Neuroradiology(1990) 32:43%448
Neuro radiology .
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.
.
.
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9 Springer-Verlag1990
MR imaging of brain surface structures: surface anatomy scanning (SAS) K. Katada Department of Radiology,Fujita Health UniversityHospital,Toyoake,Japan
Summary. MR imaging technique that permits direct and non-invasive visualization of brain surface structures (Surface Anatomy Scanning, SAS) was developed using the combination of long TE, long TR spin echo sequence and thick slice. Clinical trials in 67 patients with SAS showed excellent visualization of the sulci and the gyri on the lateral, occipital, frontal and parietal surfaces of the brain together with cortical and subcortical lesions. The results indicate that the SAS is useful for the localization of cortical and subcortical pathology, for the diagnosis of anomalous gyral patterns, and for surgical planning. Key words: Cerebral cortex - MR imaging - Migration
totally suppressed. As the brain surface is covered by subarachnoid space, it is possible to create a "relief" picture of the brain surface utilizing the CSF as natural "contrast medium" (Fig. 1). A five to eight centimeter thick slice is used to cover sufficient area of the cerebral cortex to create a "planar" image of the brain surface [5]. The use of a surface coil is helpful for further enhancement of the signal intensity of subarachnoid CSF, and it is also useful to avoid the overlap of the signals from the ventricles and other deep seated structures. In obtaining a parietal view, the surface coil can not be applied because of the limitation of RF coil direction, so that the conventional head coil is used for this purpose.
anomaly - Surgical planning
Scanning parameters The identification of cerebral surface anatomy, including cortical sulci and gyri in relation to intracranial lesion(s) has special clinical importance, and it has been one of the main interests of neuroradiology [1-4]. Recent developments in CT and MRI have made possible the non-invasive visualization of sulci and gyri as tom0graphic images [3, 4]. However, these imaging techniques are not always effective in precise localization of the lesion because of the interruption of the sulci and gyri by the tomographic section. ~. Until now, no available imaging modality permitted non-invasive and direct visualization of the brain surface anatomy. The PUrpose of this study is to introduce MR surface anatomy scanning (SAS), a new application of MR imaging technique for non-invasive visualization of brain surface structures [5], and to evaluate the clinical significance of this technique.
Method The basic concept Under the long TR and extremely long TE (more than 200 ms) spin echo sequence, the signal intensity of the cerebrospinal fluid (CSF) has been strongly enhanced, while the signals from the skin, subcutaneous tissuesl orbits, diploe of the skull and the brain itself have been
The MR scanner used in this study was a Toshiba MRT 50A - 0.5 T superconductive magnet system. The standard scanning parameters used in this method were, TR = 2000 ms, TE = 250 ms a 256 • 256 image matrix, one or two excitation(s) and 2DFT image reconstruction. Standard slice thickness was 8 cm, however, 5 or 6 cm slice was selected for small sized object. Scanning time was
il!: .... 1
SUBARACHNOID C S F
Fig.L Basicconceptof SAS. LongTE spin echo sequenceenhances the signalintensitiesof subarachnoidCSE Thicknessof the CSFlayer in the corticalsulci (,4) and overthe corticalconvolutions(B)
44(I
Fig.2. a Original SAS images of a normal volunteer (34 Y. O. male). Left lateral view. Sulci and fissures are demonstrated as bright lines owing to the long T2 of the cerebrospinal fluid, b SAS image processed by gray scale reversal and 2 D filtering. Delineation of the sulci and gyri is improved
Fig.3. Normal cortical gyriand sulcidemonstratedby SAS. (48 Y. O. male, left lateral view). SFG Superior frontal gyms; M F G Middle frontal gyms; Inferior frontal gyms: O R Pars orbitalis, TR Pars triangularis, O P Pars opercularis; P R E C G Precentral gyms; P O S T C G Postcentral gyms; S M G Supramarginal gyrus; A N G Angular gyms; S P L Superior parietal lobule; S T G Superior temporal gyms; M T G Middle temporal gyms: I T G Inferior temporal gyrus; S S L Superior semicircular lobule; I S L Inferior semicircular lobule; SFS Superior frontal sulcus; S F Sylvian fissure; (AH) Anterior horizontal ramus; (AA) Anterior ascending ramus; (P) Posterior ramus; P R E C S Precentral sulcus; CS Central sulcus; P O S T C S Postcentral sulcus; I P F Interparietal fissure; S T S Superior temporal sutcus; H F Great horizontal fissure; VTVein of Trolard; VR Vein of Roland; E A M External auditory meatus
8.5 minutes for i excitation, and 17 min for 2 excitations. O n the acquired images, post-processing including gray scale reversal and 2 D image filtering were applied to achieve b e t t e r identification of the sulci (Fig. 2 a, b).
Materials O v e r the last 1 4 - m o n t h period, 67 cases (85 images) were e x a m i n e d b y SAS. These included 6 n o r m a l volunteers, 6 n o r m a l cases, 16 intracranial neoplasms, 9 cerebral infarc-
441 tions, 5 intracranial vascular malformations, 5 with focal brain damage, 4 migration anomalies and 16 others. In two cases (one normal volunteer and a case of arteriovenous malformation), pairs of SAS images were acquired to obtain a stereographic view. The imaging direction was lateral in 53 cases, frontal in 3, frontal oblique in 6, posterior in 9 and parietal in 14. In 5 patients, SAS imaging was performed for the purpose of surgical planning. After planning the site of scalp incision by the neurosurgeon, it was marked by a water filled
plastic tube and the SAS image was obtained to estimate the relation between the lesion and the surgical field.
