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Epilepsy & Behavior 86 (2018) 37–48

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Epilepsy & Behavior

journal homepage: www.elsevier.com/locate/yebeh

Review

Emotion dysregulation in patients with psychogenic nonepileptic


seizures: A systematic review based on the extended process model
Isobel Anne Williams a,⁎, Liat Levita a, Markus Reuber b
a
Department of Psychology, The University of Sheffield, Cathedral Court, 1 Vicar Lane, Sheffield S1 2LT, United Kingdom
b
Academic Neurology Unit, The University of Sheffield, The Royal Hallamshire Hospital, Glossop Road, Sheffield S10 2JF, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: Psychogenic nonepileptic seizures (PNES) are characterized by paroxysmal alterations in motor and sensory
Received 23 April 2018 functions resembling epileptic seizures, but are not caused by epileptiform activity. In recent years, there has
Revised 21 June 2018 been increasing scientific interest in emotion dysregulation in patients with PNES (pwPNES), but the literature
Accepted 27 June 2018
has not yet been interpreted within a broader model of emotion dysregulation. The aim of this review was there-
Available online xxxx
fore to synthesize the existing literature on emotion dysregulation in pwPNES within the extended process
Keywords:
model (EPM) of emotion regulation.
Psychogenic nonepileptic seizures Methods: PubMed and Web of Science were searched for studies relevant to emotion dysregulation as defined
Emotion regulation by the EPM. These studies were subjected to a bespoke quality appraisal tool. Studies of acceptable quality
Psychopathology were categorized to the different stages of the EPM and critically appraised.
Alexithymia Results: Studies of emotion regulation in pwPNES were generally of low quality — a finding largely driven
Avoidance by small sample sizes. However, there was evidence of emotion dysregulation characterized by deficits in
Dissociation the identification of patients' own emotional states, as well as the selection and implementation of maladaptive
regulatory strategies, and altered exteroceptive emotional processing. However, heterogeneity in findings
suggests that emotion dysregulation is likely linked to other psychological factors and not common to all
pwPNES.
Significance: This review suggests that while pwPNES are likely to experience emotion dysregulation as defined
by the EPM, there is variability in the distribution of regulatory deficits in this patient population, and a person-
centered approach should be taken when working with these patients. There is a need for more high quality and
better-powered studies in this area.
© 2018 Elsevier Inc. All rights reserved.

1. Introduction trend for research on emotion dysregulation (ED) in patients with


PNES (pwPNES), and an integrative psychological model has been pro-
Psychogenic nonepileptic seizures (PNES) are assumed to be be- posed (e.g., [4]), observations of ED in pwPNES have not previously
havioral and experiential responses to aversive triggers [1]. Superficially been placed within a more general theory of emotion regulation. We
resembling epileptic seizures but unassociated with epileptiform propose the extended process model (EPM) of emotion regulation as a
activity, PNES are relatively common, associated with long-term disabil- potential model structure [5].
ity and a heavy economic burden [2]. Current biopsychosocial models
attribute PNES to a complex interaction of predisposing, precipitating,
1.1. A summary of the extended process model of emotion regulation
perpetuating, and triggering factors — several of which relate to an indi-
vidual's capacity to regulate their own emotions [3]. Relevant etiological
Emotion regulation can be defined as the process by which a person
factors include previous exposure to trauma, dissociation, coping,
modifies or controls what emotions they are experiencing, when they
alexithymia, and insecure attachment [1]. While there is a growing
have them, and the nature in which emotions are experienced
or expressed [6]. The EPM conceptualizes emotion regulation as a
series of ‘valuations’ across three stages: identification, selection, and
⁎ Corresponding author.
implementation. Each valuation also consists of three substeps, begin-
E-mail addresses: isobel.williams@sheffield.ac.uk (I.A. Williams), ning with a representation of the internal or external environment
l.levita@sheffield.ac.uk (L. Levita), m.reuber@sheffield.ac.uk (M. Reuber). (perception substep). The representation is compared against a goal–

https://doi.org/10.1016/j.yebeh.2018.06.049
1525-5050/© 2018 Elsevier Inc. All rights reserved.
38 I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48

state (valuation substep), and if there is a sufficient discrepancy be- or if the methodologies used did not directly relate to a stage of the
tween the environment and the goal–state, the action substep is trig- EPM [15, 16]. Finally, each article was clustered to one or more specific
gered. The functions of these substeps are constrained by the stage of stages of the EPM according to the methodologies or measures used.
the EPM that the valuation system is within. During identification, an The categorization of each study into stages of the EPM was proposed
ongoing emotion is identified (e.g., disgust), and a decision is made by IW and confirmed by LL.
whether or not to regulate the emotion based on the discrepancy be-
tween the current emotion and a goal emotional state. During selection, 2.3. Quality assessment
a general emotion regulation strategy (e.g., attentional deployment) is
decided upon. This triggers the implementation stage, during which Eligible articles were rated according to an appraisal tool designed
the general regulatory strategy is translated into specific tactics suitable specifically for quantitative psychological research in this field [1],
for the current situation (e.g., distraction from the disgust-eliciting which clarifies whether i) all diagnoses were video-EEG confirmed
stimulus). In the case of successful emotion regulation, the process (yes/no), ii) epilepsy was explicitly ruled out in the group with PNES
cycles through again until the regulatory goal is reached (e.g., the indi- (yes/no), iii) there was reference to a procedure ensuring PNES were
vidual is no longer feeling disgusted), in a continuous, multimodal, not misdiagnosed panic attacks (yes/no), iv) recruitment was consecu-
and iterative process. Emotion dysregulation can be thought of as a dis- tive (yes/no), and v) dependent variables were standardized (yes/no).
ruption at any substep of these stages. Number, type, and gender ratio of control groups (where appropriate)
The EPM is the most recent iteration of the widely used and tested were recorded to ensure groups were matched and did not have PNES
Process Model of Emotion Regulation [7] and has already been used to (yes/no) (a difference in gender ratio of b10% or mean age difference
conceptualize ED in a variety of populations and contexts including of bfive years between-groups was considered matched). Very few
(but not limited to) psychopathology in general [8]. The potential studies presented formal power calculations justifying sample sizes;
value in interpreting studies of ED in pwPNES within an explicit theoret- therefore, we rated sample size according to the power and effect size
ical framework such as the EPM is that i) it may allow for a more precise conventions proposed by Cohen [17] and used in a previous systematic
understanding of how and why ED occurs, and ii) it may allow for a review of PNES [1]. Sample sizes for studies were rated as being very
more direct comparison against ED in other populations. The aim of poor (b 15 participants in each group; i.e., b 80% power to detect a very
this review was therefore to synthesize the existing literature on ED in large effect size, Cohen's d = 1.1), poor (b 26 participants in each
pwPNES according the EPM [5]. group; i.e., b 80% power to detect a large effect size, d = 0.8), moderate
(26–63 participants in each group; i.e., ≥ 80% power to detect a large
2. Methods effect size, d = 0.8), or good (≥ 64 participants in each group;
i.e., ≥80% power to detect a medium effect size, d = 0.5), assuming a
A systematic review was conducted. Data were reported according two-tailed independent t-test with alpha = 0.05. Study quality was
to the Preferred Reporting Items for Systematic Reviews and Meta- calculated from these eight different quality criteria and sample power
analysis (PRISMA) checklist [9]. The definition of ED was based on the [1]. To establish interrater reliability, each article was rated by IW and
EPM [5]. The diagnosis of PNES does not map neatly onto any one MR. Any disagreements on ratings were resolved following discussion.
of the nosological categories of the Diagnostic and Statistical Manual Studies rated as ‘unacceptable’ were subsequently excluded from
of Mental Disorders, 5th Edition: DSM-5, but usually fulfils the the review.
diagnostic criteria of Functional Neurological Symptom (Conversion)
Disorder (FND) [10] as a Conversion Disorder falling under the subtype
of “with attacks or seizures”. The diagnostic process clinically defining 3. Results
PNES has been outlined in a consensus paper by the International
League Against Epilepsy [11]. 3.1. Quality assessment

