- Email: [email protected]
Severe Neurological Complications Associated With Tourette Syndrome
Accepted Manuscript Severe Neurological Complications Associated with Tourette Syndrome Amy L. Patterson, MD, Asim F. Choudhri, MD, Masanori Igarashi, MD, Kathryn McVicar, MD, Namrata Shah, MD, FRCPC, Robin Morgan, MD PII:
S0887-8994(16)30132-1
DOI:
10.1016/j.pediatrneurol.2016.05.008
Reference:
PNU 8910
To appear in:
Pediatric Neurology
Received Date: 9 March 2016 Accepted Date: 15 May 2016
Please cite this article as: Patterson AL, Choudhri AF, Igarashi M, McVicar K, Shah N, Morgan R, Severe Neurological Complications Associated with Tourette Syndrome, Pediatric Neurology (2016), doi: 10.1016/j.pediatrneurol.2016.05.008. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Severe Neurological Complications Associated with Tourette Syndrome Amy L. Patterson MD1,2, Asim F. Choudhri MD1,2, Masanori Igarashi MD1,2, Kathryn McVicar MD1,2, and Namrata Shah MD, FRCPC 1,2, Robin Morgan MD1,2
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Corresponding Author: Robin Morgan, MD Assistant Professor of Pediatric Neurology University of Tennessee Health Science Center Director, Tourette’s Clinic Le Bonheur Children’s Hospital Faculty Office Building 49 N Dunlap Street, 3rd Floor, Pediatric Neurology Memphis, TN 38103 Phone: 901-287-5208 Fax: 901-287-5325 Email: [email protected]
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of Tennessee Health Science Center. 2Le Bonheur Children’s Hospital.
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1University
Abstract
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Introduction
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Introduction: Tics and Tourette syndrome are common problems evaluated by both the general pediatrician and pediatric neurologist. The common comorbidities of tics are well known, but the severe neurological complications are rare and may not be appreciated. Methods: This is a retrospective case series and literature review. Results: We present here four adolescents with Tourette syndrome who had severe neurologic complications secondary to motor tics. We provide the history, neurologic examination, and radiological findings in addition to a review of previously reported cases of vascular and cervical cord complications associated with violent motor tics. Discussion: We highlight the importance of recognizing the presenting signs of these complications early and the need to vigorously treat violent motor tics to prevent significant neurological complications.
Tourette syndrome is a common problem seen in the pediatric neurology clinic. Tics generally are benign in nature, and many do not require medical treatment. Firstline management often involves education for patients and families about the natural course of tics. Education alone often can help to alleviate the stress associated with tics.1 However, Tourette syndrome is known to have associated behavioral and psychiatric comorbidities, including sleep disorders, attention deficit hyperactivity disorder, obsessive-compulsive behaviors and disorder, anxiety and mood disorder.2 Cheung, et al describe malignant Tourette syndrome as two or more emergency room visits or one or more hospitalization for Tourette syndrome symptoms or associated behavioral comorbidities, with only 5% of patients referred
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to a specialty clinic meeting this criteria.3 Tourette syndrome and tics may rarely be associated with serious medical complications including cervical myelopathy, cervical disc herniation, stroke and/or dissection, self-mutilation, retinal detachment, and bone fracture.3-20 These complications arise as the result of violent motor tics. We present here the clinical and radiological features of four adolescents with Tourette syndrome who were evaluated and treated for life-threatening consequences in our tertiary care center. Methods
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This is a retrospective study, from 1998 to 2014, describing the history, neurologic examination, and radiological findings in four children with severe neurologic complications of Tourette syndrome due to aggressive motor tics. These children are part of a larger cohort, approximately 300 patients, followed in our Tourette Syndrome Clinic directed by RM. Referrals to this clinic are from local pediatricians, neurologists, and the tertiary care children’s hospital with which the clinic is associated. Results
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Case 1 A 15-year-old boy with diagnosis of Tourette syndrome since the age of five years, with comorbidities of attention deficit hyperactivity disorder, anxiety, and depression. He had a history of worsening motor tics over a six-month period prior to admission with reported neck sprain three months prior. Magnetic resonance imaging (MRI) of the brain and electromyogram and nerve conduction velocities (EMG/NCV) at that time were reported as normal. His tics consisted of facial grimacing with flaring of his nostrils, mouth stretching, flexion of his arms, and violent head and neck twisting with lateral flexion to the left. Four weeks prior to admission, he began to experience numbness over his right side including his face, arm, and leg. The sensory symptoms then became bilateral with continued weakness over the right side. This progressed to impaired gait with loss of balance and frequent falls. He was seen in the emergency department one day prior to admission with complaint of frequent falls and loss of bladder control. Physical examination documented frequent motor tics, decreased sensation to touch on the right side and to temperature on the left, and weakness in the right upper and lower extremities. He returned to the emergency department the following morning due to continued falling and several episodes of bladder incontinence. He was admitted for evaluation and management. Neurologic examination was consistent with cervical myelopathy with weakness in the bilateral lower extremities and right upper extremity with decreased sensation to touch on right side and temperature and proprioception on the left. Gait was wide-based; however, deep tendon reflexes (DTRs) were not brisk. No clonus was noted. MRI of the brain showed cervical (C2) cord compression due to odontoid nonunion with anterior subluxation (Figure 1). The subluxation was not present on a
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comparison study three months prior. CT of the cervical spine revealed chronic appearing non-united odontoid fracture with sclerotic margins with approximately 3.5 mm anterior subluxation with respect to the base of the odontoid process and body of C2 (Figure 2). These findings corresponded to the area of concern on the MRI.
