Bottom-of-Sulcus Dysplasia: Imaging Features
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1 Neuroradiology/Head and Neck Imaging Original Research Hofman et al. ottom-of-sulcus Dysplasia Neuroradiology/Head and Neck Imaging Original Research Paul. M. Hofman 1,2,3 Gregory J. Fitt 4. Simon Harvey 5 Ruben I. Kuzniecky 6 Graeme Jackson 1,7,8 Hofman PM, Fitt G, Harvey S, Kuzniecky RI, Jackson G Keywords: brain, cortical dysplasia, epilepsy, focal cortical malformation, MRI DOI: /JR Received February 9, 2010; accepted after revision September 14, rain Research Institute, Florey Neuroscience Institutes, Heidelberg West, Victoria, ustralia. 2 Epilepsy Centre Kempenhaeghe, Heeze, The Netherlands. 3 Department of Radiology, Maastricht University Medical Center, PO ox 5800, 6202 Z, Maastricht, The Netherlands. ddress correspondence to P.. M. Hofman (paul.hofman@mumc.nl). 4 Department of Radiology, ustin Hospital, Heidelberg, Victoria, ustralia. 5 Children s Epilepsy Program, Children s Neuroscience Centre, Royal Children s Hospital, Parkville, Victoria, ustralia. 6 Department of Neurology, New York University Langone Medical Center, New York, NY. 7 Department of Neurology, ustin Hospital, Heidelberg, Victoria, ustralia. 8 Department of Medicine, The University of Melbourne, Royal Melbourne Hospital, Melbourne, Victoria, ustralia. JR 2011; 196: X/11/ merican Roentgen Ray Society ottom-of-sulcus Dysplasia: Imaging Features OJECTIVE. Dysplasia at the bottom of a sulcus is a subtle but distinct malformation of cortical development relevant to epilepsy. The purpose of this study was to review the imaging features important to the clinical diagnosis of this lesion. MTERILS ND METHODS. ll cases recognized as typical bottom-of-sulcus dysplasia in our comprehensive epilepsy program over the period were included in the study. RESULTS. In the 20 cases recognized, three major features were identified: cortical thickening at the bottom of a sulcus; a funnel-shaped extension of the lesion toward the ventricular surface, commonly with abnormal signal intensity; and an abnormal gyral pattern related to the bottom-of-sulcus dysplasia, sometimes with a puckered appearance. The pathologic features of the resected lesions were typical of focal cortical dysplasia. CONCLUSION. ottom-of-sulcus dysplasia is a distinctive malformation of cortical development that can be diagnosed on the basis of imaging characteristics. Reliable identification of this type of malformation of cortical development is difficult but clinically important because the lesion appears to be highly epileptogenic and because the prognosis for seizure control is excellent after focal resection. I n the 2005 revision of the arkovich classification [1], a new type of malformation of cortical development was proposed: bottom-of-sulcus dysplasia. This type of focal cortical dysplasia is classified in the group of malformations caused by abnormal proliferation: focal cortical dysplasia with balloon cells. This type of dysplasia has typically not been treated as a distinct entity in clinical practice, although it may be an important cause of intractable epilepsy [2]. It has been our clinical experience that although these lesions are often difficult to detect or are not detected at routine imaging, it is critical to recognize them in the context of epilepsy surgery. ottom-of-sulcus dysplasia is of clinical importance because it is often found only after detailed imaging and diagnostic review in the care of patients with intractable epilepsy. This type of dysplasia also appears to be a highly epileptogenic lesion, and the prognosis of seizure control after focal resection is excellent. Knowledge of the imaging features is important for recognition and detection of this malformation of cortical development. We describe our clinical experi- ence of the imaging features of this entity in the context of intractable epilepsy and discuss the pathogenesis of the lesions. Materials and Methods ll patients with typical bottom-of-sulcus dysplasia according the classification system of arkovich et al. [3] over the period were included in the study. ll patients had focal seizures and intractable epilepsy being investigated in a comprehensive epilepsy surgery program. Thirteen patients were imaged with a 3-T system. The protocol included a high-resolution sagittal T1- weighted sequence (TR/TE, 8/4; alpha, 8 ; turbo factor, 240; number of signals acquired, 1; field of view, mm; slice thickness, 1 mm), axial turbo FLIR images (11,000/125; inversion recovery time, 2800 ms; echo train length, 25; number of signals acquired, 1; field of view, mm; slice thickness, 2 mm; gap, 0 mm), coronal turbo FLIR images (11,000/125; inversion time, 2800 ms; echo train length, 27; number of signals acquired, 1; field of view, mm; slice thickness, 4.5 mm; gap, 0.5 mm), a coronal inversion recovery sequence (8000/10; inversion recovery time, 400 ms; echo train length, 10; number of signals acquired, 1; field of view, mm; slice JR:196, pril
