symptoms endorsed by patients with PNES and those with epilepsy, specificity increases, but sensitivity falls. This is best illustrated on a receiver operating characteristic (ROC) curve (Fig. 4). Each point represents a cutoff number of panic attack symptoms that a patient must have in order to be diagnosed with PNES, and each cutoff point has an associated sensitivity and specificity. The point with the highest sensitivity and specificity (i.e., the lowest 1—specificity) is considered the optimal cutoff number, and, on an ROC curve, this point lies closest to the top-left corner. In this case, both point 4 and point 5 lie near the top-left corner, but point 4 is marginally closer. Using either Table 2 Number of panic attack symptoms endorsed by each group. Number of symptoms
Group with PNES
Group with epilepsy
0 1 2 3 4 5 6 7 8 9 10 11 12 13
2 4 19 14 28 23 26 36 24 17 14 11 4 2
5 31 25 24 11 8 7 7 4 5 2 0 0 1
212
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
≥ 4 Panic Attack Symptoms Specificity
Table 3 Chi-square analysis comparing the group with PNES and the group with epilepsy showed that patients with PNES were much more likely to endorse 4 or more panic attack symptoms than those with epilepsy. ≥5 symptoms
≥6 symptoms
185 45
158 34
134 26
⁎ p b 0.001.
80 70 60
Percent
Group with PNES⁎ Group with epilepsy
≥4 symptoms
90
50 40 30
four or five as a cutoff number of symptoms results in an acceptable sensitivity (82.6% or 70.5%, respectively) and specificity (65.4% or 73.8%, respectively). Using a cutoff of six symptoms sacrifices sensitivity (59.8%) greatly, as fewer patients with PNES have six or more panic attack symptoms, and point 6 lies farthest from the top-left corner. Analysis of these data (Table 4) revealed that the group with PNES reported significantly more symptoms of heart palpitations (p b 0.001); sweating (p b 0.001); shortness of breath sensations (p b 0.001); feeling of choking (p b 0.001); chest pain or discomfort (p b 0.001); feeling dizzy, unsteady, lightheaded, or faint (p b 0.001); derealization or depersonalization (p b 0.001); fear of dying (p b 0.001); paresthesias (p b 0.001); and chills or hot flashes (p b 0.001). By contrast, there was no difference between the two groups (Table 4) for the symptoms of trembling or shaking, nausea or abdominal distress, and fear of losing control or going crazy. 4. Discussion This study has shown that the presence of panic attack symptoms can provide a useful tool in differentiating patients with PNES from those with epilepsy. Using the presence of four or more panic symptoms has a sensitivity of 82.6% and specificity of 65.4%. As the number of endorsed symptoms increases to greater than or equal to five and six, the specificity reduces to 70.5% and 59.8%, respectively, while the specificity improves to 73.8% and 80%, respectively. This suggests that using the above four or five criteria cutoff scores would provide the best combination for both high sensitivity (i.e., few false negatives) and good specificity (i.e., few false positives) to discriminate between the group with PNES and the group with epilepsy (Fig. 4). As a group, patients with PNES reported an overall higher mean number of panic attack symptoms compared with patients with epilepsy. The average number of symptoms endorsed by the group with PNES was over six, which exceeds the number of four to meet part of the criteria for a panic attack. This study did not assess the “discrete period of intense fear or discomfort” required for a diagnosis of a panic attack, although our informal observation was that this was not common. Similarly, the reported panic attack symptoms evaluated in this study could occur shortly before, during, or immediately after an event that would
20 10 0
≥ 4 Specificity
≥ 5 Specificity
≥ 6 Specificity
Fig. 2. As the number of panic attack symptoms increases from ≥4 to ≥6, specificity improves.