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Placement of cervical collar, botulinum toxin injections, and pharmacotherapy were used while awaiting surgical intervention to prevent progression. He underwent reduction of subluxation at C1-2, fusion of C1-2, and halo jacket placement. At the time of discharge from the hospital, he still had residual weakness. He was lost to follow up to the clinic but on return to our emergency department for unrelated reasons two years later had a non-focal neurological examination. Case 2
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A 15-year-old boy with Tourette syndrome, who had onset of tics at age five years, and a diagnosis of Tourette syndrome was made at age seven years. Additionally, he had comorbidities of obsessive-compulsive behaviors and attention problems. His tics consisted of biting his cheeks, face twisting, inward sucking movements of the cheeks, and dancing like movements of his leg and foot. Approximately three months prior to presentation, he began to complain of numbness of his left thumb and second digit, followed about a month later by numbness in his right thumb, second finger, and then entire right hand. Within eight weeks of the initial complaints, he developed paresthesias in his feet bilaterally up to his knees. On examination at that time, he had Tromner sign, sensory loss to touch most noticeable in his right hand, and decreased vibratory sense distally most noticeable in his right hand and left foot. Three weeks later, the numbness had advanced to the xiphoid level with increasing difficulty performing activities such as running and doing push-ups, which he was previously able to do without difficulty. Examination at that time revealed brisk reflexes throughout; flexor plantar reflex; decreased strength bilaterally in his deltoids, infraspinatus, biceps, and wrist extensors; and decreased sensation to vibration and touch, as well as reduced position sensation and stereognosis.
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MRI showed cervical disk herniation with cord compression and cord edema (Figures 3 and 4). Congenital narrowing of the anterior-posterior diameter of the central canal predisposed him to injury in the setting of this relatively small disc bulge. He underwent cervical decompression surgery followed by use of a cervical collar. At the time of follow up 15 months later, he continued to have brisk reflexes throughout, but muscle strength testing had improved to normal with the exception of mild weakness in his right deltoid. He required additional surgeries for cervical vertebrae stabilization. Case 3 A 14-year-old boy with history of motor and vocal tics for 4-5 years consisting of eye rolling, sniffing, coughing, arching of his back, neck popping, and swinging his neck
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from side to side. He had not seen a neurologist at the time of presentation and had not been previously diagnosed with Tourette syndrome. The night prior to admission, he experienced a severe headache, dizziness, numbness in his fingers, and diaphoresis after he popped his neck. He had persistent emesis and seemed to have poor coordination. He described feeling as if things were spinning around him. He was taken to an adult emergency department, where he had a CT angiogram performed and this revealed a possible right vertebral artery dissection. He was then transferred to our institution for further evaluation and management. On admission, neurologic exam was significant for horizontal nystagmus worse with left gaze and mild dysmetria of right upper extremity.
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MRI of the brain revealed focal embolic infarction involving the right inferior cerebellar hemisphere and right inferolateral aspect of the cerebellar vermis (Figures 5 and 6). Magnetic resonance (MR) angiogram revealed no appreciable flow within the V4 segment of the right vertebral artery (Figure 7). Conventional arteriography confirmed right vertebral artery dissection (Figure 8). He was admitted to the neuroscience intensive care unit (ICU) and anticoagulated with heparin followed by enoxaparin He had complete resolution of his cerebellar findings by four days after onset of symptoms. Case 4
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A 12-year-old boy with autism spectrum disorder, attention deficit hyperactivity disorder, and associated Tourette syndrome . His motor tics had increased over the three to four months prior to admission with aggressive head and neck thrusting and jerking of his body. He developed vomiting, ataxic gait, and upper extremity weakness, for which he presented to his primary care physician. He was diagnosed with a viral syndrome. The vomiting continued, and he had an episode of dizziness with near syncope four days later. He presented to the emergency department the following day due to persistent vomiting, leg weakness, and inability to walk. At that time, he was also complaining of intermittent numbness. On examination, he had left central facial weakness, right upper extremity weakness, brisk lower extremity reflexes with right ankle clonus, and right upper extremity dysmetria. CT of the head was found to have a wedge shaped hypodensity in the medial aspect of the right occipital lobe and smaller more subtle hypodensities in the right cerebellar hemisphere suggesting infarction in the territory of the right posterior cerebral artery (PCA). MRI of the brain revealed multiple areas of infarction involving the posterior inferior cerebellar artery (PICA) territory of the inferior right cerebellar hemisphere, the lateral aspect of the pons, and the parasagittal aspect of the right occipital lobe (Figures 9-10). Additional punctate areas of infarction were seen in both thalami. Diffusion tensor imaging (DTI) revealed disruption of the fibers of the descending corticospinal tract on the left at the area of the left pontine infarction correlating with the right-sided weakness (Figures 1112). MR angiogram of head and neck showed no significant flow in the V4 segment
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of the right vertebral artery; however, the V4 segment of the right vertebral artery did appear to be patent with occlusion of the extradural portions of the right vertebral artery (Figures 13-14). No flow related signal was seen in the cervical segments of the right vertebral artery with an appearance suggestive of dissection at the V3-V4 junction with proximal thrombosis.
