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Epilepsy surgery outcome in temporal lobe cavernoma and multiple sclerosis
Clinical Neurology and Neurosurgery 115 (2013) 2178–2181
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Case report
Epilepsy surgery outcome in temporal lobe cavernoma and multiple sclerosis Vladimir Bascarevic a , Nikola Vojvodic b,∗ , Aleksandar J. Ristic b , Ljubica Zovic c , Aleksandra Parojcic b , Nebojsa Stojsavljevic b , Predrag Stanarcevic b , Dragoslav Sokic b a
Clinic for Neurosurgery, Clinical Centre of Serbia, Belgrade, Serbia Neurology Clinic, Clinical Centre of Serbia, Belgrade, Serbia c St. Sava Hospital, Belgrade, Serbia b
a r t i c l e
i n f o
Article history: Received 4 April 2013 Received in revised form 25 April 2013 Accepted 18 May 2013 Available online 29 June 2013 Keywords: Epilepsy surgery Cavernoma Multiple sclerosis
1. Introduction
2. Case report
Seizures are the most common presenting symptom in patients with supratentorial cerebral cavernomas (CC) and can progress to medically refractory epilepsy in approximately 40% of cases [1]. While most studies of CC examine the risk of intracranial hemorrhage, eliminating the seizures can significantly reduce disability and improve quality of life. However, this important benefit often remains an underappreciated treatment goal in managing CC [2]. The literature documents several studies of patients with wellestablished refractory epilepsy secondary to CC, where surgery of the cerebral lesions significantly improved seizure control [1,3]. We report a patient with pharmacoresistant epilepsy due to cavernoma in the right temporal lobe and comorbid multiple sclerosis (MS) who was considered as a candidate for surgical treatment. The patient underwent anterior partial resection of the right temporal lobe. After the surgery, he remained seizure free but with severe amnestic deficit and devastating MS progression.
The patient is a 45-year-old right-handed man with 10 years of epilepsy history, and unremarkable perinatal and family history. He began experiencing seizures at 35 years of age, at the rate of one seizure per month, characterized by a sudden and strange cephalic feeling (“a storm is coming”) followed by loss of consciousness. His spouse, who witnessed the seizures, described a sudden onset of motionless staring, followed by fumbling and fidgeting movements of both arms, and lip smacking, chewing, and swallowing. These seizures infrequently continued to include loss of postural control and bilateral limb jerking. The patient regained reactivity 1 min after habitual seizure but remained confused for the next few minutes. The patient was initially treated with a titrating dose of carbamazepine (1200 mg/day) without seizure reduction. A dose of 750 mg/day of valproic acid was added and the seizures came under control. Standard scalp EEG showed interictal sharp waves in the right temporal region. Brain magnetic resonance imaging (MRI) disclosed a cavernoma in the mesial part of the right temporal lobe. The seizures recurred after 2 years (42 years of age) at a significant frequency of 1–2 per week. Further titration of carbamazepine (1600 mg/day), valproic acid (2000 mg/day), and the addition of levetiracetam (3000 mg/day) failed to improve seizure control.
∗ Corresponding author at: Epilepsy Center, Neurology Clinic, CCS, Dr Subotica 6 Street, 11 000 Belgrade, Serbia. Tel.: +381 66 8301 267/60 6680 267; fax: +381 11 2684 577. E-mail addresses: [email protected], [email protected] (N. Vojvodic). 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.05.030
V. Bascarevic et al. / Clinical Neurology and Neurosurgery 115 (2013) 2178–2181
Fig. 1. Parallel cerebrospinal fluid (CSF) and serum examination showed intrathecal presence of oligoclonal bands (black arrows).
One year later, numbness and weakness of the right leg and arm occurred. Consecutive brain MRI showed several T2 hyperintensity lesions in the white matter in addition to a cavernoma in the right temporal lobe. A diagnosis of multiple sclerosis (MS) was established after the analysis of cerebrospinal fluid (CSF) showed oligoclonal bands (Fig. 1). Administration of high doses of intravenous corticosteroids over 5 days promoted full recovery and the patient remained in clinical remission for the next 2 years. However, no influence on seizure frequency or seizure semiology was observed. The patient was referred to our telemetry unit and underwent long-term video-EEG monitoring with scalp electrodes. Three typical seizures were recorded over 5 consecutive days: after the patient felt the usual aura, he become motionless for a few seconds and then exhibited oroalimentary and exploratory automatisms. In all 3 seizures, ictal EEG showed seizure onset over the right anterior temporal region in the form of rhythmic 5 Hz theta activity. Presurgical MRI re-examination confirmed the left temporal cavernoma as well as the bilateral white matter demyelinating lesions (Fig. 2). The results of the patient’s neuropsychological assessment showed a verbal IQ score of 110 and a nonverbal IQ score of 111 with mild prefrontal dysfunction. The Edinburgh Handedness Inventory showed that he was strict right-handed. As the patient had no lefthanded family members, we concluded that epileptogenic zone was in non-dominant temporal lobe. Hence, we did not consider a functional MRI language testing.
