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Psychosomatics 48:230-238, May-June
doi: 10.1176/appi.psy.48.3.230
© 2007 Academy of Psychosomatic Medicine
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Non-Epileptic Seizures and Other Functional Neurological Symptoms: Predisposing, Precipitating, and Perpetuating Factors

Markus Reuber, M.D., Ph.D., Stephanie Howlett, M.A., M.Sc., Ajjaz Khan, M.D., and Richard A. Grünewald, D.M., D.Phil.

Received January 10, 2006; revised March 28, 2006; accepted April 11, 2006. From Sheffield Teaching Hospitals, NHS Trust Royal Hallamshire Hospital, Sheffield, S10 2JF, UK. Send correspondence and reprint requests to Markus Reuber, M.D., Ph.D., MRCP, Senior Clinical Lecturer in Neurology, Academic Neurology Unit, University of Sheffield Royal Hallamshire Hospital, Glossop Road, Sheffield, S10 2JF, UK. e-mail: mreuber{at}doctors.org.uk
© 2007 The Academy of Psychosomatic Medicine


  ABSTRACT

 
TOP
 ABSTRACT
INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 
This naturalistic study describes potential etiological factors in outpatients with functional neurological symptoms recorded during a screening interview with a single psychotherapist in 59 consecutive patients. The most commonly identified predisposing/precipitating factors were trauma (78.0%), family dysfunction (62.7%), and bereavement (62.7%). Family dysfunction (54.2%) and affective disorder (42%) were the commonest perpetuating factors. Trauma was more common in non-epileptic seizures; health anxiety, in men; family problems, in women. This study demonstrates the heterogeneity of this patient population. Further research is indicated to explore differences in predisposing, precipitating, and perpetuating factors in different patient groups with functional symptoms.


  INTRODUCTION

 
TOP
 ABSTRACT
 INTRODUCTION
METHOD
 RESULTS
 DISCUSSION
 REFERENCES
 
Functional neurological symptoms are somatic symptoms that superficially resemble those of organic disorders of the nervous system but for which no physical explanation can be found. Included are neurological symptoms that would be classified under the headings of dissociative or somatoform (conversion) disorders in the current diagnostic manuals.1,2

Reports suggest that 11% of patients in a typical neurological outpatient clinic and 9% of patients admitted to a neurological ward have symptoms that are not explained by organic pathology.3,4 Patients with functional neurological symptoms are as disabled as patients with identifiable organic pathology, but are more distressed and have higher rates of psychiatric disorders.3,5,6 Over the long-term, patients with functional symptoms often remain dependent on caregivers or social benefits.7–11 Functional symptoms therefore represent a significant challenge.

Although many questions about etiology, nosology, and management remain unanswered,12 a number of interacting predisposing, precipitating, and perpetuating etiological factors have been identified.13,14 Controlled studies suggest that potentially relevant factors include biographical features (including childhood trauma, abuse, and remote and recent life events), biological facts (such as gender), psychological features (dissociative tendencies, emotional expressiveness), psychiatric comorbidity, neurological comorbidity (for example, learning disability or epilepsy), social aspects (such as family environment, financial security, friends), broader cultural aspects (such as attitudes toward illness, gender roles) and opinions or cognitive styles (illness perceptions).6,15–24

To date, it remains unclear whether different functional syndromes or indeed different neurological symptoms are related to particular etiological factors. Some authors have interpreted functional symptoms as a primitive iconic language in which different symptoms have particular meanings.25 Others have argued that it would be better to conceptualize functional disorders with different symptoms as a single functional somatic syndrome.26

This exploratory study was first intended to describe the range of potential predisposing, precipitating, and perpetuating etiological factors identified in a consecutive group of outpatients presenting with functional neurological symptoms. Second, we wanted to explore whether there were links between particular factors and different neurological symptoms. Finally, we wanted to ascertain whether our data confirmed the observation made previously in patients with non-epileptic seizures that different etiological factors are relevant in men and women.23,27,28


  METHOD

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
RESULTS
 DISCUSSION
 REFERENCES
 
Patients
A group of consecutive patients with functional neurological symptoms was referred from a neurology outpatient service at the Barnsley District General Hospital in Barnsley, UK, to a specialist neurology–psychotherapy service based in the same hospital between January 2003 and December 2004. Functional neurological symptoms were diagnosed by one of two consultant neurologists (RAG, AK) on the basis of clinical assessment and appropriate investigation. Patients were excluded from this study if they had symptoms of organic neurological disorders and were referred purely for help with adjustment. Patients were also excluded if they had been referred but did not attend for at least an initial assessment consultation.