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He was placed on a soft cervical collar. He was anti-coagulated with intravenous heparin followed by enoxaparin. With the exception of right dysmetria, his neurological symptoms had resolved at his 3-week follow up visit, and all neurological symptoms resolved over 14 weeks.
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Discussion
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These four patients demonstrate that forceful neck tics in Tourette syndrome patients can be associated with cervical myelopathy and arterial dissection leading to potentially serious neurologic complications including spinal cord injury and stroke. Treatment for tics can include pharmacological therapy, including alpha-2 agonists, dopamine depleters, and dopamine antagonists; behavior therapy, which can lead to a significant decrease in tic severity; cervical collar, for stabilization and prevention of initial injury and/or progression of existing injury; and treatment with botulinum injections.10,21-23
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We reviewed the literature to find other cases of motor tics that lead to neuropathies, radiculopathies, and vascular complications as a result of the violent motor tics, mostly neck tics.3-14 (see Table 1) Table 1: Severe Neurological Complications Associated with Tics Gender
Tics
Complications/Imaging findings
Male
Violent motor tics with hyperflexion and hyperextension Violent hyperextension and lateral flexion of the neck Motor tics
Focal high-signal intensity cord lesion and adjacent cervical spondylotic changes
Van Meerbeeck5
12
Male
Muroi6
15
Male
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Ko4
Age (in years) 9
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Author
Goetz7
16
Female
Lehman8
18
Male
Lin9
20
Male
Krauss10
21
Male
Nomura11
22
Male
Violent backward jerking of her head Violent neck tics
Strong sudden extension of the head Violent twisting and extending movements of neck Neck flexion
MRI: right striatal stroke with secondary hemorrhage; Cerebral angiography: right vertebral artery dissection Cervical myelopathy involving hands and lower extremities with mild canal stenosis and increased signal intensity in the cervical spinal cord beginning at C4 level and continuing upward to medulla oblongata on T2-weighted images C8-T1 radiculopathy MRI: Right pontine and bilateral cerebellar infarcts ; MRA: occlusions of right vertebral and basilar arteries; CTA: occlusion of right vertebral artery at level of C2 with a configuration compatible with arterial dissection Traumatic herniation of the intervertebral disc at C34 level with associated bony injury and contusion injury of the spinal cord Compressive myelopathy
Flexion myelopathy
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Male
Dobbs12
25
Male
Brill13
27
Male
Goetz7
41
Male
Cheung3 Wong14 Wong14
43 52 52
Female Male Male
Violent clonic tics with thrusting head jerks Strong sudden flexion of his head in “sneeze-like” fashion Rapid, repetitive jerks of head and neck Rapid abduction of left thigh with external rotation of pelvis Head jerk tic
Cervical spinal canal stenosis with retrospondylosis from C3 through C5 and a Klippel-Feil malformation Small hyperintense enhancing signal on T2-weighted imaging at C5 level of the spinal cord
Herniated C6-C7 disc with resultant myelopathy
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Compressive neuropathy at sciatic notch
C3-C4 disc herniation C2-C5 myeloradiculopathy C3-C7 myeloradiculopathy
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Krauss10
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Our cases and those in the literature highlight the importance of recognizing violent motor tics as a risk factor for these serious neurological complications and of treating them aggressively. The literature review also demonstrates that this is not just a problem of childhood and adolescence but that the complications can be seen well into adulthood. This emphasizes the need to think about tics as an etiology of dissections and strokes in young adults without other obvious risk factors. In fact, minor trauma, which could include neck tics, is identified as the cause in 12-34% of spontaneous dissections.24 Conclusion
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Tic disorders and Tourette syndrome are common problems referred for evaluation in the pediatric neurology clinic. In general, education and behavioral therapy are adequate to manage most motor and vocal tics. In our practice, we advocate avoidance of pharmacotherapy for mild tics that do not interfere with the child’s academic or social functioning or cause physical pain. However, if tics are associated with aggressive flexion and extension or rotation of the neck with or without pain, then one must be aware that serious neurological complications are possible. Aggressive pharmacotherapy and botulinum injections should be considered in those patients.
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Pediatric neurologists should be aware that violent motor tics, especially those involving the neck, have the potential to result in severe neurological complications and should be treated aggressively. The families should be informed of the rational for treatment and the need for adherence with the medical regimen. References 1. 2.
Martino D, Mink JW. Tic disorders. Continuum (Minneapolis, Minn.). 2013;19(5 Movement Disorders):1287-1311. Robertson MM. Tourette syndrome, associated conditions and the complexities of treatment. Brain : a journal of neurology. 2000;123 Pt 3:425462.