2 Hofman et al. thickness, 2 mm; gap, 0 mm), and axial T2-weighted images (3000/80; echo train length, 15; number of signals acquired, 1; field of view, mm; slice thickness, 5 mm; gap, 0.5 mm). Seven patients were imaged with a 1.5-T MRI system. This protocol included a coronal turbo gradient T1-weighted sequence (1530/3; alpha, 8 ; number of signals acquired, 1; field of view, mm; slice thickness, 1.5 mm), a coronal dual-echo T2-weighted sequence (3620/15; inversion recovery time, 88; echo train length, 7; number of signals acquired, 2; field of view, mm; slice thickness, 2.4 mm; gap, 1.4 mm), a coronal inversion recovery T1-weighted sequence (6600/74; inversion time, 350 ms; echo train length, 11; number of signals acquired, 1; field of view, ; slice thickness, 4.5 mm; gap, 0.8 mm), and an axial FLIR sequence (9000/111; inversion recovery time, 2500 ms; echo train length, 17; number of signals acquired, 1; field of view, mm; slice thickness, 5 mm; gap, 2 mm). For the 12 patients with available digital data, the 3D volume images were processed at a workstation (Intel processor; Mac OS [pple]; rainsight software version 1.5, Rogue Research). The procedure has been described in detail elsewhere [4]. In brief, in 15 positions on the coronal reformat, the contour of the brain was manually outlined on top of the cortical gyri, and a curved brain surface was generated automatically. The depth of the reconstructed surface was selected for optimal visualization of the gyral pattern. The MR images were reviewed by at least three specialists experienced in the imaging of epilepsy patients, and the patients cases were reviewed at consensus clinical meetings. The study was approved by the human ethics committee at our institution, and HIP compliance was followed. Results We identified 20 cases in which the features of bottom-of-sulcus dysplasia were clear. In the cortex, as with other forms of cortical dysplasia, we found blurring of the gray-white matter junction and focal cortical thickening. This finding was seen in all patients, mostly at the bottom of the sulcus. On T2-weighted images, we also found focal increased signal intensity involving the gray-white matter junction and subcortical white matter and to a lesser degree the cortex. With respect to the tail, a rather characteristic feature, present in 12 of the cases of bottom-of-sulcus dysplasia, was a funnelshaped structure directed at the ependymal surface (Fig. 1). In three patients, the area of abnormal signal intensity did not extend to the ventricular surface. Three patients did not have adequate images. With optimal imaging, this feature may be present in all cases, but partial volume effects and signal-to-noise limitations can make it difficult to see even if present. This finding can be differentiated from normal transcortical veins on the basis of its signal characteristics and tapering shape (Figs. 1 and 2). With respect to abnormal gyral pattern, in seven cases the gyral pattern also was deranged, and local widening of the subarachnoid space was appreciated (Fig. 3). In eight cases, digital data were not available. Two patients underwent highly focal resection based on recognition of the dysplasia. One of these cases is illustrated in Figure 4. The two resection specimens were analyzed with standard histologic and immunohistologic reactions and had the typical histologic pattern of cortical dysplasia: disrupted cortical lamination, abnormal large neurons with abundant eosinophilic cytoplasm, and balloon cells. n occasional immature neuron was found, as were microcalcifications and subpial gliosis. The outcome was excellent with no seizures and no auras after surgery. s of this writing, the patient in Figure 4 did not need medications. Discussion Diagnostic Issues We report our experience with bottom-ofsulcus dysplasia in a comprehensive epilepsy program. The