Neuroimaging of Tuberous Sclerosis: Spectrum of Pathologic Findings and Frontiers in Imaging
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1 Neuroradiology Pictorial Essay Kalantari and Salamon Neuroimaging of Tuberous Sclerosis Neuroradiology Pictorial Essay Downloaded from by on 12/22/17 from IP address Copyright RRS. For personal use only; all rights reserved abak N. Kalantari 1 Noriko Salamon Kalantari N, Salamon N Keywords: FDG PET, fusion imaging, magnetoencephalography, MRI, pediatric radiology, tuberous sclerosis DOI: /JR Received July 24, 2007; accepted after revision November 13, Certificate of merit recipient at 2007 annual meeting of the merican Roentgen Ray Society, Orlando, FL. 1 oth authors: Department of Radiology, David Geffen School of Medicine at UCL, Le Conte ve., Los ngeles, C ddress correspondence to. Kalantari (Kalantari@mednet.ucla.edu). WE This is a Web exclusive article. JR 2008; 190:W304 W X/08/1905 W304 merican Roentgen Ray Society Neuroimaging of Tuberous Sclerosis: Spectrum of Pathologic Findings and Frontiers in Imaging OJECTIVE. The purpose of this article is to present neuroimaging findings in tuberous sclerosis complex, including recently developed imaging techniques that have demonstrated clinical benefit to this patient population. CONCLUSION. Neuroimaging advances have improved the diagnosis of tuberous sclerosis complex and the treatment of children with this condition. Superimposition of functional information from PET onto MRI allows accurate and noninvasive identification of epileptogenic tubers, improving surgical cure rates. Magnetic source imaging can also be used to localize epileptiform activity arising from tubers. T uberous sclerosis complex (TSC) is a multisystem congenital syndrome with widespread CNS anomalies. The clinical neurologic manifestations include epilepsy and cognitive impairment. Features of TSC The intracranial features of TSC are cortical or subcortical tubers, subependymal nodules, subependymal giant cell astrocytomas, and white matter radial migration lines. Tubers Tubers are most commonly found in the cerebrum, 90% being present in the frontal lobes [1]. On T2-weighted and FLIR MR images, tubers typically appear as areas of increased signal intensity in the cortical and subcortical regions (Figs. 1 and 2). Tubers exhibit contrast enhancement in approximately 3 4% of cases [2]. Ninety-five percent of tubers are multiple, but in rare instances solitary cortical tubers are seen [3]. lthough not widely performed, magnetization transfer T1-weighted imaging can be superior to FLIR imaging for detecting subtle tubers [4]. Less commonly than in the cerebrum, tubers are present in the cerebellum, where they may become apparent only at histologic examination. Histologically differentiating dysmorphic neurons in tubers from those of focal cortical dysplasia is difficult. However, immunohistochemical evaluation with the tissue microarray method has aided neuropathologists in making the distinction between these two entities [5]. Unlike cortical tubers, cerebellar tubers are usually wedge-shaped and not epileptogenic. Tubers rarely are found in the brainstem and spinal cord. Depending on the location of tubers, neurologic findings include abnormalities in cognition, cranial nerve deficits, focal motor or sensory abnormalities, cerebellar dysfunction, and gait abnormalities. Subependymal Nodules Subependymal nodules are found on the walls of the lateral ventricles and are either discrete or roughly confluent areas of round ed hypertrophic tissue (Fig. 3). The nodules occur anywhere along the ventricular surface but are most commonly found at the caudothalamic groove in the region of the foramen of Monro. Typically benign, sub ependymal nodules can degenerate into sub ependymal giant cell astro cytomas in 5 10% of cases. Like sub ependymal giant cell astro cytomas, sub ependymal nodules can enhance with contrast material (Fig. 4). Contrast enhancement, how ever, is not necessarily an indication that a subependymal nodule is going to grow or that surgical intervention is necessary. Subependymal Giant Cell strocytoma Subependymal giant cell astrocytomas can grow, often in an indolent manner, eventually resulting in ventricular obstruction W304 JR:190, May 2008