2.1. Search strategy Fifty one papers were identified in the search (Fig. 1), all of which
were included in the quality assessment (Appendix 1). ‘Unacceptable’
The electronic databases PubMed and Web of Science were searched ratings were given in four (7.8%), ‘low’ in 24 (47.1%), ‘medium’ in 20
on 18th January 2018 (years 1894–2017). Search terms relating to PNES (39.2%), and ‘high’ in 3 (5.9%) studies. The median case group size
were taken from a recent review article on PNES [12]. Search terms re- was 30, but only 52% of studies (case–control design) were adequately
lating to ED were taken from or synonymous with keywords in the EPM powered (defined as moderate or good power). Sixteen of the 24 low
[5]. Please see additional web content for more details of the search quality studies would have been rated medium quality if they had
terms used. Further articles were identified from the reference list of a sample size ≥26. Likewise, the four excluded studies were deemed
papers identified during the electronic database search. inadmissible because of a sample size b15; all of these studies would
have been classed moderate to high quality on the basis of the
2.2. Study selection other quality criteria. In terms of individual quality rating criteria, all
dependent variables were standardized in 92%; an explicit reference
Article titles and abstracts were screened for relevance to the re- to epilepsy being ruled out was made in 77%; all PNES cases were con-
view topic and compared against inclusion and exclusion criteria by firmed with video-EEG in 71%; anxiety attacks were ruled out in 51%,
IW. Only peer-reviewed original research reports were included. All and patients were recruited consecutively in 37% of studies subjected
other types of publications and articles not written in English were to the quality review. Forty-seven studies were included in the final
excluded from the review. Studies not directly relevant to the mecha- review.
nism of ED in pwPNES only (i.e., explicitly defined case groups with
mixed FND or with comorbid epilepsy) were also excluded at this 3.2. Categorization of studies
stage. Studies of pediatric populations or treatment for PNES, and
studies that focused on patients' support networks were considered Twenty-three studies were categorized as relevant to the identifi-
outside the scope of the review. The remaining full-text articles were cation stage of the EPM because the measures and methodologies
read in full by IW and MR. Articles were excluded if dependent vari- used captured participants' identification of their own emotions
ables were not quantitative standardized psychological measures and (Appendix 2). Thirty-three studies were deemed relevant to the selec-
were therefore incompatible with the quality rating system [13, 14] tion and implementation stages.
I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48 39

Fig. 1. PRISMA flowchart.

4. The identification stage There are three subscales measuring ‘difficulty describing feelings
(DDF)’, ‘difficulty identifying feelings (DIF)’, and ‘externally orientated
Studies pertaining to the identification stage in pwPNES were thinking (EOT)’ – the latter referring to a tendency to focus on external
grouped into two themes: i) alexithymia/emotional awareness and rather than internal events and experiences [19]. Usually, an individual
ii) perceptions of stress. reporting a total TAS-20 score of ≥ 61 is considered ‘alexithymic’, and
those scoring between 52 and 60 are considered ‘possibly alexithymic’
4.1. Alexithymia/emotional awareness [19].
Ten studies reporting a total TAS-20 score used a case–control de-
The ability of pwPNES to detect and interpret their own emotions sign (Table 1). Of these ten studies, two classified the group with
has most frequently been assessed with self-report measures of PNES as alexithymic (i.e., mean total TAS-20 N 61) with 90% and 63%
alexithymia. Alexithymia is a psychological construct describing diffi- of the group with PNES scoring above the clinical cutoff for alexithymia
culties with the identification and description of feelings as well as respectively [20, 21]. In seven studies, the mean group with PNES
their differentiation from sensations associated with physiological pro- scores were within the ‘possibly alexithymic range’ [22–28]. Patients
cesses [18]. Other studies have investigated the accuracy of patients' with PNES in five of these ten studies were compared against healthy
reporting on emotions/feelings by comparing patients' self-reported controls, patients with epilepsy in five, or patients with functional
emotions against more objective measures of the same construct. movement disorders (FMD) in two. The group with PNES scored
more highly on the total TAS-20 score than healthy controls in all
4.1.1. Self-report studies of alexithymia — the Toronto Alexithymia Scale five studies with a healthy control group [20, 21, 25, 26, 29]. Patients
(TAS-20) with PNES only scored more highly than patients with epilepsy on
The most frequently used alexithymia measure was the twenty-item the total TAS-20 in one of the three studies with a control group
TAS-20, which assesses patients' ability to identify their own emotions. with epilepsy [23]. Of the two studies with a control group with
40 I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48

