|Year : 2008 | Volume
| Issue : 1 | Page : 121-125
Surgical management of epilepsy associated with temporal lobe tumors
Suresh Sankhla, GM Khan
Department of Neurosurgery, Saifee Hospital, Dr. B. Nanavati Hospital, Mumbai, Maharashtra, India
A-503, Chaitanya Towers, Appasaheb Marathe Road, Prabhadevi, Mumbai - 400 025, Maharashtra
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Object: Despite advancement in neuroimaging and improvement in the knowledge of tumor behavior, the optimal surgical treatment of patients with temporal-lobe tumors remains unclear. Controversies still exist regarding the type of tumor surgery, i.e., lesionectomy alone or in combination with resection of mesial temporal structures and epileptogenic cortex adjacent to the tumor and the extent of tumor removal. In this retrospective study, the authors have analyzed seizure outcome in a series of children with epileptogenic temporal lobe tumors who had been treated only by lesionectomy. Materials and Methods: Sixteen patients including 7 boys and 9 girls, with a mean age of 9.9 years (range: 5-17 years) underwent lesionectomy as the only surgical treatment for temporal lobe tumor related epilepsy. The interval between onset of seizures and surgery ranged from 3 months to 7.5 year (mean 5.9 year). Ten patients (62.5%) presented with complex partial seizures and the remaining 6 (37.5%) had simple partial seizures with secondary generalization, with seizure frequency varying from several per day to only a few per month. All tumors were located within the temporal lobes: 8 temporomesial, 5 temporolateral and 3 temporobasal. Cortical dysplasia adjacent to tumor, hippocampal sclerosis or tumor infiltration was not demonstrated in any patient. Results: Gross total resection of the tumor was achieved in 11 (69%) and subtotal resection in 5 (31%) patients. The histopathological diagnosis was ganglioglioma in 6 (37.5%) patients, dysembryoplastic neuroepithelial tumor in 5 (31.3%), low-grade astrocytoma in 2 (12.5%), juvenile pilocytic astrocytoma in 2 (12.5%) and pleomorphic xanthoastrocytoma in 1 (6.3%). At a mean follow-up of 5.2 years (range, 1.4-9.3 years), 11 (69%) patients were seizure-free (Engel class I) and 4 (25%) others had a significant improvement in the seizure frequency (Engel class II). Conclusions: The results of this study suggest that good long-term seizure control can be achieved with lesionectomy alone in majority of children suffering from medically resistant epilepsy associated with temporal lobe tumors.
Keywords: Dysembryoplastic neuroepithelial tumor, epilepsy, ganglioglioma, juvenile pilocytic astrocytoma, lesionectomy, low-grade astrocytoma, pleomorphic xanthoastrocytoma, temporal lobe tumor
|How to cite this article:|
Sankhla S, Khan G M. Surgical management of epilepsy associated with temporal lobe tumors. J Pediatr Neurosci 2008;3:121-5
| Introduction|| |
Low-grade temporal lobe tumors are now increasingly recognized as the cause of seizures in children and young adults. ,,,,,,, Although our understanding of the clinicopathological behavior of these tumors has improved in the past few years, a clear consensus regarding the surgical management of these tumors is lacking. Controversies still exist whether lesionectomy alone is sufficient to control epilepsy ,,, or if epileptogenic areas adjacent to the tumor and/or mesial temporal structures should also be resected to improve the seizure outcome. ,,,,, In this report, the seizure outcome has been retrospectively analyzed in 16 children who had received lesionectomy as the only surgical treatment of their temporal lobe tumors.
