Ictal injury in psychogenic non-epileptic seizures Ali A. Asadi-Pooya a,b,*, Mehrdad Emami a, Yasaman Emami a a b
Neurosciences Research Center, Shiraz Medical School, Shiraz University of Medical Sciences, Shiraz, Iran Jefferson Comprehensive Epilepsy Center, Department of Neurology, Thomas Jefferson University, Philadelphia, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 23 November 2013 Received in revised form 5 February 2014 Accepted 6 February 2014
Purpose: Whilst ictal injuries in psychogenic non-epileptic seizures (PNES) have been reported previously, very few studies have described the spectrum of ictal injuries in these patients. In the current study, we tried to determine the spectrum of reported ictal injuries associated with PNES and to investigate the possible associated risk factors. Methods: All patients with PNES were recruited prospectively in the outpatient epilepsy clinic at Shiraz University of Medical Sciences, between 2008 and 2013. The diagnosis was made by clinical assessment and ictal video-EEG recordings. We asked all patients and their caregivers about history of any minor (e.g., tongue biting, bruises, and lacerations) or major (e.g., burns and fractures) physical injuries associated with their seizures, since their disease started. Clinical variables, factors potentially predisposing to PNES and video-EEG recordings of all patients were analyzed. Results: Two hundred and eleven patients were studied. Sixty-ﬁve patients (30.8%) reported injuries with one or more of their attacks. The most common type of reported injury was tongue biting. Lacerations, bruises, limb fractures, dental injury, and burn were also reported. Conclusion: PNES commonly produce physical injuries. Despite the shibboleth that injuries rarely occur during PNES, mild injuries commonly happen and even severe injuries such as fractures and burns are not uncommonly reported in these patients. Patients with more dramatic seizure manifestations (e.g., urinary incontinence) were more likely to report ictal injuries. ß 2014 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.
1. Introduction Patients with epilepsy often have seizures with impairment of consciousness and abnormal uncontrolled movements. As a consequence, physical injuries are common in patients with epilepsy.1–4 Psychogenic non-epileptic seizures (PNES) consist of paroxysmal changes in responsiveness, movements, feelings, or behavior that are similar to epileptic seizures, but do not have a neurological origin and are not associated with epileptic EEG changes.5–8 Ictal injury, particularly tongue biting, has been reported in patients with PNES, as these may occur in epileptic seizures.9 However, physical injuries, particularly severe ones, might be considered strongly supportive of a presumptive diagnosis of epilepsy rather than PNES.
* Corresponding author at: Neurosciences Research Center, Shiraz Medical School, Shiraz University of Medical Sciences, Shiraz, Iran. Tel.: +98 9352274990; fax: +98 711 6121065. E-mail addresses: [email protected], [email protected] (A.A. Asadi-Pooya).
Few studies have described the spectrum of ictal injuries in patients with PNES. In the present report, we determined the spectrum of ictal injuries due to PNES. We also investigated the possible risk factors for ictal injury in these patients. 2. Materials and methods In this prospective study, all patients with PNES were evaluated at the outpatient epilepsy clinic at Shiraz University of Medical Sciences, from September 2008 to June 2013. The diagnosis was made by clinical assessment and ictal recording during a 2-h videoEEG monitoring with 10–20 system electrodes and additional T1 and T2 electrodes. A typical event was recorded with no abnormal EEG correlate and behavior consistent with PNES. We routinely perform verbal suggestion to induce PNES in all patients during video-EEG recording. Toward the end of the video-EEG recording session, we inform the patient that we must see the seizures to ascertain the diagnosis for treatment purposes. At the time of interpretation of the video-EEG monitoring, we review the video with the relatives or the caregivers to verify that habitual seizures were recorded. The behavioral characteristics of PNES were
http://dx.doi.org/10.1016/j.seizure.2014.02.001 1059-1311/ß 2014 British Epilepsy Association. Published by Elsevier Ltd. All rights reserved.