Table 1 In summary, these data suggest pwPNES, as a group, are more


Mean and standard deviation (unless otherwise stated) of total TAS-20 scores for pwPNES alexithymic than healthy controls, with a tendency towards scoring
and control group(s).
within the ‘possibly alexithymic’ range (close to the clinical cutoff for
Study authors PNES HC CWE FMD alexithymia) on the TAS-20. Given the concept of alexithymia was de-
Bewley et al. (2005) 72.2 (11.8) 50.9 (11.9)a 68.6 (11.9) – veloped to capture a putatively core feature of psychosomatic disease
Demartini et al. (2016) 50.6 (12.7) 40.9 (10.1)a – 50.3 (12.6) [32], it is perhaps surprising that the total mean score of TAS-20 found
Ekanayake et al. (2017) 56.6 (12.2) – – 43.1 (10.3)c in this review did not exceed the clinical threshold. However, the gener-
Kaplan et al. (2013) 56.2 (12.4) – 51.9 (12.1)b –
ally low sample sizes and the heterogeneous psychological profiles of
Myers, Matzner et al. 54.1 (1.7) – 50.1 (2.4) –
(2013) pwPNES [33] raise the possibility that the results in these studies could
O'Brien et al. (2015) 54.7 (13.4) 39.6 (11.2)a – – be an artefact of sampling bias or insufficient sample size. Consistent
Schönenberg et al. (2015) 54.6 (11.6) 43.9 (6.7)a – – with this idea, and illustrating the psychological heterogeneity in PNES,
Tojek et al. (2000) 54.0 (11.9) – 54.4 (10.4) – a subgroup analysis found no differences in TAS-20 scores between
Urbanek et al. (2014)d 64.9 (30–9) 41.5 (22–8)a – –
Wolf et al. (2015) 54.7 (11.9) – 53.1 (10.8) –
pwPNES and patients with epilepsy, but yielded two subgroups of
Total 57.3 (6.4) 43.4 (21.4) 55.6 (27.8) 46.7 (5.1) pwPNES: one (n = 11) characterized by high total TAS-20 scores, and
a second (n = 32) characterized by relatively low total TAS-20 scores
Note. PNES = psychogenic nonepileptic seizures, HC = healthy control group, CWE =
control group with epilepsy, FMD = control group with functional movement disorder. [34]. Therefore, it may be more appropriate for designs using the
a
Healthy control group is significantly different from group with PNES. TAS-20 to accommodate this heterogeneity with larger sample sizes
b
Control group with epilepsy is significantly different from group with PNES. and subgroup analyses.
c
Control group with FMD is significantly different from group with PNES.
d
Values are median and range.

4.1.2. Other measures of alexithymia/emotional awareness


Other methodologies designed to assess emotion identification
FMD, one found a significantly higher TAS-20 score in the group with in pwPNES have yielded a more consistent pattern. A cross-sectional
PNES [22]. A total mean and standard deviation for total TAS-20 scores comparison of pwPNES against healthy controls using the Emotional
in each group in the ten studies was calculated (Table 1). This yielded a Processing Scale-25 (EPS-25) [35] found elevated scores on the
score of 57.3 (SD = 6.4). ‘impoverished emotional experience’ subscale [36]. This subscale
One study did not use the TAS-20 in a case/control design, but in- describes a detached experience of one's emotions due to poor insight.
stead correlated the Total TAS-20 score against a measure of coping Uliaszek et al. [37] used the Difficulties with Emotion Regulation
(as assessed by the Coping Inventory for Stressful Situations) [30]. Scale (DERS) to delineate two subgroup profiles of pwPNES; one with
A small negative correlation (r = − 0.26) between the TAS-20 total higher than normative values on the ‘emotional clarity’ and ‘emotional
score and task-focused coping, and a moderate-to-large positive corre- awareness’ subscales of the DERS, and one with lower than normative
lation (r = 0.54) between the total TAS-20 score and emotion-focused values on the ‘emotional awareness’ subscale [37], which supports the
coping, suggested alexithymic traits in pwPNES may be related to suggestion that pwPNES are unlikely to have uniform emotion regula-
coping style. tion deficits.
Six studies reported TAS-20 subscale values (Table 2). The DIF sub- Comparisons of patients' self-reported emotions against more ob-
scale was higher in pwPNES compared with that of the controls with jective measures also suggest pwPNES are prone to deficits in the iden-
epilepsy or healthy controls in four [20, 21, 23, 26]. The DDF subscale tification stage. Goldstein and Mellers [38] noted that pwPNES reported
was higher in pwPNES than in the controls with epilepsy or healthy more somatic symptoms of anxiety during seizures than patients with
controls in three [20, 21, 23]. There were no between-group differences epilepsy, but did not report higher subjective levels of anxiety than pa-
in EOT scores. These results suggest that alexithymic traits in pwPNES tients with epilepsy. Similarly, Dimaro et al. [39] observed a significant
might be restricted to a difficulty with identifying and describing discrepancy between scores on an implicit measure (Implicit Relational
feelings, without a tendency to focus on external events. However, the Assessment Procedure) and explicit measure (State–Trait Anxiety
conclusion that pwPNES do not exhibit a tendency to focus more on ex- Inventory) of anxiety in pwPNES but not those with epilepsy. Likewise,
ternal experiences than control groups needs to be taken with caution, Prigatano and Kirlin [40] found that while pwPNES and epilepsy
as concerns have been raised about the reliability and validity of the self-reported similar levels of psychopathology on the Personality
EOT subscale when applied to patients with somatization disorders; Assessment Inventory, pwPNES performed significantly worse on a
the EOT subscale has been shown to have lower internal consistency more objective neuropsychological measure of emotion regulation (the
than the other TAS-20 subscales, and unlike the DIF and DDF subscales, Barrow Neurological Institute Screen for Higher Cerebral Functions Affect
the EOT subscale was also found to be unrelated to the number of subtest). The fact that discrepancies between objective and subjective
somatic symptoms patients report [31]. measures of the same construct are restricted to the group with PNES

Table 2
Mean and standard deviation (unless otherwise indicated) of TAS-20 subscale scores for pwPNES and control groups.

Difficulty identifying feelings Difficulty describing feelings Externally orientated thinking

PNES HC ES PNES HC CWE PNES HC ES

Bewley et al. (2005) 27.1 (6.3) 11.9 (5.8)⁎ 25.2 (6.4) 18.5 (3.9) 12.1 (4.0)⁎ 15.7 (3.3)⁎ 26.5 (4.8) 27.1 (4.4) 27.4 (4.6)
Brown et al. (2013)a 24 (11) – 18 (12.5) 16 (8) – 12 (7) 23 (13) – 21 (9)
Kaplan et al. (2013) 20.9 (6.9) – 18.5 (7.1)⁎ 14.7 (4.6) – 13.4 (4.1)⁎ 20.61 (4.2) – 20.0 (4.4)
Urbanek et al. (2014)b 25 (11–35) – 13 (7–32)⁎ 18 (7–25) – 11 (5–25)⁎ 22 (9–34) – 17 (9–28)
Schönenberg et al. (2015) 17.6 (7.6) 12.6 (5.2)⁎ – 12.9 (4.1) 10.7 (2.6) – 24.1 (3.9) 24.8 (3.7) –
Wolf et al. (2015) 59.1 (12.1) – 55.4 (13.2) 51.7 (11.6) – 50.2 (11.2) 49.9 (11.1) – 51.2 (9.5)

Note. HC = healthy control group, CWE = control group with epilepsy.


