YEBEH-04194; No of Pages 3 Epilepsy & Behavior xxx (2015) xxx–xxx

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Brief Communication

Impact of psychogenic nonepileptic seizures on epilepsy presurgical investigation and surgical outcomes Kimberley Whitehead a,⁎, Suzanne O'Sullivan b, Matthew Walker c a b c

Sir Jules Thorn Telemetry Unit, National Hospital for Neurology and Neurosurgery, London WC1N 3BG, UK Department of Clinical Neurophysiology, National Hospital for Neurology and Neurosurgery, London WC1N 3BG, UK Department of Clinical and Experimental Epilepsy, UCL Institute of Neurology, London WC1N 3BG, UK

a r t i c l e

i n f o

Article history: Received 7 November 2014 Revised 12 January 2015 Accepted 13 January 2015 Available online xxxx Keywords: Epilepsy surgery Psychogenic nonepileptic seizures Nonepileptic attack disorder Outcomes

a b s t r a c t Introduction: We sought to determine the percentage of patients undergoing presurgical assessment that had both psychogenic nonepileptic seizures (PNESs) and epileptic seizures (ESs) captured within our telemetry unit and how this affected progression to surgery and describe eventual outcomes in patients with a history of mixed PNESs/ESs who underwent surgery. Material and methods: To determine what happened to patients who had PNESs recorded during a presurgical workup, we reviewed the records of 725 patients admitted to our telemetry unit for presurgical assessment between 2007 and 2013 and identified those with PNESs and ESs recorded. To determine outcomes postsurgery in operated patients who had mixed PNESs/ESs, we also reviewed the records of 519 patients who had had epilepsy surgery between 1999 and 2012 and identified those within this group who also had PNESs prior to surgery. Results: Nineteen of the 725 patients had PNESs captured during their presurgical telemetry along with ESs captured on either this or a previous study. Four of these patients were ultimately offered surgery. Nine of the 519 patients with a history of PNESs underwent epilepsy surgery. At 1 to 5 years of follow-up (mean: 4.1 years) of those nine patients, five were still having ESs and three patients had worsening or new-onset PNESs. At the last follow-up, four had had a worthwhile improvement. Discussion: This study suggests that recent outcomes for people with mixed PNESs/ESs are not as promising as previously described and that PNESs should remain a relative contraindication for surgery. © 2015 Elsevier Inc. All rights reserved.

1. Introduction It has been suggested that the co-occurrence of psychogenic nonepileptic seizures (PNESs) is a relative contraindication for epilepsy surgery, although the exact reasons for why it is a contraindication are not always explicitly stated [1]. Anecdotally, concerns are often due to worries about an increase in PNESs or other new somatization disorders postsurgery, possibly as compensation for improved control of epileptic seizures (ESs). Another worry is that these patients' existing PNESs may be worsened in response to the stress of a major life event like surgery. Finally, patients with extensive psychopathology may be considered unlikely to cope with the disappointment of an unsuccessful surgery. There is a scarcity of research to support clinical decision-making when it comes to the suitability of patients with mixed PNESs/ESs to undergo epilepsy surgery. The American Academy of Neurology's practice parameter for epilepsy surgery does not give any advice on this area [2].

⁎ Corresponding author. Tel.: +44 20 34483339. E-mail addresses: [email protected] (K. Whitehead), Suzanne.O'[email protected] (S. O'Sullivan), [email protected] (M. Walker).

