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Psychogenic nonepileptic seizures and health-related quality of life: The relationship with psychological distress and other physical symptoms
Epilepsy & Behavior 14 (2009) 167–171
Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Psychogenic nonepileptic seizures and health-related quality of life: The relationship with psychological distress and other physical symptoms Gemma Lawton a, Rebecca J Mayor b, Stephanie Howlett b, Markus Reuber a,* a b
Academic Neurology Unit, Royal Hallamshire Hospital, Glossop Road, Sheffield, S10 2JF, UK Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield, UK
a r t i c l e
i n f o
Article history: Received 27 August 2008 Revised 22 September 2008 Accepted 23 September 2008 Available online 6 November 2008 Keywords: Psychogenic nonepileptic seizures Health-related quality of life Psychopathology Psychological distress Somatization
a b s t r a c t This study explores the relationship between the frequency of psychogenic nonepileptic seizures (PNES) and health-related quality of life (HRQoL), as well as the effect of psychological distress and other physical symptoms on this relationship. Data were collected on 96 patients with PNES. Correlations of seizure frequency with HRQoL, psychological distress, and physical symptoms were computed. Partial correlations of seizure frequency with HRQoL while controlling for psychological distress and physical symptoms were also computed. Seizure frequency was found to be significantly related to subjective HRQoL, although the relationship with HRQoL was rendered nonsignificant when the effects of psychological distress and the number of other physical symptoms were taken into account. The results of this study suggest that summary scores of HRQoL are not independently related to frequency of PNES and that there is a close association between PNES frequency, levels of psychological distress, and number of other physical symptoms experienced. Ó 2008 Elsevier Inc. All rights reserved.
1. Introduction Psychogenic nonepileptic seizures (PNES) are episodes of paroxysmal impairment of self-control associated with a range of motor, sensory, and mental manifestations, which resemble those seen in epileptic seizures but are not associated with ictal electrical discharges in the brain. In most cases, PNES are interpreted as a dissociative response to psychological or social distress. Recent investigations have demonstrated that PNES are common and costly to patients and society. However, many questions about their etiology and treatment remain unanswered [1]. Although previous studies have demonstrated that PNES are often associated with ‘‘comorbid” psychiatric or personality pathology, and that many patients with PNES also have other somatic complaints [2– 4], it is not certain to what extent PNES themselves contribute to the poor health-related quality of life (HRQoL) reported by patients with this seizure disorder. In euthymic patients with epilepsy, the frequency of seizures is an important predictor of quality of life as measured by self-report instruments such as the Short Function (SF)-36, particularly in terms of Physical Role, Social Functioning, and General Health. The relationship between seizure frequency and HRQoL remains significant after controlling for time since last seizure, gender, and comorbid physical conditions [5]. However, several studies * Corresponding author. Fax: +44 (0) 114 271 3158. E-mail address: [email protected] (M. Reuber). 1525-5050/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2008.09.029
have demonstrated that not only is HRQoL in epilepsy determined by seizure-related factors, but that a range of psychosocial variables, such as the presence of depression [6–8], self-efficacy and social support [9], the perception of stigma [10], and fatigue [11], play an important role. When compared with patients with epileptic seizures (ES), those with PNES consistently report lower levels of HRQoL [12,13]. To some extent the difference between patients with epilepsy and those with PNES is explained by higher levels of psychopathology in the PNES group [14,15], but the difference remains if HRQoL reported by patients with PNES without depression is compared with that described by patients with epilepsy [8]. The difference in terms of HRQoL between the diagnostic groups is abolished only if differences in chronic psychological symptoms (including somatization and distress) are taken into account [16]. The relationship between PNES frequency and HRQoL is unclear. In contrast to patients with epilepsy, for whom seizure freedom can result in near-normal levels of functioning [17], around half of the patients with PNES who achieve complete remission of seizures report ongoing psychiatric symptoms or an unproductive occupational status [18]. One study of 30 patients with PNES demonstrated that despite a significant reduction in seizure frequency, HRQoL remained poor 6 months or longer after diagnosis [19]. Only when complete remission was achieved (in one-third of this sample), did patients show a significantly improved HRQoL. To determine the effect of PNES themselves (rather than associated psychopathology) on HRQoL, this study explores the
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relationship between seizure frequency and HRQoL in a much larger group of patients with PNES. We hypothesized that there would be a significant correlation between seizure frequency and HRQoL. Given that we interpret PNES as a manifestation of psychosocial distress, we further predicted that this correlation would not remain significant when psychological distress (or the number of other somatic symptoms as a correlate of distress) is taken into account. Measures of HRQoL are increasingly used to offer insights into patients’ subjective illness experience and to evaluate treatment outcomes. An improved understanding of HRQoL in PNES not only enhances our knowledge of the nature of this disorder, but can also inform our use and analysis of patient-reported outcome measures and measures of seizure frequency in future intervention studies in this patient group. 2. Methods 2.1. Patients This study is based on responses from patients referred for outpatient psychotherapy to a specialized service within the neurology departments of the Royal Hallamshire Hospital and the Barnsley District General Hospital in the United Kingdom between October 2003 and April 2008. During the recruitment period, the psychotherapy service accepted referrals of patients with functional (medically unexplained) neurological symptoms or psychological distress associated with (medically explained) neurological disorders from three different, fully trained neurologists. The findings described here are derived from the analysis of information provided by all patients with PNES referred during the study period. All referring neurologists had ready access to video/EEG and ambulatory EEG monitoring, but their clinical diagnosis of PNES was not confirmed by video/EEG monitoring in all patients. For instance, the diagnosis could also be based on home video recordings of seizures, direct observation of seizures in the clinic room, or a history and witness accounts highly suggestive of PNES, as long as other investigations (MRI, interictal EEG) did not raise any doubts about the clinical diagnosis. Patients with additional epilepsy were excluded from this study. The diagnosis of additional epilepsy was made clinically if both epileptic and nonepileptic seizures had been captured by ictal EEG or video/EEG recordings, or if the patient’s history or witness accounts suggested that the patients had additional seizures that were different from their PNES and that had not been captured by video/EEG or ambulatory EEG investigations. A diagnosis of possible additional epilepsy was also made in patients in whom interictal tests (e.g., interictal epileptiform activity) called the diagnosis of PNES (without epilepsy) into question. Patients were also excluded from this study if their PNES frequency could not be ascertained. This data set was collected in the context of an ongoing service evaluation approved by the clinical governance lead for the Sheffield Teaching Hospitals NHS Foundation Trust.