A.A. Asadi-Pooya et al. / Seizure 23 (2014) 363–366
ascertained both by an interview of patients and witnesses and by reviewing the recorded video-EEG monitoring. We asked all patients and their caregivers about history of any minor (e.g., tongue biting, bruises, and lacerations) or major (e.g., burns and fractures) physical injuries caused by seizures since their disease started. We always obtain a detailed clinical history to investigate for the possibility of a concomitant epileptic disorder in patients with PNES (i.e., presence of other seizure types, different from what we captured during the video-EEG monitoring, if the description is compatible with epileptic seizures). We also review the recorded EEG carefully to search for any interictal or ictal epileptiform discharges. An epileptologist interviewed all patients. If they agreed to share their information, they were included in the study. All personal data were kept conﬁdential through codes. Demographic variables (age, gender, education, age at seizure onset), clinical variables (seizure semiology and ictal injury), factors potentially predisposing to PNES (history of physical, emotional or sexual abuse, academic failure, head injury, any medical comorbidities, and family history of epilepsy), and video-EEG recording results were registered for all patients. All variables were summarized descriptively to characterize the study population. Pearson ChiSquare, Fisher’s Exact test, Kolmogorov–Smirnov, Shapiro–Wilk, and Mann–Whitney U test were used for statistical analyses. A P value <0.05 was considered as signiﬁcant. Subsequently, a binary logistic regression was performed on variables that were signiﬁcant in univariate analyses (P < 0.05) to correlate all the signiﬁcant independent variables with the dependent variable (i.e., ictal injury). This study was conducted with the approval by Shiraz University of Medical Sciences Review Board. 3. Results Two hundred and eleven patients were studied. One hundred and forty-one (66.8%) were female and 70 (33.2%) were male. Sixty-ﬁve patients (30.8%) reported injury with one or more attacks and 146 patients (69.2%) did not report any injury since their seizures started. The most common type of injury was tongue biting, reported by 28 patients (13.2%). Face, scalp, or limb lacerations were reported by 21 patients (9.9%); bruises by 14 patients (6.6%); fractures (leg fractures in two, nose fracture in one and pelvic fracture in another patient) by four patients (1.8%); dental injury by one (0.4%) and burned hand by one patient (0.4%). Four patients reported more than one type of injury. Demographic characteristics of patients with PNES and with ictal injury and those without injury are summarized and compared in Table 1. Clinical characteristics and semiology of patients with PNES with ictal injury and those without injury are summarized and compared in Table 2. Factors potentially predisposing to PNES in patients with injury and those without injury are summarized and compared in Table 3. The frequency of violent shaking movements (P = 0.04), nocturnal seizures (P = 0.008), urinary incontinence (P = 0.0001), postictal state (P = 0.01), and history of physical abuse (P = 0.01) was statistically signiﬁcantly higher and the duration of the
disease before reaching a correct diagnosis was signiﬁcantly longer (P = 0.01) in patients with ictal injury compared with those patients with PNES who did not have injury. The full model containing all the above predictors was statistically signiﬁcant (X2 = 41.78; P < 0.0001), indicating that the model was able to distinguish between PNES patients who report ictal injury and the others. The model correctly classiﬁed 69.2% of the patients. Within the model the following features were associated with ictal injury: urinary incontinence (P < 0.0001, Odds Ratio = 7.03, 95% conﬁdence interval = 2.62–18.8), violent shaking movements (P = 0.07, Odds Ratio = 1.83, 95% conﬁdence interval = 0.94–3.56), history of physical abuse (P = 0.08, Odds Ratio = 2.24, 95% conﬁdence interval = 0.88–5.7), duration of the disease before reaching to a correct diagnosis (P = 0.09, Odds Ratio = 0.96, 95% conﬁdence interval = 0.92–1.01), nocturnal seizures (P = 0.14, Odds Ratio = 1.64, 95% conﬁdence interval = 0.84–3.21), and postictal state (P = 0.13, Odds Ratio = 2.09, 95% conﬁdence interval = 0.79–5.56). 