Results G o o d quality brain surface images were obtained in 76 of 85 images. In two cases with brain tumors, the cortical sulci were obliterated due to severe mass effect, resulting in poor visualization of the sulci on SAS images. In one case, the signal from the cortical sulci was masked by the signal from epidural fluid collection. Severe motion artifacts were seen in 3 cases. The overlap of the signals from lateral ventricle was seen in 2 patients. It was difficult to identify sulci and gyri on a lateral SAS image of a 4 years old child with an arachnoid cyst.
N o r m a l cases
In 12 normal volunteers and normal clinical cases, major fissures and sulci were clearly visualized, and identification of cortical gyri was possible (Figs.2, 3). The SAS was sensitive enough to visualize the narrow sulci of the young volunteer aged 21 whose CT failed to show the sulci. On the lateral view, the anterior horizontal ramus, anterior ascending ramus and posterior ramus of the sylvian fissure, as well as the central, precentral and postcentral sulci,
Fig.4. Parietal view of a normal volunteer (41 Y. O., male). IHF Interhemispheric fissure; M Marginal portion of cingulate sulcus Fig.5a, b. Posterior views of a normal volunteer (40 Y.O. male). Stereogram. Interhemispheric fissure, great horizontal fissures (arrows) and left inferior hemispheric veins (arrowheads) are demonstrated
442
Fig.6 a, b. Left temporal
astrocytoma (grade III). a Axial T 1-weighted image with Gd-DTPA injection, b SAS image demonstrates the infra-sylvian location of the tumor. The sylvian fissure is elevated and deformed by the tumor
Fig.7. Subcortical hematomain the left precentral gyrus. Lateral SAS shows the location of hematoma and the swelling of the motor cortex were visualized (Fig. 3). The major cortical veins including vein of Roland and vein of Trolard were also identified. Additionally, the bulbus oculi and external auditory meatus were clearly demonstrated. On the parietal view, motor cortex and sensory cortex of both hemispheres were clearly identified together with the wide area of neighboring gyri (Fig. 4). On the posterior view, the great horizontal fissure, the interhemispheric fissure and the cerebello-cerebral interface were easily identifiable (Fig. 5 a, b).
Lesion localization Among 55 cases with intracranial pathology, SAS was effective for accurate lesion localization in 37 cases. In a case with left temporal astrocytoma, SAS clearly showed infra-sylvian location of the tumor (Fig. 6a, b). SAS was effective in evaluating the relation between the lesions and the motor cortex (Figs. 7, 8). In patients with infarction of the middle cerebral artery territory, the extent of the infarcted area was well visualized by SAS, which made
443 sult, precise site of the craniotomy was determined, and surgical damage to the motor cortex was successfully avoided. The magnified SAS image showed excellent correlation with the surgical view (Fig. 13 b). In a young patient aged 10 with left frontal low grade astrocytoma, SAS was useful to correct the planned scalp incision (Fig. 14 a-c).
Discussion
Fig.8. Meningioma in the high parietal region. On parietal SAS image, right precentral and postcentral gyrus cannot be identified due to the compressonof the large parasagittal meningioma (arrow-
heads) the estimation of affected branches of the middle cerebral artery possible (Fig. 9 a, b). SAS was also useful in the precise localization of the focal cortical damage (Fig. 10). In 2 cases with severe edema and mass effect, SAS failed to show the sulci.
Diagnosis of abnormal gyralpattern In 6 patients with suspected migration anomaly, abnormal gyral patterns were detected by SAS in 5. The flat gyri were demonstrated by lateral SAS images in a case of pacyhgyria (Fig. 11 a, b). In 3 cases with unilateral schizencephaly, characteristic pattern of anomalous clefts around the sylvian region were demonstrated (Fig. 12). A hypoplastic postcentral gyrus was detected in one patient.
