Clinical Study Received: October 21, 2013 Accepted after revision: April 24, 2014 Published online: December 9, 2014
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Outcome of Bipolar Electrocoagulation with Lesionectomy in the Treatment of Epilepsy Involving Eloquent Areas Feng Zhai a, b Jian Zhou a, b Tianfu Li a–c Zhiqiang Cui a Guoming Luan a–c
b
Department of Neurosurgery, Beijing Sanbo Brain Hospital, Capital Medical University Beijing, Beijing Key Laboratory of Epilepsy, and c Center of Epilepsy, Beijing Institute for Brain Disorders, Beijing, China
Key Words Epilepsy · Bipolar electrocoagulation on functional cortex · Lesionectomy · Multiple subpial transections
Abstract Background/Aims: We have demonstrated previously that bipolar electrocoagulation on functional cortex (BCFC) is a safe and effective approach for epilepsy involving eloquent areas. Here, we report the results of BCFC with lesionectomy for patients with epileptogenic foci partially overlapping eloquent areas. Methods: Forty patients who had been treated with lesionectomy with BCFC were retrospectively reviewed with regard to seizure outcome and neurological deficits. Ten similar patients who had received lesionectomy with multiple subpial transections (MST) were examined as a control group. Results: In the lesionectomy group with BCFC, Engel class I was achieved in 18 (45%) patients, class II in 8 (20%) patients, class III in 8 (20%) patients and class IV in 6 (15%) patients. Five (12.5%) patients developed mild hemiparesis and 1 (2.5%) patient mild sensory dysphasia. In the lesionectomy group with MST, Engel class I was achieved in 3 (30%) patients, class II in 2 (20%) patients, class III in 3 (30%)
© 2014 S. Karger AG, Basel 1011–6125/14/0931–0001$39.50/0 E-Mail [email protected] www.karger.com/sfn
patients and class IV in 2 (20%) patients. Two (20%) patients developed mild hemiparesis and 1 (10%) patient moderate hemiparesis. All these complications recovered within 1–12 months. Conclusions: Compared with MST, the outcome of BCFC with lesionectomy is similar. But since MST leads to mechanical injury, while BCFC causes thermal injury, the complications of BCFC seem less severe. © 2014 S. Karger AG, Basel
Introduction
Resection of epileptogenic foci is the main procedure of epilepsy surgery at present. Patients can get ideal seizure control or even be cured. However, if the epileptogenic foci are overlapped by functionally critical cortices, their resection might lead to unacceptable neurological deficits. In case of epileptogenic foci specifically located within eloquent areas, we have previously developed and applied a new approach. The procedure is called bipolar electrocoagulation on functional cortex (BCFC) [1–3]. The principle of BCFC is similar to multiple subpial transections (MST) [4, 5]. Guoming Luan Department of Neurosurgery, Beijing Sanbo Brain Hospital Capital Medical University Beijing No. 50 Xiangshan Yikesong Road, Haidian District, Beijing 100093 (China) E-Mail luangm3 @ 163.com
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
a
The combined therapy of resection of foci and BCFC has been shown to be effective in our previous study [2, 3]. In the present study, we describe the outcome of this method in 40 epilepsy patients and have compared the results with 10 cases of MST.
Methods
Results
Surgical Procedure The motor, sensory and language cortices and epileptogenic foci were identified with cortical stimulation or intraoperative wake-up test in order to address the epileptogenic regions located in the eloquent and noneloquent areas. After resection of nonfunctional epileptogenic cortices, electrocorticography (ECoG) (fig. 1a) was performed in functional epileptogenic regions before BCFC [1, 2]. BCFC was applied over the arachnoid membrane with an output power of 4 W. The brain surface was kept clean and moist with a saline gauze. There was a 45° angle between the forceps axis and the brain surface. The direction of electrocoagulation was perpendicular to the long axis of the brain gyrus. The tip diameter of the bipolar forceps was 2 mm. This procedure was performed at an interval of 5 mm and with 1 s duration. The brain surface was washed immediately with saline to lower the brain temperature which had been elevated by the heat of electrocoagulation. Following the BCFC procedure, ECoG was performed (fig. 1b). If significant interictal spikes persisted in the ECoG after BCFC, the BCFC procedure was repeated with 5 W. The output power never exceeded 5 W because a higher output power may damage the internal pyramidal layer and may result in unacceptable neurological deficits.
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Follow-Up The mean duration of postoperative follow-up after lesionectomy with BCFC was 25.5 (range 18–48) months. Engel class I outcome was achieved in 18 (45%) patients, class II in 8 (20%) patients, class III in 8 (20%) patients and class IV in 6 (15%) patients [6]. Follow-up MRI was performed in 35 patients 1–2 years after surgery and showed no abnormality in any patient (fig. 4a, b). EEG was performed in 35 patients, and among them, 5 patients demonstrated normal EEG. The EEG of the other patients still showed spike waves or spike slow waves. The mean duration of postoperative follow-up after lesionectomy with MST was 30.5 months. Engel class I outcome was achieved in 3 (30%) patients, class II in 2 (20%) patients, class III in 3 (30%) patients and class IV in 2 (20%) patients. Complications The primary sensory-motor cortex was involved in 37 patients, Wernicke’s area in 2 patients and Broca’s area in 1 patient. Twenty patients developed mild encephaledema identified by computed tomography at the acute stage (1–7 days) after electrocoagulation. Five patients (cases 16, 17, 21, 28 and 33), who had been treated with electrocoagulation in the primary sensory-motor cortex, developed transient mild hemiparesis of the opposite limbs and all patients fully recovered within 1 month. One patient (case 6), who had been treated with electrocoagulation in the sensory language cortex (Wernicke’s area), developed mild sensory dysphasia. The patient fully recovered within 3 months. No occurrences of hemorrhage, infection or other complications were observed. In the control group with lesionectomy with MST, 2 patients developed mild hemiparesis, which resolved within 6 months, and 1 patient developed moderate hemiparesis and recovered within 1 year. There were no occurrences of infection and other complications. Zhai/Zhou/Li/Cui/Luan
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Patients Forty patients with intractable epilepsy involving eloquent areas who underwent resection with BCFC at Beijing Sanbo Brain Hospital and Beijing Sanbo Fuxing Brain Hospital from May 2004 to May 2011 were included in this study and followed up for 18–48 (mean 25.5) months. The study group included 25 men and 15 women aged 10–35 years with a mean age of 15.5 years. On average, they had a 82.8-month recorded preoperative history of epilepsy. Seizure types included complex partial seizures, simple partial seizures, tonic seizures and generalized tonicclonic seizures. All 40 patients underwent magnetic resonance imaging (MRI) and video scalp electroencephalography (EEG) monitoring as a presurgical evaluation. Additionally, 31 patients received magnetoencephalography (MEG) and 8 patients received fluorodeoxyglucose positron emission tomography (FDGPET). The Wada test was performed in 15 patients and no functional shift of motor, sensory or language was identified. Moreover, intracranial EEG (invasive monitoring) was applied in 17 patients. The presurgical evaluations for all 40 patients are summarized in tables 1 and 2. As a control group, an additional 10 patients with intractable epilepsy involving eloquent areas were included in this study. The 5 men and 5 women in the control group were 12–30 (mean 17) years old. These patients underwent lesionectomy for noneloquent areas and lesionectomy with MST for eloquent areas. On average, all patients were followed up for 30.5 months.