Clinical Assessment
Patients were offered a psychotherapeutic intervention based on a model of brief psychodynamic therapy. This intervention has previously been shown to be helpful and cost-effective in the treatment of functional bowel disorders.29,30 All patients were seen by the same therapist (SH). Potentially relevant etiological factors were elicited during a 2-hour semistructured assessment interview that forms a key part of the therapy. Included in the interview were the following: 1) a detailed description of all current symptoms, with a particular focus on identified functional target symptoms; 2) a chronological history of the symptoms, including initial onset and periods of remission, changes, or flare-ups; 3) impact on personal relationships; 4) impact on work and social functioning; 5) assessment of triggers for the symptoms; 6) inquiry about life events in the year before symptom onset or recurrence after significant gap; and 7) a chronological life-history screening for childhood family functioning, trauma, and illness (including illness of other family members), bereavements, traumatic events in adult life, family/relationship functioning in adulthood, life pressures, other health problems, and interpersonal patterns. The data for the study were methodically extracted from structured contemporaneous notes taken by the therapist during the assessment interview.

Etiological factors described as potentially relevant in previous studies were categorized as predisposing/precipitating if they had occurred before the manifestation of functional neurological symptoms and as perpetuating if they appeared after symptom onset.13,14 For the descriptive part of this study, we made a further distinction between predisposing and precipitating factors. In line with a previous study,23 factors were considered as predisposing if they had occurred over 12 months before symptom manifestation and precipitating if they were only present in the year before symptoms started. In view of the difficulty associated with the clear separation of predisposing and precipitating factors, these categories were combined in the comparative analyses.

The factors categorized included physical and affective disorders. Also included were life events and situations that, although not externally verified, were considered to be relatively factual in nature. Although emotional coping styles and interpersonal patterns were discussed and identified as part of the initial interview, they were excluded from the list of factors considered in this study because of the complex interrelationship of such patterns, functional symptoms, and other etiological factors.

Comparison Measures
For the comparative parts of this study, the identified potentially predisposing/precipitating factors of probable etiological relevance were grouped into five domains: 1) sexual trauma (including trauma before the age of 16, sexual abuse, rape, and sexual assault), and sexual events that, although not directly traumatic to the patient, were recognized by them to have re-evoked previous sexual trauma (e.g., the start of a sexual relationship, the disclosure of abuse by a close relative); 2) non-sexual trauma (including childhood physical or emotional abuse, witnessing domestic violence in childhood, being bullied as a child, being an adult victim of domestic violence, being a victim of other assaults, involvement in accidents), and other trauma (e.g., threats to patient by armed gang, workplace bullying); 3) bereavements (only included if the patient showed affect during the interview or considered the bereavement to have had a significant emotional impact); 4) social/family factors (including family or relationship difficulties, family dysfunction or breakdown, and life pressures considered by the patient to have had a significant impact on his or her life); and 5) health issues (including physical comorbidity and epilepsy).

The identified potentially perpetuating factors were grouped into seven domains: 1) bereavement (significant bereavements that had occurred since the onset of symptoms); 2) health issues (generalized anxiety about health and symptom-focused anxiety [hypochondriasis], as well as continuing physical problems); 3) financial /social gain (referring to claims for compensation or financial benefits related to the target symptoms and illness-identity, with entrenched dependency); 4) affective disorder (depression and anxiety other than health anxiety); 5) sexual trauma (any sexual trauma, as defined above, occurring since symptom onset); 6) social pressures (including life pressures and caring responsibilities, where these were considered to be having a severe impact); continuing family dysfunction, and social isolation; and 7) other (any other situations causing distress, such as the illness of a close relative, financial problems, family estrangement, traumatic experiences after the onset of symptoms, or concerns about health of family members).

Statistical Analysis
We compared categorical variables by means of the chi-square ({chi}2) test and normally distributed continuous variables by use of the Student t-test, after applying Levene’s test for equality of variance. Continuous variables with unequal variance were treated as nonparametric and were compared by use of the Mann-Whitney U test. A level of p<0.05 (two-tailed) was considered significant.


  RESULTS

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
DISCUSSION
 REFERENCES
 
During the study period, 57 patients were referred by one neurologist (RG), and 23 patients by the second neurologist (AK). Three of these patients were excluded from this study because they were referred for problems with adjustment to organic neurological disorders. A further 18 patients were excluded because they did not attend their appointment with the therapist. Of these patients, 14 (77.8%) were women; 8 had been referred with non-epileptic seizures (NES; 44.4%). The mean age of excluded patients was 35.8 (standard deviation [SD]: 9.5); the mean number of functional neurological symptoms was 2.2 (SD: 1.1); mean symptom duration was 2.7 years (SD: 2.8). The patients excluded from this study were significantly older than the patients who were included (t=2.320; p=0.027), but there were no significant differences in other demographic or clinical parameters.