| Materials and Methods|| |
The medical records were reviewed to obtain clinical data of the children who underwent surgery for temporal lobe tumors at our institution between January 1998 and December 2004. The selection criteria included the following: (1) seizure as the main presenting feature, (2) temporal lobe mass lesion demonstrated on neuroimaging, (3) resection of the lesion, (4) histopathological confirmation of a neoplasm, (5) a minimum 16-month follow-up period. All patients underwent comprehensive pre- and postsurgical workups, including a thorough seizure history, neurological examinations, neuroimaging studies (magnetic resonance imaging with seizure protocol) and routine electroencephalogram (EEG) recordings. Preoperative and postoperative neuroimaging studies were reviewed by the author with two senior radiologists to verify the location of the lesion and its relationship to the adjacent cortex and structures of the limbic system, as well as to determine the extent of tumor removal. Follow-up examination results were obtained from patient charts. Postoperatively, all patients continued to receive anticonvulsant medications for a variable period before attempting gradual drug withdrawal. Medication was continued in those children who did not have satisfactory seizure control after surgery. Postoperative seizure outcome was categorized using the Engel classification.  Seizure frequency at the time of the last follow-up was compared with that prior to surgery.
| Results|| |
Patient characteristics and surgical outcomes are shown in [Table - 1]. There were 16 children, 7 male and 9 female, with a mean age of 9.9 years (range: 5-17 years). In almost all the cases, the onset of seizures was during infancy or childhood (range: 0.5-13 years) and the interval between the onset of seizures and surgery ranged from 3 months to 7.5 years (mean: 5.9 years). Ten patients (62.5%) suffered complex partial seizures, while the remaining 6 patients (37.5%) had presented with simple partial seizures and secondary generalization. Seizure frequency varied from several episodes per day to only a few per month. Neurologic examination was unremarkable in all patients. According to the neuroimaging studies, all tumors were located within the temporal lobes, 10 on the right side and 6 on the left. Eight tumors were classified as temporomesial, 5 as temporolateral and 3 as temporobasal. Cortical dysplasia adjacent to tumor, hippocampal sclerosis or tumor infiltration was not demonstrated in any patient. Tumor resection was gross total in 11 (69%) [Figure - 1] and subtotal in 5 (31%) patients [Figure - 2]. Because of the close proximity to the eloquent areas, smaller tumor pieces were left behind in 5 patients. The postoperative complications were observed in 4 patients (25%), including temporary hemiparesis in 2 cases, superior quadrant field defect in 3, transient psychosis in 1 and wound infection in 1. The histopathological diagnosis was ganglioglioma (GG) in 6 (37.5%) patients, dysembryoplastic neuroepithelial tumor (DNET) in 5 (31.3%), low-grade astrocytoma (LGA) in 2 (12.5%), juvenile pilocytic astrocytoma (JPA) in 2 (12.5%) and pleomorphic xanthoastrocytoma (PXA) in 1 (6.3%). The mean follow-up period was 5.2 years (range, 1.4-9.3 years). Postoperatively, good seizure outcome was observed in 94% of the cases. Eleven (69%) patients were seizure free (Engel class I) and 4 (25%) others had a significant improvement in seizure frequency (Engel class II). One patient with Engel class III outcome who had subtotal resection of the low-grade astrocytoma underwent reoperation for the residual tumor and continued on anticonvulsant treatment for 24 months until last follow-up. In 9 (56%) patients, antiepilepsy medication was gradually reduced and stopped after a minimum 2-year seizure-free period. During the last follow-up, 4 patients with recurrent seizures and 2 without seizures were receiving antiepilepsy treatment with a plan to stop all medications in the near future.
| Discussion|| |
Intrinsic low-grade temporal lobe tumors in children most commonly present with epilepsy that is often resistant to medical treatment. It has been estimated that approximately 38-76% of all cases with supratentorial tumors considered for epilepsy surgery have tumors in the temporal lobes. ,, The primary goal of treatment in these patients is to achieve complete control of seizures. Clinical data from several studies indicate that the surgical treatment is effective and provides good long-term seizure outcome. ,,, Tumor removal is not only associated with effective seizure control, it can also improve psychological and intellectual development of the patient, reduce the incidence of secondary epileptogenesis, ensure an accurate diagnosis and prevent the malignant transformation of otherwise benign tumors. ,,,,,
However, the optimal surgical treatment for children suffering from epilepsy associated with temporal-lobe tumors remains controversial. Some authors consider complete tumor resection alone as an adequate treatment, ,, whereas others recommend the additional removal of epileptogenic surrounding brain tissue to provide a good seizure outcome. ,,,,,,,, The literature is also unclear whether the extent of tumor resection has any direct impact on the long-term seizure outcomes. While some investigators ,, report significant seizure control following radical tumor removal, others  demonstrate similar results with incomplete tumor excision. From a surgical point of view, another controversial issue is the resection of mesial temporal structures in addition to the tumor removal. Whether the additional vital brain tissue resection improves the outcome significantly or not continues to be a matter of debate. It is thus obvious that a proper understanding of the pathophysiological mechanisms leading to tumoral epilepsy is essential, and without this, it may be difficult to determine the optimal surgical strategy.
