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Longitudinal changes in seizure outcomes after resection of cerebral cavernous malformations in patients presenting with seizures: a long-term follow-up of 46 patients

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Abstract

Background

Seizure is the most common presentation in patients with cerebral cavernous malformations (CCMs). Although many articles have documented seizure outcomes after resection of CCM, few have conducted long-term follow-ups; thus, the fluctuating seizure outcomes have been neglected. The purpose of this study is to describe long-term postoperative seizure outcomes in patients with CCM and to compare seizure outcomes between patients with sporadic seizures and those with chronic seizures.

Methods

Forty-six patients with CCM presenting with seizures underwent surgery. The male-to-female ratio was 1:1, and the average age at initial seizure onset was 27.6 years. The mean preoperative seizure duration was 42.7 months. Patients were divided into two groups: a chronic group (N = 20) and a sporadic group (N = 26) according to seizure frequency and duration. The mean postoperative follow-up duration was 96.3 months, and the postoperative seizure outcomes were checked annually based upon Engel’s classification.

Results

After the first year of follow-up, 80.8 % of the sporadic group and 75.0 % of the chronic group were evaluated as Engel class I. These rates increased to 100.0 % and 90.0 %, respectively, at the eighth year of follow-up. Overall, 29 (63.0 %) of the 46 patients experienced changes in seizure outcomes over the follow-up period. Despite their delayed improvements, the chronic group showed less favorable outcomes throughout follow-up (p = 0.025).

Conclusions

Long-term follow-up is indispensable for accurately assessing postoperative seizure outcomes because these outcomes change continuously. We recommend earlier surgery to achieve seizure-free status in patients with CCM. However, even in the chronic group, surgery is recommended, considering the overall delayed improvement.

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Acknowledgements

The authors would like to thank Hee-Won Jung MD, PhD; Kyu-Chang Wang MD, PhD; Chang Wan Oh MD, PhD; Sun Ha Paek MD, PhD; Seung-Ki Kim MD, PhD and Jeong Eun Kim MD, PhD for allowing us to include their patients in the present study.

Ethical standards

This research was supported by the Original Technology Research Program for Brain Science through the National Research Foundation of Korea (NRF), funded by the Ministry of Education, Science and Technology (no. 2009–0094093). This research was performed in concordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments.

Disclosure

This study was approved by the Institutional Review Board of the Seoul National University Hospital (H-1212-009-445).

Conflicts of interest

None.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, Kangwon National University Hospital, Chuncheon, Gangwon-Do, South Korea

    Jiha Kim

  2. Department of Neurosurgery, Seoul National University Hospital, Seoul, Korea

    Chi Heon Kim & Chun Kee Chung

  3. Department of Neurosurgery, Seoul National University College of Medicine, 28 Yeongeon-dong, Jongno-gu, Seoul, 110-744, South Korea

    Chi Heon Kim & Chun Kee Chung

Authors
  1. Jiha Kim
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  2. Chi Heon Kim
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  3. Chun Kee Chung
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Correspondence to Chun Kee Chung.

Additional information

Comment

The reported incidence of epilepsy in cavernoma is between 35-70 % and more than 40 % of patients progress to drug resistant epilepsy. Several studies have addressed the problem of bleeding/clinical events in the natural history of cavernomas, and epilepsy control and clinical progress of epilepsy pre/post-surgical treatment of cavernoma although being an important goal of treatment, has been underappreciated (1, 4).

In a systematic review of the literature, Englot et al. (4) analyzed 31 articles with a total of 1,226 patients. They concluded that “75 % of patients became seizure free after resection, suggesting that a microsurgical approach often leads to a favorable outcome, but also indicating considerable room for improvement”.

This interesting and well-written paper on supratentorial cavernoma associated with epilepsy addresses several important points on both the surgical strategy for cavernoma and their post-operative course in the long-term follow-up.

One of the biggest dilemmas for a neurosurgeon treating epilepsy is when to operate or if an operation is appropriate in a patient with supratentorial cavernoma associated with sporadic epilepsy. In their paper, the authors report a long-term seizure control of 100 % in patients with sporadic epilepsy, this result justifying a more aggressive approach towards supratentorial cavernoma associated with sporadic epilepsy. The chronic epilepsy group has a less good outcome (although a 90 % seizure freedom is still a very impressive result), but in this group, the dilemma is really not if to operate but when to operate. The results in this paper suggest that an early surgical treatment would be associated with a better control of the seizure, avoiding the ever-present problem of dual pathology in lesional epilepsy (changes in the mesial structure induced by the long-term seizures associated with the cavernoma temporal or extra-temporal).

The authors have not addressed three important issues on the topic of supratentorial cavernoma associated with epilepsy;

1) Surgical strategy for cavernoma in eloquent areas

2) Electro-corticography and extended lesionectomy

3) Multiple cavernomas (mCCM) and seizure control

In several cases, cavernoma may present in eloquent area associated with speech functions (dominant temporal), motor functions (primary motor or SMA), vision (optic radiation or primary visual cortex). In those cases, a multimodal approach with intra-operative monitoring (IOM)/awake procedure is necessary to preserve function and achieve optimal seizure control.

The role of EcoG in cavernoma and in general epilepsy surgery is more controversial. In our institution, I use routinely EcoG for cavernoma resection. The rational is to maximize the resection of the perilesional gliotic/hemosiderin rim around the lesion (though to be epileptogenic) and being guided by the intra-operative spikes on EcoG.

The evidence in the literature in this regard are non-conclusive, with higher seizure control in those series using EcoG, but this does not reach statistical significance (4).

Particularly in cases with persistent epilepsy despite cavernoma resection, EcoG may have a role. I tend to approach these cases (generally a minority in any surgical series) as a de novo epilepsy cases; in our institution, we try to confirm the epileptogenic focus with first non-invasive EEG and then invasive monitoring (grids and depth over the surgical resection area of the cavernoma, and depth to rule out dual pathology). Once the focus is confirmed, we perform a tailored resection with intra-operative EcoG (5, 6).

At times this aggressive strategy may not be suitable due to the anatomical location of the cavernoma and this is particularly true for insular cavernoma.

On the other hand, this strategy is possibly the best one for those cases of dual pathology and associated mesial temporal atrophy, when the seizure are not controlled after cavernoma resection. Dual pathology is more common in cases of chronic epilepsy, and possible early intervention may prevent mesial temporal lobe changes associated with temporal cavernoma.

mCCM are a complex problem, particularly in those cases in which seizure control is the primary objective. Surgical treatment when an epileptogenic focus can be identified is associated with a satisfactory seizure control; van der Brelie et al. report a 78 % of seizure freedom in a selective group of patients with mCCM (2).

I entirely agree with the authors, an aggressive surgical strategy for supratentorial cavernoma (and in general cavernoma) is supported by a better outcome both for seizure control and bleeding (clinical event) prevention. Cavernoma and in particular supratentorial cavernoma associated with sporadic or chronic epilepsy should be approached by experienced epilepsy surgeon, and a multimodal approach (IOM, DTI, fMRI) to the resection should be used to maximize seizure control and minimize neurological deficit (3).

Jibril Osman Farah

Liverpool, UK

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Kim, J., Kim, C.H. & Chung, C.K. Longitudinal changes in seizure outcomes after resection of cerebral cavernous malformations in patients presenting with seizures: a long-term follow-up of 46 patients. Acta Neurochir 156, 1539–1547 (2014). https://doi.org/10.1007/s00701-014-2121-x

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