4. Discussion Physical injuries from seizures are common in patients with epilepsy; however, most of these injuries are mild. Severe injuries rarely occur in patients with epileptic seizures other than generalized tonic-clonic seizures.4 In the present study, we observed that physical injuries are also common in patients with PNES. About one-third of the patients with PNES reported injury during one or more of their attacks. Similar to epileptic seizures, severe injuries rarely occurred in patients with PNES; however, injuries such as fractures and burns were observed. Although the frequency of tongue biting and other injuries is signiﬁcantly lower in PNES than epilepsy,4,9 the presence of ictal injuries cannot distinguish between epileptic seizures and PNES. This contrasts with what many physicians believe.9,10 The problem becomes more complicated when we consider that psychogenic nonepileptic seizures are relatively common at epilepsy clinics.11,12 Previously, authors have tried to determine the signiﬁcance of speciﬁc types of injury (i.e., lateral tongue biting), either reported by patients or observed in the video-EEG monitoring units, and concluded that lateral tongue biting, but not ‘any’ tongue biting, has diagnostic signiﬁcance in distinguishing epileptic seizures from PNES, supporting the diagnosis of epileptic seizures.9 However, in our experience, one cannot rely on lateral tongue biting to distinguish between epileptic and non-epileptic attacks with certainty. The diagnosis of PNES requires careful integration of a detailed history and other clinical information (particularly, a video-EEG monitoring) and should never be driven by any single clinical sign or symptom alone.9,13 In this study, we found a model to predict who may report injury during psychogenic seizures. Patients who report ictal urinary incontinence had an odds ratio of more than seven to one for reporting ictal injury during their PNES. Patients who reported violent shaking movements during their seizures or had history of physical abuse showed a non-signiﬁcant trend to report ictal injury. These ﬁndings could be translated into a model, which predicts that patients with more unusual and unexpected
Table 1 Demographic characteristics of PNES patients with ictal injury and those without injury.a Demographic variable
Gender (female/male) Age at referral (mean standard deviation) Age of onset (mean standard DEVIATION) Education (some/diploma/university/missing)b Marital status (single/married/divorced/widowed)
Some data were missing. ‘‘Some’’ means less than 11 years of education; diploma means 11–12 years of education.
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Table 2 Clinical characteristics and semiology of PNES patients with ictal injury and those without injury.a Seizure characteristics
Seizure frequency (daily/weekly/occasional) Aura Violent shaking movements (low frequency high amplitude) Stiffening Fine shaking movements (high frequency low amplitude) Loss of tone Loss of consciousness Eyes closed Wax and wane movements (intermittent shaking movements with episodes of inactivity) Side to side head movements Urine incontinence Fecal incontinence Postictal state Pseudostatus Nocturnal seizures Hospital admission ICU admission Duration of disease before diagnosis, in years (mean standard deviation) Taking any antiepileptic drugs (AEDs) Taking more than one AED (polytherapy) Duration of taking AED(s), in years
presentations for PNES (e.g., urinary incontinence) more likely report ictal injury. The reasons for this ﬁnding need to be explored in future studies. In a previous study, we subdivided the patients with PNES into three groups: those with PNES and without either epilepsy or family history of epilepsy (group 1), those with PNES and concomitant epilepsy, but without family history of epilepsy (group 2), and those with PNES and family history of epilepsy, but without concomitant epilepsy (group 3). The frequency of reported ictal injuries in these three groups of patients was similar: 30% in group 1; 26% in group 2; and 39% in group 3 (P = 0.2).12 Therefore, the above observation could not be explained by concomitant epilepsy or a learning process driven by experience with epilepsy. In another study, 59 patients with PNES who reported antecedent sexual abuse were compared with 117 patients who did not report sexual abuse.14 A history of nocturnal spells (P = 0.0109), injury during spells (P = 0.0056), and incontinence during spells (P = 0.0083) were more common in the patients reporting sexual abuse.14 In our study, a history of sexual abuse did not predispose to ictal injury. However, we note that the rate of reported sexual abuse was low in our patients compared with most previous studies.15 5. Conclusion Physical injuries are common in patients with PNES and in general, their presence did not distinguish between epileptic seizures and PNES. Injuries such as fractures and burns, though
rare, are reported. Patients with more dramatic seizure manifestations (e.g., urinary incontinence) were more likely to report ictal injuries. Limitations of the study 1. This was a clinic-based series and may not represent the full spectrum of patients with PNES. 2. We did not systematically assess psychiatric and psychological problems in this study. 3. In this study, the physical injuries were not objectively documented; rather, they were reported by the patients or their caregivers. We also did not examine how many times the injury (especially, the most serious ones) led to further medical intervention (i.e., ER visits). 4. These patients did not have long-term follow-up. Therefore, we do not know that how many had AEDs withdrawn and whether epileptic seizures subsequently emerged.