They were asked to complete this questionnaire and return it to the psychotherapy service to indicate that they wished to take up the offer of psychotherapy. The questionnaire comprised demographic questions and three validated measures. The SF-36 Health Survey [20] is a 36-item self-report questionnaire providing one multi-item scale measure of eight health concepts that can be added up to form summary subscores. The Physical Health Component Summary score is made up of four concepts: Physical Functioning (10 items), Role Limitation due to Physical Health Problems (4 items), Bodily Pain (2 items), and General Health (5 items). The Mental Health Component Summary score also results from the addition of four concept scores: Vitality (4 items), Social Functioning (2 items), Role Limitations due to Emotional Problems (3 items), and Mental Health (5 items). The SF-36 raw data were transformed to 0–100 scores so that comparisons could be made across the eight subscales, where low scores indicate poor health and functioning [21]. The Clinical Outcomes in Routine Evaluation (CORE-10) [22] is a patient-completed, hand-scored brief outcome measure comprising 10 items from the CORE-OM, a 34-item assessment and outcome measure. The CORE-10 taps self-reported global psychological distress, acting as a quick and easy screening tool and placing minimal demands on patients. The measure provides a balance of the 10 clinical domains from the CORE-OM: Subjective WellBeing, Anxiety, Depression, Physical, Trauma, General Functioning, Close Relationships (Functioning), Social Relationships (Functioning), Risk to Self, and Risk to Others. Each item is scored on a 5-point scale ranging from 0 to 4, with higher scores indicating a greater level of distress and disability. The CORE-10 correlates closely with the CORE-OM [22], which has been validated in large clinical and nonclinical samples and shows strong correlation with different well established measures of depression such as the Beck Depression Index [23,24]. The Patient Health Questionnaire (PHQ)-15 is composed of 15 physical symptoms that have been extracted from the PHQ. This is part of the self-administered PRIME MD diagnostic instrument for common mental disorders [25]. The 15 symptoms do not include blackouts or seizures. Symptoms over the last 4 weeks are rated as 0 (‘‘not at all bothered”), 1 (‘‘bothered a little”), or 2 (‘‘bothered a lot”) [26]. A number of studies suggest that scores on the PHQ-15 correlate with psychological distress [27–29]. 2.3. Statistical analysis Kolmogorov–Smirnov tests demonstrated that all of the variables (including SF-36 subscales) were nonnormally distributed; therefore Spearman’s correlations were carried out. Partial correlations were used to examine the correlation between seizure frequency and HRQoL when physical symptoms and global psychological distress were controlled for. The analyses were carried out using SPSS (Version 15).
2.2. Measures
3. Results
A screening questionnaire was completed by the neurologists when they made their initial referral to the psychotherapy department. This included information on the frequency and duration of patients’ seizures, as well as current physical comorbidity, current medication including anticonvulsant drugs, and past medical history. The seizure frequency at the time of referral was determined by questioning patients and carers in all cases and by checking seizure diaries when available. Patients provided information on their HRQoL, levels of psychological distress, and physical symptoms on a questionnaire they received 1 to 3 weeks after the appointment with the neurologist.
During the study period, 231 patients returned completed questionnaires to the psychotherapy service. Of these 161 patients had been referred with a diagnosis of PNES, although 58 had to be excluded because the frequency of their seizures could not be ascertained by the referring neurologist. Seven additional patients were excluded because they had additional epileptic seizures. After these exclusions, 96 patients were included in this study (see Table 1 for demographic characteristics). As the scores on the measures were not normally distributed, median values were inspected rather than means. Table 2 lists the median scores for the SF-36, PHQ-15, and CORE–10.
G. Lawton et al. / Epilepsy & Behavior 14 (2009) 167–171 Table 1 Demographics of the patient sample (n = 96) Variable Female (%) Age (mean number of years) Education (mean number of years) Duration of PNES disorder (median number of years) Frequency of seizures (median number/month) Employment status (%) School/college University Employed Self-employed Unemployed Receiving disability benefits Retired on health grounds Receiving old age pension
74 38.38 (12.47) 13.78 (5.42) 4 (39.90) 6 (899.80) 5.2 5.2 22.9 4.2 15.6 36.5 6.3 1.0
Table 2 Median scores and ranges for measures of HRQoL (SF-36), psychological distress (CORE-10), and physical symptoms (PHQ-15) Variable
Median (range)
SF-36 Physical Health Component summary Mental Health Component summary Physical Functioning Role Limitation: physical Bodily Pain General Health Vitality Social Functioning Role Limitation: emotional Mental Health Core-10 PHQ-15
36.92 (51.06) 34.9 (55.39) 50 (100) 0 (100) 35.93 (100) 37 (82) 30 (85) 37.5 (100) 33.33 (100) 50 (100) 16 (38) 14.15 (25)
To investigate more specifically the impact of the seizures on HRQoL, PNES frequency and the summary scales and subscales of the SF-36 were correlated (see Table 3 for correlation coefficients). Seizure frequency was found to be significantly correlated to all measures of HRQoL excluding Vitality and General Health, suggesting HRQoL is reduced as seizure frequency increases. Interestingly, seizure frequency was most strongly and significantly correlated with Bodily Pain and Social Functioning, suggesting patients who have more seizures also experience more Bodily Pain and report a greater impairment of social functioning. CORE-10 scores were significantly correlated with SF-36 Mental Health Component Summary scores (rs = –0.663, P < 0.001), but not Physical Component Summary scores. Similarly, PHQ-15 scores were significantly correlated with SF-36 Physical Component Summary scores (rs = 0.454, P < 0.001), but not with SF-36 Mental Table 3 Spearman’s q correlation coefficients for seizure frequency versus subscales and summary scales of the HRQoL measure (SF-36) and significance value SF-36 scale
rs
P
R2
Physical Health Component summary Mental Health Component summary Physical Functioning Role Limitation: physical Bodily Pain General Health Vitality Social functioning Role Limitation: emotional Mental Health
–0.246a –0.233a –0.219a –0.259a –0.387a –0.137 –0.141 –0.460a –0.219a –0.193a
0.016 0.022 0.032 0.011 0.00 0.184 0.172 0.00 0.032 0.059
0.061 0.054 0.048 0.067 0.150 0.019 0.020 0.212 0.048 0.037
Significantly correlated (a < 0.05).