Some authors advise that PNESs are not always a contraindication [3]. A review paper in 2007 notes a paucity of literature on postsurgical outcomes in these patients but suggested that patients in whom PNESs play a minor role in the clinical picture should not be denied surgery once psychiatric conditions are deemed stable [4]. Similarly, Foong and Flugel suggest that while not an absolute contraindication in patients with temporal lobe epilepsy (TLE), it is considered that such patients will need to have psychological interventions aimed at the resolution of PNESs prior to surgery [1]. Three recent studies have examined the progress of patients with mixed PNESs/ESs through an epilepsy surgery workup. A Brazilian study found that 4.8% of their presurgical group with TLE had mixed PNESs/ESs captured on telemetry but did not look at the outcome of this subgroup [5]. A Spanish study found that 12/630 (1.9%) of their patients admitted for telemetry had both PNESs and ESs [6]. Of this group, four patients underwent a temporal lobectomy and one underwent a frontal lobectomy with an Engel's scale outcome of I in four patients and II in one patient. However, it is not made clear whether PNESs persisted. Within a German presurgical population, 38/1342 (2.8%) patients had PNESs as well as ESs recorded [7]. All had lesions and most had TLE. Of those operated on, seven became free of both seizure

http://dx.doi.org/10.1016/j.yebeh.2015.01.017 1525-5050/© 2015 Elsevier Inc. All rights reserved.

Please cite this article as: Whitehead K, et al, Impact of psychogenic nonepileptic seizures on epilepsy presurgical investigation and surgical outcomes, Epilepsy Behav (2015), http://dx.doi.org/10.1016/j.yebeh.2015.01.017

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K. Whitehead et al. / Epilepsy & Behavior xxx (2015) xxx–xxx

types and four further patients had clinically relevant improvements but two patients became worse with recurrent pseudostatus epilepticus. The aims of this study were to determine the percentage of patients undergoing presurgical assessment that had both PNESs and ESs captured within our telemetry unit and how this affected progression to surgery and to describe eventual outcomes.

2. Material and methods For the first part of the study, which aimed to determine what happened to patients who had PNESs recorded during a presurgical workup, we reviewed the electronic records of 725 patients admitted to our video-EEG telemetry unit for presurgical assessment between 2007 and 2013 and identified those with PNESs and ESs recorded. We started from 2007 onwards because this is when we started acquiring and storing video-EEG data on our current system, so the data from this point can be easily accessed and reviewed. Patients with de novo PNESs seen only on the telemetry ward or PNESs felt to be ‘elaboration’ of epileptic auras were not included. For the second part of the study, which was to determine outcomes postsurgery, we also reviewed the records of 519 patients who had had epilepsy surgery between 1999 and 2012 and we identified those patients within this group who also had PNESs prior to surgery. The epilepsy audit lead and governance team classified the work as an audit; therefore, individual consent from patients was not required.

3. Results Nineteen of the 725 (2.6%) patients had PNESs captured during their presurgical telemetry along with ESs captured on either this or a previous telemetry study. Of those 19 with a ‘gold standard’ dual diagnosis, eight patients were not discussed at the multidisciplinary team (MDT) meeting because most of their attacks were nonepileptic. Of the 11 patients who were considered at the MDT meeting, five patients were not offered surgery — in two patients, this was solely due to the presence of PNESs and other psychiatric concerns. The specific psychiatric concerns surrounding these two patients were as follows: the first patient had a long history of anxiety and depression and somatization disorder as well as PNESs and the second patient had a history of depression and one suicide attempt plus mood and behavioral changes associated with frontal dysfunction. In three other patients, surgery was declined because of a mixture of concerns about the PNESs and insufficient information on the epileptogenic zone. Two patients who were to be

rediscussed following further tests declined a further presurgical workup. Four patients were ultimately offered surgery. In the second part of the study, we found that nine of the 519 (1.7%) patients that underwent epilepsy surgery had a history of PNESs. Seven patients had PNESs that were captured on video-EEG, one patient had a typical PNES that was witnessed by the neurology team on a ward round (documented 5 min of waxing and waning jerking with equal and reactive pupils, flexor plantars, and normal oxygen saturations), and one patient had a documented remote history of PNESs in her teenage years (#6) (Table 1). All nine underwent temporal lobe resections. Four patients had hippocampal sclerosis (HS) (#1, 2, 4, and 5); two patients had HS and data from other tests concordant with seizures arising from this area but, in addition, more widespread pathology on MRI (#7 and 8); and three patients had normal MRI (#3, 6, and 9). Patients #1, 4–6, and 8–9 did not have any psychiatric disorder diagnosed prior to surgery. Patient #2 had a history of anxiety. Patient #3 had a long-term eating disorder and a history of suicide attempts. Patient #7 had a history of depression. At 1 to 5 years of follow-up (mean: 4.1 years) of those nine patients, five were still having ESs and three patients had worsening or new-onset documented or likely PNESs. At the last follow-up, four had had a worthwhile improvement.