The exact mechanism of epilepsy in the patients with temporal-lobe tumors is unclear. The proposed hypotheses include direct pressure and irritation in the cortical tissue, gliosis, disrupted vascularization in the surrounding cortex, morphological neuronal alterations in cellular levels, changes in the level of neurotransmitters, denervation hypersensitivity and immunological activities. ,, Although the peritumoral brain tissue is generally considered as the region where epileptic discharges are generated, , there is now clear evidence that certain tumors such as GGs and DNETs have specific epileptogenic activities because of their neuronal and glial components. The neurochemical profiles of these tumors seem to demonstrate some similarities to neocortical neurons in the expression of various enzymes and receptors. ,,,, These profiles support the possibility that these tumor may have intrinsic epileptogenic properties and that the neuronal component of the tumor itself may contribute to epileptic activity.  The origin of some epileptiform activity in gangliogliomas has been demonstrated by few other authors also. , Beaumont et al .,  Zaatreh et al .  and others , demonstrated relatively low incidence of Ammon's Horn sclerosis in the hippocampus of patients who had undergone en bloc resections of epileptogenic temporal tumors. These studies indicate that the temporal lobe tumors may be the primary source of the epileptic disorder in a large number of cases.
It therefore seems logical to consider lesionectomy as the primary treatment in patients who present with epilepsy secondary to temporal lobe tumors. There are several published reports in the literature supporting good long-term seizure outcomes following tumor resection alone. In the study by Clusman et al .,  all the children who underwent only temporal lesionectomies became seizure free during follow-up. In a series of 29 children who were treated surgically for a temporal lobe tumor-related seizure disorder, Cataltepe and coworkers  concluded that resection of tumor with or without amygdalohippocampectomy provides a high rate of seizure-free outcome. Giulioni and associates  analyzed 15 children suffering from epilepsy, who were associated with glioneuronal tumors treated by simple lesionectomy, and observed that 86.6% of patients achieved excellent (Engel Class I) postoperative seizure control. Our experience with lesionectomy is similar to others. Out of 16 children who underwent lesionectomy alone for temporal lobe tumor-associated epilepsy, 15 had an outcome that can be considered as good, Engel Class I in 11 and Class II in 4. Nine patients were totally free of medication and four of them continued gradual withdrawal of antiepileptic drugs at the last follow-up.
Another controversy in the management of tumoral epilepsy is involved with the extent of tumor resection. The complete excision of the tumor is still considered as the main factor affecting seizure outcomes. ,, Blume et al .  reported seizure-free outcomes in 88% of their cases after gross-total resection, whereas only 25% of patients were seizure-free after a subtotal resection. Several other authors have reported similar results ,,, Eleven (69%) patients in our study had total tumor removal; 8 had Engel Class I and 3 had Engel Class II seizure outcomes. Interestingly, subtotal resection is not always associated with poor seizure control. Some studies have indicated favorable outcomes even in patients who had undergone incomplete tumor removal. ,,, Kirkpatrick et al .  reported seizure-free outcomes in 81% of patients with incomplete tumor resection. Three (60%) out of 5 cases with subtotal tumor resection in our series had seizure-free outcomes. It has been postulated that the favorable outcome observed in cases with incomplete tumor resection may perhaps be due to the reduced volume of critical epileptogenic mass and interruption of the critical seizure propagation pathways.  Some authors however doubt the role of subtotal tumor removal and argue that even if the seizure control is achieved in some cases, it is often temporary and increasing epileptogenic mass secondary to tumor regrowth may cause recurrence of seizures in long term. For this reason we believe that gross-total resection, where possible, should be the goal of the surgery in these patients. Complete tumor excision is also of paramount importance for preventing malignant transformation of the residual mass. , Although three of our patients with incomplete tumor removal had a good seizure outcome, we could not draw a definite conclusion from this observation because the size of our patient population is small and statistically insignificant.