Health Component Summary scores. CORE-10 and PHQ-15 scores were also significantly correlated (rs = 0.310, P < 0.002). To try and establish whether seizure frequency affects HRQoL independently of psychological distress or other physical symptoms, partial correlations were carried out. In these calculations we examined the correlation between seizure frequency and the SF-36 scores while controlling for CORE-10 and PHQ-15 scores (see Table 4 for correlation coefficients). When psychological distress and physical symptoms were controlled for, there was no significant correlation between seizure frequency and the SF-36 summary scores. However, the correlation between seizure frequency and Bodily Pain, as well as Social Functioning, remained significant. 4. Discussion
Note. Values in parentheses are ranges for median values.
a
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We examined the relationship between seizure frequency, HRQoL, psychological distress, and physical symptoms in patients with PNES. The general aim was to discover if seizure frequency was related to subjective HRQoL or, somewhat more specifically, to what extent seizures (rather than the causative or associated psychomorbidity) influence HRQoL. Our main hypothesis was confirmed; seizure frequency was found to be significantly correlated with HRQoL as measured by the SF-36 summary measures for Physical Health and Mental Health. HRQoL is reduced as seizure frequency increases. However, the correlation is relatively moderate, with seizure frequency accounting for only 6% of the variance in HRQoL. What is more, this result is rendered nonsignificant when psychological distress and physical symptoms are controlled for (either separately or in conjunction). First, this suggests that HRQoL is not independently related to seizure frequency. Second, it illustrates that there is a close association between PNES frequency, levels of psychological distress, and number of other physical symptoms experienced. Examination of the subscales of the SF-36 provides further interesting findings. Seizure frequency was significantly correlated with all SF-36 subscales with the exception of General Health and Vitality. The subscales Bodily Pain and Social Functioning were found to have the strongest correlations, accounting for 14.9 and 21.2% of the variance, respectively. Correlations at this level suggest a moderate relationship between two variables. These correlations remained significant when psychological distress and other physical symptoms were controlled for. It is not difficult to see why patients experiencing a greater number of seizures would be more disabled in their social interactions. A recent study that used Interpretative Phenomenological Analysis to examine interviews with patients with PNES after they had received the diagnosis identified social isolation as one of their biggest problems [30]. The correlation between PNES and Bodily Pain is more surprising. One previous study identified a correlation between the severity of the manifestations of the PNES syndrome and the number of physical symptoms (including pain) [4]. Another reported that chronic pain disorder and/or fibromyalgia are so regularly associated with PNES that they can be considered a diagnostic pointer [2]. It has also been reported that 75% of patients complained of moderate to severe pain 6 months after the diagnosis of PNES had been made [31]. In our clinical experience, a subgroup of patients report that their seizures are triggered by pain. Of course, both pain and PNES may be aspects of a particularly somatic focus for psychological distress. The closer inspection of the SF-36 subscores also reveals an interesting difference in scores for Physical Functioning and Role Limitation Physical. Although patients reported only average levels of limitations on the activities described due to physical health, they experienced high levels of impairment in their role functioning related to their physical health. This finding is similar to that
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Table 4 Spearman’s q correlation coefficients between seizure frequency and HRQoL (SF-36), controlling for psychological distress (CORE-10), other physical symptoms (PHQ-15), or both SF-36 scale
CORE-10
PHQ-15
PHQ-15 and CORE-10
Mental Health Component summary Physical Component summary Physical Functioning Role Limitation: physical Bodily Pain General Health Vitality Social Functioning Role Limitation: emotional Mental Health
–0.106 –0.169 –0.112 –0.130 –0.237a –0.109 –0.191 –0.238a –0.143 –0.005
–0.100 –0.156 –0.101 –0.118 –0.234a –0.098 –0.182 –0.223a –0.133 –0.017
–0.111 –0.162 –0.098 –0.118 –0.233a –0.095 –0.183 –0.233a –0.137 –0.001
a
Significantly correlated (a < 0.05).