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Cheung MY, Shahed J, Jankovic J. Malignant Tourette syndrome. Movement disorders : official journal of the Movement Disorder Society. 2007;22(12):1743-1750. Ko DY, Kim SK, Chae JH, Wang KC, Phi JH. Cervical spondylotic myelopathy caused by violent motor tics in a child with Tourette syndrome. Child's nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery. 2013;29(2):317-321. van Meerbeeck P, Behar C, Czernecki V, Roze E, Deniau E, Hartmann A. Motor tic of the neck: a probable cause of stroke in a child with Gilles de la Tourette syndrome. Movement disorders : official journal of the Movement Disorder Society. 2011;26(5):928-929. Muroi A, Matsumura A, Asakawa H, Enomoto T, Iwasaki N, Nose T. Myelopathy caused by tics in an adolescent, associated with T2 signal intensity changes of the spinal cord. Child's nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery. 2002;18(34):191-194. Goetz CG, Klawans HL. Gilles de la Tourette syndrome and compressive neuropathies. Annals of neurology. 1980;8(4):453. Lehman LL, Gilbert DL, Leach JL, Wu SW, Standridge SM. Vertebral artery dissection leading to stroke caused by violent neck tics of Tourette syndrome. Neurology. 2011;77(18):1706-1708. Lin JJ, Wang HS, Wong MC, Wu CT, Lin KL. Tourette's syndrome with cervical disc herniation. Brain & development. 2007;29(2):61-63. Krauss JK, Jankovic J. Severe motor tics causing cervical myelopathy in Tourette's syndrome. Movement disorders : official journal of the Movement Disorder Society. 1996;11(5):563-566. Nomura T, Kira J, Yoshimura T, Goto I, Hasuo K. [Flexion myelopathy due to tic of neck]. Rinsho shinkeigaku = Clinical neurology. 1989;29(2):177-179. Dobbs M, Berger JR. Cervical myelopathy secondary to violent tics of Tourette's syndrome. Neurology. 2003;60(11):1862-1863. Brill CB, Hartz WH, Mancall EL. Cervical disc herniation in the Gilles de la Tourette syndrome. Annals of neurology. 1981;9(3):311. Wong AS, Massicotte EM, Fehlings MG. Surgical treatment of cervical myeloradiculopathy associated with movement disorders: indications, technique, and clinical outcome. Journal of spinal disorders & techniques. 2005;18 Suppl:S107-114. Isaacs JD, Adams M, Lees AJ. Noncompressive myelopathy associated with violent axial tics of tourette syndrome. Neurology. 2010;74(8):697-698. Fusco C, Bertani G, Caricati G, Della Giustina E. Stress fracture of the peroneal bone secondary to a complex tic. Brain & development. 2006;28(1):52-54. Shimoyama T, Horie N, Kato T, Nasu D, Kaneko T. Tourette's syndrome with rapid deterioration by self-mutilation of the upper lip. The Journal of clinical pediatric dentistry. 2003;27(2):177-180. Eisenhauer GL, Woody RC. Self-mutilation and Tourette's disorder. Journal of child neurology. 1987;2(4):265-267.
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Lim S, Rezai KA, Abrams GW, Eliott D. Self-induced, bilateral retinal detachment in Tourette syndrome. Archives of ophthalmology (Chicago, Ill. : 1960). 2004;122(6):930-931. Gaillard MC, Wolfensberger TJ. [Self-mutilation with crystalline lens dislocation in Gilles de la Tourette disease treated with retropupillary "iris claw" lens]. Klinische Monatsblatter fur Augenheilkunde. 2004;221(5):435437. Piacentini J, Woods DW, Scahill L, et al. Behavior therapy for children with Tourette disorder: a randomized controlled trial. Jama. 2010;303(19):19291937. Kramer U, Kipervasser S, Shlitner A, Kuzniecky R. A novel portable seizure detection alarm system: preliminary results. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2011;28(1):36-38. Termine C, Selvini C, Rossi G, Balottin U. Emerging treatment strategies in Tourette syndrome: what's in the pipeline? International review of neurobiology. 2013;112:445-480. Rubinstein SM, Peerdeman SM, van Tulder MW, Riphagen I, Haldeman S. A systematic review of the risk factors for cervical artery dissection. Stroke; a journal of cerebral circulation. 2005;36(7):1575-1580.
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Figure 1
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MRI of the brain reveals near complete effacement of the CSF dorsal and ventral to the spinal cord at the level of the odontoid synchondrosis
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Figure 2
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CT of cervical spine with chronic appearing ununited odontoid fracture with sclerotic margins and with 3.5 mm anterior subluxation with respect to the base of the odontoid and body of C2
Figure 3
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MRI of the cervical spine with disc herniation and cord edema
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Figure 4
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MRI of the spine with congenital narrowing of the anterior-posterior diameter of the central canal
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Figure 5
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MRI of the brain with reduced water diffusion in the inferior aspect of the right cerebellar hemisphere and in the right inferolateral aspect of the cerebellar vermis, both consistent with focal embolic infarction
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Figure 6
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MRI of the brain shows T2 prolongation in the inferior aspect of the right cerebellar hemisphere
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Figure 7
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MR Angiography with no appreciable flow related signal within the V2, V3 or V4 segments of the right vertebral artery
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Figure 8
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Conventional arteriography confirmed right vertebral artery dissection
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Figure 9
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MRI with multiple areas of reduced water diffusion in the inferior aspect of the right cerebellar hemisphere, as well as the inferior aspect of the vermis
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Figure 10
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MRI with patchy area of reduced water diffusion in the parasagittal aspect of the right occipital lobe
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Figure 11
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Diffusion tensor imaging revealed disruption of the fibers of the descending corticospinal tract on the left at the area of the left pontine infarction (see figure 12)
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Figure 12
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Left pontine infarction
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Figure 13
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Conventional arteriography reveals complete occlusion of the right vertebral artery. The right posterior inferior cerebellar artery does not fill completely.
