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Tourette’s syndrome following temporal lobectomy for seizure control
Epilepsy & Behavior Epilepsy & Behavior 4 (2003) 564–566 www.elsevier.com/locate/yebeh
Case Report
TouretteÕs syndrome following temporal lobectomy for seizure control Zeina Chemalia,* and Edward Bromfieldb a
Brigham Behavioral Neurology Group, Memory Disorders Unit, Brigham and WomenÕs Hospital, Harvard Medical School, 221 Longwood Avenue, Boston, MA 02115, USA b Neurology Department, Brigham and WomenÕs Hospital, 75 Francis Street, Boston, MA 02115, USA Received 17 April 2003; revised 9 June 2003; accepted 9 June 2003
Abstract Gilles de la TouretteÕs syndrome (TS) is a neurobehavioral disorder characterized by multiple motor and vocal tics, occurring longer than a year and causing marked distress along with social and occupational impairments in level of functioning. It can be accompanied by obsessive–compulsive behavior and attention deficit disorder. This report discusses the case of a young woman with a simple motor tic disorder and intractable seizures who, after right temporal lobectomy for medically intractable epilepsy, developed TS with complex motor and vocal tics, severe obsessive–compulsive disorder, and paranoia. This neurobehavioral complication has not to our knowledge been previously reported after epilepsy surgery. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Seizure; Temporal lobectomy; Gilles de la TouretteÕs syndrome; Tics; Obsessive–compulsive; Depression
1. Case The patient is a 48-year-old right-handed woman with a history of a simple motor tic disorder and gestational diabetes who underwent a right temporal lobectomy for intractable seizures after a poor response to multiple medication trials. She had had simple febrile seizures when she was 3 years old, and then was seizure free until age 16, when she had a generalized tonic– clonic seizure immediately after head trauma. She subsequently developed on average two to four complex partial seizures and two to eight secondarily generalized seizures per month. The patient is Catholic and quite religious and many of her seizures occurred in church. Auras included nausea and formed visual and often olfactory hallucinations (ammonia), and were usually followed by unresponsiveness with staring and lip smacking. The patientÕs family history was significant for a twin sister with severe attention deficit disorder, a daughter * Corresponding author. Fax: +617-738-9122. E-mail address: [email protected] (Z. Chemali).
1525-5050/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S1525-5050(03)00152-5
with generalized tonic–clonic seizures, and a mother with obsessive–compulsive disorder. Unsuccessful medication trials included phenobarbital, carbamazepine, phenytoin, primidone, clonazepam, felbamate, lamotrigine, and valproic acid. In 1991 she underwent her first seizure surgery evaluation, which revealed generalized as well as right-sided ictal and interictal discharges using surface-sphenoidal electrodes. MRI was normal. Neuropsychological testing did not show strong lateralization of cognitive function. She underwent a phase II evaluation with broad subdural electrode coverage of the right hemisphere, but a definite focus was not found. Following this procedure she developed variable tics of the left lower extremity, which subsided over several months. Four years later, MRI revealed a subtle heterotopia lining the temporal horn of the right lateral ventricle and extending to the atrium; this could be seen retrospectively on the earlier study. On depth electrodes placed longitudinally in the right temporal and occipital lobes, ictal and interictal discharges were recorded. She underwent a modified right temporal lobectomy. Pathology revealed gliosis; neuronal
Case Report / Epilepsy & Behavior 4 (2003) 564–566
heterotopia was not confirmed, probably because of fragmentation of the specimen. She had a dramatic reduction in seizures, with only two secondarily generalized events; these occurred 3 years later after an attempt to withdraw primidone. Valproate was successfully withdrawn. She remains on primidone and lamotrigine. Simple partial seizures consisting mainly of nausea and anxiety have occurred in clusters every several months and responded to oral and sublingual benzodiazepines. There have been rare nighttime episodes of lip smacking and questionable responsiveness, but no daytime complex partial seizures. More notably, following surgery she became variably depressed and anxious. She was easily confused and impatient and had trouble with organizational skills. She also complained of memory loss, though neuropsychological testing showed no significant change from her preoperative status. She was started on sertraline, which helped her mood and anxiety. She had anger outbursts and an uncontrollable impulse to ‘‘utter bad words and swear.’’ This had never happened to her before. She obsessed about what she was going to say. She described time-consuming rituals, checking repetitively for safety in her house. Although she had simple tics prior to the surgery, such as eye blinking and intermittent throat clearing, following surgery she developed complex motor tics involving the face and neck. She felt fearful and paranoid and was very guarded in public places. She decreased the hours of her part-time job, and then stopped working completely. On neuropsychiatric evaluation, she was very fidgety and restless. Motor tics were noted. She made grunting noises despite obvious efforts to control her vocalizations. She had trouble comprehending the conversation at times. She had poor memory and spatial skills. She was paranoid and anxious, but had relatively good insight into her problems.