features that allow this diagnosis are abnormally thick bottom of the sulcus with a tail and change in signal intensity, often related to an overlying gyral pattern abnormality. We have become increasingly sensitive to this lesion but cannot be sure how many of these lesions were not detected in our lesion-negative cases. ottom-ofsulcus dysplasia poses a diagnostic challenge because of the small size and the location of the lesion. The lesion can be subtle and easily missed at initial examination of the images. Diagnosis is greatly aided when the images have a good signal-to-noise ratio, so that the blurring of the gray-white junction at the bottom of the sulcus can be properly appreciated, as can the increased signal intensity of the cortex and underlying white matter on T2- weighted images. Efforts to acquire thin slices and isotropic voxels to avoid partial volume effects can be counterproductive, however, if the signal-to-noise ratio decreases, because the signal change in the subcortical white matter and cortex can be subtle. In these instances the advantage of increased spatial resolution is outweighed by the decrease in contrast resolution, and lesions can become invisible. The optimal clinical protocol depends on the specifications available on the MRI system. We have optimized our protocol for our MRI system, but the most advanced clinical protocol would include thin-slice ( mm) 3D T1-weighted and 3D FLIR sequences combined with an axial T2-weighted sequence with 3- to 5-mm slice thickness. n additional gradient-echo T2- or susceptibility-weighted sequence and a thin-slice (2 mm) diffusionweighted sequence also should be added. This Fig year-old man with focal epilepsy. Example of typical bottom-of-sulcus dysplasia in left superior frontal sulcus., Coronal inversion recovery image shows focal thickening of cortex (arrow), widening of sulcus (asterisk), and area of funnel-shaped intermediate signal intensity extending from depths of sulcus to ventricular surface (arrowhead)., Coronal FLIR image shows same characteristics as (arrow, asterisk, and arrowhead). C, xial FLIR image shows focal increased signal intensity in lesion, as often is present in lesions with balloon cells. C 882 JR:196, pril 2011
3 ottom-of-sulcus Dysplasia Fig. 2 Differential diagnosis of bottom-of-sulcus dysplasia., 26-year-old man with subcortical white matter lesion who was healthy control in another study. MR image shows cortex has normal signal intensity, white matter lesion does not have broad base toward cortex, and there is no extension toward ventricular surface. White matter lesion does not have funnel shape characteristic of bottom-of-sulcus dysplasia., 30-year-old woman with seizures. MR image shows transmantle veins are pencil-thin structures of high signal intensity with linear shape clearly different from funnel-shaped extensions of bottomof-sulcus dysplasia. protocol requires a 32-channel head coil on a 3-T MRI system. dditional techniques, such as arterial spin labeling and diffusion tensor imaging also may prove valuable, and computer-assisted diagnosis of focal cortical dysplasia can be a valuable technique [5 10]. Once identified, bottom-of-sulcus dysplasia is a readily recognizable archetype of focal cortical dysplasia that has specific imaging features. The pathologic features of resected specimens are identical to those of any focal cortical dysplasia. The differential diagnosis includes normal variation with a distinct transmantle vein and subcortical white matter lesions, which can be difficult to differentiate (Fig. 2). Clinical localization of seizure onset often is useful for guiding detailed radiologic assessment of a brain region. Clinically Important Epileptogenic Lesion Detection of bottom-of-sulcus dysplasia is critical because this lesion appears to be at least as epileptogenic as other forms of focal cortical dysplasia, and many patients with bottom-of-sulcus dysplasia have intractable seizures. Furthermore, postsurgical outcome appears to be excellent after complete resection [11], as reflected in two of our cases. It appears that the disturbance is highly focal and the surrounding brain is not affected in a regional manner, as it can be in other developmental disorders. Previous reports [4, 5, 12 16] have described examples of bottom-of-sulcus dysplasia without specifically treating these dysplasias as a subtype. In one study [11] it was found that 21% of focal cortical