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Figure 14
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MR angiography of the head and neck showed no significant flow in the V4 segment of the right vertebral artery. The V4 segment however did appear to be patent with occlusion of the extradural portions of the right vertebral artery.
S0887-8994(16)30132-1
DOI:
10.1016/j.pediatrneurol.2016.05.008
Reference:
PNU 8910
To appear in:
Pediatric Neurology
Received Date: 9 March 2016 Accepted Date: 15 May 2016
Please cite this article as: Patterson AL, Choudhri AF, Igarashi M, McVicar K, Shah N, Morgan R, Severe Neurological Complications Associated with Tourette Syndrome, Pediatric Neurology (2016), doi: 10.1016/j.pediatrneurol.2016.05.008. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
Severe Neurological Complications Associated with Tourette Syndrome Amy L. Patterson MD1,2, Asim F. Choudhri MD1,2, Masanori Igarashi MD1,2, Kathryn McVicar MD1,2, and Namrata Shah MD, FRCPC 1,2, Robin Morgan MD1,2
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Corresponding Author: Robin Morgan, MD Assistant Professor of Pediatric Neurology University of Tennessee Health Science Center Director, Tourette’s Clinic Le Bonheur Children’s Hospital Faculty Office Building 49 N Dunlap Street, 3rd Floor, Pediatric Neurology Memphis, TN 38103 Phone: 901-287-5208 Fax: 901-287-5325 Email: [email protected]
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of Tennessee Health Science Center. 2Le Bonheur Children’s Hospital.
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1University
Abstract
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Introduction
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Introduction: Tics and Tourette syndrome are common problems evaluated by both the general pediatrician and pediatric neurologist. The common comorbidities of tics are well known, but the severe neurological complications are rare and may not be appreciated. Methods: This is a retrospective case series and literature review. Results: We present here four adolescents with Tourette syndrome who had severe neurologic complications secondary to motor tics. We provide the history, neurologic examination, and radiological findings in addition to a review of previously reported cases of vascular and cervical cord complications associated with violent motor tics. Discussion: We highlight the importance of recognizing the presenting signs of these complications early and the need to vigorously treat violent motor tics to prevent significant neurological complications.
Tourette syndrome is a common problem seen in the pediatric neurology clinic. Tics generally are benign in nature, and many do not require medical treatment. Firstline management often involves education for patients and families about the natural course of tics. Education alone often can help to alleviate the stress associated with tics.1 However, Tourette syndrome is known to have associated behavioral and psychiatric comorbidities, including sleep disorders, attention deficit hyperactivity disorder, obsessive-compulsive behaviors and disorder, anxiety and mood disorder.2 Cheung, et al describe malignant Tourette syndrome as two or more emergency room visits or one or more hospitalization for Tourette syndrome symptoms or associated behavioral comorbidities, with only 5% of patients referred
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to a specialty clinic meeting this criteria.3 Tourette syndrome and tics may rarely be associated with serious medical complications including cervical myelopathy, cervical disc herniation, stroke and/or dissection, self-mutilation, retinal detachment, and bone fracture.3-20 These complications arise as the result of violent motor tics. We present here the clinical and radiological features of four adolescents with Tourette syndrome who were evaluated and treated for life-threatening consequences in our tertiary care center. Methods
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This is a retrospective study, from 1998 to 2014, describing the history, neurologic examination, and radiological findings in four children with severe neurologic complications of Tourette syndrome due to aggressive motor tics. These children are part of a larger cohort, approximately 300 patients, followed in our Tourette Syndrome Clinic directed by RM. Referrals to this clinic are from local pediatricians, neurologists, and the tertiary care children’s hospital with which the clinic is associated. Results
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Case 1 A 15-year-old boy with diagnosis of Tourette syndrome since the age of five years, with comorbidities of attention deficit hyperactivity disorder, anxiety, and depression. He had a history of worsening motor tics over a six-month period prior to admission with reported neck sprain three months prior. Magnetic resonance imaging (MRI) of the brain and electromyogram and nerve conduction velocities (EMG/NCV) at that time were reported as normal. His tics consisted of facial grimacing with flaring of his nostrils, mouth stretching, flexion of his arms, and violent head and neck twisting with lateral flexion to the left. Four weeks prior to admission, he began to experience numbness over his right side including his face, arm, and leg. The sensory symptoms then became bilateral with continued weakness over the right side. This progressed to impaired gait with loss of balance and frequent falls. He was seen in the emergency department one day prior to admission with complaint of frequent falls and loss of bladder control. Physical examination documented frequent motor tics, decreased sensation to touch on the right side and to temperature on the left, and weakness in the right upper and lower extremities. He returned to the emergency department the following morning due to continued falling and several episodes of bladder incontinence. He was admitted for evaluation and management. Neurologic examination was consistent with cervical myelopathy with weakness in the bilateral lower extremities and right upper extremity with decreased sensation to touch on right side and temperature and proprioception on the left. Gait was wide-based; however, deep tendon reflexes (DTRs) were not brisk. No clonus was noted. MRI of the brain showed cervical (C2) cord compression due to odontoid nonunion with anterior subluxation (Figure 1). The subluxation was not present on a
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comparison study three months prior. CT of the cervical spine revealed chronic appearing non-united odontoid fracture with sclerotic margins with approximately 3.5 mm anterior subluxation with respect to the base of the odontoid process and body of C2 (Figure 2). These findings corresponded to the area of concern on the MRI.