2
Red and white stripes at regular intervals were clearly visible on the electrocoagulated cortex (fig. 2a). BCFC was applied over the arachnoid mater and the blood vessels located in the pial mater remained undamaged except for the capillaries (fig. 3a). After BCFC, the cortex was covered by the artificial dura, which can significantly reduce the occurrence of adhesions and epilepsy (fig. 2b).
Table 1. Findings in 40 patients who underwent BCFC and lesionectomy
Case No.
Sex
Age, years
DOE, months
MCST
Postoperative deficits
FU, months
Postoperative EEG
Engel outcome
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40
F F M M M F M M F F M M F M M M M M F M M M M M M M M F F F F M M F F M F M M F
10 12 14 20 22 10 15 13 35 18 28 15 12 22 18 12 12 16 23 16 12 12 15 18 17 25 31 14 27 28 20 10 17 13 13 20 25 20 15 14
48 55 41 120 170 46 140 64 180 72 60 55 41 50 70 72 72 90 30 12 72 70 38 60 48 60 240 36 180 190 180 240 360 26 36 84 180 48 60 24
SPS CPS SPS, GTC SPS, GTC SPS, GTC CPS CPS, GTC SPS, GTC GTC SPS SPS, CPS SPS, CPS SPS SPS, CPS, GTC SPS SPS, SGTC SPS, GTC SPS, CPS SPS, GTC SPS, GTC SPS, SGTC SPS, CPS SPS, SGTC SPS, TS SPS, SGTC SPS, GTC SPS, SGTC SPS, GTC SPS SPS, GTC SPS, CPS SPS, SGTC GTC CPS GTC SPS, GTC SPS, SGTC SPS, SGTC SPS, GTC SPS, CPS
none none none none none mild dysphasia none none none none none none none none none mild hemiparesis mild hemiparesis none none none mild hemiparesis none none none none none none mild hemiparesis none none none none mild hemiparesis none none none none none none none
18 24 30 25 32 40 24 32 48 18 24 24 18 24 18 18 25 26 22 36 28 36 38 24 18 25 26 24 26 18 30 18 18 36 18 22 25 18 20 24
R/frontoparietal normal EEG L/frontal R/hemisphere R/frontoparietal L/frontotemporal R/frontoparietal R/frontoparietal normal EEG R/frontoparietal R/frontotemporal L/temporal L/frontoparietal bilateral (left > right) diffuse L/hemisphere diffuse R/frontoparietal R/frontoparietal R/hemisphere normal EEG R/frontoparietal R/frontoparietal R/frontoparietal L/frontoparietal L/hemisphere L/frontoparietal normal EEG R/hemisphere diffuse L/frontoparietal normal EEG R/hemisphere diffuse L/anterior head R/frontal-central bilateral anterior head L/temporal R/hemisphere n.d. n.d. n.d. n.d. n.d.
I I I III I II I II I II I III II IV IV II II III I I III II III IV III I III IV I IV I I I I IV I III I I II
The therapy of functional epilepsy has always been a difficult problem for surgeons. BCFC is a surgical technique that can reduce cortex-related seizures by destructing the epileptic region with thermal energy. Combining BCFC and resection surgery is an effective surgical pro-
cedure to treat functional epilepsy. After resection of nonfunctional epileptogenic regions, the functional epileptogenic region was electrocoagulated, and no permanent complications were observed. Morrell et al. [4] suggested that the functional arrangement in the cortex is primarily oriented vertically and the intracortical fibers, which are thought to be responsible
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Discussion
3
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
DOE = Duration of epilepsy; MCST = major clinical seizure types; FU = follow-up; SPS = simple partial seizure; CPS = complex partial seizure; GTC = generalized tonic-clonic seizure; TS = tonic seizure; SGTC = secondary generalized tonic-clonic seizure; n.d. = not done.
Table 2. Neuroimaging, video EEG and MEG Video scalp EEG
Invasive monitoring
MEG
interictal EEG
ictal EEG
interictal EEG
ictal EEG
1
R/frontal hyperintense
R/hemisphere
bilateral (right > left)
R/frontoparietal
R/frontal
n.d.
2
R/frontal FCD
R/frontoparietal
bilateral diffuse
R/frontoparietal
R/frontal
R/frontal
3
L/frontal softened focus
L/frontal
L/anterior head
n.d.
L/frontal-central
4
R/frontal FCD
R/frontal
R/hemisphere diffuse
n.d.
R/frontoparietal
5
R/frontoparietal softened focus
R/frontoparietal
R/hemisphere
R/frontoparietal
6
L/temporal FCD
L/frontoparietal, posttemporal
L/hemisphere
n.d.
7
no abnormality detected
R/frontoparietal
R/hemisphere
R/frontoparietal
8
R/frontoparietal gray matter
R/hemisphere
R/frontal-central
n.d.
9
no abnormality detected
R/frontoparietal
R/hemisphere
R/frontoparietal
10
R/frontoparietal softened focus
R/frontoparietal
R/frontoparietal
n.d.
11
R/frontal FCD
R/anterior head
R/anterior head
R/frontotemporal
12
L/temporal FCD
bilateral anterior head
bilateral anterior head (left > right)
n.d.
L/frontotemporal
13
L/parietal FCD
L/frontotemporoparietal L/frontoparietal
n.d.
L/parietal
14
L/frontoparietal hyperintense
bilateral (left > right)
bilateral (left > right) diffuse
L/frontoparietal
L/frontoparietal
L/multiple lobes
15
L/frontal FCD
L/frontoparietal
L/hemisphere
L/frontoparietal
L/frontoparietal
n.d.
16
R/frontal FCD
R/anterior head
R/anterior head
n.d.
R/frontal
17
R/frontal FCD
R/hemisphere diffuse
R/anterior head
n.d.
R/frontal
18
no abnormality detected
R/hemisphere
R/hemisphere
R/frontoparietal
R/frontoparietal
n.d.
19
L/frontal FCD
L/anterior head
normal EEG
L/frontotemporal
L/frontal
n.d.
20
R/frontotemporal softened focus
R/hemisphere
R/hemisphere
n.d.
R/frontotemporal
21
R/frontal FCD
bilateral anterior head (right > left)
R/frontoparietal
n.d.
R/frontoparietal
22
R/frontal FCD
R/frontoparietal
R/frontoparietal
n.d.