Surgicalplanning The preoperative localisation of the scalp incision was performed in 5 patients with intracranial pathology using SAS and a water filled plastic tube as a marker. In a case of thrombosed arteriovenous malformation in the right postcentral gyrus, parietal SAS image demonstrated the precise localization of the lesion, and the relation between the lesion and the scalp markers indicating the planned site of incision was well estimated (Fig. 13 a). Based on this re-
As the cerebral cortex has highly specified functional localization, the identification of the cortical gyri on radiological images has special clinical importance, and it has been one of the main objects in neuroradiological diagnosis [14]. Pneumoencephalography (PEG) can demonstrate the cortical sulci [1] but it is not consistent especially when the amount of injected gas is small. Detailed analysis of a cerebral angiogram also aids the localization of the gyri and sulci [2]. However, both PEG and angiography are invasive procedures and cause pain and risk to the patient. The introduction of CT and MRI had improved this surface localization dramatically [3, 4, 6, 7]. The sulci and gyri over the high parietal region are well demonstrated on axial CT and MRI. MRI parasagittal sections also give an excellent orientation of the sulci and gyri of the medial surface of the cerebrum. However, with respect to the visualization of the lateral surface of the brain, CT and MRI do not always give good results. This is due to the interruption of the sulci and gyri by the tomographic slice, making it difficult to identify the gyrus as a continuous cortical "strip". And the major part of the effort in CT interpretation of cerebral gyri is to convert the anatomical map of the cerebral cortex from the tomographic sections [3, 4]. The technique proposed in this paper (SAS) is a noninvasive and a practical method capable of direct visualization of the brain surface structures [5]. With a long TE spin echo sequence, the signals from the brain, diploe, and the subcutaneous tissue have almost completely decayed, and the images, therefore, primarily display CSF which has the longest T2. As the brain surface is covered by CSF within the subarachnoid space, the signals from deep sulci and fissures are integrated and intensely opacifled, while the cortical convolutions, where the layer of CSF is thin, are only slightly opacified. Thus, the CSF is utilized as a physiological contrast medium to create a "relief picture" of the brain surface (Fig. 2). At the same time, as the signals from the skin, subcutaneous tissue, cortical bone and diploe of the skull are negligible at this pulse sequence, so it is possible for us to "look through" the brain surface from the outside the skull with the aid of the surface coil and a thick slice. Although the slicing gradients are employed in the imaging processes, the acquired images are considered to be identical to the planar images. On the original image of the SAS, the cortical sulci were demonstrated as bright lines on the brain surface, representing high signal intensity from CSF owing to the Long TE, Long TR spin echo sequence (Fig. 2 a). Several
444
Fig. 9 a, b. Cerebral infarction in the left middle cerebral artery territory, a Axial T2-weighted image, b SAS image, left lateral view demonstrates the extent of the infarction. Note that the posterior part of the superior and middle temporal gyrus as well as the inferior portion of the motor cortex are involved by the lesion, while the pars triangularis of the inferior frontal gyrus and the inferior parietal lobule are spared
Fig.10. Focal epilepsy. Alateral SAS image shows focal cortical damage in the left middle temporal gyrus post processing techniques were applied to improve the visualization of the sulci. The reversed image, which m a k e s the sulci dark in appearance, greatly improved the delineation. Two dimensional filtering was applied in order to enhance the gyral edges (Fig. 2b). Clinical trials with SAS showed excellent results in the demonstration of cortical sulci and gyri. Most of the sulci and fissures of the brain surface can be clearly visualized. On the lateral view, three rami of the sylvian fissure (anterior horizontal, anterior ascending and posterior ramus) were constantly identified (Figs. 2, 3), which is often difficult to identify on conventional CT or MRI. This was con-
sidered to have certain advantages in the localization of Broca's area. Differentiation between the anterior ascending ramus of the sylvian fissure and the lower part of the precentral sulcus was readily possible with SAS, though occasionally difficult on axial CT and M R I images. Also the precise localization of the supramarginal gyrus and angular gyrus are often difficult on conventional CT and M R I . SAS has significant advantages in the localization of these lower parietal gyri because SAS usually demonstrates the ascending ramus of the superior t e m p o r a l sulcus as well as the ascending part of the posterior ramus of the sylvian fissure.
445 For the parietal view, SAS offers a much wider field of view than conventional CT and MRI, and is helpful in improving the orientation (Fig. 4). On the posterior view, the interhemispheric fissure, interparietal fissure and other occipital sulci were easily identifiable (Fig. 5). In the cerebellum, the great horizontal fissure separating the superior and inferior semicircular lobule was identified consistently both on the lateral view and posterior view. Although anatomical variations are occasionally present, SAS is considered to improve the interpretation of these cortical structures in clinical practice. It was an unexpected favorable result that SAS can also visualize the major cortical veins - veins of Trolard,