2179
The patient’s case and the possibility for surgical treatment were discussed at a multidisciplinary meeting. There were some questions regarding the possible influence of MS on postoperative outcome and the influence of surgical treatment on the course of MS, respectively. The conclusion was that epilepsy due to the right temporal mediobasal cavernoma significantly decreased the patient’s quality of life, and the patient was referred for epilepsy surgery. The patient underwent epilepsy surgery in April 2011. Anterior partial resection of the right temporal lobe was performed, including amygdalo-hippocampectomy and lesionectomy. The histopathological investigation proved, in correlation with MRI finding, the presence of a cavernoma. In the immediate postoperative course, severe amnestic syndrome with global declarative memory deficits were noticed. The patient was unable to retain any new verbal information (names of new hospital staff or the information that he read each day in the newspapers). He also demonstrated impaired retrograde episodic memory but intact memory for information regarding his semantic knowledge and previously learned skills. His short-term verbal memory and repetitive speech were normal. A brain MRI performed 10 days after the surgery revealed postoperative tissue defect in the right temporal region and the existence of new demyelinating lesions in the left thalamus (Fig. 3). One year after the surgery, the patient was seizure free and classified as Engel I. In the meantime, several relapses of MS occurred with progressive neurological deterioration and severe functional deficit. As high doses of intravenous corticosteroids failed to improve functional disability, mitoxantrone was introduced. The control neuropsychological assessment showed that verbal memory function was significantly decreased in comparison to presurgical scores, with poor recall and poor recognition of previously presented information. The patient’s inability to form new episodic memories remained the most significant behavioral symptom.
Fig. 2. Presurgical coronal FLAIR image (1.5 T) showing a cerebral cavernoma in the mesial part of the right temporal lobe (white arrow) and bilateral demyelinating lesions in white matter (A). Ictal EEG revealed seizure onset zone (black arrow) over the right anterior temporal region (B).
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V. Bascarevic et al. / Clinical Neurology and Neurosurgery 115 (2013) 2178–2181
Fig. 3. Brain MRI axial sections (FLAIR images) at the level of thalamus and basal ganglia before (A) and after (B) the surgery showing new lesions in the left thalamus (white arrows).
3. Discussion Cerebral cavernomas (CC) are hamartomous vascular lesions of the brain which constitute nearly 10% of all vascular cerebral malformations [2]. Seizures are the most common clinical presentations in supratentorial CC. Overall, epilepsy affects 35–70% of patients with CC, with approximately 40% of individuals progressing to medically refractory epilepsy, especially in patients with temporal lobe localization [1,3]. In a paper by Iakovlev et al., the frequency of temporal lobe localization of CC was much higher among the patients with pharmacoresistant epilepsy (63% vs. 19%; p < 0.01) [3]. On the other hand, the literature documents that intractable epilepsy associated with CC is better controlled after surgery than with medication only [1,2]. In these patients, a detailed preoperative work-up is necessary and should be followed by wide resection, especially in the temporal lobe [3]. Our patient had medically refractory lesional epilepsy of the right mesial temporal lobe caused by CC, and reached seizure freedom after temporal resection that included lesionectomy and amygdalo-hippocampectomy. The case was exceptional due to MS as a comorbidity and its negative influence on postoperative outcome. After the surgery, the patient demonstrated global amnestic deficit, which was probably induced by the bilateral disconnection of the Papez circuit: amygdalo-hippocampectomy on the right and MS lesions in the thalamus on the left side. Although the patient was seizure free, this cognitive outcome very much diminished the patient’s quality of life and compromised the surgical treatment. On the other hand, dramatic progression of MS with severe disability occurred within the months following the surgery. This raised some questions regarding the possible influence of surgery on the course of MS. In one meta-analysis performed by Goodon et al., which investigated the relationship of MS to physical trauma, the authors included one study that showed deterioration in the MS clinical course after surgery in 14% of patients [4]. Similarly, Ehling et al. described the progression of MS within a few months after the selective amygdalo-hippocampectomy in a patient with temporal lobe epilepsy and MS. The authors indicated that a traumatic disruption of the blood–brain barrier represented a risk factor for