4. Discussion The percentage of our presurgical candidates that had PNESs and ESs captured was similar to that found in studies within specialist referral centers similar to ours (2.6% in our study vs. 2.8% [7] and 1.9% [6]). Psychogenic nonepileptic seizures captured during presurgical telemetry had an important impact. Despite the fact that 58% of patients with mixed ESs and PNESs were taken forward for surgical consideration, only 21% were offered a resection. In five/seven patients discussed at the MDT meeting but were not offered surgery, all or a significant part of the reasoning behind this decision hinged on the presence of PNESs and other psychiatric concerns. Another possible concern – when deciding how much of a patient's seizure burden has an epileptic etiology – is that in patients with mixed ESs and PNESs, it may not be possible to confidently extrapolate from the ES:PNES ratio seen on the monitoring unit and from that occurring at home. Patients with rare PNESs are likely to differ from those with frequent PNESs with respect to the course of this disorder before and after surgery. Those patients with PNESs identified prior to surgery had a mixed outcome. In five/nine patients, events believed to be ESs continued postsurgery. Only one of these patients had HS without more widespread pathology. Thus, the failure of seizures in these five patients to

Table 1 Postsurgery follow-up. Postsurgery follow-up 1 year #1 Seizure-free.

#2 Non-organic jerks/spasms have worsened. Other events are likely nonepileptic but cannot be distinguished from simple partial seizures. #3 Seizure-free. Deterioration of eating disorder. #4 Seizure-free.

3 years

5 years

Seizures — initially, the possibility of a nonepileptic etiology was discussed with the patient but seizures were managed as being epileptic. Events continue. Nonepileptic seizures were triggered by a new trauma.

Seizures continue.

Free of all events/seizures. Non-organic jerks/spasms continue.

Epileptic seizures return; semiology was unchanged. Seizures continue. New events of loss of awareness; semiology was not typical Events have largely been resolved. for seizures. Events are resolved now that stress levels have decreased. Seizure-free.

#5 Events at the time of new stressors are likely nonepileptic, and interictal EEG and ictal EEG are normal but cannot be distinguished from simple partial seizures. #6 Epileptic seizures have different semiology to presurgery; a new Epileptic seizures continue. pattern of interictal epileptiform activity was consistent with this. #7 Epileptic seizures continue; semiology was unchanged. Epileptic seizures continue with some further nonepileptic attacks and stress reactions. #8 Epileptic seizures continue; semiology was unchanged. #9 Seizure-free.

Epileptic seizures continue. Epileptic seizures continue;nonepileptic attacks appear to have been resolved.

Please cite this article as: Whitehead K, et al, Impact of psychogenic nonepileptic seizures on epilepsy presurgical investigation and surgical outcomes, Epilepsy Behav (2015), http://dx.doi.org/10.1016/j.yebeh.2015.01.017