veins of Roland, superficial middle cerebral vein and others (Figs. 2, 3). These veins on the SAS images may give the neurosurgeons an excellent orientation of the operative field prior to craniotomy. The cortical branches of the cerebral arteries were not identifiable on the SAS images. In a case of arteriovenous malformation, the nidus together with dilated draining veins were demonstrated. Since the surface coil could not totally eliminate the signals from deep structures, various cortical and subcortical lesions were demonstrated on the SAS images, so that the precise localization of the lesion was possible. Excellent visualization of normal and abnormal cortical pattern by SAS indicates that it can be a powerful modality in the diagnosis of migration anomaly (Figs. 11, 12). Preoperative assessment of surgical field is an important subject for neurosurgeons, and, so far, a number of modalities including plain skull radiographs, PEG, cerebral angiography, ultrasound, CT [6-11] and M R I [12] have been used for this purpose. SAS can demonstrate not only the lesion itself, but also the major cortical veins as well as the detailed pattern of the cortical sulci and gyri. Simultaneously, it can also show the planned lines of the scalp incisions by the application of water filled plastic tubes (Figs. 13c, 14). Thus, the exact relation between the lesion, cerebral cortex and the site of skin incision can be visualized on a single image, which makes accurate planning of the surgical approach possible. This SAS is thought to have higher clinical potential than three dimensional surface reconstruction images derived
Fig. 12. Unilateral schizencephaly.Lateral SAS image shows characteristic clefts (arrows) in right premotor area and the abnormal pattern of the adjacent gyri
Fig.lla, b. Pachygyria. a T 1-weighted image, b Lateral SAS image demonstrates the flat gyri neighboring the sylvian fissure. The anterior ascending ramus and anterior horizontal ramus of the sylvianfissure are absent
446 from multiple CT and MRI sections (3 D-CT, 3 D-MRI) [13, 14], the other technique which can demonstrate gyral patterns. In 3 D - C T or 3 D-MRI, it is essential to extract the outline of the brain prior to the reconstruction, which usually requires a manual procedure. In addition, to achieve similar results to those of SAS, one has to extract the outline of the subcortical lesion as well as the site of the skin incision, and to synthesize these three factors in a single image. These are time consuming processes and not possible to apply for every surgical patient in daily clinical practice, which is feasible with SAS. There are several limitations in the diagnostic capabilities of SAS. As with conventional MRI, it is contraindicated for patients with intracranial surgical clips or cardiac pacemakers. Although SAS can tolerate a moderate degree of mass effect, a severe mass effect caused by the intracranial lesions may totally obliterate the sulci, and eliminate the CSF within them, resulting in their poor visualization. SAS was sensitive enough to visualize the sulci of a young patient aged 10, but it failed to show the sulci of a 4 year old pediatric patient, whose sulci were too narrow to visualize. A n o t h e r pitfall of SAS is diffuse accumulation of the fluid on the surface of the brain. The strong signal intensity from the subdural, epidural or subcutaneous effusion may mask the signals from the brain surface, making it difficult to visualize cortical sulci and gyri. Overlap of signals from the deep structures (especially the signals from the lateral ventricle) may sometimes occur, and cause some difficulty in recognizing the sulci. This problem can be overcome by the careful setting of the slice, or by obtaining a stereogram. The acquisition time of the SAS (8.5 min for single excitation, 17 minutes for two excitation), is comparable to that of a conventional MRI T 2 weighted image, and the total examination time is less than 30 min including pa-
Fig. 13 a, b. Thrombosed arteriovenous malformation in the right postcentral gyms, a Parietal SAS image shows that the lesion (-k) located in the postcentral gyrus. The lesion is identified in the center of the planned site of the skin incision ( 9 which indicates correct preoperative planning of the skin incision, b Surgicalview of the same patient (right) shows excellent correlation with magnified SAS image (left). The lesion ( ~ ), which cannot be identified from the brain surface, was successfully excised through the corticotomyin the postcentral sulcus (long arrows) just behind the cortical vein (short arrows)
tient positioning, scanning, and postprocessing, and is considered as practical. However, it is also true that this scanning time is not short enough to eliminate motion artifact completely. Recently, higher speed imaging of brain surface structures became possible with the aid of modified CE-FAST sequence, a variation of gradient echo technique (Fig. 15). This allows us to obtain brain surface images in between 41 s and 2 min - variable according to the number of excitations. The results with high speed brain surface imaging are still preliminary, but it will be a modality of choice in the near future.
447
Fig.14a-c. Left frontal astrocytoma (10 years old, male), a Oblique SAS with skin marking indicates the inadequate setting of the skin incision marker (arrowheads). b Second SAS obtained after the correction of skin incision line by the neurosurgeon. The lesion in the right premotor area locates in the center of the planned operative field (arrows). c Skin incision planning of the same patient. Original (arrowheads) and corrected (arrows) skin marking. Note the water-filled plastic tube as a marker As the ocular bulb and the external auditory meatus are consistently demonstrated on the lateral SAS images, SAS can be utilized as the pilot scan for conventional MRI. Furthermore, the superior ability of SAS in lesion localization indicates possible applications of SAS in the field of radiation therapy planning.
It should be emphasized that, the techniques employed for SAS are not special but are the combination of conventional M R I techniques. This means that, almost all M R systems can be equipped with SAS without any modification of the hardware. Considering the recent explosive spread of M R I units, this will be a significant clinical advantage.
448 Fig. 15. High speed brain surface imaging using modified CE-FAST sequence demonstrates successful visualization of cortical gyri and sulci. The image was obtained in 41 s, using 1.5 T superconducting magnet (Shimadzu SMT-150) with the parameters of TR = 80 ms, TE = 46 ms, Flip angle = 60~
Acknowledgements. The author wishes to thank Prof. S. Koga and the staff of the Department of Radiology and Prof. T. Kanno and the staff of Department of Neurosurgery for there cooperation. Special thanks go to H. Suzuki, Toshiba corp., for his assistance in the development of SAS, N. Iijima from Shimadzu Corp. for developing high speed brain surface imaging, and E. Asai and Y. Yamaguchi for there help in manuscript preparation.