dysplastic lesions were located at the bottom of a sulcus. In another study [2], 68% of all focal cortical dysplastic lesions were located in the depth of a sulcus. Differentiating ottom-of-sulcus Dysplasia From Transmantle Dysplasia The extent and the localization of bottom-of-sulcus dysplasia differentiates it from Fig. 3 9-year-old girl with focal epilepsy and gyral abnormality., Cortical reconstruction image shows abnormal left parietal gyral pattern and multiple converging sulci (arrow)., Cortical reconstruction image shows normal gyral pattern of right hemisphere. C, Coronal FLIR image shows increased signal intensity at bottom of sulcus and blurring of gray-white matter junction and thickening of cortex. C JR:196, pril
4 Hofman et al. Fig year-old man with focal seizures. Preoperative MR image (left) shows left frontal bottom-of-sulcus dysplasia (arrow) extends from central sulcus with blurring of gray-white matter junction. fter focal resection (right), patient was seizure free. transmantle dysplasia and other forms of focal cortical dysplasia. In the initial description of transmantle dysplasia [13], bottom-of-sulcus dysplasia and transmantle dysplasia were not differentiated. s recognized in the 2005 classification [1], it has become clear that these entities are different because bottom-ofsulcus dysplasia has different imaging characteristics, poses a specific diagnostic problem in detection, and possibly has a different embryologic basis. Fig. 5 Schematic generated with morphogenetic model shows development of convolutions:, initial condition with smooth surface;, expanding surface with radial constraints resulting in convolutions; C, focal cortical dysplasia with mechanical restriction resulting in dysplasia at bottom of sulcus. Timing of bnormality The distinctive imaging features of bottom-of-sulcus dysplasia in each case suggest a common mechanism affecting cortical development. The bulk of neurons form before 20 weeks gestation. From the germinal matrix, neurons migrate to the cerebral surface, facilitated by radial glial cells. In the human brain, neuronal migration is complete between 20 and 24 weeks gestation [17, 18]. poptosis peaks between 22 and 29 weeks gestational age and is linked to differentiation and synaptogenesis [19]. The abnormal cell types of bottom-of-sulcus dysplasia and the distinctive tail suggest that it results from a combination of abnormal migration and abnormal apoptosis and therefore may be related to a highly focal process that occurs at weeks gestation, when migration and apoptosis are both active. The observation that the histopathologic mechanism of bottom-of-sulcus dysplasia is similar to that of other forms of focal cortical dysplasia is probably a reflection of the fact the histopathologic mechanism of bottom-of-sulcus dysplasia is not described separately. It is likely that many reports on the histopathologic features of focal cortical dysplasia include bottom-of-sulcus dysplasia. Examples are the reports by Urbach et al. [11], Tassi et al. [20], and Sisodiya et al. [21]. bnormal Gyral Pattern t the end of the migration phase, weeks gestational age, the cortical surface is predominantly smooth. During the second half of gestation, secondary and tertiary fissures develop [22]. etween 29 weeks gestation and term, cortical gray matter volume increases from approximately 60 to 160 ml owing to glial cell migration, neuronal differentiation, and organizational changes in the developing cortex [23]. In a model based on the mechanical properties of the cerebral cortex (Fig. 5), the mechanical characteristics of the axial and glial bundles that cause radial pulling have been found to result in the development of convolutions [24, 25]. The formation of a normal gyral pattern depends at least partially on even volumetric expansion of the cerebral cortex, which can be focally abnormal in bottom-of-sulcus dysplasia. This would mean that the abnormal glial and axial bundles tether the convoluting cortex and maintain the focal cortical dysplasia at the bottom of a sulcus during subsequent brain growth. The imagery is that bottom-of-sulcus dysplasia has tethered the gyri, causing puckering of the sulcal pattern to form a stellate gyral complex with the bottom-of-sulcus dysplasia at the center (arrow, Figure 3). It is also known that the sulcal pattern can be subtly abnormal in many cases of lesionnegative epilepsy, and this finding may be a marker of