2. Discussion Temporal lobectomy is an effective treatment for medically refractory epilepsy, although several behavioral changes have been reported, particularly depression [1–3]. To the best of our knowledge, this is the first report to describe TouretleÕs syndrome (TS) following temporal lobectomy. Rare reports describe the association of TS and epilepsy as brain disorders leading to a general disturbance in behavior [4]. Lin et al. reported three cases of TS with epileptiform discharges [5]. They and others noted that the incidence of epileptiform discharges in TS is higher than in the normal population. Neurological soft focal signs were noted on some patient examinations [6–8]. One report by Anson and Kuhlman mentioned a postictal Kluver–Bucy syndrome after temporal lobectomy [9]. Gillingham reported that
565
temporal lobectomy reduced seizures and restored personality [10]. Interestingly, in the sample studied by Lin et al., when the electroencephalogram reverted to normal, the involuntary movement became more prominent. All cases improved significantly with haloperidol. To understand the complex phenomena of neural circuitry in TS, neuroscientists refer to links between the basal ganglia and the cortex. The striatum receives projection neurons that segregate into two neurochemically different compartments: the striosomes and the matrix. The striosomes receive mainly convergent limbic inputs while the matrix receives convergent input from motor and sensory cortices [11]. In normal circumstances, activity in the matrix is greater than in the striosomes, preventing overactivation. However, if this balance is reversed, tics are likely to arise [12]. In addition, genetic studies have demonstrated that the TS gene causes imbalance of the mesolimbic pathways, resulting in disinhibition of the limbic system and its frontocortical connections [13]. One may speculate that following a temporal lobectomy, the limbic input to the striosomes is altered, changing the balance and causing tics and stereotypies, potentially leading to a de novo TS presentation or aggravating an existing one. Complex motor and phonic tics are believed to result from the disinhibition of the loop connecting the basal ganglia, the limbic cortex, and the frontocortical circuitry, with a major role given to dopamine modulation in these areas [14]. In our patient, the electroencephalogram did not normalize and her seizure disorder improved markedly but did not resolve. Nevertheless, the possibility of ‘‘forced normalization’’ must be considered. Her motor tics worsened and she developed new vocal tics and coprolalia. She suffered from a new-onset depression, obsessive–compulsive disorder, and paranoia. TS was diagnosed postsurgically from her constellation of symptoms. It is possible that her motor tic disorder preceding the surgery and her family history of obsessive–compulsive disorder and attention deficit disorder had put her at a higher risk for TS. Less likely, her symptoms may have been postictal or due to ictal dysfunction of a remaining focus. She declined taking a neuroleptic out of fear that her seizures would worsen. She continued to exhibit waxing and waning symptoms over the ensuing months. She had some success trying a behavioral approach to control her tics and continued with sertraline.
