Novel Insights from Clinical Practice Pediatr Neurosurg DOI: 10.1159/000503114 Received: June 5, 2019 Accepted after revision: September 3, 2019 Published online: October 7, 2019 Paediatric Moyamoya Disease and Tourette’s Syndrome: An Unusual Association Responding Favourably to Direct and Indirect Cerebral Revascularisation Surgery Ratnadip Bose Anirban Deep Banerjee Department of Neurosurgery, Institute of Neurosciences, Medanta – The Medicity, Gurgaon, India Established Facts • Moyamoya disease is an uncommon chronic intra-cerebral arteriopathy. • Tourette’s syndrome is a rare neurological disorder in which the patient displays repetitive, stereotyped involuntary movements and vocalisations called tics. • Although several areas of the brain are involved, morphological changes in the caudate nucleus, within the cortico-striatal-thalamo-cortical circuits, play a central role in the clinical manifestations of Tourette’s syndrome. Novel Insights • Ours is probably the first case reporting an association of paediatric Moyamoya disease with Tourette’s syndrome. • Such a case of Tourette’s syndrome may resolve with cerebral revascularisation surgery. Abstract Background: Moyamoya disease, an uncommon chronic intra-cerebral arteriopathy asymmetrically affecting the proximal vasculature, is rarely associated with clinical features pertaining to movement disorders. Case Description: A 5-year-and-9-month-old boy developed repetitive episodic involuntary winking of the right eye along with ipsilateral shoulder shrugging movements in an absolutely conscious © 2019 S. Karger AG, Basel E-Mail karger@karger.com www.karger.com/pne state, associated with paroxysmal shouts and loud laughs and punctuated with abusive verbal expressions (coprolalia). These episodic features, over the course of the next 1.5 years, got progressively accentuated by situations which evoked stress. In addition, there was progressive regression of verbal and cognitive milestones, emotional lability and aspects of attention deficit hyperkinetic disorder. The child was evaluated by a neurologist with magnetic resonance imaging of the brain, which showed characteristic ischaemic areas involving the basal ganglia and fronto-parietal cortical areas along the middle cerebral artery territory, predominantly on the left side. Subsequent cerebral angiography revealed extensive stenosis of bilateral (predominantly left- Dr. Anirban Deep Banerjee, MD, MCh Institute of Neurosciences, Medanta – The Medicity Sector 38 Gurgaon, Haryana 122001 (India) E-Mail anirbandeepbanerjee @ yahoo.com Downloaded by: Uppsala Universitetsbibl. 130.238.7.40 - 10/8/2019 11:06:40 AM Keywords Paediatric patient · Moyamoya disease · Tourette’s syndrome · Cerebral revascularisation sided) internal cerebral arteries and middle cerebral arteries with evidence of diffuse leptomeningeal collaterals. The electroencephalography was reported to be normal. He was eventually diagnosed to be suffering from Moyamoya disease with associated Tourette’s syndrome. Subsequently, the child underwent left-sided superficial temporal artery to middle cerebral artery anastomosis along with encephaloduro-arterio-myo-synangiosis. Significant clinico-radiological improvement was noted after 3 months. The clinical deficiencies had dramatically resolved. There was evidence of excellent development of both direct and indirect surgical collaterals along the left middle cerebral artery territory. He could go back to school. Conclusion: Ours is probably the first case reporting an association of paediatric Moyamoya disease with Tourette’s syndrome, which significantly resolved after cerebral revascularisation surgery. © 2019 S. Karger AG, Basel Background Moyamoya disease is an uncommon progressive disease of the cerebral vasculature affecting both children and adults, leading to ischaemic or haemorrhagic insults to the brain. Rarely, it causes movement disorders. We report here a paediatric case of Moyamoya disease with distinctive features of Tourette’s syndrome that resolved completely within 3 months following cerebral revascularisation surgery. Case Description A 5-year-and-9-month-old male child presented at our hospital with complaints of repetitive winking of the right eye and ipsilateral shoulder shrugging in a fully conscious state with paroxysmal bouts of shouting and loud laughter punctuated with abusive Fig. 1. Pre-operative axial magnetic reso- 2 Pediatr Neurosurg DOI: 10.1159/000503114 Bose/Banerjee Downloaded by: Uppsala Universitetsbibl. 130.238.7.40 - 10/8/2019 11:06:40 AM nance images showing hyperintense ischaemic frontoparietal, middle cerebral artery–posterior cerebral artery watershed areas and basal ganglionic (predominantly caudate nucleus) areas. and vocal tics improved considerably and his follow-up DSA (Fig. 3) showed profound improvement in blood flow in the previously affected middle cerebral artery territory with development of new collaterals. On current follow-up at 6 months after the surgery, he is doing well and is going to school again. Discussion ing poor flow in the left middle cerebral artery territory and “puff of smoke” appearance of basal collaterals. Moyamoya disease was first described in 1957 by Takeuchi and Shimizu [1] as a disorder with hypoplasia of bilateral internal carotid arteries. Suzuki and Kodama [2] called it Moyamoya, which means “puff of smoke,” representing the angiographic view of compensatory collaterals. It is defined as a progressive occlusion of the internal carotid arteries with development of basal cerebral collaterals. Its global incidence is 0.54 per 100,000 patients [3]. The incidence peaks at 10 years of age and again at 30–40 years of age [4]. Eighty percent of paediatric Moyamoya disease patients present with cerebral ischaemia and 20% with haemorrhage [4, 5]. Children may present with transient ischaemic attacks, headache, seizures, involuntary movements and progressive decline in intellectual ability with features of attention deficit [4, 6–8]. Involuntary movement is a rare presentation in Moya­ moya disease, and the pathology lies in ischaemic dysfunction and imbalance in the cortical-subcortical-ganglionic-thalamic-cortical circuitry [9]. Similarly, other authors [10] have also reported movement disorders as rare presentations after ischaemic cerebral insult. Usually, these include dystonia, chorea, hemiballismus or myoclonus. Cognitive decline in Moyamoya disease has also been separately reported along with its subsequent improvement after cerebral revascularisation surgery [8]. Tourette’s syndrome is a rare neurological disorder in which the patient displays repetitive, stereotyped involuntary movements and vocalisations called tics. It was first described by Dr Georges Gilles de la Tourette, a French neurologist, in 1885. It is more common in males, and the age of onset is before 18 years [11]. One study has reported the prevalence of Tourette’s syndrome to be 0.7– 5.3 per 10,000 with a male:female ratio of 4:1 [12]. The patient may manifest simple motor tics, such as blinking and shoulder shrugging, or complex ones, such as foot stamping, jumping, etc. Phonic tics may range from simple ones, such as grunting and sniffing, to complex ones, such as coprolalia (inappropriate or vulgar words), echolalia (repeating others’ words) or palilalia (repeating one’s own words), etc. [13]. Tourette’s syndrome is often associated with attention deficit hyperactivity disorder [14]. Paediatric Moyamoya Disease with Tourette’s Syndrome Pediatr Neurosurg DOI: 10.1159/000503114 Fig. 2. Pre-operative digital subtraction angiography image show- 3 Downloaded by: Uppsala Universitetsbibl. 130.238.7.40 - 10/8/2019 11:06:40 AM verbal expressions (coprolalia) for the last 1.5 years. These episodic features got accentuated by stressful situations. The boy underwent comprehensive neuropsychiatric evaluation and was found to have progressive regression of verbal and cognitive milestones, emotional lability and aspects of attention deficit hyperactivity disorder. He was evaluated by a neurologist, and his electroencephalogram was reported to be normal. He was diagnosed with Tourette’s syndrome. Magnetic resonance imaging of the brain was done, which revealed multiple ischaemic areas involving the basal ganglia, especially the caudate nuclei and frontoparietal cortical areas along the middle cerebral artery–posterior cerebral artery watershed territory, predominantly on the left side (Fig. 1). Subsequently, digital subtraction angiography (DSA) of the brain was done, which revealed extensive stenosis of bilateral (predominantly left-sided) internal cerebral and middle cerebral arteries with diffuse leptomeningeal collaterals (Fig. 2). This led to the final diagnosis of Moyamoya disease in association with Tourette’s syndrome. He was started on anti-platelet agents and surgery was planned. Subsequently, the patient underwent both direct (superficial temporal artery–middle cerebral artery bypass) and indirect (encephalo-duro-arterio-myo-synangiosis [EDAMS]) cerebral revascularisation surgery at the same seating. The procedure was uneventful. Three months after the surgery, the patient showed significant clinical as well as radiological improvement. His motor Fig. 3. Post-operative follow-up digital subtraction angiography (left external carotid artery run) images showing significantly improved flow in the left middle cerebral artery territory with development of new collaterals. LT, left; ECA, external carotid artery; AP, antero-posterior; RAO, right antero-oblique; LAO, left antero-oblique. 4 Pediatr Neurosurg DOI: 10.1159/000503114 history of any drug intake or of any medical condition which may have caused such symptoms. Several genetic and environmental causative factors have been implicated, but no definitive aetiology has been Bose/Banerjee Downloaded by: Uppsala Universitetsbibl. 130.238.7.40 - 10/8/2019 11:06:40 AM The current diagnostic criteria of Tourette’s syndrome [15] include presence of 2 or more motor tics and at least 1 vocal tic (which may not be concurrent), beginning before 18 years of age and lasting for at least 1 year and no confirmed [11]. However, disturbance in the dopaminergic pathways in the basal ganglia, causing loss of neuronal inhibition in the sensorimotor loop and frontocortical compensation, has been proposed to be the final pathway in the pathogenesis of the disorder [16]. One neuroimaging study has shown that the volume of bilateral caudate, lentiform and globus pallidus nuclei is smaller in these patients than in controls [17]. Another study has shown that although several areas of the brain are involved, morphological changes in the caudate nucleus, within the cortico-striatal-thalamo-cortical circuits, play a central role in the clinical manifestations of Tourette’s syndrome [18]. However, paediatric Moyamoya disease associated with distinctive features of Tourette’s syndrome has never been reported. Our patient showed dramatic improvement after cerebral revascularisation surgery. His clinical improvement paralleled the improved blood flow to the previously affected areas, which is evident from the new collaterals seen on follow-up DSA. Statement of Ethics The parents of the subject have given their written informed consent to publish this case (including publication of images). At no point, the identity of the subject has been revealed. Disclosure Statement The authors have no conflicts of interest to declare. Funding Sources No funding whatsoever has been received in relation to this case report. 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