The role of resection of the cortex surrounding the epileptogenic tumor and/or the mesial temporal structures, in addition to tumor excision is debatable. Although it has been estimated that approximately 40% of glioneuronal tumors are associated with dysplasia, no clear association has yet been established between epilepsy and dysplasia of the cortex adjacent to the tumor. ,,,,, Jooma et al .  in 1995 reviewed their experience in 30 patients with seizures who received surgery in the form of resection of the temporal mass lesions. The seizure-free outcome was significantly lower in these patients as compared to those who underwent electrophysiologically guided resection of the lesion and epileptogenic focus. In contrast, Khajavi et al .  and Zaatreh  found that the seizure-free outcomes correlated with the extent of the tumor resection but not with the additional excision of the surrounding epileptogenic zone. They concluded that radical resection of the tumor either removes the primary epileptogenic drive completely or reduces the epileptogenic tissue beyond a critical mass required to generate clinical seizures.
There are convincing data regarding surgical strategy if the temporal lobe tumor is associated with hippocampal sclerosis, in which case a resection of the mesial temporal structures is recommended along with lesionectomy. Hippocampectomy as the treatment of tumor-associated epilepsy in the absence of hippocampal atrophy is debatable. The proponents of the amygdalohippocampectomy argue that the mesial temporal structures are capable of generating independent seizures and that their epileptogenicity is because of the abnormal synaptic reorganization of the hippocampi induced by seizures secondary to temporal tumors. ,, Mathern et al .  found that in patients with temporal lobe lesions, ictal EEG onset started in the mesial temporal contacts in 94% of the patients. However, the continuity of epileptogenic capability after the removal of the lesion is almost unknown. Furthermore, there is no clear evidence that the hippocampi in patients with tumor-related epilepsy are morphologically abnormal.  Therefore, it is now generally believed that the mesial structures may be resected only when the tumor is involving the mesial structures and should be preserved in all other cases. ,, Giulioni and coworkers  reported surgical results in 15 children with tumoral epilepsy and concluded that lesionectomy alone may be sufficient to provide good long-term seizure control and additional resection of the surrounding brain tissue or mesial temporal structures may not be necessary in majority of cases. Our results further support the findings of these authors. In none of the patients in our series, there was any evidence of hippocampal abnormality on MRI or cortical dysplasia on histopathological examination.
Although the duration of seizure has been reported to be adversely related to the seizure outcome by some authors, , we have not observed any definite association between the seizure control and duration, type or frequency of seizure and age of the patient. Because of the small number of patients in this study, it was also not possible to establish any meaningful relationship between the type of tumor and seizure outcome. Surgical complications were essentially minor, transient and treatable. No recurrence or regrowth of the residual tumor was documented in our study.
| Conclusions|| |
The epileptogenic temporal lobe tumors are usually slow-growing and histopathologically benign or low-grade lesions. Gross-total resection of the tumor is associated with a good seizure-free outcome and should, therefore, be the goal of surgery. Although the results of incomplete tumor excision are not completely unfavorable in this study, a larger patient population may be required to draw more meaningful conclusions. Our findings further indicate that lesionectomy alone can result in good seizure outcome in majority of patients and additional surgical procedures such as amygdalo-hippocampectomy and the resection of the adjacent epileptogenic cortex should be reserved for the selected patients who have dual pathology such as the mesial temporal sclerosis or cortical dysplasis in association with temporal lobe tumor.
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[Figure - 1], [Figure - 2]
[Table - 1]