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Surgery after intracranial investigation with subdural electrodes in patients with drug-resistant focal epilepsy: outcome and complications

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Abstract

Video–EEG monitoring with intracranial subdural electrodes is a useful assessment tool for the localization of the epileptogenic zone in patients with drug-resistant focal epilepsy. We aimed at assessing the morbidity related to electrode implantation and the surgical outcome in patients who underwent epilepsy surgery after intracranial EEG monitoring. All patients (N = 58) admitted to our Epilepsy Surgery Centre for drug-resistant focal epilepsy who underwent resective surgery after intracranial monitoring with subdural electrodes and were followed up for at least 2 years were included in the study. Their mean age was 30.4 years (range 8–60 years), 25 (43 %) were female, and 44 (76 %) had a preoperatively detected structural lesion. The mean duration of invasive recording was 2.3 days (range 1–14 days). Extraoperative ECoG allowed the identification of the epileptogenic focus in all cases. The temporal lobe was involved in 21 (36 %) patients, whereas extratemporal foci were identified in 24 (41 %) patients. Thirteen patients (23 %) had multilobar involvement. Functional brain mapping was performed in 15 (26 %) patients. Transient complications related to electrode implantation occurred in three patients. Among patients with evidence of lesion on preoperative MRI, lesionectomy alone was performed in 12 cases (27 %), while it was combined with tailored cortical resection in the remaining cases. Tailored cortical resection was also performed in patients without evidence of lesion on MRI. After resective surgery, transient neurological deficits occurred in five cases, while another patient experienced permanent lateral homonymous hemianopia. At the last follow-up observation, 34 (57 %) patients were seizure-free (Engel class I). This study suggests that invasive EEG recording with subdural electrodes may be useful and fairly safe for many candidates for epilepsy surgery.

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Acknowledgments

This study was supported by the ‘Neurone’ Foundation for research in neuropsychobiology and clinical neurosciences.

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Authors and Affiliations

  1. Epilepsy Surgery Unit, Department of Neurological Sciences, IRCCS Neuromed, 86077, Pozzilli, Isernia, Italy

    Roberta Morace, Giancarlo Di Gennaro, Pier Paolo Quarato, Antonio Sparano, Addolorata Mascia, Giulio Nicolò Meldolesi, Liliana Graciela Grammaldo, Marco De Risi & Vincenzo Esposito

  2. Center of Epidemiology, Surveillance and Health Promotion, Italian National Institute of Health, Rome, Italy

    Angelo Picardi

  3. Department of Neurosurgery, “La Sapienza” University, Rome, Italy

    Vincenzo Esposito

  4. ‘Neurone’ Foundation for Research in Neuropsychobiology and Clinical Neurosciences, Rome, Italy

    Giulio Nicolò Meldolesi

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  1. Roberta Morace
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  2. Giancarlo Di Gennaro
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  7. Giulio Nicolò Meldolesi
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  8. Liliana Graciela Grammaldo
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Correspondence to Giancarlo Di Gennaro.

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Comments

Steven G. Ojemann, Aurora, USA

Morace et al. report on 58 patients who underwent resective surgery at their Epilepsy Center following invasive monitoring. They detail the morbidity related to invasive monitoring and resective surgery and outcomes in terms of seizure control with a minimum follow-up of 2 years in this series.

Ictal intracranial EEG represents the definitive method for localizing an individual’s ictal onset zone, and intracranial electrodes can overcome many of the limitations of scalp EEG, which include problems with volume conduction effects, difficulty identifying deeply located current sources, and problems with physiological artifacts. As the authors demonstrate, intracranial electrodes also provide the opportunity to perform electrical stimulation mapping of essential sites for critical functions such as language.

These advantages of invasive recordings potentially come at a price. Complications are well described in numerous articles cited by the authors, and their series further informs this literature. The authors report three complications related to electrode placement: one patient with brain edema and two with subdural hemorrhages. They do not report other types of complications such as wound infections, deeper infections, CSF leaks, or need for additional electrode placement or repositioning, which have been described in many of the other large series of invasive recording cited by the authors.