3. Conclusion This case illustrates a complex case of epilepsy, its surgical treatment, and the behavioral complications that followed, including TS. Patients may be too embarrassed to talk about their symptoms and may be so
566
Case Report / Epilepsy & Behavior 4 (2003) 564–566
focused on seizure control that these features are never discussed, thus delaying the diagnosis and treatment. Patients and physicians alike should be more aware of the wide variety of behavioral changes that occur after temporal lobectomy. More research is needed to explain the neuropsychiatric correlates of such behaviors. References [1] Fenwick P. Long term psychiatric outcome after epilepsy surgery. In: Luders HO, editor. Epilepsy surgery. New York: Raven Press; 1992. p. 647–52. [2] Fricchione GL, Bromfield E, Dworestsky B et al. Psychiatric disturbances after epilepsy surgery. Epilepsia 1998;39(suppl. 6):242. [3] Quigg M, Broshek DK, Heidal-Schlitz S, Maedgen JW, Bertram EH. Depression in intractable partial epilepsy varies by laterality of focus and surgery. Epilepsia 2003;44:419–24. [4] Rickards H. Tics and fits: the current status of Gilles de la Tourette syndrome and its relationship with epilepsy. Seizure 1995;4:259–66. [5] Lin CK, Hsu WY, Wang PJ, Shen YJ. Gilles de la Tourette syndrome associated with epileptiform discharges: report of three
[6]
[7]
[8]
[9]
[10] [11] [12] [13]
[14]
cases. Zhonghua Min Guo Xiao Er Ke Yi Hui Za Zhi 1989;30(1):61–5. Verma NP, Syrigou-Papavasiliou A, LeWitt PA. Electroencephalographic findings in unmedicated, neurologically and intellectually intact Tourette syndrome patients. Electroencephalogr Clin Neurophysiol 1986;64:12–20. Marra TR, Reynolds Jr NC, Dahl DS. Tourette syndrome, an acquired encephalopathy? A report of two cases with epileptiform dysrhythmia. Clin Electroencephalogr 1980;11:118–23. Semerci ZB. Neurological soft signs and EEG findings in children and adolescents with Gilles de la Tourette syndrome. Turk J Pediatr 2000;42:53–5. Anson JA, Kuhlman DT. Post-ictal Kluver–Bucy syndrome after temporal lobectomy. J Neurol Neurosurg Psychiatry 1993;56:311– 3. Gillingham FJ. Surgical treatment of epilepsy: restoration of personality? Acta Neurochir Suppl (Wien) 1988;44:102–5. Leckman J. TouretteÕs syndrome. Lancet 2002;360:1577–86. Canales JJ, Graybiel AM. A measure of striatal function predicts motor stereotypy. Nat Neurosci 2000;3:377–83. Comings DE. Summary: a common genetic disorder causing disinhibition of the limbic system. Am J Hum Genet 1987;41:839– 66. Mink JW. Basal ganglia dysfunction in TouretteÕs syndrome: a new hypothesis. Pediatr Neurol 2001;25:190–8.
Case Report
TouretteÕs syndrome following temporal lobectomy for seizure control Zeina Chemalia,* and Edward Bromfieldb a
Brigham Behavioral Neurology Group, Memory Disorders Unit, Brigham and WomenÕs Hospital, Harvard Medical School, 221 Longwood Avenue, Boston, MA 02115, USA b Neurology Department, Brigham and WomenÕs Hospital, 75 Francis Street, Boston, MA 02115, USA Received 17 April 2003; revised 9 June 2003; accepted 9 June 2003
Abstract Gilles de la TouretteÕs syndrome (TS) is a neurobehavioral disorder characterized by multiple motor and vocal tics, occurring longer than a year and causing marked distress along with social and occupational impairments in level of functioning. It can be accompanied by obsessive–compulsive behavior and attention deficit disorder. This report discusses the case of a young woman with a simple motor tic disorder and intractable seizures who, after right temporal lobectomy for medically intractable epilepsy, developed TS with complex motor and vocal tics, severe obsessive–compulsive disorder, and paranoia. This neurobehavioral complication has not to our knowledge been previously reported after epilepsy surgery. Ó 2003 Elsevier Inc. All rights reserved. Keywords: Seizure; Temporal lobectomy; Gilles de la TouretteÕs syndrome; Tics; Obsessive–compulsive; Depression
1. Case The patient is a 48-year-old right-handed woman with a history of a simple motor tic disorder and gestational diabetes who underwent a right temporal lobectomy for intractable seizures after a poor response to multiple medication trials. She had had simple febrile seizures when she was 3 years old, and then was seizure free until age 16, when she had a generalized tonic– clonic seizure immediately after head trauma. She subsequently developed on average two to four complex partial seizures and two to eight secondarily generalized seizures per month. The patient is Catholic and quite religious and many of her seizures occurred in church. Auras included nausea and formed visual and often olfactory hallucinations (ammonia), and were usually followed by unresponsiveness with staring and lip smacking. The patientÕs family history was significant for a twin sister with severe attention deficit disorder, a daughter * Corresponding author. Fax: +617-738-9122. E-mail address: [email protected] (Z. Chemali).