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Placement of cervical collar, botulinum toxin injections, and pharmacotherapy were used while awaiting surgical intervention to prevent progression. He underwent reduction of subluxation at C1-2, fusion of C1-2, and halo jacket placement. At the time of discharge from the hospital, he still had residual weakness. He was lost to follow up to the clinic but on return to our emergency department for unrelated reasons two years later had a non-focal neurological examination. Case 2
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A 15-year-old boy with Tourette syndrome, who had onset of tics at age five years, and a diagnosis of Tourette syndrome was made at age seven years. Additionally, he had comorbidities of obsessive-compulsive behaviors and attention problems. His tics consisted of biting his cheeks, face twisting, inward sucking movements of the cheeks, and dancing like movements of his leg and foot. Approximately three months prior to presentation, he began to complain of numbness of his left thumb and second digit, followed about a month later by numbness in his right thumb, second finger, and then entire right hand. Within eight weeks of the initial complaints, he developed paresthesias in his feet bilaterally up to his knees. On examination at that time, he had Tromner sign, sensory loss to touch most noticeable in his right hand, and decreased vibratory sense distally most noticeable in his right hand and left foot. Three weeks later, the numbness had advanced to the xiphoid level with increasing difficulty performing activities such as running and doing push-ups, which he was previously able to do without difficulty. Examination at that time revealed brisk reflexes throughout; flexor plantar reflex; decreased strength bilaterally in his deltoids, infraspinatus, biceps, and wrist extensors; and decreased sensation to vibration and touch, as well as reduced position sensation and stereognosis.
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MRI showed cervical disk herniation with cord compression and cord edema (Figures 3 and 4). Congenital narrowing of the anterior-posterior diameter of the central canal predisposed him to injury in the setting of this relatively small disc bulge. He underwent cervical decompression surgery followed by use of a cervical collar. At the time of follow up 15 months later, he continued to have brisk reflexes throughout, but muscle strength testing had improved to normal with the exception of mild weakness in his right deltoid. He required additional surgeries for cervical vertebrae stabilization. Case 3 A 14-year-old boy with history of motor and vocal tics for 4-5 years consisting of eye rolling, sniffing, coughing, arching of his back, neck popping, and swinging his neck
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from side to side. He had not seen a neurologist at the time of presentation and had not been previously diagnosed with Tourette syndrome. The night prior to admission, he experienced a severe headache, dizziness, numbness in his fingers, and diaphoresis after he popped his neck. He had persistent emesis and seemed to have poor coordination. He described feeling as if things were spinning around him. He was taken to an adult emergency department, where he had a CT angiogram performed and this revealed a possible right vertebral artery dissection. He was then transferred to our institution for further evaluation and management. On admission, neurologic exam was significant for horizontal nystagmus worse with left gaze and mild dysmetria of right upper extremity.
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MRI of the brain revealed focal embolic infarction involving the right inferior cerebellar hemisphere and right inferolateral aspect of the cerebellar vermis (Figures 5 and 6). Magnetic resonance (MR) angiogram revealed no appreciable flow within the V4 segment of the right vertebral artery (Figure 7). Conventional arteriography confirmed right vertebral artery dissection (Figure 8). He was admitted to the neuroscience intensive care unit (ICU) and anticoagulated with heparin followed by enoxaparin He had complete resolution of his cerebellar findings by four days after onset of symptoms. Case 4
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A 12-year-old boy with autism spectrum disorder, attention deficit hyperactivity disorder, and associated Tourette syndrome . His motor tics had increased over the three to four months prior to admission with aggressive head and neck thrusting and jerking of his body. He developed vomiting, ataxic gait, and upper extremity weakness, for which he presented to his primary care physician. He was diagnosed with a viral syndrome. The vomiting continued, and he had an episode of dizziness with near syncope four days later. He presented to the emergency department the following day due to persistent vomiting, leg weakness, and inability to walk. At that time, he was also complaining of intermittent numbness. On examination, he had left central facial weakness, right upper extremity weakness, brisk lower extremity reflexes with right ankle clonus, and right upper extremity dysmetria. CT of the head was found to have a wedge shaped hypodensity in the medial aspect of the right occipital lobe and smaller more subtle hypodensities in the right cerebellar hemisphere suggesting infarction in the territory of the right posterior cerebral artery (PCA). MRI of the brain revealed multiple areas of infarction involving the posterior inferior cerebellar artery (PICA) territory of the inferior right cerebellar hemisphere, the lateral aspect of the pons, and the parasagittal aspect of the right occipital lobe (Figures 9-10). Additional punctate areas of infarction were seen in both thalami. Diffusion tensor imaging (DTI) revealed disruption of the fibers of the descending corticospinal tract on the left at the area of the left pontine infarction correlating with the right-sided weakness (Figures 1112). MR angiogram of head and neck showed no significant flow in the V4 segment
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of the right vertebral artery; however, the V4 segment of the right vertebral artery did appear to be patent with occlusion of the extradural portions of the right vertebral artery (Figures 13-14). No flow related signal was seen in the cervical segments of the right vertebral artery with an appearance suggestive of dissection at the V3-V4 junction with proximal thrombosis.