chronic progression of MS but concluded that a time-related coincidence in a patient who had both epilepsy and MS was also possible [5]. Unlike the previous paper, the case we present here represents a more clear temporal connection between surgery and MS progression. The occurrence of lesions in the contralateral thalamus led to severe amnestic syndrome which made the surgical outcome unfavorable in terms of the quality of life. 4. Conclusion Our case illustrates that comorbid MS in a patient who is a candidate for epilepsy surgery could have a negative influence on postoperative outcome. Accordingly, every similar case should have a very careful presurgical assessment and all possible risks should be taken into account. The question of whether brain surgery can affect the progression of MS remains open. However, this issue needs to be investigated in further studies. Conflicts of interest None of the authors has any conflict of interest to disclose. Acknowledgments The authors wish to thank Professors Branko Djurovic, Miroslav Samardzic and Jelena Drulovic for their useful suggestions and support. Also, many thanks to Anne Johnson for grammatical assistance and language editing. References [1] Englot DJ, Han SJ, Lawton MT, Chang EF. Predictors of seizure freedom in the surgical treatment of supratentorial cavernous malformations. Journal of Neurosurgery 2011;115:1169–74. [2] Fernandez S, Miro J, Falip M, Coello A, Plans G, Castaner S, et al. Surgical versus conservative treatment in patients with cerebral cavernomas and non refractory epilepsy. Seizure 2012;21:785–8.
V. Bascarevic et al. / Clinical Neurology and Neurosurgery 115 (2013) 2178–2181 [3] Iakovlev G, Devaux B, Ghossoub M, Beuvon F, Brami F, Roux FX. Cerebral cavernomas: epilepsy and seizures. Natural history and therapeutic strategy. Neurochirurgie 2005;51(1):3–14. [4] Goodin DS, Ebers GC, Johnson KP, Rodriguez M, Sibley WA, Wolinsky JS. The relationship of MS to physical trauma and psychological stress: report of the Therapeutics and Technology Assessment
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Subcommittee of the American Academy of Neurology. Neurology 1999;52: 1737–45. [5] Ehling R, Dobesberger J, Unterberger I, Benke T, Gotwald T, Ortler M, et al. Selective amygdalo-hippocampectomy as a potential trigger for disease progression in multiple sclerosis. Clinical Neurology and Neurosurgery 2011;113(2011):136–8.
Contents lists available at ScienceDirect
Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Case report
Epilepsy surgery outcome in temporal lobe cavernoma and multiple sclerosis Vladimir Bascarevic a , Nikola Vojvodic b,∗ , Aleksandar J. Ristic b , Ljubica Zovic c , Aleksandra Parojcic b , Nebojsa Stojsavljevic b , Predrag Stanarcevic b , Dragoslav Sokic b a
Clinic for Neurosurgery, Clinical Centre of Serbia, Belgrade, Serbia Neurology Clinic, Clinical Centre of Serbia, Belgrade, Serbia c St. Sava Hospital, Belgrade, Serbia b
a r t i c l e
i n f o
Article history: Received 4 April 2013 Received in revised form 25 April 2013 Accepted 18 May 2013 Available online 29 June 2013 Keywords: Epilepsy surgery Cavernoma Multiple sclerosis
1. Introduction
2. Case report
Seizures are the most common presenting symptom in patients with supratentorial cerebral cavernomas (CC) and can progress to medically refractory epilepsy in approximately 40% of cases [1]. While most studies of CC examine the risk of intracranial hemorrhage, eliminating the seizures can significantly reduce disability and improve quality of life. However, this important benefit often remains an underappreciated treatment goal in managing CC [2]. The literature documents several studies of patients with wellestablished refractory epilepsy secondary to CC, where surgery of the cerebral lesions significantly improved seizure control [1,3]. We report a patient with pharmacoresistant epilepsy due to cavernoma in the right temporal lobe and comorbid multiple sclerosis (MS) who was considered as a candidate for surgical treatment. The patient underwent anterior partial resection of the right temporal lobe. After the surgery, he remained seizure free but with severe amnestic deficit and devastating MS progression.