1525-5050/$ - see front matter Ó 2003 Elsevier Inc. All rights reserved. doi:10.1016/S1525-5050(03)00152-5
with generalized tonic–clonic seizures, and a mother with obsessive–compulsive disorder. Unsuccessful medication trials included phenobarbital, carbamazepine, phenytoin, primidone, clonazepam, felbamate, lamotrigine, and valproic acid. In 1991 she underwent her first seizure surgery evaluation, which revealed generalized as well as right-sided ictal and interictal discharges using surface-sphenoidal electrodes. MRI was normal. Neuropsychological testing did not show strong lateralization of cognitive function. She underwent a phase II evaluation with broad subdural electrode coverage of the right hemisphere, but a definite focus was not found. Following this procedure she developed variable tics of the left lower extremity, which subsided over several months. Four years later, MRI revealed a subtle heterotopia lining the temporal horn of the right lateral ventricle and extending to the atrium; this could be seen retrospectively on the earlier study. On depth electrodes placed longitudinally in the right temporal and occipital lobes, ictal and interictal discharges were recorded. She underwent a modified right temporal lobectomy. Pathology revealed gliosis; neuronal
Case Report / Epilepsy & Behavior 4 (2003) 564–566
heterotopia was not confirmed, probably because of fragmentation of the specimen. She had a dramatic reduction in seizures, with only two secondarily generalized events; these occurred 3 years later after an attempt to withdraw primidone. Valproate was successfully withdrawn. She remains on primidone and lamotrigine. Simple partial seizures consisting mainly of nausea and anxiety have occurred in clusters every several months and responded to oral and sublingual benzodiazepines. There have been rare nighttime episodes of lip smacking and questionable responsiveness, but no daytime complex partial seizures. More notably, following surgery she became variably depressed and anxious. She was easily confused and impatient and had trouble with organizational skills. She also complained of memory loss, though neuropsychological testing showed no significant change from her preoperative status. She was started on sertraline, which helped her mood and anxiety. She had anger outbursts and an uncontrollable impulse to ‘‘utter bad words and swear.’’ This had never happened to her before. She obsessed about what she was going to say. She described time-consuming rituals, checking repetitively for safety in her house. Although she had simple tics prior to the surgery, such as eye blinking and intermittent throat clearing, following surgery she developed complex motor tics involving the face and neck. She felt fearful and paranoid and was very guarded in public places. She decreased the hours of her part-time job, and then stopped working completely. On neuropsychiatric evaluation, she was very fidgety and restless. Motor tics were noted. She made grunting noises despite obvious efforts to control her vocalizations. She had trouble comprehending the conversation at times. She had poor memory and spatial skills. She was paranoid and anxious, but had relatively good insight into her problems.
2. Discussion Temporal lobectomy is an effective treatment for medically refractory epilepsy, although several behavioral changes have been reported, particularly depression [1–3]. To the best of our knowledge, this is the first report to describe TouretleÕs syndrome (TS) following temporal lobectomy. Rare reports describe the association of TS and epilepsy as brain disorders leading to a general disturbance in behavior [4]. Lin et al. reported three cases of TS with epileptiform discharges [5]. They and others noted that the incidence of epileptiform discharges in TS is higher than in the normal population. Neurological soft focal signs were noted on some patient examinations [6–8]. One report by Anson and Kuhlman mentioned a postictal Kluver–Bucy syndrome after temporal lobectomy [9]. Gillingham reported that
565
temporal lobectomy reduced seizures and restored personality [10]. Interestingly, in the sample studied by Lin et al., when the electroencephalogram reverted to normal, the involuntary movement became more prominent. All cases improved significantly with haloperidol. To understand the complex phenomena of neural circuitry in TS, neuroscientists refer to links between the basal ganglia and the cortex. The striatum receives projection neurons that segregate into two neurochemically different compartments: the striosomes and the matrix. The striosomes receive mainly convergent limbic inputs while the matrix receives convergent input from motor and sensory cortices [11]. In normal circumstances, activity in the matrix is greater than in the striosomes, preventing overactivation. However, if this balance is reversed, tics are likely to arise [12]. In addition, genetic studies have demonstrated that the TS gene causes imbalance of the mesolimbic pathways, resulting in disinhibition of the limbic system and its frontocortical connections [13]. One may speculate that following a temporal lobectomy, the limbic input to the striosomes is altered, changing the balance and causing tics and stereotypies, potentially leading to a de novo TS presentation or aggravating an existing one. Complex motor and phonic tics are believed to result from the disinhibition of the loop connecting the basal ganglia, the limbic cortex, and the frontocortical circuitry, with a major role given to dopamine modulation in these areas [14]. In our patient, the electroencephalogram did not normalize and her seizure disorder improved markedly but did not resolve. Nevertheless, the possibility of ‘‘forced normalization’’ must be considered. Her motor tics worsened and she developed new vocal tics and coprolalia. She suffered from a new-onset depression, obsessive–compulsive disorder, and paranoia. TS was diagnosed postsurgically from her constellation of symptoms. It is possible that her motor tic disorder preceding the surgery and her family history of obsessive–compulsive disorder and attention deficit disorder had put her at a higher risk for TS. Less likely, her symptoms may have been postictal or due to ictal dysfunction of a remaining focus. She declined taking a neuroleptic out of fear that her seizures would worsen. She continued to exhibit waxing and waning symptoms over the ensuing months. She had some success trying a behavioral approach to control her tics and continued with sertraline.