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He was placed on a soft cervical collar. He was anti-coagulated with intravenous heparin followed by enoxaparin. With the exception of right dysmetria, his neurological symptoms had resolved at his 3-week follow up visit, and all neurological symptoms resolved over 14 weeks.
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Discussion
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These four patients demonstrate that forceful neck tics in Tourette syndrome patients can be associated with cervical myelopathy and arterial dissection leading to potentially serious neurologic complications including spinal cord injury and stroke. Treatment for tics can include pharmacological therapy, including alpha-2 agonists, dopamine depleters, and dopamine antagonists; behavior therapy, which can lead to a significant decrease in tic severity; cervical collar, for stabilization and prevention of initial injury and/or progression of existing injury; and treatment with botulinum injections.10,21-23
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We reviewed the literature to find other cases of motor tics that lead to neuropathies, radiculopathies, and vascular complications as a result of the violent motor tics, mostly neck tics.3-14 (see Table 1) Table 1: Severe Neurological Complications Associated with Tics Gender
Tics
Complications/Imaging findings
Male
Violent motor tics with hyperflexion and hyperextension Violent hyperextension and lateral flexion of the neck Motor tics
Focal high-signal intensity cord lesion and adjacent cervical spondylotic changes
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Muroi6
15
Male
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Age (in years) 9
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Goetz7
16
Female
Lehman8
18
Male
Lin9
20
Male
Krauss10
21
Male
Nomura11
22
Male
Violent backward jerking of her head Violent neck tics
Strong sudden extension of the head Violent twisting and extending movements of neck Neck flexion
MRI: right striatal stroke with secondary hemorrhage; Cerebral angiography: right vertebral artery dissection Cervical myelopathy involving hands and lower extremities with mild canal stenosis and increased signal intensity in the cervical spinal cord beginning at C4 level and continuing upward to medulla oblongata on T2-weighted images C8-T1 radiculopathy MRI: Right pontine and bilateral cerebellar infarcts ; MRA: occlusions of right vertebral and basilar arteries; CTA: occlusion of right vertebral artery at level of C2 with a configuration compatible with arterial dissection Traumatic herniation of the intervertebral disc at C34 level with associated bony injury and contusion injury of the spinal cord Compressive myelopathy
Flexion myelopathy
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Male
Dobbs12
25
Male
Brill13
27
Male
Goetz7
41
Male
Cheung3 Wong14 Wong14
43 52 52
Female Male Male
Violent clonic tics with thrusting head jerks Strong sudden flexion of his head in “sneeze-like” fashion Rapid, repetitive jerks of head and neck Rapid abduction of left thigh with external rotation of pelvis Head jerk tic
Cervical spinal canal stenosis with retrospondylosis from C3 through C5 and a Klippel-Feil malformation Small hyperintense enhancing signal on T2-weighted imaging at C5 level of the spinal cord
Herniated C6-C7 disc with resultant myelopathy
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Compressive neuropathy at sciatic notch
C3-C4 disc herniation C2-C5 myeloradiculopathy C3-C7 myeloradiculopathy
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Krauss10
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Our cases and those in the literature highlight the importance of recognizing violent motor tics as a risk factor for these serious neurological complications and of treating them aggressively. The literature review also demonstrates that this is not just a problem of childhood and adolescence but that the complications can be seen well into adulthood. This emphasizes the need to think about tics as an etiology of dissections and strokes in young adults without other obvious risk factors. In fact, minor trauma, which could include neck tics, is identified as the cause in 12-34% of spontaneous dissections.24 Conclusion
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Tic disorders and Tourette syndrome are common problems referred for evaluation in the pediatric neurology clinic. In general, education and behavioral therapy are adequate to manage most motor and vocal tics. In our practice, we advocate avoidance of pharmacotherapy for mild tics that do not interfere with the child’s academic or social functioning or cause physical pain. However, if tics are associated with aggressive flexion and extension or rotation of the neck with or without pain, then one must be aware that serious neurological complications are possible. Aggressive pharmacotherapy and botulinum injections should be considered in those patients.
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Pediatric neurologists should be aware that violent motor tics, especially those involving the neck, have the potential to result in severe neurological complications and should be treated aggressively. The families should be informed of the rational for treatment and the need for adherence with the medical regimen. References 1. 2.
Martino D, Mink JW. Tic disorders. Continuum (Minneapolis, Minn.). 2013;19(5 Movement Disorders):1287-1311. Robertson MM. Tourette syndrome, associated conditions and the complexities of treatment. Brain : a journal of neurology. 2000;123 Pt 3:425462.