The patient is a 45-year-old right-handed man with 10 years of epilepsy history, and unremarkable perinatal and family history. He began experiencing seizures at 35 years of age, at the rate of one seizure per month, characterized by a sudden and strange cephalic feeling (“a storm is coming”) followed by loss of consciousness. His spouse, who witnessed the seizures, described a sudden onset of motionless staring, followed by fumbling and fidgeting movements of both arms, and lip smacking, chewing, and swallowing. These seizures infrequently continued to include loss of postural control and bilateral limb jerking. The patient regained reactivity 1 min after habitual seizure but remained confused for the next few minutes. The patient was initially treated with a titrating dose of carbamazepine (1200 mg/day) without seizure reduction. A dose of 750 mg/day of valproic acid was added and the seizures came under control. Standard scalp EEG showed interictal sharp waves in the right temporal region. Brain magnetic resonance imaging (MRI) disclosed a cavernoma in the mesial part of the right temporal lobe. The seizures recurred after 2 years (42 years of age) at a significant frequency of 1–2 per week. Further titration of carbamazepine (1600 mg/day), valproic acid (2000 mg/day), and the addition of levetiracetam (3000 mg/day) failed to improve seizure control.
∗ Corresponding author at: Epilepsy Center, Neurology Clinic, CCS, Dr Subotica 6 Street, 11 000 Belgrade, Serbia. Tel.: +381 66 8301 267/60 6680 267; fax: +381 11 2684 577. E-mail addresses: [email protected], [email protected] (N. Vojvodic). 0303-8467/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.clineuro.2013.05.030
V. Bascarevic et al. / Clinical Neurology and Neurosurgery 115 (2013) 2178–2181
Fig. 1. Parallel cerebrospinal fluid (CSF) and serum examination showed intrathecal presence of oligoclonal bands (black arrows).
One year later, numbness and weakness of the right leg and arm occurred. Consecutive brain MRI showed several T2 hyperintensity lesions in the white matter in addition to a cavernoma in the right temporal lobe. A diagnosis of multiple sclerosis (MS) was established after the analysis of cerebrospinal fluid (CSF) showed oligoclonal bands (Fig. 1). Administration of high doses of intravenous corticosteroids over 5 days promoted full recovery and the patient remained in clinical remission for the next 2 years. However, no influence on seizure frequency or seizure semiology was observed. The patient was referred to our telemetry unit and underwent long-term video-EEG monitoring with scalp electrodes. Three typical seizures were recorded over 5 consecutive days: after the patient felt the usual aura, he become motionless for a few seconds and then exhibited oroalimentary and exploratory automatisms. In all 3 seizures, ictal EEG showed seizure onset over the right anterior temporal region in the form of rhythmic 5 Hz theta activity. Presurgical MRI re-examination confirmed the left temporal cavernoma as well as the bilateral white matter demyelinating lesions (Fig. 2). The results of the patient’s neuropsychological assessment showed a verbal IQ score of 110 and a nonverbal IQ score of 111 with mild prefrontal dysfunction. The Edinburgh Handedness Inventory showed that he was strict right-handed. As the patient had no lefthanded family members, we concluded that epileptogenic zone was in non-dominant temporal lobe. Hence, we did not consider a functional MRI language testing.
2179
The patient’s case and the possibility for surgical treatment were discussed at a multidisciplinary meeting. There were some questions regarding the possible influence of MS on postoperative outcome and the influence of surgical treatment on the course of MS, respectively. The conclusion was that epilepsy due to the right temporal mediobasal cavernoma significantly decreased the patient’s quality of life, and the patient was referred for epilepsy surgery. The patient underwent epilepsy surgery in April 2011. Anterior partial resection of the right temporal lobe was performed, including amygdalo-hippocampectomy and lesionectomy. The histopathological investigation proved, in correlation with MRI finding, the presence of a cavernoma. In the immediate postoperative course, severe amnestic syndrome with global declarative memory deficits were noticed. The patient was unable to retain any new verbal information (names of new hospital staff or the information that he read each day in the newspapers). He also demonstrated impaired retrograde episodic memory but intact memory for information regarding his semantic knowledge and previously learned skills. His short-term verbal memory and repetitive speech were normal. A brain MRI performed 10 days after the surgery revealed postoperative tissue defect in the right temporal region and the existence of new demyelinating lesions in the left thalamus (Fig. 3). One year after the surgery, the patient was seizure free and classified as Engel I. In the meantime, several relapses of MS occurred with progressive neurological deterioration and severe functional deficit. As high doses of intravenous corticosteroids failed to improve functional disability, mitoxantrone was introduced. The control neuropsychological assessment showed that verbal memory function was significantly decreased in comparison to presurgical scores, with poor recall and poor recognition of previously presented information. The patient’s inability to form new episodic memories remained the most significant behavioral symptom.
Fig. 2. Presurgical coronal FLAIR image (1.5 T) showing a cerebral cavernoma in the mesial part of the right temporal lobe (white arrow) and bilateral demyelinating lesions in white matter (A). Ictal EEG revealed seizure onset zone (black arrow) over the right anterior temporal region (B).