The authors cite one series in which complications were correlated with the number of contacts implanted, though others have failed to find such a correlation [1]. Insufficient coverage risks failure to adequately define the epileptic focus and potentially requires return to the operating room for additional electrode placement or repositioning in cases where ictal onset appears to arise outside of the covered area. Striking a balance between the questions of accuracy and safety requires judiciousness regarding when to employ intracranial monitoring and what territory one should monitor. These choices are best made in collaboration with an experienced, multidisciplinary team taking into consideration multiple sources of data including evaluation of the ictal semiology, ictal electroencephalographic monitoring, high-resolution MR imaging, intracarotid amobarbital (Wada) testing, neuropsychological measures, and sometimes additional imaging which has been shown to have clinical value, such as ictal single photon emission computed tomography or 18F-fluorodeoxyglucose and 11C-flumazenil positron emission tomography. In cases of mesial temporal lobe epilepsy, when there is a high degree of concordance between these different measures of cerebral structure and ictal and interictal dysfunction, then good results have been obtained by proceeding to resection without first employing intracranial recording techniques [2].

With respect to mapping of essential sites for critical functions, the authors point out that mapping with subdural arrays can be performed over a longer time period and with greater patient comfort than one can typically achieve with intraoperative mapping. Intraoperative stimulation mapping, however, does offer the opportunity to assess function as the resection progresses and can often define the maximum extent of a resection that encroaches on an “eloquent” locus to a higher degree than extraoperative mapping can achieve. Intraoperative mapping also affords the opportunity to map subcortical white matter pathways when deeper resections are undertaken [3, 4]. Therefore, I would suggest that extraoperative and intraoperative mapping techniques each have advantages and disadvantages and can be used in a complementary manner.

Ablative or disconnective surgery for the treatment of epilepsy requires precise definition of the zone of ictal onset and precise definition of proximate or potentially overlapping sites that are essential for critical neurologic functions. In many cases, these zones and sites are associated with no structural features or abnormalities that can be defined with current imaging. Invasive recording and mapping techniques are therefore a fundamental part of the armamentarium of any center performing epilepsy surgery, and this article further informs the literature about the associated risks and benefits.

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2. Cukiert A, Cukiert CM, Argentoni M et al (2009) Outcome after corticoamygdalohippocampectomy in patients with refractory temporal lobe epilepsy and mesial temporal sclerosis without preoperative ictal recording. Epilepsia 50(6):1371–1376.

3. Duffau H, Peggy Gatignol ST, Mandonnet E et al (2008) Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. J Neurosurg 109(3):461–471

4. Keles GE, Lundin DA, Lamborn KR et al (2004) Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. J Neurosurg 100(3):369–375

Johannes Schramm, Bonn, Germany

The authors report on a medium-sized series of 58 cases who needed invasive presurgical evaluation with implanted strip and grid electrodes before epilepsy surgery. A minimum follow-up of 2 years is available. The array of diagnoses is a bit atypical with a high number of gliosis cases, an expected number of dysplasia cases, but only about 14 % tumors. In other series, tumors may account for 30–50 % of drug-resistant epilepsy cases.

The techniques used are pretty standard and well illustrated in the two figures. The tables provide detailed information about the electrodes that one can use, which may be pretty useful. This invasive evaluation allowed the authors to make a decision between those cases that needed lesionectomy alone compared to extended lesionectomy, i.e., lesionectomy combined with tailored cortical resection. The good coverage of recent references allows the reader to gain a good impression of this technique by reading the article or looking-up the references in addition.

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Morace, R., Di Gennaro, G., Picardi, A. et al. Surgery after intracranial investigation with subdural electrodes in patients with drug-resistant focal epilepsy: outcome and complications. Neurosurg Rev 35, 519–526 (2012). https://doi.org/10.1007/s10143-012-0382-5

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