focal epileptogenesis. Some of these lesions may be undetected or be an extremely subtle bottom-of-sulcus dysplasia. ottom-of-sulcus dysplasia is an archetype of a malformation of cortical development that can be diagnosed on the basis of its characteristic MRI features. Knowledge of the imaging characteristics and acquisition of highquality images are important for its detection because the lesions are often subtle and not seen at initial routine evaluation, particularly on images that have a poor signal-to-noise ratio. The correct classification and reliable detection of this lesion in prospective studies will enhance our knowledge of its specific neuropathologic and clinical features. References 1. arkovich J, Kuzniecky RI, Jackson GD, Guerrini R, Dobyns W. developmental and genetic classification for malformations of cortical development. Neurology 2005; 65: esson P, ndermann F, Dubeau F, ernasconi. Small focal cortical dysplasia lesions are located at the bottom of a deep sulcus. rain 2008; 131(pt 12): arkovich J, Kuzniecky RI, Jackson GD, Guerrini R, Dobyns W. Classification system for 884 JR:196, pril 2011
5 ottom-of-sulcus Dysplasia malformations of cortical development: update 10. Focke NK, onelli S, Yogarajah M, Scott C, aging surgical epilepsy in children. Childs Nerv Neurology 2001; 57: Symms MR, Duncan JS. utomated normalized Syst 2006; 22: astos C, Comeau RM, ndermann F, et al. Di- FLIR imaging in MRI-negative patients with re- 17. de Graaf-Peters V, Hadders-lgra M. Ontogeny agnosis of subtle focal dysplastic lesions: curvilin- fractory focal epilepsy. Epilepsia 2009; 50:1484 of the human central nervous system: what is hap- ear reformatting from three-dimensional magnetic 1490 pening when? Early Hum Dev 2006; 82: resonance imaging. nn Neurol 1999; 46: Focke NK, Symms MR, urdett JL, Duncan JS. Voxel-based analysis of whole brain FLIR at 3T detects focal cortical dysplasia. Epilepsia 2008; 49: Kassubek J, Huppertz H, Spreer J, Schulze-onhage. Detection and localization of focal cortical dysplasia by voxel-based 3-D MRI analysis. Epilepsia 2002; 43: Huppertz HJ, Kurthen M, Kassubek J. Voxelbased 3D MRI analysis for the detection of epileptogenic lesions at single subject level. Epilepsia 2009; 50: ntel S, Collins DL, ernasconi N, et al. utomated detection of focal cortical dysplasia lesions using computational models of their MRI characteristics and texture analysis. Neuroimage 2003; 19: Colliot O, ernasconi N, Khalili N, ntel S, Naessens V, ernasconi. Individual voxelbased analysis of gray matter in focal cortical dysplasia. Neuroimage 2006; 29: Urbach H, Scheffler, Heinrichsmeier T, et al. Focal cortical dysplasia of Taylor s balloon cell type: a clinicopathological entity with characteristic neuroimaging and histopathological features, and favorable postsurgical outcome. Epilepsia 2002; 43: Colombo N, Tassi L, Galli C, et al. Focal cortical dysplasias: MR imaging, histopathologic, and clinical correlations in surgically treated patients with epilepsy. JNR 2003; 24: arkovich J, Kuzniecky RI, ollen W, Grant PE. Focal transmantle dysplasia: a specific malformation of cortical development. Neurology 1997; 49: Chassoux F. Stereo-EEG: the Sainte-nne experience in focal cortical dysplasias. Epileptic Disord 2003; 5(suppl 2):S95 S Matsuda K, Mihara T, Tottori T, et al. Neuroradiologic findings in focal cortical dysplasia: histologic correlation with surgically resected specimens. Epilepsia 2001; 42(suppl 6): Raybaud C, Shroff M, Rutka JT, Chuang SH. Im- 18. Kriegstein R. Constructing circuits: neurogenesis and migration in the developing neocortex. Epilepsia 2005; 46(suppl 7): Rakic S, Zecevic N. Programmed cell death in the developing human telencephalon. Eur J Neurosci 2000; 12: Tassi L, Colombo N, Garbelli R, et al. Focal cortical dysplasia: neuropathological subtypes, EEG, neuroimaging and surgical outcome. rain 2002; 125: Sisodiya SM, Fauser S, Cross JH, Thom M. Focal cortical dysplasia type II: biological features and clinical perspectives. Lancet Neurol 2009; 8: Chi JG, Dooling EG, Gilles FH. Gyral development of the human brain. nn Neurol 1977; 1: Volpe JJ. Neurology of the newborn. Philadelphia, P: W Saunders, Caviness VS Jr. Mechanical model of brain convolutional development. Science 1975; 189: Toro R, urnod Y. morphogenetic model for the development of cortical convolutions. Cereb Cortex 2005; 15: JR:196, pril
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