a
Values are median and interquartile range.
b
Values are median and range.
⁎ Statistically significantly different from PNES values.
I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48 41

suggests that emotion identification may be a particular problem for healthy controls [36, 52, 53]. An over-reliance on emotion-focused cop-
pwPNES and not for those with epilepsy. ing strategies might be explained by an external locus of health control;
pwPNES have been demonstrated to perceive more situations as be-
4.2. Perceptions of stress yond their control and to have a stronger health-related external locus
of control than healthy controls [51, 54]. Therefore, case–control studies
Impaired emotion identification does not mean that pwPNES experi- suggest that pwPNES rely on emotion-focused coping to manage nega-
ence an absence of affect. This is reflected in studies investigating tive emotion, with some indication that this is related to an external
patients' perceptions of how stressful their lives are. Four studies locus of control.
demonstrated pwPNES perceive their lives as more stressful than Studies including cluster and subgroup analyses provide a
healthy controls or the general population [26, 28, 41, 42]. One might more nuanced picture of coping in PNES. Myers et al. [55] categorized
argue that this is to be expected given the known detrimental effect of pwPNES according to several criteria, one of which was the presence/
living with a disability on quality of life [43]. However, pwPNES subjec- absence of psychological trauma. Traumatized patients were charac-
tively rated stressful life events as more distressing than patients with terized by a significant elevation on the demoralization scale of
epilepsy, even though objectively they did not experience any more the Dutch Short Minnesota Multiphasic Personality Inventory
stressful life events than the controls with epilepsy and healthy controls (MMPI) [56], implying a ‘persistent failure to cope internally or exter-
[44]. This finding suggests that pwPNES may have magnified percep- nally with life’. This suggested that only traumatized pwPNES had
tions of stress over and above that of individuals living with nonfunc- difficulties with coping. In another subgroup analysis using the
tional seizure disorders. DERS [57], only one of two subgroups scored more highly than
An increased tendency to perceive life as stressful is also reflected normative data on the strategies subscale. Items on this subscale indi-
in measures of personality. Ekanayake et al. [22] observed significantly cate the individual believes little can be done to regulate negative
higher scores on the neuroticism subscale of the NEO Personality emotions when one is upset [37]. Myers et al. [30] demonstrated
Inventory Revised (NEO-PI-R) compared to patients with FMD — that an increased reliance on emotion-focused coping strategies in
elevations on this subscale reflect a ‘persistent, life-long tendency pwPNES was associated with comorbid psychological symptoms
to experience events negatively’. Other personality assessments in (e.g., depression and somatic complaints). Conversely, task-orientated
pwPNES have shown that clusters of this group exhibit elevated levels coping was negatively associated with alexithymia and low positive
of neuroticism compared to patients with epilepsy on the NEO-PI-R emotions as measured by the MMPI. Taken together, these studies sug-
[45], and as measured by the Dimensional Assessment of Personality gest that a reliance on emotion-focused coping strategies in pwPNES is
Pathology — Basic Questionnaire (DAPP-PQ) [46]. Furthermore, these related to other psychological factors such as trauma and depression in
latter two studies of personality pathology went on to identify sub- subgroups of pwPNES.
groups of personality styles characterized by higher and lower levels
of neuroticism. As such, it may be the case that only subgroups of 5.1.2. Avoidance
pwPNES exhibit a personality style prone to perceive their lives as Avoidance can be defined as a disinclination to sustain contact
stressful. with aversive private experiences (including emotions, thoughts,
bodily sensations, memories, and behavioral predispositions) or action
5. The selection and implementation stages taken to alter experiences or the events that give rise to them [58].
A tendency to overvalue and select avoidance becomes problematic
Two themes relevant to the selection and implementation stages because the short-term relief does little to relieve the cause of the
emerged: i) the selection/implementation of potentially maladaptive emotion or emotion-eliciting situation.
regulatory strategies (specifically emotion-focused coping, avoidance, Nine self-report studies investigated avoidance in pwPNES. With re-
and dissociation), and ii) a tendency to misrepresent exteroceptive spect to the avoidance of events or emotion-eliciting situations, pwPNES
emotional information. No experimental designs allowed for clear dis- endorsed a greater use of escape-avoidance strategies on the WOCS
tinction between the selection and implementation stages of the EPM; than healthy controls in two studies [49, 54]. Increased self-reported
therefore, research pertaining to the selection and implementation avoidance of negative emotional triggers in pwPNES versus healthy
stages is discussed together. controls has been reported on the EPS-25 [36]. Patients with PNES
reported elevated scores on the harm-avoidance subscale of the
5.1. Selection/implementation of maladaptive regulatory strategies Temperament and Character Inventory (Dutch version), indicating a
personality style characterized by behavioral inhibition in response to
5.1.1. Emotion-focused coping signals of punishment and frustrative nonreward [41]. Furthermore,
Coping is frequently categorized as either emotion-focused or responses on the Fear Questionnaire [59] indicated that pwPNES have
problem-focused [47]. Problem-focused coping describes attempts to a greater tendency to avoid situations that may elicit feelings of
relieve negative emotion by changing some aspect of the distress- agoraphobia than those with epilepsy [38]. Patients' tendency to avoid
causing situation. Emotion-focused coping, however, describes at- aversive private experiences has also been investigated. Dimaro et al.
tempts to reduce negative emotions rather than modify their cause [39] demonstrated that pwPNES scored significantly higher on the
(e.g., venting). Emotion-focused coping is therefore generally consid- Multidimensional Experiential Avoidance Questionnaire [60] than
ered to be less adaptive than problem-focused coping [47]. controls with epilepsy and healthy controls. Experiential avoidance
Nine studies assessed emotion- and problem-focused coping ten- scores positively correlated with self-reported anxiety scores and sei-
dencies in pwPNES. Using the Ways of Coping Scale (WOCS) [48], zure frequency in pwPNES but not those with epilepsy. Furthermore,
pwPNES were shown to be less likely to use ‘planful problem solving’ experiential avoidance and somatization scores delineated the two
than healthy controls [42]. Other researchers observed greater scores patient groups in a logistic regression model [39]. Finally, Uliaszek
on the ‘distancing-coping’ subscale of the WOCS in pwPNES relative to et al. identified a subgroup of pwPNES who scored significantly lower
healthy controls, which negatively predicted health-related quality of than normative values on the DERS [37]. The study authors interpreted
life [49]. Using the Utrecht Coping List [50], pwPNES self-reported a this as reflecting a predisposition to emotional avoidance. Despite the
greater tendency towards a passive wait-and-see attitude in response variety of avoidance measures used, an elevated level of avoidance
to problems than healthy controls, suggesting that they felt unable to endorsed by pwPNES is a consistent finding.
address the cause of their distress [51]. Other researchers have observed A tendency to select and implement avoidance as an emotion regu-
greater use of emotional and expressive suppression in pwPNES than lation strategy may be related to previous psychological trauma, which
42 I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48