R/frontoparietal
23
L/frontoparietal FCD
L/frontoparietal
bilateral diffuse
L/frontoparietal
24
L/frontal FCD
bilateral frontoparietal
L/frontoparietal
n.d.
25
L/frontoparietal FCD
L/frontoparietal
L/hemisphere
L/frontoparietal
26
L/frontal softened focus
L/frontoparietal
L/anterior head
n.d.
L/frontoparietal lobe
27
R/frontotemporoparietal softened focus
R/hemisphere
R/frontoparietal
n.d.
R/frontotemporal lobes
28
no abnormality detected
L/hemisphere
L/hemisphere
L/frontoparietal
4
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
R/frontoparietal
R/frontoparietal L/temporal
R/frontoparietal
R/frontoparietal junctional zone n.d.
R/frontal
n.d. R/frontoparietal
R/frontal
L/frontoparietal
R/frontal
L/multiple lobes L/frontoparietal
L/frontoparietal
L/frontoparietal
Zhai/Zhou/Li/Cui/Luan
n.d.
L/multiple lobes Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Case MRI findings No.
Table 2. (continued) Case MRI findings No.
Video scalp EEG
Invasive monitoring
interictal EEG
ictal EEG
interictal EEG
MEG ictal EEG
29
L/frontal FCD
L/frontal-central
L/frontal-central
n.d.
30
R/frontoparietal FCD
R/hemisphere
R/hemisphere
R/frontoparietal
31
L/frontal softened focus
L/anterior head
L/frontal
n.d.
L/frontal and central
32
multiple nodules (TSC)
R/frontal-central
R/frontal-central
n.d.
R/frontal
33
R/frontal FCD
bilateral anterior head
R/frontoparietal
n.d.
R/frontal
34
L/temporal softened focus
L/temporal
normal EEG
n.d.
L/temporal
35
R/frontoparietal FCD
R/hemisphere
R/hemisphere
R/frontotemporoparietal
36
R/frontal FCD
R/anterior head
R/anterior head
n.d.
37
no abnormality detected
bilateral anterior head (right > left)
R/anterior head
R/frontoparietal
R/frontoparietal
R/frontotemporal
38
L/frontal FCD
L/hemisphere
L/anterior head
L/frontoparietal
L/frontal
n.d.
39
R/frontotemporal softened R/anterior head focus
R/frontotemporal
n.d.
R/frontal
40
R/frontal softened focus
R/frontoparietal
n.d.
R/frontal
R/frontoparietal
L/frontal lobe R/frontoparietal
R/frontoparietal
n.d.
L/multiple lobes R/frontal
for seizure spread, are oriented horizontally; therefore, these horizontal fibers can be sectioned without causing cortical dysfunction. This technique was termed ‘multiple subpial transections’ (MST) [4, 5, 7–10]. By MST, the horizontal synchronizing neuronal networks are interrupted, whereas the vertical functional units are preserved. Based on the principle of MST, in 1999, we applied BCFC in animal models and demonstrated the efficacy of BCFC in treating epilepsy [11]. We also found that electrocoagulation with an output power of 4–5 W can damage the nerve fibers of the external molecular layer and the external granular layer. The horizontal fibers are mostly located at the superficial cortical level [4]. However, the damage of electrocoagulation only reaches to the third layer of the cortex with the internal pyramidal layer and nerve fibers (fig. 3b, c) remaining untouched. Therefore, the surgical procedure did not lead to unacceptable neurological deficits. We have previously demonstrated the efficacy of BCFC alone in the treatment of refractory epilepsy with an effective rate of 73.3% [1]. Luan et al. [2] also compared lesionectomy with BCFC with lesionectomy alone.
It was demonstrated that lesionectomy with BCFC is significantly more effective than lesionectomy alone [2, 3]. However, so far, lesionectomy with BCFC for the treatment of refractory seizures involving eloquent areas has not been well established. Here, we report 40 patients treated with BCFC and lesionectomy, whose epileptogenic regions were partially overlapped by eloquent areas. In this study, 20 patients developed mild encephaledema at the acute stage following the electrocoagulation procedure. But the encephaledema disappeared within 1–2 weeks. MRI showed no abnormalities after 1–2 years of follow-up. Five patients (cases 16, 17, 21, 28 and 33), who had been treated with electrocoagulation in the primary sensory-motor cortex, developed mild hemiparesis. One patient (case 6), who had been electrocoagulated in the sensory language cortex, developed mild sensory dysphasia. When the patients were discharged from the hospital, the neurological deficits had improved significantly. All the neurological deficits disappeared within 3 months. No subdural hemorrhages and infections were observed. In the control group with lesionectomy with MST, 2 patients developed mild hemiparesis, which resolved within 6 months, and 1 patient
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
5
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
TSC = Tuberous sclerosis complex; n.d. = not done.
a
b
developed moderate hemiparesis and recovered within 1 year. There were no occurrences of infection and other complications. Our results can be summed up as follows. In the lesionectomy group with BCFC, the symptoms of 34 (85%) patients improved (Engel class I–III). Eighteen (45%) patients with class I outcome remained seizure free for 18–48 months after surgery. In the lesionectomy group with MST, the symptoms of 8 (80%) patients improved (Engel class I–III) and 3 (30%) patients remained seizure free. 6
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Reports on the efficacy of pure MST or resection with MST have differed widely. Schramm et al. [5] reported 20 patients who underwent pure MST. Nine (45%) patients achieved a worthwhile improvement (Engel class I–III) in a mean follow-up period of 58 months. Mulligan et al. [8] reported 12 patients who underwent pure MST or resection and MST. Among them, 5 (42%) patients experienced a significant improvement in seizure frequency and in 2 patients, the severity of seizures markedly decreased. Orbach et al. [9] reported 54 patients who underwent MST with a mean follow-up period of 56 months. Zhai/Zhou/Li/Cui/Luan
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Fig. 1. a ECoG before BCFC reveals multiple spikes and slow waves in the central cortex. b ECoG after BCFC shows reduced spikes and slow waves with decreased amplitude.
a
b
a
b
c
d
arachnoid turned blue, mild shrivel was visible and no blood vessels were damaged. HE. ×40. b After electrocoagulation, the number of neurons in layers I–III decreased and the deep structure was normal. NeuN. ×40. c Remarkable edema was found in the axons
of the superficial neurons and the number of axons decreased, while the deep nerve fiber axons were intact. MAP. ×100. d PreBCFC pathology of the sensory area. Radial abnormal cortical layering and some pyknotic neurons were detected (FCD IA). HE. ×40.
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Fig. 3. a Electrocoagulation was applied over the arachnoid. The
7
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Fig. 2. a Intraoperative view after BCFC. Red and white stripes at regular intervals are visible in the electrocoagulated central area. b The artificial dura covered the electrocoagulated cortex without adhesions.
a
Central sulcus
Area of resection
b
Area of electrocoagulation
Fig. 4. a The FCD was observed in the central area with axial FLAIR-weighted MRI. b Eighteen months after BCFC and resection, no abnormality was found in the electrocoagulated central area with axial FLAIR-weighted MRI.