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Cheung MY, Shahed J, Jankovic J. Malignant Tourette syndrome. Movement disorders : official journal of the Movement Disorder Society. 2007;22(12):1743-1750. Ko DY, Kim SK, Chae JH, Wang KC, Phi JH. Cervical spondylotic myelopathy caused by violent motor tics in a child with Tourette syndrome. Child's nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery. 2013;29(2):317-321. van Meerbeeck P, Behar C, Czernecki V, Roze E, Deniau E, Hartmann A. Motor tic of the neck: a probable cause of stroke in a child with Gilles de la Tourette syndrome. Movement disorders : official journal of the Movement Disorder Society. 2011;26(5):928-929. Muroi A, Matsumura A, Asakawa H, Enomoto T, Iwasaki N, Nose T. Myelopathy caused by tics in an adolescent, associated with T2 signal intensity changes of the spinal cord. Child's nervous system : ChNS : official journal of the International Society for Pediatric Neurosurgery. 2002;18(34):191-194. Goetz CG, Klawans HL. Gilles de la Tourette syndrome and compressive neuropathies. Annals of neurology. 1980;8(4):453. Lehman LL, Gilbert DL, Leach JL, Wu SW, Standridge SM. Vertebral artery dissection leading to stroke caused by violent neck tics of Tourette syndrome. Neurology. 2011;77(18):1706-1708. Lin JJ, Wang HS, Wong MC, Wu CT, Lin KL. Tourette's syndrome with cervical disc herniation. Brain & development. 2007;29(2):61-63. Krauss JK, Jankovic J. Severe motor tics causing cervical myelopathy in Tourette's syndrome. Movement disorders : official journal of the Movement Disorder Society. 1996;11(5):563-566. Nomura T, Kira J, Yoshimura T, Goto I, Hasuo K. [Flexion myelopathy due to tic of neck]. Rinsho shinkeigaku = Clinical neurology. 1989;29(2):177-179. Dobbs M, Berger JR. Cervical myelopathy secondary to violent tics of Tourette's syndrome. Neurology. 2003;60(11):1862-1863. Brill CB, Hartz WH, Mancall EL. Cervical disc herniation in the Gilles de la Tourette syndrome. Annals of neurology. 1981;9(3):311. Wong AS, Massicotte EM, Fehlings MG. Surgical treatment of cervical myeloradiculopathy associated with movement disorders: indications, technique, and clinical outcome. Journal of spinal disorders & techniques. 2005;18 Suppl:S107-114. Isaacs JD, Adams M, Lees AJ. Noncompressive myelopathy associated with violent axial tics of tourette syndrome. Neurology. 2010;74(8):697-698. Fusco C, Bertani G, Caricati G, Della Giustina E. Stress fracture of the peroneal bone secondary to a complex tic. Brain & development. 2006;28(1):52-54. Shimoyama T, Horie N, Kato T, Nasu D, Kaneko T. Tourette's syndrome with rapid deterioration by self-mutilation of the upper lip. The Journal of clinical pediatric dentistry. 2003;27(2):177-180. Eisenhauer GL, Woody RC. Self-mutilation and Tourette's disorder. Journal of child neurology. 1987;2(4):265-267.
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Lim S, Rezai KA, Abrams GW, Eliott D. Self-induced, bilateral retinal detachment in Tourette syndrome. Archives of ophthalmology (Chicago, Ill. : 1960). 2004;122(6):930-931. Gaillard MC, Wolfensberger TJ. [Self-mutilation with crystalline lens dislocation in Gilles de la Tourette disease treated with retropupillary "iris claw" lens]. Klinische Monatsblatter fur Augenheilkunde. 2004;221(5):435437. Piacentini J, Woods DW, Scahill L, et al. Behavior therapy for children with Tourette disorder: a randomized controlled trial. Jama. 2010;303(19):19291937. Kramer U, Kipervasser S, Shlitner A, Kuzniecky R. A novel portable seizure detection alarm system: preliminary results. Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society. 2011;28(1):36-38. Termine C, Selvini C, Rossi G, Balottin U. Emerging treatment strategies in Tourette syndrome: what's in the pipeline? International review of neurobiology. 2013;112:445-480. Rubinstein SM, Peerdeman SM, van Tulder MW, Riphagen I, Haldeman S. A systematic review of the risk factors for cervical artery dissection. Stroke; a journal of cerebral circulation. 2005;36(7):1575-1580.
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Figure 1
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MRI of the brain reveals near complete effacement of the CSF dorsal and ventral to the spinal cord at the level of the odontoid synchondrosis
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Figure 2
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CT of cervical spine with chronic appearing ununited odontoid fracture with sclerotic margins and with 3.5 mm anterior subluxation with respect to the base of the odontoid and body of C2
Figure 3
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MRI of the cervical spine with disc herniation and cord edema
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Figure 4
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MRI of the spine with congenital narrowing of the anterior-posterior diameter of the central canal
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Figure 5
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MRI of the brain with reduced water diffusion in the inferior aspect of the right cerebellar hemisphere and in the right inferolateral aspect of the cerebellar vermis, both consistent with focal embolic infarction
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Figure 6
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MRI of the brain shows T2 prolongation in the inferior aspect of the right cerebellar hemisphere
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Figure 7
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MR Angiography with no appreciable flow related signal within the V2, V3 or V4 segments of the right vertebral artery
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Figure 8
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Conventional arteriography confirmed right vertebral artery dissection
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Figure 9
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MRI with multiple areas of reduced water diffusion in the inferior aspect of the right cerebellar hemisphere, as well as the inferior aspect of the vermis
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Figure 10
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MRI with patchy area of reduced water diffusion in the parasagittal aspect of the right occipital lobe
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Figure 11
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Diffusion tensor imaging revealed disruption of the fibers of the descending corticospinal tract on the left at the area of the left pontine infarction (see figure 12)
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Figure 12
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Left pontine infarction
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Figure 13
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Conventional arteriography reveals complete occlusion of the right vertebral artery. The right posterior inferior cerebellar artery does not fill completely.
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Figure 14
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MR angiography of the head and neck showed no significant flow in the V4 segment of the right vertebral artery. The V4 segment however did appear to be patent with occlusion of the extradural portions of the right vertebral artery.