References 1. Taverus JM, Wood EH (1976) Intracranial pneumography. In: Taverus JM, Wood EH (eds) Diagnostic neuroradiology, vol 1, 2nd edn. Williams & Wilkins, Baltimore, pp 231-542 2. Szikla G, B ouvier G, Hori T, Petrov V (1977) Angiography of the human brain cortex. Springer, Berlin Heidelberg New York 3. Salamon G, Lecaque G (1978) Choice of plane of incidence for computed tomography of the cerebral cortex. J Comput Assist Tomogr 2:93-97 4. Gado M, Hanaway J, Frank R (1979) Functional Anatomy of the cerebral cortex by computed tomography. J Comput Assist Tomogr 3:1-19 5. Katada K, Takesita G, Koga S, Asahina M, Kanno T, Asahina K (1987) MR imaging of brain surface structures: surface anatomy scanning (abstract). Radiology 165 [Suppl]: 303 6. Wehrfi FW, MacFall JR, Newton TH (1983) Parameters determining the appearance of NMR images. In: Newton TH, Potts DG (eds) Modern neuroradiology, vol 2. Advanced Imaging techniques. Clavadel Press, San Anseimo, pp 81-117
7. Norman D, Newton TH (1975) Locafization with the EMI scanner. Am J Roentgenol Radium Ther Nuc Med 125:961-964 8. O'Lealy DH, Lavyne MH (1978) Localization of vertex lesions seen on CT scan. J Neurosurg 49:71-74 9. Rubin JM, Sayre RE (1978) A computer-aided technique for overlaying cerebral angiograms onto computed tomograms. Invest Radio113:362-367 10. Hayman LA, Evans RA, Hinck VS (1979) Scalp markers for precise craniotomy siting, using computed tomography. J Comput Assist Tomogr 3:701-702 11. Naldich TP, Yu RH, King DG, Wholahan JD (1980) Superimposition reformatted CT for preoperative lesions localization and surgical planning. J Comput Assist Tomogr 4:693-696 12. Peters TM, Clark JA, Olivier A, Marchand EP, Mawko G, Dieumegarde M, Muresan LV, Ethier R (1986) Integrated stereotaxic imaging with CT, MR imaging and digital subtraction angiography. Radiology 161:821-826 13. Herman GT (1987) Computerized three-dimensional imaging of the brain. J Cereb Blood Flow Metab 7: S 22-8 23 14. Levin DN, Hu X, Tan KK, Galhotra BA (1989) Surface of the brain: three-dimensional MR imaging created with volume ren~ dering. Radiology 171:277-280 Prof. K. Katada Fujita Health University School of Hygiene 1-98 Dengakugakubo Kutukake-cho Toyoake Aichi 470-11 Japan
Neuro radiology .
.
.
.
.
.
9 Springer-Verlag1990
MR imaging of brain surface structures: surface anatomy scanning (SAS) K. Katada Department of Radiology,Fujita Health UniversityHospital,Toyoake,Japan
Summary. MR imaging technique that permits direct and non-invasive visualization of brain surface structures (Surface Anatomy Scanning, SAS) was developed using the combination of long TE, long TR spin echo sequence and thick slice. Clinical trials in 67 patients with SAS showed excellent visualization of the sulci and the gyri on the lateral, occipital, frontal and parietal surfaces of the brain together with cortical and subcortical lesions. The results indicate that the SAS is useful for the localization of cortical and subcortical pathology, for the diagnosis of anomalous gyral patterns, and for surgical planning. Key words: Cerebral cortex - MR imaging - Migration
totally suppressed. As the brain surface is covered by subarachnoid space, it is possible to create a "relief" picture of the brain surface utilizing the CSF as natural "contrast medium" (Fig. 1). A five to eight centimeter thick slice is used to cover sufficient area of the cerebral cortex to create a "planar" image of the brain surface [5]. The use of a surface coil is helpful for further enhancement of the signal intensity of subarachnoid CSF, and it is also useful to avoid the overlap of the signals from the ventricles and other deep seated structures. In obtaining a parietal view, the surface coil can not be applied because of the limitation of RF coil direction, so that the conventional head coil is used for this purpose.
anomaly - Surgical planning
Scanning parameters The identification of cerebral surface anatomy, including cortical sulci and gyri in relation to intracranial lesion(s) has special clinical importance, and it has been one of the main interests of neuroradiology [1-4]. Recent developments in CT and MRI have made possible the non-invasive visualization of sulci and gyri as tom0graphic images [3, 4]. However, these imaging techniques are not always effective in precise localization of the lesion because of the interruption of the sulci and gyri by the tomographic section. ~. Until now, no available imaging modality permitted non-invasive and direct visualization of the brain surface anatomy. The PUrpose of this study is to introduce MR surface anatomy scanning (SAS), a new application of MR imaging technique for non-invasive visualization of brain surface structures [5], and to evaluate the clinical significance of this technique.
Method The basic concept Under the long TR and extremely long TE (more than 200 ms) spin echo sequence, the signal intensity of the cerebrospinal fluid (CSF) has been strongly enhanced, while the signals from the skin, subcutaneous tissuesl orbits, diploe of the skull and the brain itself have been
The MR scanner used in this study was a Toshiba MRT 50A - 0.5 T superconductive magnet system. The standard scanning parameters used in this method were, TR = 2000 ms, TE = 250 ms a 256 • 256 image matrix, one or two excitation(s) and 2DFT image reconstruction. Standard slice thickness was 8 cm, however, 5 or 6 cm slice was selected for small sized object. Scanning time was
il!: .... 1
SUBARACHNOID C S F
Fig.L Basicconceptof SAS. LongTE spin echo sequenceenhances the signalintensitiesof subarachnoidCSE Thicknessof the CSFlayer in the corticalsulci (,4) and overthe corticalconvolutions(B)
44(I
Fig.2. a Original SAS images of a normal volunteer (34 Y. O. male). Left lateral view. Sulci and fissures are demonstrated as bright lines owing to the long T2 of the cerebrospinal fluid, b SAS image processed by gray scale reversal and 2 D filtering. Delineation of the sulci and gyri is improved
Fig.3. Normal cortical gyriand sulcidemonstratedby SAS. (48 Y. O. male, left lateral view). SFG Superior frontal gyms; M F G Middle frontal gyms; Inferior frontal gyms: O R Pars orbitalis, TR Pars triangularis, O P Pars opercularis; P R E C G Precentral gyms; P O S T C G Postcentral gyms; S M G Supramarginal gyrus; A N G Angular gyms; S P L Superior parietal lobule; S T G Superior temporal gyms; M T G Middle temporal gyms: I T G Inferior temporal gyrus; S S L Superior semicircular lobule; I S L Inferior semicircular lobule; SFS Superior frontal sulcus; S F Sylvian fissure; (AH) Anterior horizontal ramus; (AA) Anterior ascending ramus; (P) Posterior ramus; P R E C S Precentral sulcus; CS Central sulcus; P O S T C S Postcentral sulcus; I P F Interparietal fissure; S T S Superior temporal sutcus; H F Great horizontal fissure; VTVein of Trolard; VR Vein of Roland; E A M External auditory meatus
8.5 minutes for i excitation, and 17 min for 2 excitations. O n the acquired images, post-processing including gray scale reversal and 2 D image filtering were applied to achieve b e t t e r identification of the sulci (Fig. 2 a, b).