likely extend beyond the ten-minute interval to develop abruptly and reach a peak during an actual panic attack. Psychogenic nonepileptic “seizures” are classified as a conversion disorder in the DSM-IV-TR [29]. Despite some similarities, patients with PNES are distinct from those diagnosed with a panic attack with probably the most obvious feature being the marked shaking behaviors frequently observed in the former. Notably, over 84% of the group with PNES (Table 4) reported the trembling/shaking symptom. As all patients with PNES in this study had an alteration in awareness, this also is not consonant with a diagnosis of a panic attack. Prior studies of the clinical features of PNES have often focused on the physical semiology of the “seizures” [31] (for a recent review, see [32]). Although the physical manifestations of a psychogenic “seizure” are useful, as Goldstein and Mellers [33] advocated, what is of importance to the treating clinician is the patient's description of the physiological and mental processes associated with their PNES. This study provided some of that crucial missing information. As hypothesized, patients with PNES endorsed significantly more heart palpitations, sweating, breathing difficulties, choking sensation, feeling dizzy or unsteady, derealization or depersonalization, fear of dying, paresthesias, and chills or hot flashes compared with patients with epilepsy. As predicted, there was no difference between patients with PNES and those with epilepsy for the shaking and stomach distress symptoms. There was also no difference between the two groups for the fear of losing control or going crazy symptom, which was somewhat surprising given the psychological etiology of PNES. However, as documented in Table 4, this was not frequent, with less than 18% of the patients in either group reporting this symptom.
Panic Attack Symptoms Present 90
PNES*
≥ 4 Panic Attack Symptoms Sensitivity
80
Epilepsy
90 70 80 60
Percent
70
Percent
60 50 40
50 40 30
30 20 20 10
10
0
0 ≥ 4 Sensitivity
≥ 5 Sensitivity
≥ 6 Sensitivity
Fig. 1. As the number of panic attack symptoms increases from ≥4 to ≥6, sensitivity reduces.
≥4 Symptoms
≥5 Symptoms
≥ 6 Symptoms
Fig. 3. Patients with PNES endorsed significantly more panic attack symptoms than patients with epilepsy. *p b 0.001.
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
Fig. 4. The ROC curve depicts how the sensitivity and specificity of the diagnostic test are affected as the cutoff number of panic attack symptoms changes.
Based on these results, addressing anxiety-type symptoms could assist in formulating a treatment plan for the majority of patients with PNES. The most common panic attack symptoms differentially endorsed by individuals with PNES versus those with epilepsy were heart palpitations, sweating, shortness of breath, feeling dizzy/unsteady/ lightheaded, derealization/depersonalization, paresthesias, and chills or hot flashes. With the exception of dizziness, all the above symptoms were reported by 46% to 61.6% of those with PNES but only by 13.8% to 29.2% of those with epilepsy (Table 4). The dizziness symptom was noted by exactly half the patients with epilepsy but over 78% of the patients with PNES. Cognitive–behavioral psychotherapy could implement generalized strategies focusing on these numerous physiological symptoms, along with the more cognitive symptom (e.g., derealization or depersonalization). In addition, individualized psychotherapy could be developed for each patient based on their specific panic attack symptoms. Given the high number of panic attack features in this population, it is interesting to speculate if pharmacological management of these symptoms, even without self-reported anxiety during a spell or at other times, would be beneficial for at least some of these patients. These results provide further proof of the preponderance of women [34,35] but otherwise considerable heterogeneity of this population. Although the group with PNES reported an average of over six panic attack symptoms, as noted in Table 2, two subjects did not endorse any, and four subjects only reported one. Thus, not all patients with PNES experience numerous symptoms reflective of a panic attack. This variability again argues for the need of “one size does not fit all” treatment interventions [36]. Table 4 Chi-square analyses of the panic attack symptoms endorsed by each group. With the exception of three panic attack criteria, statistically significant differences between the groups exist for the remainder of the symptoms.
Heart palpitations⁎ Sweating⁎ Trembling/shaking Shortness of breath⁎ Choking feeling⁎ Chest pain or discomfort⁎ Nausea or abdominal distress Feeling dizzy, unsteady, lightheaded, or faint⁎ Derealization or depersonalization⁎ Fear of losing control/going crazy Fear of dying⁎ Paresthesias⁎ Chills or hot flashes⁎ ⁎ p b 0.001.