reported by Szaflarski and Szaflarski [8]. The questions contributing to the Physical Functioning score of the SF-36 are quite strongly based on patients’ mobility and may not reflect other aspects of physical dysfunction associated with PNES sufficiently well. Alternatively, the impairment of role functioning in patients with PNES may be related to avoidance and self-imposed restrictions on activity due to fear of having a seizure rather than actual physical disability. Finally, it may be characteristic of patients with PNES to overstate disability despite relatively well-preserved functioning. These findings need to be considered in relation to the limitations of this study. Despite the fact that our method of data collection ensured that we were able to capture responses from all patients who accessed our service, our findings may have been affected by selection bias: This sample was derived from patients who had decided to opt in to psychotherapy but who had not yet commenced treatment. We are aware that the patients referred for treatment were preselected by the neurologists involved in our treatment pathway. They did not refer patients with PNES who were explicitly hostile to the idea of psychotherapy. They may also not have referred patients with particularly ‘‘mild” or recent PNES disorders. It is possible that the exclusion of some of the most severe and some of the least disabled cases has affected our results. What is more, we previously found that about 20% of the patients referred by neurologists do not return their opt-in questionnaires [32]. We do not have any information on patients who were referred and patients with PNES not referred or on patients who were referred but chose not to opt in. We are therefore unable to comment on any similarities or differences between responders and nonresponders. It may be that the patients who opted in to treatment had higher levels of psychopathology than the PNES patient population as a whole. However, the mean score of our patient group on the CORE-10 was 15.7, which actually lies between the mean scores expected for nonclinical and clinical populations (4.7 and 19.7, respectively) [22]. It is also important to note that, at this point, our results should not be generalized beyond the interval between diagnosis of PNES and commencement of psychological treatment without further confirmation. The fact that no patients had the time to be considered ‘‘under remission” is an important limitation; the relationship between PNES frequency and HRQoL may have been stronger if we had included patients in remission or conducted a longitudinal study involving a longer latency between communication of the diagnosis and determination of seizure outcome and HRQoL. This limitation is especially important because one much smaller previous study demonstrated a relatively robust effect of remission on HRQOL [19], and others demonstrate that seizure frequency can improve or remit merely by clear and compassionate explanation, rather than by any more formal psychological or psychiatric treatments [33].
Another potential weakness of this study was the ascertainment of patients’ seizure frequency. Seizure diaries or witness confirmation was not available in all cases. It may be that the self-estimate of seizure frequency reflected the level of patients’ distress at the time of the consultation. What is more, the other measures were completed 1 to 3 weeks following the encounter with the neurologist. It is thus possible that a patient’s seizure frequency had changed by the time HRQoL was determined, although the patients seen had had PNES for a mean of 4 years at the time of referral for psychotherapy. Despite these limitations, our findings provide further information about the nature of PNES. The relationship between seizure frequency and subjective quality of life is clearly complex. Our study suggests that this relationship is mediated by psychological distress as well as physical symptoms. Our results also show that patients report being more limited by their physical health than their reported physical functioning might suggest. This would imply that treatments targeted at PNES should not focus solely on the reduction of seizures, but should also take into account levels of psychological distress and physical symptoms when aiming to improve patient’s HRQoL. Techniques that could improve patients’ ability to tolerate pain and measures that would tackle avoidance and reduce social isolation might be particularly beneficial. The correlation between seizure frequency and HRQoL suggests that a seizure reduction (rather than only a cessation of seizures) is likely to represent a worthwhile treatment outcome. There is, therefore, a justification for treatment studies to report intervention effects on seizure frequency. Our results also support the validity of the SF-36, CORE-10, and PHQ-15 in this population, as the CORE-10 correlated significantly with the SF-36 Mental Health Component, but not the Physical Health Component, and the PHQ15 correlated significantly with the Physical Health Component, but not the Mental Health Component. Future research should aim to evaluate the relationship between seizure frequency and HRQoL in a longitudinal fashion and assess whether therapy targeted at decreasing seizure frequency results in a corresponding improvement in HRQoL. References [1] Reuber M. Psychogenic nonepileptic seizures: answers and questions. Epilepsy Behav 2008;12:622–35. [2] Benbadis SR. A spell in the epilepsy clinic and a history of ‘‘chronic pain” or ‘‘fibromyalgia” independently predict a diagnosis of psychogenic seizures. Epilepsy Behav 2005;6:264–5. [3] Bowman ES, Markand ON. Psychodynamics and psychiatric diagnoses of pseudoseizure subjects. Am J Psychiatry 1996;153:57–63. [4] Reuber M, House AO, Pukrop R, Bauer J, Elger CE. Somatization, dissociation and general psychopathology in patients with psychogenic non-epileptic seizures. Epilepsy Res 2003;57:159–67. [5] Leidy NK, Elixhauser A, Vickrey B, Means E, Willian MK. Seizure frequency and the health-related quality of life of adults with epilepsy. Neurology 1999;53:162. [6] Boylan LS, Flint LA, Labovitz DL, Jackson SC, Starner K, Devinsky O. Depression but not seizure frequency predicts quality of life in treatment-resistant epilepsy. Neurology 2004;62:258–61. [7] Loring DW, Meador KJ, Lee GP. Determinants of quality of life in epilepsy. Epilepsy Behavior 2004;5:976–80. [8] Szaflarski JP, Szaflarski M. Seizure disorders, depression, and health-related quality of life. Epilepsy Behav 2004;5:50–7. [9] Amir M, Roziner I, Knoll A, Neufeld MY. Self-efficacy and social support as mediators in the relation between dsease severity and quality of life in patients with epilepsy. Epilepsia 1999;40:216–24. [10] Suurmeijer TPBM, Reuvekamp MF, Aldenkamp BP. Social functioning, psychological functioning, and quality of life in epilepsy. Epilepsia 2001;42:1160–8. [11] Senol V, Soyuer F, Arman F, Öztürk A. Influence of fatigue, depression, and demographic, socioeconomic, and clinical variables on quality of life of patients with epilepsy. Epilepsy Behav 2007;10:96–104. [12] Al Marzooqi SM, Baker GA, Reilly J, Salmon P. The perceived health status of people with psychologically derived non-epileptic attack disorder and epilepsy: a comparative study. Seizure 2004;13:71–5.