Materials O v e r the last 1 4 - m o n t h period, 67 cases (85 images) were e x a m i n e d b y SAS. These included 6 n o r m a l volunteers, 6 n o r m a l cases, 16 intracranial neoplasms, 9 cerebral infarc-
441 tions, 5 intracranial vascular malformations, 5 with focal brain damage, 4 migration anomalies and 16 others. In two cases (one normal volunteer and a case of arteriovenous malformation), pairs of SAS images were acquired to obtain a stereographic view. The imaging direction was lateral in 53 cases, frontal in 3, frontal oblique in 6, posterior in 9 and parietal in 14. In 5 patients, SAS imaging was performed for the purpose of surgical planning. After planning the site of scalp incision by the neurosurgeon, it was marked by a water filled
plastic tube and the SAS image was obtained to estimate the relation between the lesion and the surgical field.
Results G o o d quality brain surface images were obtained in 76 of 85 images. In two cases with brain tumors, the cortical sulci were obliterated due to severe mass effect, resulting in poor visualization of the sulci on SAS images. In one case, the signal from the cortical sulci was masked by the signal from epidural fluid collection. Severe motion artifacts were seen in 3 cases. The overlap of the signals from lateral ventricle was seen in 2 patients. It was difficult to identify sulci and gyri on a lateral SAS image of a 4 years old child with an arachnoid cyst.
N o r m a l cases
In 12 normal volunteers and normal clinical cases, major fissures and sulci were clearly visualized, and identification of cortical gyri was possible (Figs.2, 3). The SAS was sensitive enough to visualize the narrow sulci of the young volunteer aged 21 whose CT failed to show the sulci. On the lateral view, the anterior horizontal ramus, anterior ascending ramus and posterior ramus of the sylvian fissure, as well as the central, precentral and postcentral sulci,
Fig.4. Parietal view of a normal volunteer (41 Y. O., male). IHF Interhemispheric fissure; M Marginal portion of cingulate sulcus Fig.5a, b. Posterior views of a normal volunteer (40 Y.O. male). Stereogram. Interhemispheric fissure, great horizontal fissures (arrows) and left inferior hemispheric veins (arrowheads) are demonstrated
442
Fig.6 a, b. Left temporal
astrocytoma (grade III). a Axial T 1-weighted image with Gd-DTPA injection, b SAS image demonstrates the infra-sylvian location of the tumor. The sylvian fissure is elevated and deformed by the tumor
Fig.7. Subcortical hematomain the left precentral gyrus. Lateral SAS shows the location of hematoma and the swelling of the motor cortex were visualized (Fig. 3). The major cortical veins including vein of Roland and vein of Trolard were also identified. Additionally, the bulbus oculi and external auditory meatus were clearly demonstrated. On the parietal view, motor cortex and sensory cortex of both hemispheres were clearly identified together with the wide area of neighboring gyri (Fig. 4). On the posterior view, the great horizontal fissure, the interhemispheric fissure and the cerebello-cerebral interface were easily identifiable (Fig. 5 a, b).
Lesion localization Among 55 cases with intracranial pathology, SAS was effective for accurate lesion localization in 37 cases. In a case with left temporal astrocytoma, SAS clearly showed infra-sylvian location of the tumor (Fig. 6a, b). SAS was effective in evaluating the relation between the lesions and the motor cortex (Figs. 7, 8). In patients with infarction of the middle cerebral artery territory, the extent of the infarcted area was well visualized by SAS, which made
443 sult, precise site of the craniotomy was determined, and surgical damage to the motor cortex was successfully avoided. The magnified SAS image showed excellent correlation with the surgical view (Fig. 13 b). In a young patient aged 10 with left frontal low grade astrocytoma, SAS was useful to correct the planned scalp incision (Fig. 14 a-c).
Discussion
Fig.8. Meningioma in the high parietal region. On parietal SAS image, right precentral and postcentral gyrus cannot be identified due to the compressonof the large parasagittal meningioma (arrow-
heads) the estimation of affected branches of the middle cerebral artery possible (Fig. 9 a, b). SAS was also useful in the precise localization of the focal cortical damage (Fig. 10). In 2 cases with severe edema and mass effect, SAS failed to show the sulci.
Diagnosis of abnormal gyralpattern In 6 patients with suspected migration anomaly, abnormal gyral patterns were detected by SAS in 5. The flat gyri were demonstrated by lateral SAS images in a case of pacyhgyria (Fig. 11 a, b). In 3 cases with unilateral schizencephaly, characteristic pattern of anomalous clefts around the sylvian region were demonstrated (Fig. 12). A hypoplastic postcentral gyrus was detected in one patient.