Group with PNES
Group with epilepsy
103 (46.0%) 114 (50.9%) 190 (84.8%) 125 (55.8%) 51 (22.8%) 82 (36.6%) 69 (30.8%) 175 (78.1%) 138 (61.6%) 40 (17.9%) 63 (28.1%) 130 (58.0%) 119 (53.1%)
30 (23.1%) 34 (26.2%) 104 (80.0%) 18 (13.8%) 5 (03.8%) 16 (12.3%) 31 (23.8%) 65 (50.0%) 38 (29.2%) 16 (12.3%) 16 (12.3%) 30 (23.1%) 37 (28.5%)
213
There are several limitations of this study. The thirteen symptoms for a panic attack were assessed, but the clinical interview for this study did not inquire about the accompanying fear/distress and abrupt onset with ten-minute development to meet criteria for a panic attack. Those were not included as patients were asked about the symptoms over a potentially longer time span, including shortly before a “seizure,” during an event, and immediately afterwards. Thus, this study did not evaluate all necessary criteria for a diagnosis of panic attack that could have potentially been fruitful for further treatment planning. Another limitation was the focus on the physiological and mental experiences rather than on the emotions in this psychological disorder. However, as noted in an earlier study [28], physiological symptoms may occur without the associated anxiety or fear in patients with PNES. Many individuals with PNES may be similar to a subset of patients who experience panic attacks without the fear component [37]. Our study is also limited as this was a retrospective study and although the majority, but not everyone during this time interval, who participated in Neuropsychological or Psychological Testing had a panic attack interview. It is plausible that, however unlikely, those patients may have responded differently to the panic attack criteria. This study also excluded patients with a dual diagnosis of epilepsy and PNES, and, therefore, these results may not be applicable to that population. 5. Conclusion All patients in this study had an alteration of awareness during their events and thus did not have a simple partial seizure. Using a cutoff score of four or five of the thirteen DSM-IV-TR panic attack criteria provided a good combination of sensitivity and specificity in differentiating those with PNES from those with epilepsy. Our study has assisted in delineating part of what an individual experiences in PNES. Although patients with PNES are not a homogenous population, the current findings have revealed that a large proportion report panic attack symptoms during their spells. Incorporating this direct source of knowledge can increase communication between patients and health-care professionals. The details of what is actually experienced during PNES should be helpful for clinicians to develop better and more individualized treatment plans to potentially improve the frequently poor outcomes for these patients. Conflict of interest None of the authors has any conflicts of interest to disclose. References [1] Martin R, Burneo JG, Prasad A, Powell T, Faught E, Knowlton R, et al. Frequency of epilepsy in patients with psychogenic seizures monitored by video-EEG. Neurology 2003:1791–2. [2] Benbadis SR, O'Neill E, Tatum WO, Heriaud L. Outcome of prolonged video-EEG monitoring at a typical referral epilepsy center. Epilepsia 2004:1150–3. [3] Krumholz A, Hopp J. Psychogenic (nonepileptic) seizures. Semin Neurol 2006;26: 341–50. [4] Betts T, Boden S. Diagnosis, management and prognosis of a group of 128 patients with non-epileptic attack disorder. Part 1. Seizure 1992;1:19–26. [5] Lancman ME, Brotherton TA, Asconape JJ, Penry JK. Psychogenic seizures in adults: a longitudinal study. Seizure 1993;2:281–6. [6] Walczak TS, Papacostas S, Williams DT, Scheuer ML, Lebowitz N, Notarfrancesco A. Outcome after diagnosis of psychogenic nonepileptic seizures. Epilepsia 1995;36:1131–7. [7] Reuber M, Pukrop R, Bauer J, Helmstaedter C, Tessendorf N, Elger CE. Outcome in psychogenic nonepileptic seizures: 1 to 10 year follow-up in 164 patients. Ann Neurol 2003;53:305–11. [8] McKenzie P, Oto M, Russell A, Pelosi A, Duncan R. Early outcomes and predictors in 260 patients with psychogenic nonepileptic attacks. Neurology 2010;74:64–9. [9] Reuber M, Fernandez G, Bauer J, Helmstaedter C, Elger CE. Diagnostic delay in psychogenic nonepileptic seizures. Neurology 2002;58:493–5. [10] Bowman ES, Markand ON. Psychodynamics and psychiatric diagnoses of pseudoseizure subjects. Am J Psychiatry 1996;153:57–63. [11] Lacey C, Cook M, Salzberg M. The neurologist, psychogenic nonepileptic seizures and borderline personality disorder. Epilepsy Behav 2007;11:492–8. [12] Selwa LM, Geyer J, Nikakhtar N, Brown MB, Schuh LA, Drury I. Nonepileptic seizure outcome varies by type of spell and duration of illness. Epilepsia 2000;41:1330–4.