Forty-three (79.6%) patients had a consistent and significant reduction in seizure frequency and 27 (50%) patients were entirely seizure free. However, 10 (18.6%) patients had an increase in seizure frequency several years after surgery following initial postoperative improvement [9]. Devinsky et al. [12] also reported 10 of 13 (77%) patients who improved after MST and resection. Among them, 1 patient who underwent right partial frontal lobectomy and frontal MST suffered from the lasting postoperative 8
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Zhai/Zhou/Li/Cui/Luan
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
FCD
complication of facial weakness. In 1 of 4 patients who had MST over temporal language areas, mild dysphasia developed and resolved within 6 months [12]. Blount et al. [13] reported that in 26 patients who underwent cortical resection with MST, 12 (46%) patients were seizure free (Engel class I), while 11 (42%) patients achieved Engel class II and III and 3 (12%) patients Engel class IV. Another study reported 2 patients with atypical infantile spasms who underwent pure MST and achieved a favorable outcome [14]. In general, compared with lesionectomy with MST, the outcome and complications of lesionectomy with BCFC are similar. On the one hand, BCFC was applied over the arachnoid membrane; on the other hand, BCFC causes thermal injury, while MST leads to mechanical injury. So BCFC reduced the subarachnoidal hemorrhage and small intraparenchymal clots that are seen after MST and with less scar. Therefore, the complications of BCFC are less severe. Six (15%) cases with class IV outcome showed persistent epileptiform activity in either the ipsilateral or bilateral hemispheres. MEG spikes within multiple lobes were observed in 4 out of 6 patients with class IV outcome. The reason might be that the epileptogenic regions were larger than the regions of interest of resection and BCFC. We conjectured that a more accurate localization of epileptogenic regions may further improve surgical efficacy. Follow-up EEG was performed in 35 patients and, among them, 5 patients demonstrated normal EEG with class I outcome. The data suggest that postoperative normalization of EEG correlates with good surgical outcome for seizure control. Five patients had no abnormality and 2 patients (case 1 and 14) showed hyperintensity detected by MRI. However, the pathology of all excised epileptogenic regions proved that they were focal cortical dysplasias (FCDs). In case 18, before BCFC, a small piece of the sensory cortex was snapped and the pathology proved that this was FCD (fig. 3d). So, we inferred that the MRI abnormality was not correlated with the outcome of BCFC. However, there are limitations of applying BCFC for the treatment of epilepsy involving eloquent areas. The area of the sulci accounts for two thirds of all brain cortices. It appeared that inadequate damage to the two lateral cortical banks of a gyrus, which reach down into two adjoining sulci, could lead to remaining seizures. So, the remaining cortices in sulci without coagulation could still induce seizures. No correlations were observed between the outcome of treatment and factors such as sex and age of patients,
type and frequency of seizures, the brain hemisphere and the cortical location of the electrocoagulation procedure.
ping area between the epileptogenic regions and the eloquent area. Further studies will need to focus on the prospective outcome of BCFC in patients with intractable epilepsy involving an eloquent cortex.
Conclusions Acknowledgements
Combined bipolar electrocoagulation with lesionectomy is a new and effective method in the treatment of epilepsy involving eloquent areas. The treatment effect of lesionectomy with BCFC for eloquent areas is similar to that of lesionectomy with MST. MST leads to mechanical injury, while BCFC causes only thermal injury. Therefore, the complications of BCFC are less severe. BCFC does not result in permanent neurological deficits because no resections are applied within the overlap-
This work was supported by the Construction Project of the National Clinical Key Specialties (SG2011-02-1-4) and Beijing Municipal Science and Technology Commission (Z121107001012063) in China.
Disclosure Statement None of the authors has any conflict of interest to disclose.
References
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
6 Engel J, Van Ness P, Rasmussen TB, Ojemann LM: Outcome with respect to epileptic seizures; in Engel J (ed): Surgical Treatment of the Epilepsies, ed 2. New York, Raven Press, 1993, pp 609–621. 7 Hufnagel A, Zentner J, Fernandez G, Wolf HK, Schramm J, Elger CE: Multiple subpial transection for control of epileptic seizures: effectiveness and safety. Epilepsia 1997; 38: 678–688. 8 Mulligan LP, Spencer DD, Spencer SS: Multiple subpial transection: the Yale experience. Epilepsia 2001;42:226–229. 9 Orbach D, Romanelli P, Devinsky O, Doyle W: Late seizure recurrence after multiple subpial transection. Epilepsia 2001; 42: 1130– 1133. 10 Spencer SS, Schramm J, Wyler A, O’Connor M, Orbach D, Krauss G, Sperling M, Devinsky O, Elger C, Lesser R, Mulligan L, Westerveld M: Multiple subpial transection for intractable partial epilepsy: an international metaanalysis. Epilepsia 2002;43:141–145.
11 Meng H, Luan GM: The experimental surgical technique research of cats’ sensorimotor area cortex epileptogenic focus induced by penicillin. Part 2: histological observation. Chin J Stereotact Funct Neurosurg 1999; 12: 7–9. 12 Devinsky O, Romanelli P, Orbach D, Pacia S, Doyle W: Surgical treatment of multifocal epilepsy involving eloquent cortex. Epilepsia 2003;44:718–723. 13 Blount JP, Langburt W, Otsubo H, Chitoku S, Ochi A, Weiss S, Snead OC, Rutka JT: Multiple subpial transections in the treatment of pediatric epilepsy. J Neurosurg 2004; 100: 118–124. 14 Chuang MF, Harnod T, Wang PJ, Chen YH, Hsin YL: Effect of multiple subpial transection on patients with uncontrolled atypical infantile spasms. Epilepsia 2006; 47: 659– 660.
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
9
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
1 Cui ZQ, Luan GM, Zhou J: Pure bipolar electro-coagulation on functional cortex in the treatment of epilepsy involving eloquent areas. Epilepsy Res 2012;99:139–146. 2 Luan GM, Sun ZR, Bai Q, Wang C: Surgical treatment of intractable epilepsy combined with bipolar electro-coagulation on functional cortex. Stereotact Funct Neurosurg 2001; 77:233–238. 3 Yang ZX, Luan GM: Treatment of symptomatic epilepsy with lesionectomies combined with bipolar coagulation of the surrounding cortex. Chin Med J 2003;116:1930–1932. 4 Morrell F, Whisler WW, Bleck TP: Multiple subpial transection: a new approach to the surgical treatment of focal epilepsy. J Neurosurg 1989;70:231–239. 5 Schramm J, Aliashkevich AF, Grunwald T: Multiple subpial transections: outcome and complications in 20 patients who did not undergo resection. J Neurosurg 2002;97:39–47.