Surgicalplanning The preoperative localisation of the scalp incision was performed in 5 patients with intracranial pathology using SAS and a water filled plastic tube as a marker. In a case of thrombosed arteriovenous malformation in the right postcentral gyrus, parietal SAS image demonstrated the precise localization of the lesion, and the relation between the lesion and the scalp markers indicating the planned site of incision was well estimated (Fig. 13 a). Based on this re-
As the cerebral cortex has highly specified functional localization, the identification of the cortical gyri on radiological images has special clinical importance, and it has been one of the main objects in neuroradiological diagnosis [14]. Pneumoencephalography (PEG) can demonstrate the cortical sulci [1] but it is not consistent especially when the amount of injected gas is small. Detailed analysis of a cerebral angiogram also aids the localization of the gyri and sulci [2]. However, both PEG and angiography are invasive procedures and cause pain and risk to the patient. The introduction of CT and MRI had improved this surface localization dramatically [3, 4, 6, 7]. The sulci and gyri over the high parietal region are well demonstrated on axial CT and MRI. MRI parasagittal sections also give an excellent orientation of the sulci and gyri of the medial surface of the cerebrum. However, with respect to the visualization of the lateral surface of the brain, CT and MRI do not always give good results. This is due to the interruption of the sulci and gyri by the tomographic slice, making it difficult to identify the gyrus as a continuous cortical "strip". And the major part of the effort in CT interpretation of cerebral gyri is to convert the anatomical map of the cerebral cortex from the tomographic sections [3, 4]. The technique proposed in this paper (SAS) is a noninvasive and a practical method capable of direct visualization of the brain surface structures [5]. With a long TE spin echo sequence, the signals from the brain, diploe, and the subcutaneous tissue have almost completely decayed, and the images, therefore, primarily display CSF which has the longest T2. As the brain surface is covered by CSF within the subarachnoid space, the signals from deep sulci and fissures are integrated and intensely opacifled, while the cortical convolutions, where the layer of CSF is thin, are only slightly opacified. Thus, the CSF is utilized as a physiological contrast medium to create a "relief picture" of the brain surface (Fig. 2). At the same time, as the signals from the skin, subcutaneous tissue, cortical bone and diploe of the skull are negligible at this pulse sequence, so it is possible for us to "look through" the brain surface from the outside the skull with the aid of the surface coil and a thick slice. Although the slicing gradients are employed in the imaging processes, the acquired images are considered to be identical to the planar images. On the original image of the SAS, the cortical sulci were demonstrated as bright lines on the brain surface, representing high signal intensity from CSF owing to the Long TE, Long TR spin echo sequence (Fig. 2 a). Several
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Fig. 9 a, b. Cerebral infarction in the left middle cerebral artery territory, a Axial T2-weighted image, b SAS image, left lateral view demonstrates the extent of the infarction. Note that the posterior part of the superior and middle temporal gyrus as well as the inferior portion of the motor cortex are involved by the lesion, while the pars triangularis of the inferior frontal gyrus and the inferior parietal lobule are spared
Fig.10. Focal epilepsy. Alateral SAS image shows focal cortical damage in the left middle temporal gyrus post processing techniques were applied to improve the visualization of the sulci. The reversed image, which m a k e s the sulci dark in appearance, greatly improved the delineation. Two dimensional filtering was applied in order to enhance the gyral edges (Fig. 2b). Clinical trials with SAS showed excellent results in the demonstration of cortical sulci and gyri. Most of the sulci and fissures of the brain surface can be clearly visualized. On the lateral view, three rami of the sylvian fissure (anterior horizontal, anterior ascending and posterior ramus) were constantly identified (Figs. 2, 3), which is often difficult to identify on conventional CT or MRI. This was con-
sidered to have certain advantages in the localization of Broca's area. Differentiation between the anterior ascending ramus of the sylvian fissure and the lower part of the precentral sulcus was readily possible with SAS, though occasionally difficult on axial CT and M R I images. Also the precise localization of the supramarginal gyrus and angular gyrus are often difficult on conventional CT and M R I . SAS has significant advantages in the localization of these lower parietal gyri because SAS usually demonstrates the ascending ramus of the superior t e m p o r a l sulcus as well as the ascending part of the posterior ramus of the sylvian fissure.