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Contents lists available at ScienceDirect
Epilepsy & Behavior journal homepage: www.elsevier.com/locate/yebeh
Psychogenic nonepileptic seizures and health-related quality of life: The relationship with psychological distress and other physical symptoms Gemma Lawton a, Rebecca J Mayor b, Stephanie Howlett b, Markus Reuber a,* a b
Academic Neurology Unit, Royal Hallamshire Hospital, Glossop Road, Sheffield, S10 2JF, UK Sheffield Teaching Hospitals NHS Foundation Trust, Sheffield, UK
a r t i c l e
i n f o
Article history: Received 27 August 2008 Revised 22 September 2008 Accepted 23 September 2008 Available online 6 November 2008 Keywords: Psychogenic nonepileptic seizures Health-related quality of life Psychopathology Psychological distress Somatization
a b s t r a c t This study explores the relationship between the frequency of psychogenic nonepileptic seizures (PNES) and health-related quality of life (HRQoL), as well as the effect of psychological distress and other physical symptoms on this relationship. Data were collected on 96 patients with PNES. Correlations of seizure frequency with HRQoL, psychological distress, and physical symptoms were computed. Partial correlations of seizure frequency with HRQoL while controlling for psychological distress and physical symptoms were also computed. Seizure frequency was found to be significantly related to subjective HRQoL, although the relationship with HRQoL was rendered nonsignificant when the effects of psychological distress and the number of other physical symptoms were taken into account. The results of this study suggest that summary scores of HRQoL are not independently related to frequency of PNES and that there is a close association between PNES frequency, levels of psychological distress, and number of other physical symptoms experienced. Ó 2008 Elsevier Inc. All rights reserved.
1. Introduction Psychogenic nonepileptic seizures (PNES) are episodes of paroxysmal impairment of self-control associated with a range of motor, sensory, and mental manifestations, which resemble those seen in epileptic seizures but are not associated with ictal electrical discharges in the brain. In most cases, PNES are interpreted as a dissociative response to psychological or social distress. Recent investigations have demonstrated that PNES are common and costly to patients and society. However, many questions about their etiology and treatment remain unanswered [1]. Although previous studies have demonstrated that PNES are often associated with ‘‘comorbid” psychiatric or personality pathology, and that many patients with PNES also have other somatic complaints [2– 4], it is not certain to what extent PNES themselves contribute to the poor health-related quality of life (HRQoL) reported by patients with this seizure disorder. In euthymic patients with epilepsy, the frequency of seizures is an important predictor of quality of life as measured by self-report instruments such as the Short Function (SF)-36, particularly in terms of Physical Role, Social Functioning, and General Health. The relationship between seizure frequency and HRQoL remains significant after controlling for time since last seizure, gender, and comorbid physical conditions [5]. However, several studies * Corresponding author. Fax: +44 (0) 114 271 3158. E-mail address: [email protected] (M. Reuber). 1525-5050/$ - see front matter Ó 2008 Elsevier Inc. All rights reserved. doi:10.1016/j.yebeh.2008.09.029
have demonstrated that not only is HRQoL in epilepsy determined by seizure-related factors, but that a range of psychosocial variables, such as the presence of depression [6–8], self-efficacy and social support [9], the perception of stigma [10], and fatigue [11], play an important role. When compared with patients with epileptic seizures (ES), those with PNES consistently report lower levels of HRQoL [12,13]. To some extent the difference between patients with epilepsy and those with PNES is explained by higher levels of psychopathology in the PNES group [14,15], but the difference remains if HRQoL reported by patients with PNES without depression is compared with that described by patients with epilepsy [8]. The difference in terms of HRQoL between the diagnostic groups is abolished only if differences in chronic psychological symptoms (including somatization and distress) are taken into account [16]. The relationship between PNES frequency and HRQoL is unclear. In contrast to patients with epilepsy, for whom seizure freedom can result in near-normal levels of functioning [17], around half of the patients with PNES who achieve complete remission of seizures report ongoing psychiatric symptoms or an unproductive occupational status [18]. One study of 30 patients with PNES demonstrated that despite a significant reduction in seizure frequency, HRQoL remained poor 6 months or longer after diagnosis [19]. Only when complete remission was achieved (in one-third of this sample), did patients show a significantly improved HRQoL. To determine the effect of PNES themselves (rather than associated psychopathology) on HRQoL, this study explores the
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relationship between seizure frequency and HRQoL in a much larger group of patients with PNES. We hypothesized that there would be a significant correlation between seizure frequency and HRQoL. Given that we interpret PNES as a manifestation of psychosocial distress, we further predicted that this correlation would not remain significant when psychological distress (or the number of other somatic symptoms as a correlate of distress) is taken into account. Measures of HRQoL are increasingly used to offer insights into patients’ subjective illness experience and to evaluate treatment outcomes. An improved understanding of HRQoL in PNES not only enhances our knowledge of the nature of this disorder, but can also inform our use and analysis of patient-reported outcome measures and measures of seizure frequency in future intervention studies in this patient group. 2. Methods 2.1. Patients This study is based on responses from patients referred for outpatient psychotherapy to a specialized service within the neurology departments of the Royal Hallamshire Hospital and the Barnsley District General Hospital in the United Kingdom between October 2003 and April 2008. During the recruitment period, the psychotherapy service accepted referrals of patients with functional (medically unexplained) neurological symptoms or psychological distress associated with (medically explained) neurological disorders from three different, fully trained neurologists. The findings described here are derived from the analysis of information provided by all patients with PNES referred during the study period. All referring neurologists had ready access to video/EEG and ambulatory EEG monitoring, but their clinical diagnosis of PNES was not confirmed by video/EEG monitoring in all patients. For instance, the diagnosis could also be based on home video recordings of seizures, direct observation of seizures in the clinic room, or a history and witness accounts highly suggestive of PNES, as long as other investigations (MRI, interictal EEG) did not raise any doubts about the clinical diagnosis. Patients with additional epilepsy were excluded from this study. The diagnosis of additional epilepsy was made clinically if both epileptic and nonepileptic seizures had been captured by ictal EEG or video/EEG recordings, or if the patient’s history or witness accounts suggested that the patients had additional seizures that were different from their PNES and that had not been captured by video/EEG or ambulatory EEG investigations. A diagnosis of possible additional epilepsy was also made in patients in whom interictal tests (e.g., interictal epileptiform activity) called the diagnosis of PNES (without epilepsy) into question. Patients were also excluded from this study if their PNES frequency could not be ascertained. This data set was collected in the context of an ongoing service evaluation approved by the clinical governance lead for the Sheffield Teaching Hospitals NHS Foundation Trust.