K. Whitehead et al. / Epilepsy & Behavior xxx (2015) xxx–xxx

become fully controlled was not significantly different to their predicted odds of ES freedom and is in line with a large study from our own center [8]. That study identified long-term outcomes in 649 people undergoing epilepsy surgery from 1990 to 2008 (our patients #1–5 had their surgery within this period). Five years after surgery, the seizure-free rates (excluding simple partial seizures) were 55–56% for temporal lobe resections but those with other malformations or no detected abnormality had significantly earlier relapses than did those with HS. Although the ES outcome of the nine patients is broadly within expected limits, three of the four patients that were free of ESs were affected by worsening or new-onset (different from their previous PNES semiology) PNESs. Only one out of the nine patients was free of any events, epileptic or nonepileptic, postsurgery, but that patient only had one-year follow-up. Numerous studies have associated PNESs with low quality of life. Overall, this audit supports the currently held belief that coexistent PNESs should remain a relative contraindication for epilepsy surgery. The limitations of this study include its retrospective nature and the small (n = 9) sample of patients with mixed PNESs/ESs that had surgery. The latter makes it difficult to draw any definite conclusions on postsurgical outcomes. We carried out this study in light of the good results described in the Reuber et al. paper [7], but in the years that have passed since that study, it is likely that more challenging patients are being referred for a presurgical workup. Moreover, four patients with good outcomes in that study had follow-up of 13 months or less, and our study indicates that PNESs can reappear after a good response at 1 year. A further limitation to our study is the classification of the patients' postsurgical events which have largely been determined without the benefit of video-EEG. Although features such as semiology identical to previously captured ESs and a new distribution of spikes on EEG suggest events that are truly epileptic, without video-telemetry confirmation, it is possible that some of these patients' events are actually PNESs. Similarly, some of the assumed PNESs could be epileptic. Nevertheless, this

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study suggests that recent outcomes for people with mixed PNESs/ESs are not as promising as previously described and that PNESs should remain a relative contraindication for surgery. Conflict of interest We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome. References [1] Foong J, Flugel D. Psychiatric outcome of surgery for temporal lobe epilepsy and presurgical considerations. Epilepsy Res 2007;75:84–96. [2] Engel J, Wiebe S, French J, Sperling M, Williamson P, Spencer D, et al. Practice parameter: temporal lobe and localized neocortical resections for epilepsy: report of the quality standards subcommittee of the American Academy of Neurology, in association with the American Epilepsy Society and the American Association of Neurological Surgeons. Neurology 2003;60:538–47. [3] Benbadis SR. Psychogenic nonepileptic seizures. In: Wyllie E, editor. The treatment of epilepsy: principles and practice. 4th ed. Philadelphia: Lippincott, Williams & Wilkins; 2005. p. 623–30. [4] Castro LHM. Epilepsy surgery in patients with coexisting psychogenic nonepileptic seizures: diagnosis and treatment. J Epilepsy Clin Neurophysiol 2007;13:36–8. [5] Da Conceição PO, Nascimento PP, Mazetto L, Alonso NB, Yacubian EM, de Araujo Filho GM. Are psychiatric disorders exclusion criteria for video-EEG monitoring and epilepsy surgery in patients with mesial temporal sclerosis? Epilepsy Behav 2013;27: 310–4. [6] Vega-Zelaya L, Alvarez M, Ezquiaga E, Nogeiras J, Toledo M, Sola RG, et al. Psychogenic non-epileptic seizures in a surgical epilepsy unit: experience and a comprehensive review. In: Holmes M, editor. Psychogenic non-epileptic seizures in a surgical epilepsy unit: experience and a comprehensive review, epilepsy topics; 2014 [Available at: http://www.intechopen.com/books/epilepsy-topics/psychogenic-non-epilepticseizures-in-a-surgical-epilepsy-unit-experience-and-a-comprehensive-review. Accessed September 26, 2014]. [7] Reuber M, Kurthen M, Fernández G, Schramm J, Elger CE. Epilepsy surgery in patients with additional psychogenic seizures. Arch Neurol 2002;59:82–6. [8] de Tisi J, Bell GS, Peacock JL, McEvoy AW, Harkness WFJ, Sander JW, et al. The longterm outcome of adult epilepsy surgery, patterns of seizure remission, and relapse: a cohort study. Lancet 2011;378:1388–95.

Please cite this article as: Whitehead K, et al, Impact of psychogenic nonepileptic seizures on epilepsy presurgical investigation and surgical outcomes, Epilepsy Behav (2015), http://dx.doi.org/10.1016/j.yebeh.2015.01.017

Impact of psychogenic nonepileptic seizures on epilepsy presurgical investigation and surgical outcomes.

We sought to determine the percentage of patients undergoing presurgical assessment that had both psychogenic nonepileptic seizures (PNESs) and epilep...
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