2 Neuroimaging of Tuberous Sclerosis Downloaded from by on 12/22/17 from IP address Copyright RRS. For personal use only; all rights reserved and hydro cephalus. t some medical centers, sur geons resect subependymal giant cell astro cytomas that exhibit interval growth on serial images. t other centers, more frequent imaging studies are performed when a lesion becomes larger, provided no signs or symptoms of ventricular obstruction, new neuro logic defi cit, or increased intracranial pres sure are de tected. Lesions sometimes stabilize or stop growing sponta neously after the size in creases. Oral rapamycin (sirolimus) therapy has shown promise in inducing regression of sub ependymal giant cell astrocytomas and may be an alternative to surgical resection [6] (Fig. 5). Rapamycin targets the mtor protein signaling pathway. This regulator of a number of diverse biologic processes important for cell growth and proliferation has been found to be hyperactive in patients with TSC. Radial Migration Lines Radial migration lines are believed to represent heterotopic glia and neurons along the expected path of cortical migration [7]. Radial migration lines are primarily located in the subcortical white matter and are occasionally seen in relation to tubers (Fig. 6). Microcephaly Patients with TSC have been found to have cerebral gray and white matter volumes lower than those of age-matched controls [8] (Fig. 7). Statistically significant microencephaly is found in both TSC patients with and those without a history of epilepsy. Epilepsy in TSC pproximately 90% of patients with TSC have seizures, and intractable epilepsy develops in 25 30% of patients [9]. The natural history of epilepsy in patients with TSC typically begins in infancy and is characterized by increasing seizure frequency and severity, poor response to antiepileptic drugs, and diminished quality of life as the result of seizures and adverse medication effects. The ictal onset zone is often related to a tuber and adjoining cerebral cortex. Patients usually have multiple tubers, and identifying the one responsible for the onset of epileptogenic activity is difficult with video electroencephalography and conventional MRI. For children with TSC and drugresistant epilepsy, timely surgical resection of the epileptogenic tuber should be considered. Tuberectomy should ideally be performed before or during the critical time before the occurrence of secondary epileptogenesis and multifocal epilepsy. Diffusion Tensor MRI Diffusion tensor imaging has two parameters: the apparent diffusion coefficient, which is a measure of the overall magnitude of water diffusion, and the fractional anisotropy value, which is a measure of the directionality of diffusion motion. High apparent diffusion coefficients are observed in tubers, and low fractional anisotropy is seen in perilesional white matter, reflecting the presence of gliosis and hypomyelination [10]. Statistically significant increased apparent diffusion co efficients have been observed in normal-appearing supratentorial white matter distant from cortical and subcortical tubers, suggesting extensive white matter disorganization in TSC patients compared with age-matched controls [11]. The in formation acquired with diffusion tensor imaging can be helpful in understanding the propagation pattern of epileptogenesis and in predicting the degree of cognitive impair ment in TSC patients with chronic epilepsy. PET/MRI Fusion Imaging Until recently, identification of the epileptogenic tuber from among many tubers was a challenge without invasive electroencephalography or intraoperative electrocorticography. Super imposition of functional infor mation from 18 F-FDG PET onto MR images has shown great promise for accurate and non invasive identification of epileptogenic tubers, improving surgical cure rates [10] (Fig. 8). tuber with a dis proportionately large area of hypo metab olism compared with its size on MR