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Outcome of Bipolar Electrocoagulation with Lesionectomy in the Treatment of Epilepsy Involving Eloquent Areas Feng Zhai a, b Jian Zhou a, b Tianfu Li a–c Zhiqiang Cui a Guoming Luan a–c
b
Department of Neurosurgery, Beijing Sanbo Brain Hospital, Capital Medical University Beijing, Beijing Key Laboratory of Epilepsy, and c Center of Epilepsy, Beijing Institute for Brain Disorders, Beijing, China
Key Words Epilepsy · Bipolar electrocoagulation on functional cortex · Lesionectomy · Multiple subpial transections
Abstract Background/Aims: We have demonstrated previously that bipolar electrocoagulation on functional cortex (BCFC) is a safe and effective approach for epilepsy involving eloquent areas. Here, we report the results of BCFC with lesionectomy for patients with epileptogenic foci partially overlapping eloquent areas. Methods: Forty patients who had been treated with lesionectomy with BCFC were retrospectively reviewed with regard to seizure outcome and neurological deficits. Ten similar patients who had received lesionectomy with multiple subpial transections (MST) were examined as a control group. Results: In the lesionectomy group with BCFC, Engel class I was achieved in 18 (45%) patients, class II in 8 (20%) patients, class III in 8 (20%) patients and class IV in 6 (15%) patients. Five (12.5%) patients developed mild hemiparesis and 1 (2.5%) patient mild sensory dysphasia. In the lesionectomy group with MST, Engel class I was achieved in 3 (30%) patients, class II in 2 (20%) patients, class III in 3 (30%)
© 2014 S. Karger AG, Basel 1011–6125/14/0931–0001$39.50/0 E-Mail [email protected] www.karger.com/sfn
patients and class IV in 2 (20%) patients. Two (20%) patients developed mild hemiparesis and 1 (10%) patient moderate hemiparesis. All these complications recovered within 1–12 months. Conclusions: Compared with MST, the outcome of BCFC with lesionectomy is similar. But since MST leads to mechanical injury, while BCFC causes thermal injury, the complications of BCFC seem less severe. © 2014 S. Karger AG, Basel
Introduction
Resection of epileptogenic foci is the main procedure of epilepsy surgery at present. Patients can get ideal seizure control or even be cured. However, if the epileptogenic foci are overlapped by functionally critical cortices, their resection might lead to unacceptable neurological deficits. In case of epileptogenic foci specifically located within eloquent areas, we have previously developed and applied a new approach. The procedure is called bipolar electrocoagulation on functional cortex (BCFC) [1–3]. The principle of BCFC is similar to multiple subpial transections (MST) [4, 5]. Guoming Luan Department of Neurosurgery, Beijing Sanbo Brain Hospital Capital Medical University Beijing No. 50 Xiangshan Yikesong Road, Haidian District, Beijing 100093 (China) E-Mail luangm3 @ 163.com
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
a
The combined therapy of resection of foci and BCFC has been shown to be effective in our previous study [2, 3]. In the present study, we describe the outcome of this method in 40 epilepsy patients and have compared the results with 10 cases of MST.
Methods
Results
Surgical Procedure The motor, sensory and language cortices and epileptogenic foci were identified with cortical stimulation or intraoperative wake-up test in order to address the epileptogenic regions located in the eloquent and noneloquent areas. After resection of nonfunctional epileptogenic cortices, electrocorticography (ECoG) (fig. 1a) was performed in functional epileptogenic regions before BCFC [1, 2]. BCFC was applied over the arachnoid membrane with an output power of 4 W. The brain surface was kept clean and moist with a saline gauze. There was a 45° angle between the forceps axis and the brain surface. The direction of electrocoagulation was perpendicular to the long axis of the brain gyrus. The tip diameter of the bipolar forceps was 2 mm. This procedure was performed at an interval of 5 mm and with 1 s duration. The brain surface was washed immediately with saline to lower the brain temperature which had been elevated by the heat of electrocoagulation. Following the BCFC procedure, ECoG was performed (fig. 1b). If significant interictal spikes persisted in the ECoG after BCFC, the BCFC procedure was repeated with 5 W. The output power never exceeded 5 W because a higher output power may damage the internal pyramidal layer and may result in unacceptable neurological deficits.
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Follow-Up The mean duration of postoperative follow-up after lesionectomy with BCFC was 25.5 (range 18–48) months. Engel class I outcome was achieved in 18 (45%) patients, class II in 8 (20%) patients, class III in 8 (20%) patients and class IV in 6 (15%) patients [6]. Follow-up MRI was performed in 35 patients 1–2 years after surgery and showed no abnormality in any patient (fig. 4a, b). EEG was performed in 35 patients, and among them, 5 patients demonstrated normal EEG. The EEG of the other patients still showed spike waves or spike slow waves. The mean duration of postoperative follow-up after lesionectomy with MST was 30.5 months. Engel class I outcome was achieved in 3 (30%) patients, class II in 2 (20%) patients, class III in 3 (30%) patients and class IV in 2 (20%) patients. Complications The primary sensory-motor cortex was involved in 37 patients, Wernicke’s area in 2 patients and Broca’s area in 1 patient. Twenty patients developed mild encephaledema identified by computed tomography at the acute stage (1–7 days) after electrocoagulation. Five patients (cases 16, 17, 21, 28 and 33), who had been treated with electrocoagulation in the primary sensory-motor cortex, developed transient mild hemiparesis of the opposite limbs and all patients fully recovered within 1 month. One patient (case 6), who had been treated with electrocoagulation in the sensory language cortex (Wernicke’s area), developed mild sensory dysphasia. The patient fully recovered within 3 months. No occurrences of hemorrhage, infection or other complications were observed. In the control group with lesionectomy with MST, 2 patients developed mild hemiparesis, which resolved within 6 months, and 1 patient developed moderate hemiparesis and recovered within 1 year. There were no occurrences of infection and other complications. Zhai/Zhou/Li/Cui/Luan
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Patients Forty patients with intractable epilepsy involving eloquent areas who underwent resection with BCFC at Beijing Sanbo Brain Hospital and Beijing Sanbo Fuxing Brain Hospital from May 2004 to May 2011 were included in this study and followed up for 18–48 (mean 25.5) months. The study group included 25 men and 15 women aged 10–35 years with a mean age of 15.5 years. On average, they had a 82.8-month recorded preoperative history of epilepsy. Seizure types included complex partial seizures, simple partial seizures, tonic seizures and generalized tonicclonic seizures. All 40 patients underwent magnetic resonance imaging (MRI) and video scalp electroencephalography (EEG) monitoring as a presurgical evaluation. Additionally, 31 patients received magnetoencephalography (MEG) and 8 patients received fluorodeoxyglucose positron emission tomography (FDGPET). The Wada test was performed in 15 patients and no functional shift of motor, sensory or language was identified. Moreover, intracranial EEG (invasive monitoring) was applied in 17 patients. The presurgical evaluations for all 40 patients are summarized in tables 1 and 2. As a control group, an additional 10 patients with intractable epilepsy involving eloquent areas were included in this study. The 5 men and 5 women in the control group were 12–30 (mean 17) years old. These patients underwent lesionectomy for noneloquent areas and lesionectomy with MST for eloquent areas. On average, all patients were followed up for 30.5 months.