3. Conclusion This case illustrates a complex case of epilepsy, its surgical treatment, and the behavioral complications that followed, including TS. Patients may be too embarrassed to talk about their symptoms and may be so
566
Case Report / Epilepsy & Behavior 4 (2003) 564–566
focused on seizure control that these features are never discussed, thus delaying the diagnosis and treatment. Patients and physicians alike should be more aware of the wide variety of behavioral changes that occur after temporal lobectomy. More research is needed to explain the neuropsychiatric correlates of such behaviors. References [1] Fenwick P. Long term psychiatric outcome after epilepsy surgery. In: Luders HO, editor. Epilepsy surgery. New York: Raven Press; 1992. p. 647–52. [2] Fricchione GL, Bromfield E, Dworestsky B et al. Psychiatric disturbances after epilepsy surgery. Epilepsia 1998;39(suppl. 6):242. [3] Quigg M, Broshek DK, Heidal-Schlitz S, Maedgen JW, Bertram EH. Depression in intractable partial epilepsy varies by laterality of focus and surgery. Epilepsia 2003;44:419–24. [4] Rickards H. Tics and fits: the current status of Gilles de la Tourette syndrome and its relationship with epilepsy. Seizure 1995;4:259–66. [5] Lin CK, Hsu WY, Wang PJ, Shen YJ. Gilles de la Tourette syndrome associated with epileptiform discharges: report of three
[6]
[7]
[8]
[9]
[10] [11] [12] [13]
[14]
cases. Zhonghua Min Guo Xiao Er Ke Yi Hui Za Zhi 1989;30(1):61–5. Verma NP, Syrigou-Papavasiliou A, LeWitt PA. Electroencephalographic findings in unmedicated, neurologically and intellectually intact Tourette syndrome patients. Electroencephalogr Clin Neurophysiol 1986;64:12–20. Marra TR, Reynolds Jr NC, Dahl DS. Tourette syndrome, an acquired encephalopathy? A report of two cases with epileptiform dysrhythmia. Clin Electroencephalogr 1980;11:118–23. Semerci ZB. Neurological soft signs and EEG findings in children and adolescents with Gilles de la Tourette syndrome. Turk J Pediatr 2000;42:53–5. Anson JA, Kuhlman DT. Post-ictal Kluver–Bucy syndrome after temporal lobectomy. J Neurol Neurosurg Psychiatry 1993;56:311– 3. Gillingham FJ. Surgical treatment of epilepsy: restoration of personality? Acta Neurochir Suppl (Wien) 1988;44:102–5. Leckman J. TouretteÕs syndrome. Lancet 2002;360:1577–86. Canales JJ, Graybiel AM. A measure of striatal function predicts motor stereotypy. Nat Neurosci 2000;3:377–83. Comings DE. Summary: a common genetic disorder causing disinhibition of the limbic system. Am J Hum Genet 1987;41:839– 66. Mink JW. Basal ganglia dysfunction in TouretteÕs syndrome: a new hypothesis. Pediatr Neurol 2001;25:190–8.