445 For the parietal view, SAS offers a much wider field of view than conventional CT and MRI, and is helpful in improving the orientation (Fig. 4). On the posterior view, the interhemispheric fissure, interparietal fissure and other occipital sulci were easily identifiable (Fig. 5). In the cerebellum, the great horizontal fissure separating the superior and inferior semicircular lobule was identified consistently both on the lateral view and posterior view. Although anatomical variations are occasionally present, SAS is considered to improve the interpretation of these cortical structures in clinical practice. It was an unexpected favorable result that SAS can also visualize the major cortical veins - veins of Trolard,
veins of Roland, superficial middle cerebral vein and others (Figs. 2, 3). These veins on the SAS images may give the neurosurgeons an excellent orientation of the operative field prior to craniotomy. The cortical branches of the cerebral arteries were not identifiable on the SAS images. In a case of arteriovenous malformation, the nidus together with dilated draining veins were demonstrated. Since the surface coil could not totally eliminate the signals from deep structures, various cortical and subcortical lesions were demonstrated on the SAS images, so that the precise localization of the lesion was possible. Excellent visualization of normal and abnormal cortical pattern by SAS indicates that it can be a powerful modality in the diagnosis of migration anomaly (Figs. 11, 12). Preoperative assessment of surgical field is an important subject for neurosurgeons, and, so far, a number of modalities including plain skull radiographs, PEG, cerebral angiography, ultrasound, CT [6-11] and M R I [12] have been used for this purpose. SAS can demonstrate not only the lesion itself, but also the major cortical veins as well as the detailed pattern of the cortical sulci and gyri. Simultaneously, it can also show the planned lines of the scalp incisions by the application of water filled plastic tubes (Figs. 13c, 14). Thus, the exact relation between the lesion, cerebral cortex and the site of skin incision can be visualized on a single image, which makes accurate planning of the surgical approach possible. This SAS is thought to have higher clinical potential than three dimensional surface reconstruction images derived
Fig. 12. Unilateral schizencephaly.Lateral SAS image shows characteristic clefts (arrows) in right premotor area and the abnormal pattern of the adjacent gyri
Fig.lla, b. Pachygyria. a T 1-weighted image, b Lateral SAS image demonstrates the flat gyri neighboring the sylvian fissure. The anterior ascending ramus and anterior horizontal ramus of the sylvianfissure are absent
446 from multiple CT and MRI sections (3 D-CT, 3 D-MRI) [13, 14], the other technique which can demonstrate gyral patterns. In 3 D - C T or 3 D-MRI, it is essential to extract the outline of the brain prior to the reconstruction, which usually requires a manual procedure. In addition, to achieve similar results to those of SAS, one has to extract the outline of the subcortical lesion as well as the site of the skin incision, and to synthesize these three factors in a single image. These are time consuming processes and not possible to apply for every surgical patient in daily clinical practice, which is feasible with SAS. There are several limitations in the diagnostic capabilities of SAS. As with conventional MRI, it is contraindicated for patients with intracranial surgical clips or cardiac pacemakers. Although SAS can tolerate a moderate degree of mass effect, a severe mass effect caused by the intracranial lesions may totally obliterate the sulci, and eliminate the CSF within them, resulting in their poor visualization. SAS was sensitive enough to visualize the sulci of a young patient aged 10, but it failed to show the sulci of a 4 year old pediatric patient, whose sulci were too narrow to visualize. A n o t h e r pitfall of SAS is diffuse accumulation of the fluid on the surface of the brain. The strong signal intensity from the subdural, epidural or subcutaneous effusion may mask the signals from the brain surface, making it difficult to visualize cortical sulci and gyri. Overlap of signals from the deep structures (especially the signals from the lateral ventricle) may sometimes occur, and cause some difficulty in recognizing the sulci. This problem can be overcome by the careful setting of the slice, or by obtaining a stereogram. The acquisition time of the SAS (8.5 min for single excitation, 17 minutes for two excitation), is comparable to that of a conventional MRI T 2 weighted image, and the total examination time is less than 30 min including pa-
Fig. 13 a, b. Thrombosed arteriovenous malformation in the right postcentral gyms, a Parietal SAS image shows that the lesion (-k) located in the postcentral gyrus. The lesion is identified in the center of the planned site of the skin incision ( 9 which indicates correct preoperative planning of the skin incision, b Surgicalview of the same patient (right) shows excellent correlation with magnified SAS image (left). The lesion ( ~ ), which cannot be identified from the brain surface, was successfully excised through the corticotomyin the postcentral sulcus (long arrows) just behind the cortical vein (short arrows)
tient positioning, scanning, and postprocessing, and is considered as practical. However, it is also true that this scanning time is not short enough to eliminate motion artifact completely. Recently, higher speed imaging of brain surface structures became possible with the aid of modified CE-FAST sequence, a variation of gradient echo technique (Fig. 15). This allows us to obtain brain surface images in between 41 s and 2 min - variable according to the number of excitations. The results with high speed brain surface imaging are still preliminary, but it will be a modality of choice in the near future.
447
Fig.14a-c. Left frontal astrocytoma (10 years old, male), a Oblique SAS with skin marking indicates the inadequate setting of the skin incision marker (arrowheads). b Second SAS obtained after the correction of skin incision line by the neurosurgeon. The lesion in the right premotor area locates in the center of the planned operative field (arrows). c Skin incision planning of the same patient. Original (arrowheads) and corrected (arrows) skin marking. Note the water-filled plastic tube as a marker As the ocular bulb and the external auditory meatus are consistently demonstrated on the lateral SAS images, SAS can be utilized as the pilot scan for conventional MRI. Furthermore, the superior ability of SAS in lesion localization indicates possible applications of SAS in the field of radiation therapy planning.
It should be emphasized that, the techniques employed for SAS are not special but are the combination of conventional M R I techniques. This means that, almost all M R systems can be equipped with SAS without any modification of the hardware. Considering the recent explosive spread of M R I units, this will be a significant clinical advantage.
448 Fig. 15. High speed brain surface imaging using modified CE-FAST sequence demonstrates successful visualization of cortical gyri and sulci. The image was obtained in 41 s, using 1.5 T superconducting magnet (Shimadzu SMT-150) with the parameters of TR = 80 ms, TE = 46 ms, Flip angle = 60~
Acknowledgements. The author wishes to thank Prof. S. Koga and the staff of the Department of Radiology and Prof. T. Kanno and the staff of Department of Neurosurgery for there cooperation. Special thanks go to H. Suzuki, Toshiba corp., for his assistance in the development of SAS, N. Iijima from Shimadzu Corp. for developing high speed brain surface imaging, and E. Asai and Y. Yamaguchi for there help in manuscript preparation.
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