2
Red and white stripes at regular intervals were clearly visible on the electrocoagulated cortex (fig. 2a). BCFC was applied over the arachnoid mater and the blood vessels located in the pial mater remained undamaged except for the capillaries (fig. 3a). After BCFC, the cortex was covered by the artificial dura, which can significantly reduce the occurrence of adhesions and epilepsy (fig. 2b).
Table 1. Findings in 40 patients who underwent BCFC and lesionectomy
Case No.
Sex
Age, years
DOE, months
MCST
Postoperative deficits
FU, months
Postoperative EEG
Engel outcome
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40
F F M M M F M M F F M M F M M M M M F M M M M M M M M F F F F M M F F M F M M F
10 12 14 20 22 10 15 13 35 18 28 15 12 22 18 12 12 16 23 16 12 12 15 18 17 25 31 14 27 28 20 10 17 13 13 20 25 20 15 14
48 55 41 120 170 46 140 64 180 72 60 55 41 50 70 72 72 90 30 12 72 70 38 60 48 60 240 36 180 190 180 240 360 26 36 84 180 48 60 24
SPS CPS SPS, GTC SPS, GTC SPS, GTC CPS CPS, GTC SPS, GTC GTC SPS SPS, CPS SPS, CPS SPS SPS, CPS, GTC SPS SPS, SGTC SPS, GTC SPS, CPS SPS, GTC SPS, GTC SPS, SGTC SPS, CPS SPS, SGTC SPS, TS SPS, SGTC SPS, GTC SPS, SGTC SPS, GTC SPS SPS, GTC SPS, CPS SPS, SGTC GTC CPS GTC SPS, GTC SPS, SGTC SPS, SGTC SPS, GTC SPS, CPS
none none none none none mild dysphasia none none none none none none none none none mild hemiparesis mild hemiparesis none none none mild hemiparesis none none none none none none mild hemiparesis none none none none mild hemiparesis none none none none none none none
18 24 30 25 32 40 24 32 48 18 24 24 18 24 18 18 25 26 22 36 28 36 38 24 18 25 26 24 26 18 30 18 18 36 18 22 25 18 20 24
R/frontoparietal normal EEG L/frontal R/hemisphere R/frontoparietal L/frontotemporal R/frontoparietal R/frontoparietal normal EEG R/frontoparietal R/frontotemporal L/temporal L/frontoparietal bilateral (left > right) diffuse L/hemisphere diffuse R/frontoparietal R/frontoparietal R/hemisphere normal EEG R/frontoparietal R/frontoparietal R/frontoparietal L/frontoparietal L/hemisphere L/frontoparietal normal EEG R/hemisphere diffuse L/frontoparietal normal EEG R/hemisphere diffuse L/anterior head R/frontal-central bilateral anterior head L/temporal R/hemisphere n.d. n.d. n.d. n.d. n.d.
I I I III I II I II I II I III II IV IV II II III I I III II III IV III I III IV I IV I I I I IV I III I I II
The therapy of functional epilepsy has always been a difficult problem for surgeons. BCFC is a surgical technique that can reduce cortex-related seizures by destructing the epileptic region with thermal energy. Combining BCFC and resection surgery is an effective surgical pro-
cedure to treat functional epilepsy. After resection of nonfunctional epileptogenic regions, the functional epileptogenic region was electrocoagulated, and no permanent complications were observed. Morrell et al. [4] suggested that the functional arrangement in the cortex is primarily oriented vertically and the intracortical fibers, which are thought to be responsible
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Discussion
3
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
DOE = Duration of epilepsy; MCST = major clinical seizure types; FU = follow-up; SPS = simple partial seizure; CPS = complex partial seizure; GTC = generalized tonic-clonic seizure; TS = tonic seizure; SGTC = secondary generalized tonic-clonic seizure; n.d. = not done.
Table 2. Neuroimaging, video EEG and MEG Video scalp EEG
Invasive monitoring
MEG
interictal EEG
ictal EEG
interictal EEG
ictal EEG
1
R/frontal hyperintense
R/hemisphere
bilateral (right > left)
R/frontoparietal
R/frontal
n.d.
2
R/frontal FCD
R/frontoparietal
bilateral diffuse
R/frontoparietal
R/frontal
R/frontal
3
L/frontal softened focus
L/frontal
L/anterior head
n.d.
L/frontal-central
4
R/frontal FCD
R/frontal
R/hemisphere diffuse
n.d.
R/frontoparietal
5
R/frontoparietal softened focus
R/frontoparietal
R/hemisphere
R/frontoparietal
6
L/temporal FCD
L/frontoparietal, posttemporal
L/hemisphere
n.d.
7
no abnormality detected
R/frontoparietal
R/hemisphere
R/frontoparietal
8
R/frontoparietal gray matter
R/hemisphere
R/frontal-central
n.d.
9
no abnormality detected
R/frontoparietal
R/hemisphere
R/frontoparietal
10
R/frontoparietal softened focus
R/frontoparietal
R/frontoparietal
n.d.
11
R/frontal FCD
R/anterior head
R/anterior head
R/frontotemporal
12
L/temporal FCD
bilateral anterior head
bilateral anterior head (left > right)
n.d.
L/frontotemporal
13
L/parietal FCD
L/frontotemporoparietal L/frontoparietal
n.d.
L/parietal
14
L/frontoparietal hyperintense
bilateral (left > right)
bilateral (left > right) diffuse
L/frontoparietal
L/frontoparietal
L/multiple lobes
15
L/frontal FCD
L/frontoparietal
L/hemisphere
L/frontoparietal
L/frontoparietal
n.d.
16
R/frontal FCD
R/anterior head
R/anterior head
n.d.
R/frontal
17
R/frontal FCD
R/hemisphere diffuse
R/anterior head
n.d.
R/frontal
18
no abnormality detected
R/hemisphere
R/hemisphere
R/frontoparietal
R/frontoparietal
n.d.
19
L/frontal FCD
L/anterior head
normal EEG
L/frontotemporal
L/frontal
n.d.
20
R/frontotemporal softened focus
R/hemisphere
R/hemisphere
n.d.
R/frontotemporal
21
R/frontal FCD
bilateral anterior head (right > left)
R/frontoparietal
n.d.
R/frontoparietal
22
R/frontal FCD
R/frontoparietal
R/frontoparietal
n.d.
R/frontoparietal
23
L/frontoparietal FCD
L/frontoparietal
bilateral diffuse
L/frontoparietal
24
L/frontal FCD
bilateral frontoparietal
L/frontoparietal
n.d.