is common in pwPNES [61, 62]. For example, when pwPNES were cate- to exist [75]. For instance, Alper et al. found that DES scores in pwPNES
gorized according to whether they self-reported trauma or not, the trau- were higher than in the general population, but did not differentiate
matized group also self-reported higher levels of ‘defensive-avoidance’ between pwPNES and epilepsy [74]. However, when total DES scores
on the Trauma Symptom Inventory (TSI-2) [55]. Higher scores on the were subjected to a principal components analysis, the resulting compo-
defensive-avoidance subscale indicate a tendency to make intentional nents did differentiate between patient groups. A depersonalization–
efforts to avoid unwanted internal experiences and emotion-eliciting derealization component accounted for more variance in DES scores
environments. Likewise, Bodde et al. identified greater levels of ‘harm in the group with PNES than the epilepsy group. An absorption–
avoidance’ in a subgroup of pwPNES who had been traumatized than imagination component was only raised in patients who reported
those who had not [41]. Therefore, a predisposition in pwPNES towards childhood abuse, irrespective of seizure diagnosis. Finally, an ‘amnesic’
the selection of avoidance as a regulatory strategy may also be a product factor was only raised in patients with epilepsy. This finding raises
of other psychological factors. the possibility that perhaps some types of dissociation are unique
to PNES, in this case depersonalization–derealization. Accordingly,
5.1.3. Dissociation Demartini et al. [29] compared pwPNES, patients with FMD, and healthy
Psychogenic nonepileptic seizures have been conceptualized as a controls on three different types of dissociation; ‘psychoform’ (DES),
dissociative response to overwhelming emotion [63, 64]. Dissociation, ‘compartmentalisation’ (The Somatoform Dissociation Questionnaire
the breakdown in the normal integration of cognitive functions, has (SDQ-20) [66]), and ‘detachment’ (The Cambridge Depersonalisation
been considered such an important symptom of PNES that it is classified Scale (CDS) [76]). Patients with PNES scored significantly higher on
as a dissociative disorder in the ICD-10 [65]. However, the definition of the DES and CDS than both groups, but lower on the SDQ-20 than the
dissociation and its relationship to PNES is a contentious subject [64]. group with FMD. These results suggest pwPNES can be differentiated
Dissociative symptoms in pwPNES have largely been investigated from patients with other forms of FND, by a susceptibility to psychoform
using self-report questionnaires. The Dissociative Experiences Scale dissociation and compartmentalization, but not detachment [29]. In
(DES) is one such instrument [66], which gives a total score and summary, the type of dissociation pertinent to PNES requires further
subscores measuring amnesic dissociation, absorption and imaginative clarification.
involvement, depersonalization, and derealization. Total scores of 20 Given that 75% of studies using the DES found elevated levels of
or more are considered consistent with dissociative disorders, including dissociation in pwPNES compared to the control groups with epilepsy
post-traumatic stress disorder, dissociative identity disorder, and and/or healthy control groups, it can be concluded that pwPNES
schizophrenia [66]. Thirteen studies were identified in which the DES are likely to select and implement dissociation as a regulatory
was administered to pwPNES (Table 3). strategy. Corroborating this interpretation, higher levels of dissociative
Across all studies, the mean total score is above the cutoff of 20 symptoms in pwPNES than in control groups have also been observed
(Table 3), indicating pwPNES experience levels of dissociative symp- using other self-report measures including the Dissociation Question-
toms consistent with the understanding of PNES as a dissociative disor- naire (DIS-Q) [77], the TSI-2 [55,78], the SDQ [77], and using structured
der. Furthermore, for ten of these studies, pwPNES scored significantly clinical interviews [79]. A case series of pwPNES demonstrated that pa-
higher on the DES total score than control groups [29, 38, 54, 67–73]. tients would recall upsetting childhood memories without expressing
Although the mean DES score for pwPNES in Fleisher et al. [62] was the emotion one would expect to be associated with such events, such
not greater than that of controls with epilepsy, a higher percentage of as sadness or anger. The authors argue that this reflects a dissociation
pwPNES than patients with epilepsy scored above the clinical cutoff between memories and normally associated feelings [80], although
(30 in this case). Notably, the Alper et al. study, which was rated as it should be added that this study had a very small sample size
being of high quality and which has the largest sample size of all studies (N = 15), and so, these findings may not be generalized.
using the DES in this review, did not report DES scores exceeding the There is evidence of other psychological factors interacting with
clinical cutoff, or scores, which were greater than those of patients dissociation; a subgroup of pwPNES who scored more highly on
with epilepsy [74]. measures of ED were also shown to self-report more dissociative
The mixed findings on dissociation in studies of pwPNES may symptoms [37]. Other researchers have found pwPNES and comorbid
be due to the failure of single construct questionnaires such as the psychiatric impairment had more frequent dissociative experiences
DES to capture the multiple forms of dissociation that are thought than pwPNES and comorbid neurological impairment or without co-

Table 3
Means and standard deviations (unless otherwise stated) of Dissociative Experience Scale scores included in review.

Study PNES CWE CWE + PNES FMD HC


a
Akyuz et al. (2004) 29.8 (20.0) 17.6 (15.5) – – –
Alper et al. (1997) 15.1 (13.5) 12.7 (10.8) – – –
Bowman et al. (2000) 20.2 (18.2) 10.7 (11.3)a – – –
Demartini et al. (2016) 17.2 (10.6) – – 7.9 (13.9)a 8.2 (7.5)a
Ekanayake et al. (2017) 15.9 (12.2) – – 5.6 (5.1)a –
Dikel et al. (2003) 22.8⁎ 14.11⁎a – – –
Fleisher et al. (2002) 22.7 (20.1) 15.1 (12.8) – – –
Goldstein et al. (2006) 24.9 (16.5) 14.5 (10.2)a – – –
Goldstein et al. (2000) 22.6 (16.4) – – – 13.1 (11.8)a
Lawton et al. (2008) 20.2 (34.1) 11.8 (15.5) – – –
Mazza et al. (2009) 17.6 (8.9) 6.4 (5.8)a – – 4.5 (2.9)a
Proenca et al. (2011) 54.3 (23.2) 22 (16.4)a – – –
Prueter et al. (2002) 32.0 (26.8) 6.5 (2.9)a 17.9 (9.5)a – –
Reuber et al. (2003) 17.2 (14.0) 8.8 (8.1)a – – –
Total mean (SD) 23.75 (10.1) 12.74 (4.7) 17.9 (9.5) 6.8 (1.6) 8.6 (4.3)