They were asked to complete this questionnaire and return it to the psychotherapy service to indicate that they wished to take up the offer of psychotherapy. The questionnaire comprised demographic questions and three validated measures. The SF-36 Health Survey [20] is a 36-item self-report questionnaire providing one multi-item scale measure of eight health concepts that can be added up to form summary subscores. The Physical Health Component Summary score is made up of four concepts: Physical Functioning (10 items), Role Limitation due to Physical Health Problems (4 items), Bodily Pain (2 items), and General Health (5 items). The Mental Health Component Summary score also results from the addition of four concept scores: Vitality (4 items), Social Functioning (2 items), Role Limitations due to Emotional Problems (3 items), and Mental Health (5 items). The SF-36 raw data were transformed to 0–100 scores so that comparisons could be made across the eight subscales, where low scores indicate poor health and functioning [21]. The Clinical Outcomes in Routine Evaluation (CORE-10) [22] is a patient-completed, hand-scored brief outcome measure comprising 10 items from the CORE-OM, a 34-item assessment and outcome measure. The CORE-10 taps self-reported global psychological distress, acting as a quick and easy screening tool and placing minimal demands on patients. The measure provides a balance of the 10 clinical domains from the CORE-OM: Subjective WellBeing, Anxiety, Depression, Physical, Trauma, General Functioning, Close Relationships (Functioning), Social Relationships (Functioning), Risk to Self, and Risk to Others. Each item is scored on a 5-point scale ranging from 0 to 4, with higher scores indicating a greater level of distress and disability. The CORE-10 correlates closely with the CORE-OM [22], which has been validated in large clinical and nonclinical samples and shows strong correlation with different well established measures of depression such as the Beck Depression Index [23,24]. The Patient Health Questionnaire (PHQ)-15 is composed of 15 physical symptoms that have been extracted from the PHQ. This is part of the self-administered PRIME MD diagnostic instrument for common mental disorders [25]. The 15 symptoms do not include blackouts or seizures. Symptoms over the last 4 weeks are rated as 0 (‘‘not at all bothered”), 1 (‘‘bothered a little”), or 2 (‘‘bothered a lot”) [26]. A number of studies suggest that scores on the PHQ-15 correlate with psychological distress [27–29]. 2.3. Statistical analysis Kolmogorov–Smirnov tests demonstrated that all of the variables (including SF-36 subscales) were nonnormally distributed; therefore Spearman’s correlations were carried out. Partial correlations were used to examine the correlation between seizure frequency and HRQoL when physical symptoms and global psychological distress were controlled for. The analyses were carried out using SPSS (Version 15).
2.2. Measures
3. Results
A screening questionnaire was completed by the neurologists when they made their initial referral to the psychotherapy department. This included information on the frequency and duration of patients’ seizures, as well as current physical comorbidity, current medication including anticonvulsant drugs, and past medical history. The seizure frequency at the time of referral was determined by questioning patients and carers in all cases and by checking seizure diaries when available. Patients provided information on their HRQoL, levels of psychological distress, and physical symptoms on a questionnaire they received 1 to 3 weeks after the appointment with the neurologist.
During the study period, 231 patients returned completed questionnaires to the psychotherapy service. Of these 161 patients had been referred with a diagnosis of PNES, although 58 had to be excluded because the frequency of their seizures could not be ascertained by the referring neurologist. Seven additional patients were excluded because they had additional epileptic seizures. After these exclusions, 96 patients were included in this study (see Table 1 for demographic characteristics). As the scores on the measures were not normally distributed, median values were inspected rather than means. Table 2 lists the median scores for the SF-36, PHQ-15, and CORE–10.
G. Lawton et al. / Epilepsy & Behavior 14 (2009) 167–171 Table 1 Demographics of the patient sample (n = 96) Variable Female (%) Age (mean number of years) Education (mean number of years) Duration of PNES disorder (median number of years) Frequency of seizures (median number/month) Employment status (%) School/college University Employed Self-employed Unemployed Receiving disability benefits Retired on health grounds Receiving old age pension
74 38.38 (12.47) 13.78 (5.42) 4 (39.90) 6 (899.80) 5.2 5.2 22.9 4.2 15.6 36.5 6.3 1.0
Table 2 Median scores and ranges for measures of HRQoL (SF-36), psychological distress (CORE-10), and physical symptoms (PHQ-15) Variable
Median (range)
SF-36 Physical Health Component summary Mental Health Component summary Physical Functioning Role Limitation: physical Bodily Pain General Health Vitality Social Functioning Role Limitation: emotional Mental Health Core-10 PHQ-15
36.92 (51.06) 34.9 (55.39) 50 (100) 0 (100) 35.93 (100) 37 (82) 30 (85) 37.5 (100) 33.33 (100) 50 (100) 16 (38) 14.15 (25)
To investigate more specifically the impact of the seizures on HRQoL, PNES frequency and the summary scales and subscales of the SF-36 were correlated (see Table 3 for correlation coefficients). Seizure frequency was found to be significantly correlated to all measures of HRQoL excluding Vitality and General Health, suggesting HRQoL is reduced as seizure frequency increases. Interestingly, seizure frequency was most strongly and significantly correlated with Bodily Pain and Social Functioning, suggesting patients who have more seizures also experience more Bodily Pain and report a greater impairment of social functioning. CORE-10 scores were significantly correlated with SF-36 Mental Health Component Summary scores (rs = –0.663, P < 0.001), but not Physical Component Summary scores. Similarly, PHQ-15 scores were significantly correlated with SF-36 Physical Component Summary scores (rs = 0.454, P < 0.001), but not with SF-36 Mental Table 3 Spearman’s q correlation coefficients for seizure frequency versus subscales and summary scales of the HRQoL measure (SF-36) and significance value SF-36 scale
rs
P
R2
Physical Health Component summary Mental Health Component summary Physical Functioning Role Limitation: physical Bodily Pain General Health Vitality Social functioning Role Limitation: emotional Mental Health
–0.246a –0.233a –0.219a –0.259a –0.387a –0.137 –0.141 –0.460a –0.219a –0.193a
0.016 0.022 0.032 0.011 0.00 0.184 0.172 0.00 0.032 0.059
0.061 0.054 0.048 0.067 0.150 0.019 0.020 0.212 0.048 0.037
Significantly correlated (a < 0.05).