25
L/frontoparietal FCD
L/frontoparietal
L/hemisphere
L/frontoparietal
26
L/frontal softened focus
L/frontoparietal
L/anterior head
n.d.
L/frontoparietal lobe
27
R/frontotemporoparietal softened focus
R/hemisphere
R/frontoparietal
n.d.
R/frontotemporal lobes
28
no abnormality detected
L/hemisphere
L/hemisphere
L/frontoparietal
4
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
R/frontoparietal
R/frontoparietal L/temporal
R/frontoparietal
R/frontoparietal junctional zone n.d.
R/frontal
n.d. R/frontoparietal
R/frontal
L/frontoparietal
R/frontal
L/multiple lobes L/frontoparietal
L/frontoparietal
L/frontoparietal
Zhai/Zhou/Li/Cui/Luan
n.d.
L/multiple lobes Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Case MRI findings No.
Table 2. (continued) Case MRI findings No.
Video scalp EEG
Invasive monitoring
interictal EEG
ictal EEG
interictal EEG
MEG ictal EEG
29
L/frontal FCD
L/frontal-central
L/frontal-central
n.d.
30
R/frontoparietal FCD
R/hemisphere
R/hemisphere
R/frontoparietal
31
L/frontal softened focus
L/anterior head
L/frontal
n.d.
L/frontal and central
32
multiple nodules (TSC)
R/frontal-central
R/frontal-central
n.d.
R/frontal
33
R/frontal FCD
bilateral anterior head
R/frontoparietal
n.d.
R/frontal
34
L/temporal softened focus
L/temporal
normal EEG
n.d.
L/temporal
35
R/frontoparietal FCD
R/hemisphere
R/hemisphere
R/frontotemporoparietal
36
R/frontal FCD
R/anterior head
R/anterior head
n.d.
37
no abnormality detected
bilateral anterior head (right > left)
R/anterior head
R/frontoparietal
R/frontoparietal
R/frontotemporal
38
L/frontal FCD
L/hemisphere
L/anterior head
L/frontoparietal
L/frontal
n.d.
39
R/frontotemporal softened R/anterior head focus
R/frontotemporal
n.d.
R/frontal
40
R/frontal softened focus
R/frontoparietal
n.d.
R/frontal
R/frontoparietal
L/frontal lobe R/frontoparietal
R/frontoparietal
n.d.
L/multiple lobes R/frontal
for seizure spread, are oriented horizontally; therefore, these horizontal fibers can be sectioned without causing cortical dysfunction. This technique was termed ‘multiple subpial transections’ (MST) [4, 5, 7–10]. By MST, the horizontal synchronizing neuronal networks are interrupted, whereas the vertical functional units are preserved. Based on the principle of MST, in 1999, we applied BCFC in animal models and demonstrated the efficacy of BCFC in treating epilepsy [11]. We also found that electrocoagulation with an output power of 4–5 W can damage the nerve fibers of the external molecular layer and the external granular layer. The horizontal fibers are mostly located at the superficial cortical level [4]. However, the damage of electrocoagulation only reaches to the third layer of the cortex with the internal pyramidal layer and nerve fibers (fig. 3b, c) remaining untouched. Therefore, the surgical procedure did not lead to unacceptable neurological deficits. We have previously demonstrated the efficacy of BCFC alone in the treatment of refractory epilepsy with an effective rate of 73.3% [1]. Luan et al. [2] also compared lesionectomy with BCFC with lesionectomy alone.
It was demonstrated that lesionectomy with BCFC is significantly more effective than lesionectomy alone [2, 3]. However, so far, lesionectomy with BCFC for the treatment of refractory seizures involving eloquent areas has not been well established. Here, we report 40 patients treated with BCFC and lesionectomy, whose epileptogenic regions were partially overlapped by eloquent areas. In this study, 20 patients developed mild encephaledema at the acute stage following the electrocoagulation procedure. But the encephaledema disappeared within 1–2 weeks. MRI showed no abnormalities after 1–2 years of follow-up. Five patients (cases 16, 17, 21, 28 and 33), who had been treated with electrocoagulation in the primary sensory-motor cortex, developed mild hemiparesis. One patient (case 6), who had been electrocoagulated in the sensory language cortex, developed mild sensory dysphasia. When the patients were discharged from the hospital, the neurological deficits had improved significantly. All the neurological deficits disappeared within 3 months. No subdural hemorrhages and infections were observed. In the control group with lesionectomy with MST, 2 patients developed mild hemiparesis, which resolved within 6 months, and 1 patient
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
5
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
TSC = Tuberous sclerosis complex; n.d. = not done.
a
b
developed moderate hemiparesis and recovered within 1 year. There were no occurrences of infection and other complications. Our results can be summed up as follows. In the lesionectomy group with BCFC, the symptoms of 34 (85%) patients improved (Engel class I–III). Eighteen (45%) patients with class I outcome remained seizure free for 18–48 months after surgery. In the lesionectomy group with MST, the symptoms of 8 (80%) patients improved (Engel class I–III) and 3 (30%) patients remained seizure free. 6
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Reports on the efficacy of pure MST or resection with MST have differed widely. Schramm et al. [5] reported 20 patients who underwent pure MST. Nine (45%) patients achieved a worthwhile improvement (Engel class I–III) in a mean follow-up period of 58 months. Mulligan et al. [8] reported 12 patients who underwent pure MST or resection and MST. Among them, 5 (42%) patients experienced a significant improvement in seizure frequency and in 2 patients, the severity of seizures markedly decreased. Orbach et al. [9] reported 54 patients who underwent MST with a mean follow-up period of 56 months. Zhai/Zhou/Li/Cui/Luan
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Fig. 1. a ECoG before BCFC reveals multiple spikes and slow waves in the central cortex. b ECoG after BCFC shows reduced spikes and slow waves with decreased amplitude.
a
b
a
b
c
d
arachnoid turned blue, mild shrivel was visible and no blood vessels were damaged. HE. ×40. b After electrocoagulation, the number of neurons in layers I–III decreased and the deep structure was normal. NeuN. ×40. c Remarkable edema was found in the axons
of the superficial neurons and the number of axons decreased, while the deep nerve fiber axons were intact. MAP. ×100. d PreBCFC pathology of the sensory area. Radial abnormal cortical layering and some pyknotic neurons were detected (FCD IA). HE. ×40.
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Fig. 3. a Electrocoagulation was applied over the arachnoid. The
7
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
Fig. 2. a Intraoperative view after BCFC. Red and white stripes at regular intervals are visible in the electrocoagulated central area. b The artificial dura covered the electrocoagulated cortex without adhesions.
a
Central sulcus
Area of resection
b
Area of electrocoagulation
Fig. 4. a The FCD was observed in the central area with axial FLAIR-weighted MRI. b Eighteen months after BCFC and resection, no abnormality was found in the electrocoagulated central area with axial FLAIR-weighted MRI.