Fifty-nine patients were included (Table 1). Their mean age was 42.0 years (range: 18–72 years; SD: 11.5), and 41 of 59 patients (69.5%) were women. Patients had a mean of 2.3 functional neurological symptoms (SD: 1.3; range: 1–7); the mean duration of symptoms was 7.7 years (SD: 11.9; range: 0–59 years). The spectrum and frequency of neurological symptoms is shown in Figure 1. In all, 81 of 126 symptoms (64.3%) were identified by the referring neurologists; the remaining symptoms were volunteered during the screening interview. The symptoms included non-epileptic seizures (NES) in 30 of 59 patients (50.8%). Patients with NES had a median of one further functional neurological symptom (range: 0–4). In addition to the functional neurological symptoms included in the figure, eight patients complained of panic attacks. One of the patients included in this study had a recent history of alcohol addiction, and one patient admitted to using illicit drugs (marijuana). No patients were known to be involved in ongoing criminal investigations. Table 1 (sections A and B) show that there were no significant differences in terms of important clinical and demographic features of patients with NES as compared with patients without NES or of male versus female patients.


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TABLE 1. Demographic and Clinical Features




Figure 1
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FIGURE 1.  Number of Patients With Different Functional Neurological Symptoms

NES: non-epileptic seizures.


Predisposing, Precipitating, and Perpetuating Factors
Table 2 gives an overview of the prevalence of individual predisposing and precipitating factors we identified and patients who reported factors from each of the five domains. Patients reported potential etiological factors from a mean of 2.4 domains. We elicited a history of any form of severe trauma (sexual or non-sexual) from 78.0% of all patients. No factors could be identified in two patients (3.4%). Table 3 gives an overview of the prevalence of possible perpetuating factors in each of the seven domains. No relevant factors were found in six patients (10.2%). In one of these patients, no potentially predisposing or precipitating factors were identified, either. There was a mean of 1.7 domains in which perpetuating factors were noted.


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TABLE 2. Overview of Predisposing and Precipitating Factors and Proportion of Patients in Whom Individual Factors Were Identified




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TABLE 3. Overview of Perpetuating Factors and Proportion of Patients in Whom Individual Factors Were Identified



The relative frequency of predisposing or precipitating factors identified in the five domains in patients with and without NES and in male versus female patients is shown in Table 4 (sections A and B). The comparison of perpetuating factors in patients with NES and other functional symptoms yielded no significant differences. The relative prevalence of various perpetuating factors in men as compared with women is shown in Table 4 (C).


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TABLE 4. Comparison of the Prevalence of Etiological Factors in Different Patient Groups




  DISCUSSION

 
TOP
 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
REFERENCES
 
The range of functional neurological symptoms described by the patients referred for psychotherapy from a general-neurology outpatient clinic is similar to that previously reported in neurological inpatients or at tertiary referral centers.4,18,23,31,32 The number of patients with NES in this outpatient population was similar to the 35.7% described by Ljungberg in his study of 381 patients with a diagnosis of hysteria.33 The mean number of functional symptoms in individual patients was relatively low in this study. Data from a previous study based on a questionnaire asking specifically about a range of possible unexplained symptoms yielded much higher prevalence rates in a similar patient population (e.g., back pain: 60.8%, dizziness/poor coordination: 57.0%, fatiguability: 56.3%).34 This finding suggests that our patients may have considered only some of their symptoms as suitable for discussion with a neurologist or therapist.

Factors of potential etiological significance were identified here with a similar frequency to that reported previously in patients with conversion disorder,6,15 NES,18,22,23,35,36 or somatization disorder.16 The idea that functional neurological symptoms have a multifactorial etiology, with predisposing, precipitating, and perpetuating factors is not new. Clinical and neurobiological studies have demonstrated how biological factors, experiences in earlier life, and ongoing conflicts or stressors can combine to cause psychiatric conditions or disorders characterized by functional somatic symptoms.15,37–42 Detailed analyses of patients with NES have illustrated the interaction of predisposing, precipitating, and perpetuating factors and indicate how a particular stressor may become pathogenic in the presence of other contributing factors.23,32

The most prominent etiological factors identified in this study were a history of trauma (in three-quarters of patients), significant problems in the family or close social environment, and relevant bereavement (both found in nearly two-thirds of the patients). An association with trauma has been recognized most clearly in patients with NES, prompting the suggestion that NES could be interpreted as a variant of posttraumatic stress disorder.43,44 However, the direct link between trauma or stress and NES has also been challenged, and it has been argued that experiences such as incest are as much a marker of family dysfunction as they are a traumatizing event in their own right.45,46 In view of the absence of an appropriate "healthy" control group, this study cannot prove that trauma is of etiological relevance, although the rates of trauma reported by patients with functional neurological symptoms exceeded those reported by patients in the National Comorbidity Survey, which was also based on an interview (the rates of any trauma/rape/sexual molestation were 60.7%, 0.7%, and 2.8%, respectively, in men and 51.2%, 9.2%, and 12.3%, respectively, in women).47

Potentially perpetuating factors were identified in nearly 90% of patients. The most prevalent factors were family dysfunction or discord (over 50% of patients), affective disorders (in over 40%), and health anxiety or hypochondriasis (in nearly one-quarter of patients). Although the majority of patients have therefore been exposed to trauma and suffer different forms of anxiety, the diversity of individual factor-profiles and symptom manifestations suggests that there may be no single pathogenesis for functional neurological symptoms.