Note. PNES = psychogenic nonepileptic seizures, CWE = control group with epilepsy, CWE + PNES = control group with comorbid epilepsy and PNES, FMD = control group with func-
tional movement disorder, HC = healthy control group.
a
Control group significantly different from group with PNES.
⁎ SD not reported, women only.
I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48 43

existing psychiatric or neurological impairments [33], and 70.2% of overmentalize the emotional meaning behind the actions of characters
variance in DES scores was explained by psychological distress as in the movie, a tendency, which positively correlated with stress-
measured by the Brief Symptom Inventory [81]. Lawton et al., found vulnerability as measured by the Perceived Stress Scale. Critically,
that compartmentalization scores did not differentiate between this was not a result of an impaired ability to identify emotion expres-
pwPNES and epilepsy after controlling for anxiety and depression sion in others, as basal facial expression recognition was intact when
[82]. In another study, DES scores did not discriminate between viewing animated movies of neutral expressions slowly changing to
pwPNES and epilepsy in a logistic regression model, whereas levels full-blown emotions. In contrast, Prigatano and Kirlin [40] found
of somatization and psychopathology did and a positive correlation pwPNES were impaired in their ability to identify emotions in draw-
between DES scores and a NEAD severity index lost significance ings of affective expressions relative to patients with epilepsy. This
when somatization and psychopathology were controlled for [67]. discrepancy might be accounted for by the greater cognitive demand
Finally, when pwPNES were followed up for 4–6 years postdiagnosis, imposed by interpreting expression from more abstract representa-
those with reduced seizure frequency also experienced fewer disso- tions of faces. Overall, these studies suggest pwPNES can accurately
ciative symptoms [83]. Taken together, these findings suggest self- recognize emotion expression in others, but that they ascribe too
report measures of dissociation are closely related to current distress much meaning to that emotional content — a phenomenon that could
or psychopathology. Indeed, a relationship has been observed be- conceivably drive hypervigilance and impaired cognitive–affective con-
tween dissociative symptoms and trauma or trauma-related distress trol. Deficits in complex mentalizing ability have also been observed
in other populations [84], raising the possibility that dissociation is se- in another patient group characterized by ED, those with Borderline
lected/implemented as regulatory strategy to mitigate negative affect (emotionally unstable) Personality Disorder [89]. Given that features
in some pwPNES. Therefore, dissociation may not be a core feature of Borderline Personality Disorder are relatively common in pwPNES
of PNES etiology, rather, dissociative experiences could be an artefact [46, 90], it is conceivable that there are overlapping mechanisms
of the psychological distress associated with PNES. in both disorders causing mentalizing deficits, which could disrupt
appraisal of the external world and precipitate ED.
5.2. Appraisal of external world
6. Discussion
According to the EPM, successful implementation of a regulatory
strategy relies on an accurate representation of the external world — The studies reviewed suggest that, at group level, ED in pwPNES is
including the agents or situations one is interacting with [5]. For exam- characterized by deficits in the identification, selection, and imple-
ple, one might implement reappraisal to lessen feelings of anger if they mentation stages of the EPM. Identification stage difficulties relate to
perceived an apology to be sincere rather than insincere. an impaired ability to detect and understand one's own emotions as
There is some evidence pwPNES experience deficits in their ap- well as heightened stress vulnerability. While it was not possible to
praisals of exteroceptive emotional information. This evidence comes separate the selection and implementation stages clearly from the
from experimental studies including emotional imagery (pictures methodologies reported, there is also evidence that pwPNES tend to
of faces or scenes) as stimuli. Roberts et al. compared responses to select and implement potentially maladaptive regulatory strategies
standard affective pictures in pwPNES against seizure-free individuals (emotion-focused coping, avoidance, and dissociation). Altered pro-
with high or low trauma levels [85]. Groups did not differ in their cessing of exteroceptive emotional information may also interfere
pleasantness/unpleasantness ratings of the images but pwPNES with external world representations and impede the implementation
reported more intense emotional experiences in reaction to the stage.
images and displayed less positive emotional behavior. Gul and Importantly, cluster analyses point to considerable variability of
Ahmad [53] asked participants to make emotional and nonemotional ED across this patient group, perhaps linked to the etiological hetero-
judgements about images of faces. Patients with PNES had greater geneity of PNES disorders. One explanation is that ED is related to fac-
difficulty switching from emotional to nonemotional judgements tors such as trauma, personality, and current psychological distress.
than healthy controls. This switching bias correlated positively with Therefore, pwPNES who have experienced greater trauma may also
the self-reported use of a maladaptive regulatory strategy (expressive experience more severe symptomology and ED than those who have
suppression) and negatively with a healthier regulatory strategy experienced less trauma. As such, future studies employing subgroup
(cognitive reappraisal). Altered processing of exteroceptive emotional analyses based on psychological or clinical variables (c.f. [37, 51, 91]),
information in pwPNES has also been demonstrated by Bakvis et al., or including relevant psychiatric control groups (c.f. [85, 92])
who showed that social distractors (happy, neutral, or angry faces) would constitute useful designs to elucidate this potential source of
impaired working memory performance relative to healthy controls heterogeneity.
whether data were collected at baseline or following stress induction Some studies included in this review found no differences in
[86]. Bakvis et al. also demonstrated that, compared to healthy some measures of ED between pwPNES and patients with epilepsy
controls, pwPNES exhibited a preconscious positive attentional bias (e.g., [27, 34, 62, 74]). It is possible that both groups experience
to angry faces during a masked emotional Stroop Test [87]. Hyper- ED, for some overlapping and some distinct reasons. For example,
vigilance to negatively valenced emotional information correlated both pwPNES and epilepsy may carry a similar emotional burden as-
positively with self-reported sexual trauma, indicating a potential sociated with experiencing seizures, although the two seizure disor-
mechanism by which hypervigilance to social threat may be medi- ders, or their consequences in terms of ED, are not the result of the
ated. A further analysis of data from Bakvis et al. found basal cortisol same pathological process [93]. Further exploration of neural corre-
levels correlated positively with threat vigilance in patients but not lates of ED in PNES may help clarify its neural substrate and further
healthy controls, suggesting a relationship between the endocrine elucidate psychological heterogeneity. One study identified in the
stress response and threat vigilance restricted to pwPNES [88]. These literature search has examined the neural correlates of dissociation
results allude to a hypervigilant attentional system biased towards in pwPNES [94], but was excluded due to insufficient sample size.
processing exteroceptive emotional information, which might be The fact that pwPNES are a heterogeneous group reinforces the im-
related to trauma exposure. portance of taking a person-centered approach to working with this
Cognitive–affective biases in pwPNES may also be related abnormal- population.
ities in theory of mind. Schönenberg et al., found impaired theory of Given that ED is considered to play a role in the precipitation and
mind in pwPNES relative to healthy controls when observing the maintenance of Axis 1 disorders, and these disorders are frequently
Movie for Assessment of Social Cognition [26]. PwPNES tended to comorbid with PNES [1], it is perhaps unsurprising that ED is also
44 I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48