Forty-three (79.6%) patients had a consistent and significant reduction in seizure frequency and 27 (50%) patients were entirely seizure free. However, 10 (18.6%) patients had an increase in seizure frequency several years after surgery following initial postoperative improvement [9]. Devinsky et al. [12] also reported 10 of 13 (77%) patients who improved after MST and resection. Among them, 1 patient who underwent right partial frontal lobectomy and frontal MST suffered from the lasting postoperative 8
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
Zhai/Zhou/Li/Cui/Luan
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
FCD
complication of facial weakness. In 1 of 4 patients who had MST over temporal language areas, mild dysphasia developed and resolved within 6 months [12]. Blount et al. [13] reported that in 26 patients who underwent cortical resection with MST, 12 (46%) patients were seizure free (Engel class I), while 11 (42%) patients achieved Engel class II and III and 3 (12%) patients Engel class IV. Another study reported 2 patients with atypical infantile spasms who underwent pure MST and achieved a favorable outcome [14]. In general, compared with lesionectomy with MST, the outcome and complications of lesionectomy with BCFC are similar. On the one hand, BCFC was applied over the arachnoid membrane; on the other hand, BCFC causes thermal injury, while MST leads to mechanical injury. So BCFC reduced the subarachnoidal hemorrhage and small intraparenchymal clots that are seen after MST and with less scar. Therefore, the complications of BCFC are less severe. Six (15%) cases with class IV outcome showed persistent epileptiform activity in either the ipsilateral or bilateral hemispheres. MEG spikes within multiple lobes were observed in 4 out of 6 patients with class IV outcome. The reason might be that the epileptogenic regions were larger than the regions of interest of resection and BCFC. We conjectured that a more accurate localization of epileptogenic regions may further improve surgical efficacy. Follow-up EEG was performed in 35 patients and, among them, 5 patients demonstrated normal EEG with class I outcome. The data suggest that postoperative normalization of EEG correlates with good surgical outcome for seizure control. Five patients had no abnormality and 2 patients (case 1 and 14) showed hyperintensity detected by MRI. However, the pathology of all excised epileptogenic regions proved that they were focal cortical dysplasias (FCDs). In case 18, before BCFC, a small piece of the sensory cortex was snapped and the pathology proved that this was FCD (fig. 3d). So, we inferred that the MRI abnormality was not correlated with the outcome of BCFC. However, there are limitations of applying BCFC for the treatment of epilepsy involving eloquent areas. The area of the sulci accounts for two thirds of all brain cortices. It appeared that inadequate damage to the two lateral cortical banks of a gyrus, which reach down into two adjoining sulci, could lead to remaining seizures. So, the remaining cortices in sulci without coagulation could still induce seizures. No correlations were observed between the outcome of treatment and factors such as sex and age of patients,
type and frequency of seizures, the brain hemisphere and the cortical location of the electrocoagulation procedure.
ping area between the epileptogenic regions and the eloquent area. Further studies will need to focus on the prospective outcome of BCFC in patients with intractable epilepsy involving an eloquent cortex.
Conclusions Acknowledgements
Combined bipolar electrocoagulation with lesionectomy is a new and effective method in the treatment of epilepsy involving eloquent areas. The treatment effect of lesionectomy with BCFC for eloquent areas is similar to that of lesionectomy with MST. MST leads to mechanical injury, while BCFC causes only thermal injury. Therefore, the complications of BCFC are less severe. BCFC does not result in permanent neurological deficits because no resections are applied within the overlap-
This work was supported by the Construction Project of the National Clinical Key Specialties (SG2011-02-1-4) and Beijing Municipal Science and Technology Commission (Z121107001012063) in China.
Disclosure Statement None of the authors has any conflict of interest to disclose.
References
Bipolar Electrocoagulation with Lesionectomy in Epilepsy
6 Engel J, Van Ness P, Rasmussen TB, Ojemann LM: Outcome with respect to epileptic seizures; in Engel J (ed): Surgical Treatment of the Epilepsies, ed 2. New York, Raven Press, 1993, pp 609–621. 7 Hufnagel A, Zentner J, Fernandez G, Wolf HK, Schramm J, Elger CE: Multiple subpial transection for control of epileptic seizures: effectiveness and safety. Epilepsia 1997; 38: 678–688. 8 Mulligan LP, Spencer DD, Spencer SS: Multiple subpial transection: the Yale experience. Epilepsia 2001;42:226–229. 9 Orbach D, Romanelli P, Devinsky O, Doyle W: Late seizure recurrence after multiple subpial transection. Epilepsia 2001; 42: 1130– 1133. 10 Spencer SS, Schramm J, Wyler A, O’Connor M, Orbach D, Krauss G, Sperling M, Devinsky O, Elger C, Lesser R, Mulligan L, Westerveld M: Multiple subpial transection for intractable partial epilepsy: an international metaanalysis. Epilepsia 2002;43:141–145.
11 Meng H, Luan GM: The experimental surgical technique research of cats’ sensorimotor area cortex epileptogenic focus induced by penicillin. Part 2: histological observation. Chin J Stereotact Funct Neurosurg 1999; 12: 7–9. 12 Devinsky O, Romanelli P, Orbach D, Pacia S, Doyle W: Surgical treatment of multifocal epilepsy involving eloquent cortex. Epilepsia 2003;44:718–723. 13 Blount JP, Langburt W, Otsubo H, Chitoku S, Ochi A, Weiss S, Snead OC, Rutka JT: Multiple subpial transections in the treatment of pediatric epilepsy. J Neurosurg 2004; 100: 118–124. 14 Chuang MF, Harnod T, Wang PJ, Chen YH, Hsin YL: Effect of multiple subpial transection on patients with uncontrolled atypical infantile spasms. Epilepsia 2006; 47: 659– 660.
Stereotact Funct Neurosurg 2015;93:1–9 DOI: 10.1159/000363146
9
Downloaded by: University of Hong Kong 198.143.53.1 - 2/3/2016 7:50:35 AM
1 Cui ZQ, Luan GM, Zhou J: Pure bipolar electro-coagulation on functional cortex in the treatment of epilepsy involving eloquent areas. Epilepsy Res 2012;99:139–146. 2 Luan GM, Sun ZR, Bai Q, Wang C: Surgical treatment of intractable epilepsy combined with bipolar electro-coagulation on functional cortex. Stereotact Funct Neurosurg 2001; 77:233–238. 3 Yang ZX, Luan GM: Treatment of symptomatic epilepsy with lesionectomies combined with bipolar coagulation of the surrounding cortex. Chin Med J 2003;116:1930–1932. 4 Morrell F, Whisler WW, Bleck TP: Multiple subpial transection: a new approach to the surgical treatment of focal epilepsy. J Neurosurg 1989;70:231–239. 5 Schramm J, Aliashkevich AF, Grunwald T: Multiple subpial transections: outcome and complications in 20 patients who did not undergo resection. J Neurosurg 2002;97:39–47.