images is most likely epileptogenic (Figs. 9 and 10). lpha- 11 C-Methyl-l-Tryptophan PET The use in PET of the tryptophan analogue α- 11 C-methyl-l-tryptophan is another avenue for locating epileptogenic tubers in TSC pa tients. When correlated with intracranial electro encephalographic recordings, increased interictal α- 11 C-methyl-l t r y p t o phan uptake has been observed in epilep togenic tubers in approximately two thirds of TSC patients [12]. The precise mechanism under lying the increased α- 11 C-methyl-ltrypto phan uptake is not known but may be related to increased serotonin synthesis from an epileptogenic focus [13]. The α- 11 C- methyl-l-tryptophan tracer is currently not available at most institutions, limiting its clinical application. Magnetoencephalography/Magnetic Source Imaging y measuring the magnetic fields produced by the electric current flowing within neurons, spatially localized epileptiform data from magneto encephalo graphy can be registered to anatomic image inform ation from MRI to generate magnetic source images [14] (Fig. 11). The magnetic source images can be used in conjunction with PET/MRI fusion images to acquire additional information for identification of epileptogenic tubers [15] (Fig. 12). Conclusion dvances in neuroimaging are improving the diagnosis of TSC and the treatment of children with this condition. Multipletechnique imaging with MRI, PET/MRI fusion, and magnetoencephalography/magnetic source imaging plays an important role in the noninvasive localization of epi leptogenic tubers for possible surgical resection. References 1. Houser OW, Gomez MR. CT and MR imaging of intracranial tuberous sclerosis. J Dermatol 1992; 19: raffman H, ilaniuk LT, Naidich TP, et al. MR imaging of tuberous sclerosis: pathogenesis of this phakomatosis, use of gadopentetate dimeglumine, and literature review. Radiology 1992; 183: DiPaolo D, Zimmerman R. Solitary cortical tubers. m J Neuroradiol 1995; 16: Girard N, Zimmerman R, Schnur RE, Haselgrove J, Christensen K. Magnetization transfer in investigation of patients with tuberous sclerosis. Neuroradiology 1997; 39: Miyata H, Chiang C, Vinters HV. Insulin signaling pathways in cortical dysplasia and TSC-tubers: tissue microarray analysis. nn Neurol 2004; 56: Franz DN, Leonard J, Tudor C, et al. Rapamycin causes regression of astrocytomas in tuberous sclerosis nn Neurol 2006; 59: Griffiths PD, olton P, Verity C. White matter abnormalities in tuberous sclerosis cta Radiol 1998; 39: Chandra PS, Salamon N, Nguyen ST, et al. Infantile spasm-associated microencephaly in tuberous sclerosis complex and cortical dysplasia. Neurology 2007; 68: Curatolo P, ombardieri R, Verdecchia M, Seri S. Intractable seizures in tuberous sclerosis complex: JR:190, May 2008 W305
3 Kalantari and Salamon from molecular pathogenesis to rationale for treat brain apparent diffusion coefficient in tuberous 5: ment. J Child Neurol 2005; 20: sclerosis. Radiology 2004; 232: Makela JP, Forss N, Jaaskelainen J, Kirveskari E, 10. Chandra PS, Salamon N, Huang J, et al. FDG- 12. Sood S, Chugani HT. Functional neuroimaging in Korvenoja, Paetau R. Magnetoencephalography PET/MRI coregistration and diffusion-tensor im preoperative evaluation of children with drug-re in neurosurgery. Neurosurgery 2006; 59: aging distinguish epileptogenic tubers and cortex sistant epilepsy. Childs Nerv Syst 2006; 22: 15. Wu JY, Sutherling WW, Koh S, et al. Magnetic in patients with tuberous sclerosis complex: pre source imaging localizes epileptogenic zone in Downloaded from by on 12/22/17 from IP address Copyright RRS. For personal use only; all rights reserved liminary report. Epilepsia 2006; 47: Garaci FG, Floris R, ozzao, et al. Increased Fig. 1 4-year-old girl with tuberous sclerosis and, xial T1-weighted () and T2-weighted () MR images show T1 hypointensity (arrows, ) and T2 hyperintensity (arrows, ) in subcortical white matter of left frontal and right parietal lobes. Gray white matter differentiation is partially obliterated. Findings are characteristic of cortical and subcortical tubers. 13. Chugani HT, Chugani DC. Imaging of serotonin mechanisms in epilepsy. Epilepsy Curr 2005; children with tuberous sclerosis Neurology 2006; 66: Fig month-old boy with tuberous sclerosis and, xial FLIR MR images show subtle bilateral cortical and subcortical tubers (arrow) in right frontal () and left parietal () lobes. W306 JR:190, May 2008