commonly observed in pwPNES. However, the case–control design of The studies reviewed here were not designed explicitly to examine
most of the studies discussed here makes it impossible to say with cer- emotion regulation according to the EPM, so we have clustered the
tainty whether ED is a cause, consequence, or correlate of PNES. It is also literature post hoc. While this categorization was double-rated,
unlikely that the relationship between ED and PNES is the same for this method does introduce risk of bias. Ideally, studies of ED in
every patient. Nevertheless, ED is likely to contribute to the pathogene- PNES would be designed to test hypotheses generated from theories
sis of PNES and PNES-associated disabilities for at least some patients. of emotion regulation. However, the majority of studies in this area
The demonstrated effectiveness of psychotherapeutic techniques de- are observational, which can cause interpretative difficulties within
signed to target emotion regulation difficulties in PNES supports this frameworks that they were not designed to fit. Furthermore, the selec-
proposition [95–100], although more work is needed to understand tion and implementation stages are arguably more difficult to isolate
the mechanism of treatment. and study than the identification stage. The experimental manipula-
tion of regulatory strategies could possibly remedy this issue; other re-
6.1. Limitations and recommendations searchers have instructed volunteers to suppress or enhance negative
emotion elicited by unpleasant pictures [107]. Versions of this para-
Many studies in this field are underpowered; a small sample digm have been applied to other patient populations characterized
size was the only reason why some studies were considered to be by ED, such as those with major depression (e.g., [108]). These designs
of such uncertain quality that they were excluded from the review could present a powerful way to empirically test the implementation
[92, 101–103]. Small studies cannot account for the obvious heteroge- stage of the EPM in pwPNES. There are also other models of emotion
neity of the population with PNES. Although there may be particular regulation, which could facilitate our understanding of PNES [109,
problems with recruiting pwPNES to clinical studies (e.g., low patient 110]. In spite of the fact that there is at present only ‘modest’ support
numbers in single centers, problems with transport or engagement in for the EPM and that the substeps require further empirical assess-
research) the ongoing CODES treatment study in the UK, to which ment [8], we chose the EPM as it is the most recent iteration of a
over 600 patients have been recruited to date, demonstrates that well-established and widely used model. The EPM may not bear up
large-scale research is possible in this area with sufficient funding to future scientific scrutiny; however, there is value in adopting the
[104]. more structured approach of grounding studies within broader psy-
In addition to a need for larger studies, there is a need for higher chological theory.
standard of reporting in this area. There was a tendency for studies to
not explicitly state methodological criteria of importance, such as 7. Conclusions
whether PNES had been formally differentiated from panic attacks
or whether patients were recruited consecutively. As recommended Existing research suggests that ED in pwPNES includes deficits in the
elsewhere [1], work should draw on established publication guidelines identification, selection, and implementation stages of the EPM [5].
(e.g., www.strobe-statement.org), to improve both the quality of study However, the manifestation of these deficits in the PNES population is
design and reporting in this area. heterogeneous and likely linked to other psychological factors. Future
It is worth mentioning that while avoidance, emotion-focused studies of ED in PNES should seek to elucidate subgroups of patients
coping, dissociation, and hypervigilance are considered maladaptive in based on the presenting style of ED, as well as the relationship between
this review; the utility of a regulatory strategy is context-dependent. ED and other psychological or clinical variables.
For example, because reappraisal difficulty increases with emotional
intensity and requires cognitive effort [105], an individual who is
vulnerable or compromised might be better-off implementing a Declarations of interest
‘maladaptive’ strategy such as dissociation rather than not regulate
at all. Furthermore, strategies that involve the redirection of attentional None.
resources (like avoidance) are more effective in reducing short-term
negative affect than reappraisal in high-emotional intensity conditions Role of the funding source
[106]. Although arguably, a habitual tendency to select these strategies
irrespective of context might still be considered an example of This review was produced as part of a PhD project funded by a grant
dysregulation. from The Neuroscience Research Fund (004) 2013.
Appendix 1. Quality rating assessment of studies identified in the literature search

Study Study design Sample size Type of Quality rating criteria EPM stage
(b15 = very poor, control
Video-EEG Epilepsy Anxiety Consecutive Standardized ≤10% ≤5 years % of Overall Identification Selection/
15–26 = poor, group
excluded excluded sampling measures difference difference ‘Yes’ rating implementation
26–63 = moderate,
in female in age ratings
≥63 = good)

Akyuz et al. (2004) Case–control Moderate CWE N Y Y N Y Y Y 71 Medium ✓


Alper et al. (1997) Case–control Good CWE Y Y Y Y Y Y Y 100 High ✓
Bakvis, Roelofs, et al. Case–control Poor HC Y Y Y N Y Y Y 71 Low ✓
(2009)
Bakvis, Spinhoven, Case–control Poor HC & CWE Y Y Y N Y N N 57 Low ✓
et al. (2009)
Bakvis, Spinhoven, Case–control Very poor HC Y Y Y Y Y N N 57 Unacceptable – –
et al. (2011)
Bakvis et al. (2010) Case–control Poor HC Y Y N N Y Y Y 100 Low ✓
Baslet et al. (2010) Case series – – N N N Y Y – – 29 Low ✓
Bewley et al. (2005) Case–control Poor HC & CWE Y Y N N Y Y Y 71 Low ✓
Bodde et al. (2013) Case series – – Y N Y Y Y – – 57 Medium ✓ ✓
Bodde et al. (2007) Case series – – Y Y N Y Y – – 57 Medium ✓
Bowman et al. (2000) Case–control Poor CWE Y N N N Y Y Y 57 Low ✓
Brown et al. (2013) Case–control Moderate CWE N Y N N Y Y Y 57 Medium ✓
Cohen et al. (2014) Case series Moderate – Y Y Y Y Y – – 71 Medium ✓
Cragar et al. (2005) Case–control Very good CWE Y Y N Y Y N Y 71 Medium ✓
Cronje and Pretorious Case–control Poor HC Y Y N N Y Y Y 71 Low ✓
(2013)
Demartini et al. Case–control Poor HC & FMD Y Y Y Y Y Y Y 100 Low ✓ ✓
(2016)
Dikel et al. (2003) Case–control Poor CWE Y N N N Y N Y 43 Low ✓
Dimaro et al. (2014) Case–control Moderate HC & CWE Y Y N N Y Y Y 71 Medium ✓ ✓
I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48

Ekanayake et al. Case–control Moderate FMD Y Y N Y Y Y N 71 Medium ✓ ✓


(2017)
Fleisher et al. (2002) Case–control Moderate CWE Y N Y N Y Y Y 71 Medium ✓
Frances et al. (1999) Case–control Moderate CWE & HC N Y Y N Y Y Y 71 Medium ✓ ✓
Goldstein et al. (2000) Case–control Poor HC N Y Y N Y Y Y 71 Low ✓
Goldstein et al. (2006) Case–control Poor CWE N Y Y N Y N Y 57 Low ✓ ✓
Gul and Ahmad Case–control Good HC N Y Y N Y Y Y 71 Medium ✓
(2014)
Hendrickson et al. Case–control Good CWE Y Y Y Y N N N 57 medium ✓
(2014)