214
R. Hendrickson et al. / Epilepsy & Behavior 37 (2014) 210–214
[13] Bowman ES. Etiology and clinical course of pseudoseizures. Relationship to trauma, depression, and dissociation. Psychosomatics 1993;4:333–42. [14] Baslet G, Roiko A, Prensky E. Heterogeneity in psychogenic nonepileptic seizures: understanding the role of psychiatric and neurological factors. Epilepsy Behav 2010;17:236–41. [15] Kuyk J, Siffels MC, Bakvis P, Swinkels WAM. Psychological treatment of patients with psychogenic non-epileptic seizures: an outcome study. Seizure 2008;17:595–603. [16] LaFrance WC, Barry JJ. Update on treatments of psychological nonepileptic seizures. Epilepsy Behav 2005;7:364–74. [17] Goldstein LH, Deale AC, Mitchell-O'Malley SJ, Toone BK, Mellers JDC. An evaluation of cognitive behavioral therapy as treatment for dissociative seizures. A pilot study. Cogn Behav Neurol 2004;17:41–9. [18] LaFrance WC, Miller IW, Ryan CE, Blum AS, Solomon DA, Kelley JE, et al. Cognitive behavioral therapy for psychogenic nonepileptic seizures. Epilepsy Behav 2009;14: 591–6. [19] Goldstein LH, Chalder T, Chigwedere C, Khondoker MR, Moriarty J, Toone BK, et al. Cognitive–behavioral therapy for psychogenic nonepileptic seizures. A pilot RCT. Neurology 2010;74:1986–94. [20] Watson NF, Doherty MJ, Dodrill CB, Farrell D, Miller JW. The experience of earthquakes by patients with epileptic and psychogenic nonepileptic seizures. Epilepsia 2002:317–20. [21] Weilburg JB, Bear DM, Sachs G. Three patients with concomitant panic disorders and seizure disorder: possible clues to the neurology of anxiety. Am J Psychiatry 1987;144:1053–6. [22] Thompson SA, Duncan JS, Smith SJM. Partial seizures presenting as panic attacks. BMJ 2000;321:1002–3. [23] Bernik MA, Corregiari FM, Braun IM. Panic attacks in the differential diagnosis and treatment of resistant epilepsy. Depress Anxiety 2002;15:190–2. [24] Vein AM, Djukova G, Vorobieva OV. Is panic attack a mask of psychogenic seizures?— A comparative analysis of phenomenology of psychogenic seizures and panic attacks. Funct Neurol 1994;9:153–9.
[25] Young GB, Chandarana PC, Blume WT, McLachlan RS, Munoz DG, Girvin JP. Mesial temporal lobe seizures presenting as anxiety disorders. J Neuropsychiatry Clin Neurosci 1995;3:352–7. [26] Plotnik AN, Carney P, Schweder P, O'Brien TJ, Velakoulis D, Drummond KJ. Seizures initially misdiagnosed as panic attacks: case series. Aust N Z J Psychiatry 2009;9: 878–82. [27] Witgert ME, Wheless JW, Breier JI. Frequency of panic symptoms in psychogenic nonepileptic seizures. Epilepsy Behav 2005;6:174–8. [28] Goldstein LH, Mellers JDC. Ictal symptoms of anxiety, avoidance behavior, and dissociation in patients with dissociative seizures. J Neurol Neurosurg Psychiatry 2006;77:616–21. [29] American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders—4th Edition-Text Revision. Washington, DC: American Psychiatric Association; 2000. [30] Dixit R, Popescu A, Bagic A, Ghearing G, Hendrickson R. Medical comorbidities in patients with psychogenic nonepileptic spells (PNES) referred for video-EEG monitoring. Epilepsy Behav 2013;28:137–40. [31] Seneviratne U, Reutens D, D'Souza W. Stereotypy of psychogenic nonepileptic seizures: insights from video-EEG monitoring. Epilepsia 2010;51:1159–68. [32] Mostacci B, Bisulli F, Alvisi L, Licchetta L, Baruzzi A, Tinuper P. Ictal characteristics of psychogenic nonepileptic seizures: what we learned from video/EEG recordings—a literature review. Epilepsy Behav 2011;22:144–53. [33] Goldstein LH, Mellers JD. Recent developments in our understanding of the semiology and treatment of psychogenic nonepileptic seizures. Curr Neurol Neurosci Rep 2012;12:436–44. [34] Lesser RP. Psychogenic seizures. Neurology 1996;46:1499–507. [35] Rosenbaum M. Psychogenic seizures—why women? Psychosomatics 2000;41:147–9. [36] LaFrance WC. Treating patients with functional disorders: one size does not fit all. J Psychosom Res 2007;63:633–5. [37] Russell JL, Kushner MG, Beitman BD, Bartels KM. Nonfearful panic disorder in neurology patients validated by lactate challenge. Am J Psychiatry 1991;148:361–4.