2180
V. Bascarevic et al. / Clinical Neurology and Neurosurgery 115 (2013) 2178–2181
Fig. 3. Brain MRI axial sections (FLAIR images) at the level of thalamus and basal ganglia before (A) and after (B) the surgery showing new lesions in the left thalamus (white arrows).
3. Discussion Cerebral cavernomas (CC) are hamartomous vascular lesions of the brain which constitute nearly 10% of all vascular cerebral malformations [2]. Seizures are the most common clinical presentations in supratentorial CC. Overall, epilepsy affects 35–70% of patients with CC, with approximately 40% of individuals progressing to medically refractory epilepsy, especially in patients with temporal lobe localization [1,3]. In a paper by Iakovlev et al., the frequency of temporal lobe localization of CC was much higher among the patients with pharmacoresistant epilepsy (63% vs. 19%; p < 0.01) [3]. On the other hand, the literature documents that intractable epilepsy associated with CC is better controlled after surgery than with medication only [1,2]. In these patients, a detailed preoperative work-up is necessary and should be followed by wide resection, especially in the temporal lobe [3]. Our patient had medically refractory lesional epilepsy of the right mesial temporal lobe caused by CC, and reached seizure freedom after temporal resection that included lesionectomy and amygdalo-hippocampectomy. The case was exceptional due to MS as a comorbidity and its negative influence on postoperative outcome. After the surgery, the patient demonstrated global amnestic deficit, which was probably induced by the bilateral disconnection of the Papez circuit: amygdalo-hippocampectomy on the right and MS lesions in the thalamus on the left side. Although the patient was seizure free, this cognitive outcome very much diminished the patient’s quality of life and compromised the surgical treatment. On the other hand, dramatic progression of MS with severe disability occurred within the months following the surgery. This raised some questions regarding the possible influence of surgery on the course of MS. In one meta-analysis performed by Goodon et al., which investigated the relationship of MS to physical trauma, the authors included one study that showed deterioration in the MS clinical course after surgery in 14% of patients [4]. Similarly, Ehling et al. described the progression of MS within a few months after the selective amygdalo-hippocampectomy in a patient with temporal lobe epilepsy and MS. The authors indicated that a traumatic disruption of the blood–brain barrier represented a risk factor for
chronic progression of MS but concluded that a time-related coincidence in a patient who had both epilepsy and MS was also possible [5]. Unlike the previous paper, the case we present here represents a more clear temporal connection between surgery and MS progression. The occurrence of lesions in the contralateral thalamus led to severe amnestic syndrome which made the surgical outcome unfavorable in terms of the quality of life. 4. Conclusion Our case illustrates that comorbid MS in a patient who is a candidate for epilepsy surgery could have a negative influence on postoperative outcome. Accordingly, every similar case should have a very careful presurgical assessment and all possible risks should be taken into account. The question of whether brain surgery can affect the progression of MS remains open. However, this issue needs to be investigated in further studies. Conflicts of interest None of the authors has any conflict of interest to disclose. Acknowledgments The authors wish to thank Professors Branko Djurovic, Miroslav Samardzic and Jelena Drulovic for their useful suggestions and support. Also, many thanks to Anne Johnson for grammatical assistance and language editing. References [1] Englot DJ, Han SJ, Lawton MT, Chang EF. Predictors of seizure freedom in the surgical treatment of supratentorial cavernous malformations. Journal of Neurosurgery 2011;115:1169–74. [2] Fernandez S, Miro J, Falip M, Coello A, Plans G, Castaner S, et al. Surgical versus conservative treatment in patients with cerebral cavernomas and non refractory epilepsy. Seizure 2012;21:785–8.
V. Bascarevic et al. / Clinical Neurology and Neurosurgery 115 (2013) 2178–2181 [3] Iakovlev G, Devaux B, Ghossoub M, Beuvon F, Brami F, Roux FX. Cerebral cavernomas: epilepsy and seizures. Natural history and therapeutic strategy. Neurochirurgie 2005;51(1):3–14. [4] Goodin DS, Ebers GC, Johnson KP, Rodriguez M, Sibley WA, Wolinsky JS. The relationship of MS to physical trauma and psychological stress: report of the Therapeutics and Technology Assessment
2181
Subcommittee of the American Academy of Neurology. Neurology 1999;52: 1737–45. [5] Ehling R, Dobesberger J, Unterberger I, Benke T, Gotwald T, Ortler M, et al. Selective amygdalo-hippocampectomy as a potential trigger for disease progression in multiple sclerosis. Clinical Neurology and Neurosurgery 2011;113(2011):136–8.