(continued on next page)


45
46

Appendix
(continued)
A (continued)

Study Study design Sample size Type of Quality rating criteria EPM stage
(b15 = very poor, control
Video-EEG Epilepsy Anxiety Consecutive Standardized ≤10% ≤5 years % of Overall Identification Selection/
15–26 = poor, group
excluded excluded sampling measures difference difference ‘Yes’ rating implementation
26–63 = moderate,
in female in age ratings
≥63 = good)

Hingray et al. (2011) Case–control Very poor PNES-T Y N Y Y Y N N 57 Unacceptable – –


Kaplan et al. (2013) Case–control Good CWE Y N N N Y N Y 43 Medium ✓
Kuyk et al. (1999) Case–control Good CWE N Y N N Y N N 43 Low ✓
Lawton et al. (2008) Case–control Moderate CWE N Y N N Y N Y 43 Low ✓
Martino et al. (2017) Case–control Very poor MMDD Y Y Y Y Y Y Y 100 Unacceptable – –
Mazza et al. (2009) Case–control Moderate CWE & HC Y N Y Y Y Y Y 86 Medium ✓
Myers, Fleming et al. Case series – – Y Y N Y Y – – 57 High ✓ ✓
(2013)
Myers, Matzner et al. Case–control Moderate ES Y Y N Y Y N Y 86 Medium ✓
(2013)
Myers, Perinne, et al. Case series Good PNES-T Y Y Y Y Y Y Y 86 High ✓
(2013)
Novakova et al. Case–control Moderate HC N N N Y Y N N 29 Low ✓ ✓
(2015)
O'Brien et al. (2015) Case–control Poor HC Y Y Y N Y Y Y 86 Low ✓
Ozcetin et al. (2009) Case–control Moderate HC Y Y Y N Y Y Y 86 Medium ✓
Prigatano et al. (2002) Case series – – Y N N N N – – 14 Low ✓
Prigatano et al. (2009) Case–control Poor CWE Y Y N N N N Y 43 Low ✓
Proenca et al. (2011) Case–control Poor CWE Y Y N N Y Y Y 71 Low ✓
Prueter et al. (2002) Case–control Poor CWE & N Y N N Y N N 29 Low ✓
CWE +
PNES
Reuber et al. (2003) Case–control Good CWE N Y N N Y N Y 43 Medium ✓
Reuber et al. (2004) Case–control Very good CWE & HC Y Y N Y Y N Y 57 Medium ✓
I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48

Roberts et al. (2012) Case–control Poor High T & Y Y Y N Y N Y 71 Low ✓


Low T
Schonenberg et al. Case–control Poor HC Y Y N Y Y Y Y 86 Low ✓ ✓
(2015)
Testa et al.(2012) Case–control Moderate HC & CWE Y Y Y N Y N Y 71 Medium ✓ ✓
Tojek et al. (2000) Case–control Poor CWE Y Y N N N Y Y 57 Low ✓
Uliaszek et al. (2012) Case series – – N N Y N Y – – 29 Low ✓ ✓
Urbanek et al. (2014) Case–control Good HC N N N N Y Y N 29 Low ✓
Van der Kruijs et al. Case–control Very poor HC N Y Y N Y Y Y 71 Unacceptable – –
(2012)
Wolf et al. (2015) Case–control Good CWE Y Y Y N Y N Y 86 Medium ✓

Key: HC = healthy control group, CWE = control group with epilepsy, FMD = functional movement disorder, PNES-T = nontraumatized control with PNES, CWE + PNES = control group with comorbid epilepsy and PNES, High T = high trauma
control group, Low T = low trauma control group, MMDD = mild major depressive disorder, – = not applicable, EEG: electroencephalography.
I.A. Williams et al. / Epilepsy & Behavior 86 (2018) 37–48 47

Appendix 2. Categorization of measures and methodologies into stages of the extended process model

EPM stage Construct Methodology/measures used

Identification Emotional TAS-20, EPS-25 impoverished emotional experience subscale, patient endorsed ictal somatic panic symptoms versus panic item
awareness/alexithymia on HADS, patient endorsed ictal emotions, BNI Screen for Higher Cognitive Function (affect subscale) vs. patient-reported
irritability.
Perceived stress PERI (Life Events Scale), EPCL, LEC, PSS, NEO-PI-R Neuroticism subscale, DAPP-BQ
Selection and Regulatory/coping style DERS, UCS, COPE Inventory, CERQ, WOC, MHLOC, ERQ, REM, MMPI, CISS, EPS-25, The Courthauld Emotional Control Scale,
implementation Dissociation DES, CADDS, DIS-Q, Somatoform Dissociation Questionnaire, SCID-D, CDS, patient endorsed ictal dissociative symptomology,
TSI-2 Dissociation subscale
Avoidance Short TCI (Avoidance subscale), WOC, MEAQ, Fear Questionnaire, CISS Avoidance subscale, EPS-25 Avoidance subscale,
Appraisal of external Emotional N-Back Task, Emotional Stroop Task, Task-switching experiment (emotional categorization), Animated Morph Task,
world / cognitive-affective biases Movie for Assessment of Social Cognition

Note. TAS-20 = Toronto Alexithymia Scale — 20, EPS-25 = Emotional Processing Scale-25, HADS = Hospital Anxiety and Depression Scale, PERI = Psychiatric Epidemiology Research
Interview, EPCL = Everyday Problems Checklist, LEC = Life Events Checklist, PSS = Perceived Stress Scale, NEO-PI-R = NEO Personality Inventory Revised, DERS = Difficulties
in Emotion Regulation Scale, UCS = Utrecht Coping Scale, DES = Dissociative Experiences Scale, CADDS = Clinician Administered Dissociative States Scale, DIS-Q = The
Dissociation Questionnaire, CERQ = Cognitive Emotion Regulation Questionnaire, Short TCI = Short Temperament and Character Inventory, SCID-D = Structured Clinical Interview
for Dissociative Disorders, WOC = Ways of Coping Scale, CDS = Cambridge Depersonalisation Scale, MEAQ = Multidimensional Experiential Avoidance Questionnaire, MHLOC =
Multidimensional Health Locus of Control Scale, ERQ = Emotion Regulation Questionnaire, REM = Response Evaluation Measure, TSI-2 = Trauma Symptom Inventory, MMPI =
Minnesota Multiphasic Personality Inventory, CISS = Coping Inventory for Stressful Situations, DAPP-PQ = Dimensional Assessment of Personality Pathology – Basic Questionnaire.

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