Health Component Summary scores. CORE-10 and PHQ-15 scores were also significantly correlated (rs = 0.310, P < 0.002). To try and establish whether seizure frequency affects HRQoL independently of psychological distress or other physical symptoms, partial correlations were carried out. In these calculations we examined the correlation between seizure frequency and the SF-36 scores while controlling for CORE-10 and PHQ-15 scores (see Table 4 for correlation coefficients). When psychological distress and physical symptoms were controlled for, there was no significant correlation between seizure frequency and the SF-36 summary scores. However, the correlation between seizure frequency and Bodily Pain, as well as Social Functioning, remained significant. 4. Discussion
Note. Values in parentheses are ranges for median values.
a
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We examined the relationship between seizure frequency, HRQoL, psychological distress, and physical symptoms in patients with PNES. The general aim was to discover if seizure frequency was related to subjective HRQoL or, somewhat more specifically, to what extent seizures (rather than the causative or associated psychomorbidity) influence HRQoL. Our main hypothesis was confirmed; seizure frequency was found to be significantly correlated with HRQoL as measured by the SF-36 summary measures for Physical Health and Mental Health. HRQoL is reduced as seizure frequency increases. However, the correlation is relatively moderate, with seizure frequency accounting for only 6% of the variance in HRQoL. What is more, this result is rendered nonsignificant when psychological distress and physical symptoms are controlled for (either separately or in conjunction). First, this suggests that HRQoL is not independently related to seizure frequency. Second, it illustrates that there is a close association between PNES frequency, levels of psychological distress, and number of other physical symptoms experienced. Examination of the subscales of the SF-36 provides further interesting findings. Seizure frequency was significantly correlated with all SF-36 subscales with the exception of General Health and Vitality. The subscales Bodily Pain and Social Functioning were found to have the strongest correlations, accounting for 14.9 and 21.2% of the variance, respectively. Correlations at this level suggest a moderate relationship between two variables. These correlations remained significant when psychological distress and other physical symptoms were controlled for. It is not difficult to see why patients experiencing a greater number of seizures would be more disabled in their social interactions. A recent study that used Interpretative Phenomenological Analysis to examine interviews with patients with PNES after they had received the diagnosis identified social isolation as one of their biggest problems [30]. The correlation between PNES and Bodily Pain is more surprising. One previous study identified a correlation between the severity of the manifestations of the PNES syndrome and the number of physical symptoms (including pain) [4]. Another reported that chronic pain disorder and/or fibromyalgia are so regularly associated with PNES that they can be considered a diagnostic pointer [2]. It has also been reported that 75% of patients complained of moderate to severe pain 6 months after the diagnosis of PNES had been made [31]. In our clinical experience, a subgroup of patients report that their seizures are triggered by pain. Of course, both pain and PNES may be aspects of a particularly somatic focus for psychological distress. The closer inspection of the SF-36 subscores also reveals an interesting difference in scores for Physical Functioning and Role Limitation Physical. Although patients reported only average levels of limitations on the activities described due to physical health, they experienced high levels of impairment in their role functioning related to their physical health. This finding is similar to that
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Table 4 Spearman’s q correlation coefficients between seizure frequency and HRQoL (SF-36), controlling for psychological distress (CORE-10), other physical symptoms (PHQ-15), or both SF-36 scale
CORE-10
PHQ-15
PHQ-15 and CORE-10
Mental Health Component summary Physical Component summary Physical Functioning Role Limitation: physical Bodily Pain General Health Vitality Social Functioning Role Limitation: emotional Mental Health
–0.106 –0.169 –0.112 –0.130 –0.237a –0.109 –0.191 –0.238a –0.143 –0.005
–0.100 –0.156 –0.101 –0.118 –0.234a –0.098 –0.182 –0.223a –0.133 –0.017
–0.111 –0.162 –0.098 –0.118 –0.233a –0.095 –0.183 –0.233a –0.137 –0.001
a
Significantly correlated (a < 0.05).