Conﬂict of interest statement None. Acknowledgments We thank Dr. Michael R. Sperling for his thoughtful comments. We also thank the Neurosciences Research Center, Shiraz University of Medical Sciences for ﬁnancial support of this study. This study was performed on the same series of patients as in our previously published papers.11,12,15 References 1. Sapna CS, Sheeba SL, John J, Thomas SV. Accidents and injuries in people with epilepsy attending a tertiary care center in India. Epileptic Disord 2008;10(4): 276–81. 2. Neufeld MY, Vishne T, Chistik V, Korczyn AD. Life-long history of injuries related to seizures. Epilepsy Res 1999;34(2–3):123–7. 3. Buck D, Baker GA, Jacoby A, Smith DF, Chadwick DW. Patients’ experiences of injury as a result of epilepsy. Epilepsia 1997;38(4):439–44. 4. Asadi-Pooya AA, Nikseresht AR, Yaghoobi E, Nei M. Physical injuries in patients with epilepsy and their associated risk factors. Seizure 2012;21:165–8.
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5. O’Sullivan SS, Spillane JE, McMahon EM, Sweeney BJ, Galvin RJ, McNamara B, et al. Clinical characteristics and outcome of patients diagnosed with psychogenic non-epileptic seizures: a 5-year review. Epilepsy Behav 2007;11(1): 77–84. 6. Binzer M, Stone J, Sharpe M. Recent onset pseudoseizures-clues to etiology. Seizure 2004;13:146–55. 7. Hubsch C, Baumann C, Hingray C, Gospodaru N, Vignal JP, Vespignani H, et al. Clinical classiﬁcation of psychogenic non-epileptic seizures based on video-EEG analysis and automatic clustering. J Neurol Neurosurg Psychiatry 2011;82: 955–60. 8. Bodde NM, Brooks JL, Baker GA, Boon PA, Hendriksen JG, Mulder OG, et al. Psychogenic non-epileptic seizures—deﬁnition, etiology, treatment and prognostic issues: a critical review. Seizure 2009;18:543–53. 9. Brigo F, Storti M, Lochner P, Tezzon F, Fiaschi A, Bongiovanni LG, et al. Tongue biting in epileptic seizures and psychogenic events: an evidence-based perspective. Epilepsy Behav 2012;25:251–5.
10. de Timary P, Fouchet P, Sylin M, Indriets JP, de Barsy T, Lefe`bvre A, et al. Nonepileptic seizures: delayed diagnosis in patients presenting with electroencephalographic (EEG) or clinical signs of epileptic seizures. Seizure 2002;11(3):193–7. 11. Asadi-Pooya AA, Emami M. Juvenile and adult-onset psychogenic non-epileptic seizures. Clin Neurol Neurosurg 2013;115(9):1697–700. 12. Asadi-Pooya AA, Emami M. Demographic and clinical manifestations of psychogenic non-epileptic seizures: the impact of co-existing epilepsy in patients or their family members. Epilepsy Behav 2013;27(1):1–3. 13. Cuthill FM, Espie CA. Sensitivity and speciﬁcity of procedures for the differential diagnosis of epileptic and non-epileptic seizures: a systematic review. Seizure 2005;14:293–303. 14. Selkirk M, Duncan R, Oto M, Pelosi A. Clinical differences between patients with non-epileptic seizures who report antecedent sexual abuse and those who do not. Epilepsia 2008;49(8):1446–50. 15. Asadi-Pooya AA, Emami Y, Emami M. Psychogenic non-epileptic seizures in Iran. Seizure 2013. http://dx.doi.org/10.1016/j.seizure.2013.11.005.
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