The differences detected in the comparison of potentially predisposing, precipitating, and perpetuating factors in patients with NES and other functional neurological symptoms further demonstrate the etiological heterogeneity of symptoms in this patient group. One previous study by Stone et al.,31 comparing patients with NES and patients with motor conversion symptoms, found higher rates of adverse childhood experience, incest, family breakdown, and negative life events in patients with NES. These results are in keeping with our finding that a history of trauma was significantly more common in patients with NES (90% of patients) than in those with other functional neurological symptoms (two-thirds of patients). Stone et al. also found a significant difference in age at onset, with patients with NES presenting at a younger age. Although the mean age at onset in the NES group was also lower in our study, the difference was not statistically significant. One reason for this may be that, compared with larger patient populations in which the mean age at manifestation is typically between age 20 and 30,48 NES had an unusually late onset in our patient group.

Although, as reported by others,49 there were many similarities between functional neurological symptoms in men and women, the comparison of etiological factors also yielded important differences. In this study, sexual trauma was only reported by women. Discord and stress in the immediate social environment or family dysfunction and breakdown also appeared more relevant in women. Health anxiety and hypochondriasis were identified more commonly in men, affecting half of all male patients. These results are in line with a study of gender differences in patients with NES, which found that sexual abuse was reported eight times more often by women.27 Our findings are also in line with a study focusing on gender differences in the Minnesota Multiphasic Personality Inventory (MMPI), which found that men with NES had higher Hypochondriasis and Hysteria scores than women with NES or men and women with epilepsy.28 Although neurobiological differences have been reported between men and women in brain networks that underpin decision-making, social or emotional functioning, and memory,50–52 we should point out that rather than true differences at a population level, the gender-related findings may only reflect differences in symptom-reporting and healthcare-accessing behavior, which have been well documented in studies of somatic symptoms in men and women.53

The strength of this study is that it describes "real" clinical practice in an unselected, consecutive group of patients referred from neurology outpatient clinics in a district hospital. Previous studies in this area were either more exclusive or based on inpatient or tertiary referral-center populations.18,23,31,32 However, this study also has a number of weaknesses. These include the lack of prospectively-identified referral criteria (leaving room for referral bias), the identification of potentially relevant etiological factors in a single interview with one particular therapist, the reliance on the therapist’s contemporaneous records, rather than a quantitative screening tool for etiological factors (both introducing potential identification bias), the grouping of different factors for statistical analysis, and the relatively large numbers of statistical comparisons performed in a small patient sample (increasing the risk of false positive and negative findings). Furthermore, although personality pathology, alexithymia, non-neurological somatoform symptoms, or dissociative tendencies are clearly important in this area,34,54,55 patients were not formally screened for personality or dissociative disorders, and data on non-neurological functional symptoms were incomplete. Alexithymia was identified clinically, but was not measured with a standardized instrument.

These drawbacks mean that the findings of this study can only be regarded as preliminary and exploratory. The further confirmation of the results by hypothesis-driven, prospective studies is essential. Moreover, in view of the possibility of referral bias (patients with psychosocial problems may have been referred preferentially) and the absence of a healthy-control group, this study cannot prove the etiological relevance of the factors discussed.

However, given that the same methodology was used to identify factors in all patients, within-group comparisons were possible, and add to existing knowledge. These comparisons suggest that there are important differences between patients with different functional neurological presentations. These differences indicate that it might be helpful to make further distinctions in the diagnostic categories of somatoform (conversion) or dissociative disorder, rather than lump different presentations together into a single functional syndrome.56 At the same time, the significant differences found between men and women demonstrate that it would not be appropriate to base a reorganization of the diagnostic categories of somatoform or dissociative disorder entirely on a somatic-disease model or the type of presenting physical symptom. A multidimensional approach might describe patients most appropriately.

This study also adds to existing knowledge by demonstrating that trauma and anxiety can be considered as important core targets for treatment programs in this area. However, even leaving aside the fact that trauma and anxiety can affect patients in very different ways, treatments intended to alleviate the effects of trauma or improve anxiety are not going to be universally applicable.


  REFERENCES

 
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 ABSTRACT
 INTRODUCTION
 METHOD
 RESULTS
 DISCUSSION
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R. Duncan and M. Oto
Predictors of antecedent factors in psychogenic nonepileptic attacks: Multivariate analysis
Neurology, September 23, 2008; 71(13): 1000 - 1005.
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