reported by Szaflarski and Szaflarski [8]. The questions contributing to the Physical Functioning score of the SF-36 are quite strongly based on patients’ mobility and may not reflect other aspects of physical dysfunction associated with PNES sufficiently well. Alternatively, the impairment of role functioning in patients with PNES may be related to avoidance and self-imposed restrictions on activity due to fear of having a seizure rather than actual physical disability. Finally, it may be characteristic of patients with PNES to overstate disability despite relatively well-preserved functioning. These findings need to be considered in relation to the limitations of this study. Despite the fact that our method of data collection ensured that we were able to capture responses from all patients who accessed our service, our findings may have been affected by selection bias: This sample was derived from patients who had decided to opt in to psychotherapy but who had not yet commenced treatment. We are aware that the patients referred for treatment were preselected by the neurologists involved in our treatment pathway. They did not refer patients with PNES who were explicitly hostile to the idea of psychotherapy. They may also not have referred patients with particularly ‘‘mild” or recent PNES disorders. It is possible that the exclusion of some of the most severe and some of the least disabled cases has affected our results. What is more, we previously found that about 20% of the patients referred by neurologists do not return their opt-in questionnaires [32]. We do not have any information on patients who were referred and patients with PNES not referred or on patients who were referred but chose not to opt in. We are therefore unable to comment on any similarities or differences between responders and nonresponders. It may be that the patients who opted in to treatment had higher levels of psychopathology than the PNES patient population as a whole. However, the mean score of our patient group on the CORE-10 was 15.7, which actually lies between the mean scores expected for nonclinical and clinical populations (4.7 and 19.7, respectively) [22]. It is also important to note that, at this point, our results should not be generalized beyond the interval between diagnosis of PNES and commencement of psychological treatment without further confirmation. The fact that no patients had the time to be considered ‘‘under remission” is an important limitation; the relationship between PNES frequency and HRQoL may have been stronger if we had included patients in remission or conducted a longitudinal study involving a longer latency between communication of the diagnosis and determination of seizure outcome and HRQoL. This limitation is especially important because one much smaller previous study demonstrated a relatively robust effect of remission on HRQOL [19], and others demonstrate that seizure frequency can improve or remit merely by clear and compassionate explanation, rather than by any more formal psychological or psychiatric treatments [33].
Another potential weakness of this study was the ascertainment of patients’ seizure frequency. Seizure diaries or witness confirmation was not available in all cases. It may be that the self-estimate of seizure frequency reflected the level of patients’ distress at the time of the consultation. What is more, the other measures were completed 1 to 3 weeks following the encounter with the neurologist. It is thus possible that a patient’s seizure frequency had changed by the time HRQoL was determined, although the patients seen had had PNES for a mean of 4 years at the time of referral for psychotherapy. Despite these limitations, our findings provide further information about the nature of PNES. The relationship between seizure frequency and subjective quality of life is clearly complex. Our study suggests that this relationship is mediated by psychological distress as well as physical symptoms. Our results also show that patients report being more limited by their physical health than their reported physical functioning might suggest. This would imply that treatments targeted at PNES should not focus solely on the reduction of seizures, but should also take into account levels of psychological distress and physical symptoms when aiming to improve patient’s HRQoL. Techniques that could improve patients’ ability to tolerate pain and measures that would tackle avoidance and reduce social isolation might be particularly beneficial. The correlation between seizure frequency and HRQoL suggests that a seizure reduction (rather than only a cessation of seizures) is likely to represent a worthwhile treatment outcome. There is, therefore, a justification for treatment studies to report intervention effects on seizure frequency. Our results also support the validity of the SF-36, CORE-10, and PHQ-15 in this population, as the CORE-10 correlated significantly with the SF-36 Mental Health Component, but not the Physical Health Component, and the PHQ15 correlated significantly with the Physical Health Component, but not the Mental Health Component. Future research should aim to evaluate the relationship between seizure frequency and HRQoL in a longitudinal fashion and assess whether therapy targeted at decreasing seizure frequency results in a corresponding improvement in HRQoL. References [1] Reuber M. Psychogenic nonepileptic seizures: answers and questions. Epilepsy Behav 2008;12:622–35. [2] Benbadis SR. A spell in the epilepsy clinic and a history of ‘‘chronic pain” or ‘‘fibromyalgia” independently predict a diagnosis of psychogenic seizures. Epilepsy Behav 2005;6:264–5. [3] Bowman ES, Markand ON. Psychodynamics and psychiatric diagnoses of pseudoseizure subjects. Am J Psychiatry 1996;153:57–63. [4] Reuber M, House AO, Pukrop R, Bauer J, Elger CE. Somatization, dissociation and general psychopathology in patients with psychogenic non-epileptic seizures. Epilepsy Res 2003;57:159–67. [5] Leidy NK, Elixhauser A, Vickrey B, Means E, Willian MK. Seizure frequency and the health-related quality of life of adults with epilepsy. Neurology 1999;53:162. [6] Boylan LS, Flint LA, Labovitz DL, Jackson SC, Starner K, Devinsky O. Depression but not seizure frequency predicts quality of life in treatment-resistant epilepsy. Neurology 2004;62:258–61. [7] Loring DW, Meador KJ, Lee GP. Determinants of quality of life in epilepsy. Epilepsy Behavior 2004;5:976–80. [8] Szaflarski JP, Szaflarski M. Seizure disorders, depression, and health-related quality of life. Epilepsy Behav 2004;5:50–7. [9] Amir M, Roziner I, Knoll A, Neufeld MY. Self-efficacy and social support as mediators in the relation between dsease severity and quality of life in patients with epilepsy. Epilepsia 1999;40:216–24. [10] Suurmeijer TPBM, Reuvekamp MF, Aldenkamp BP. Social functioning, psychological functioning, and quality of life in epilepsy. Epilepsia 2001;42:1160–8. [11] Senol V, Soyuer F, Arman F, Öztürk A. Influence of fatigue, depression, and demographic, socioeconomic, and clinical variables on quality of life of patients with epilepsy. Epilepsy Behav 2007;10:96–104. [12] Al Marzooqi SM, Baker GA, Reilly J, Salmon P. The perceived health status of people with psychologically derived non-epileptic attack disorder and epilepsy: a comparative study. Seizure 2004;13:71–5.
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