4 Neuroimaging of Tuberous Sclerosis Downloaded from by on 12/22/17 from IP address Copyright RRS. For personal use only; all rights reserved Fig. 3 7-year-old boy with tuberous sclerosis xial T1-weighted MR image shows small subependymal nodule (arrow) projecting into lumen of right lateral ventricle. Fig. 5 9-year-old girl with tuberous sclerosis complex and partial complex seizures., Coronal contrast-enhanced T1-weighted image shows homogeneously enhancing multilobulated subependymal giant cell astrocytoma (black arrow) measuring 238 mm 2 in region of left foramen of Monro. Patient has undergone left temporal lobe resection (white arrow)., Coronal contrast-enhanced T1-weighted image obtained 3 months after initiation of oral rapamycin therapy shows size of subependymal giant cell astrocytoma (black arrow) has decreased to 126 mm 2. White arrow indicates site of left temporal lobe resection. Fig. 4 4-year-old girl with tuberous sclerosis and, xial unenhanced T1-weighted () and contrast-enhanced T1-weighted () MR images show enhancing subependymal nodule (black arrow) projecting into lumen of left lateral ventricle. Subependymal nodules, which contain more calcification, tend to become less enhanced, as in case of nodule (white arrow) located near left atrium. Fig. 6 8-year-old boy with tuberous sclerosis xial FLIR MR image shows cortical and subcortical tuber (black arrow) and radial migration line (white arrow). JR:190, May 2008 W307
5 Kalantari and Salamon Fig. 7 6-year-old girl with tuberous sclerosis and, Three-dimensional MRI reconstructions show total cerebral volume of 994 cm 3 () compared with 1,290 cm 3 in age-matched patient without tuberous sclerosis complex (). Downloaded from by on 12/22/17 from IP address Copyright RRS. For personal use only; all rights reserved Fig. 8 9-year-old boy with tuberous sclerosis and, xial 18 F-FDG PET () and PET/MRI fusion () images show multiple areas of hypometabolism corresponding to tubers (arrows). Fig month-old boy with tuberous sclerosis complex and intractable seizures., xial FLIR MR image shows cortical and subcortical tubers (arrows) in both temporal lobes., xial MRI/PET fusion image shows multiple areas of hypometabolism corresponding to tubers (white arrows). Tuber (red arrow) in right anterior temporal lobe shows disproportionately large area of hypometabolism compared with its size in, indicating zone is probably epileptogenic. C, xial T2-weighted MR image shows right temporal region after resection of epileptogenic focus (arrow). Patient became seizure-free. C W308 JR:190, May 2008
6 Neuroimaging of Tuberous Sclerosis Downloaded from by on 12/22/17 from IP address Copyright RRS. For personal use only; all rights reserved Fig year-old girl with tuberous sclerosis complex and seizures., xial T2-weighted image shows left cerebellar tuber with typical wedge-shaped configuration (arrow)., xial MRI/PET fusion image shows area of hypometabolism approximately equal in size to cerebellar tuber (arrow) in keeping with fact that cerebellar tubers are rarely epileptogenic. Fig. 11 Photograph shows magnetoencephalography machine. (Courtesy of MEG International Services Ltd.) Fig year-old boy with tuberous sclerosis complex and intractable seizures., xial FLIR MR image shows multiple bilateral cortical and subcortical tubers (arrows)., xial PET/MRI fusion image shows multiple areas of hypometabolism (red arrows) corresponding to tubers. Tuber in left posterior temporal lobe shows disproportionate area hypometabolism (orange arrow) compared with size in, indicating zone is probably epileptogenic. C, xial T1-weighted magnetic source image shows epileptiform activity (yellow lines) arising from location of tuber that exhibits hypometabolism in. C JR:190, May 2008 W309
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