Symptomatic subependymoma: a clinicopathological and flow cytometric study
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1 J Neurosurg 75: , 1991 Symptomatic subependymoma: a clinicopathological and flow cytometric study DANIELA LOMBARDI, M.D., BERND W. SCHEITHAUER~ M.D., FREDRIC B. MEYER, M.D., GLENN S. FORBES, M.D., EDWARD G. SHAW, M.D., DONNA J. GIBNEY, AND JERRY A. KATZMANN, PH.D. Departments of Neurosurgery, Laboratory Medicine and Pathology, and Diagnostic Radiology, and Division of Radiation Oncology, Mayo Clinic, Rochester, Minnesota t/ Twenty-one intracranial subependymomas were reviewed with regard to presentation, diagnosis, operative findings, and long-term follow-up data. The histopathological features were critically reviewed, and deoxyribunucleic acid analysis was performed by flow cytometry. The patients' mean age was 48.5 years (range 32 to 72 years). In 14 cases the tumor was located in the fourth ventricle, in six within a lateral ventricle, and in one in the third ventricle with extension into the lateral ventricle. Radiographic characteristics included isodensity with minimal enhancement on computerized tomography, frequent dystrophic calcification, and isointensity on T:weighted or slight hyperintensity on T2-weighted magnetic resonance images. The predominant histological features in all cases were those of classic subependymoma. Nonetheless, pathological examination showed a minor ( < 20%) ependymoma component in five cases, significant cytological atypia in seven, mitoses in l 1, endothelial prominence in four, and focal hemorrhage-associated necrosis in two. Flow cylometry revealed a diploid pattern in 12 patients, tetraploidy in two, and aneuploidy in one. Two patients died in the perioperative period. Of the remaining 19, 12 underwent gross total resection (two of whom received postoperative irradiation) and seven underwent subtotal resection (five of whom received irradiation). None of the 12 non-irradiated patients developed tumor progression or died of direct tumorrelated causes. Of the seven irradiated patients, follow-up imaging studies demonstrated their tumors to be radioresponsive, particularly with doses of 5000 cgy or greater. Despite the presence of cytological atypia and mitotic activity in the majority of cases, the prognostic effects of such factors as tumor location and the extent of surgical resection outweighed those of the standard histopathological parameters. Routine postoperative irradiation is not recommended, but should be reserved for cases with a symptomatic ~sidual or recurrent subependymomas following surgery. KEY WORDS 9 glioma 9 subependymoma 9 radiation therapy 9 prognosis 9 flow cytometry T HB subependymoma obtained recognition as a distinct histopathological entity following a report of seven cases by Scheinker in ~4 This tumor remained of interest primarily to pathologists because, in most instances, it represented an incidental finding at autopsy. More recently, subependymomas have come to the attention of neurosurgeons as clinical series and case reports of symptomatic examples appear 1 8 I in the literature. " " 9 Data regarding neuroimaging, surgery, and the role of radiotherapy are limited. Accordingly, we analyzed the Mayo Clinic's experience with 21 patients operated on between 1950 and 1989, with particular attention to diagnostic, operative, and therapeutic factors. In addition, histopathological and deoxyribonucleic acid (DNA) flow cytometric charac- teristics were analyzed in an effort to identify additional prognostic indicators. Clinical Material and Methods The files of the Mayo Clinic Tissue Registry were searched for cases of subependymoma occurring between 1950 and Microscopic sections were reexamined and, where necessary, paraffin blocks were recut and stained by the hematoxylin and eosin method. In addition, DNA flow cytometric analysis was performed in 17 cases utilizing paraffin-embedded tissues. Cells were prepared from paraffin-embedded blocks according to the procedure previously described by Vindelev, et all 7 For DNA flow cytometry, a modifi- J. Neurosurg. / Volume 75 /October
2 D. Lombardi, et al. Fit;. 1. Radiographic sludies in a case of fourth-vcntricular subependymoma. Left: Computerized tomography scan showing a well-demarcated Iobulated lbunh vcntricular mass with moderate contrast enhancement and slight dystrophic calcification. Ceuter and Right: On magnetic resonance imaging, the tumor appears isointense with central low intensity on the T~-weighted images (center) and hyperintense on the spindensity' image (righo. cation of the method of Hedley 7 was used. The clinical, neuroradiological, operative, and radiotherapeutic data were reviewed, and follow-up information was obtained in each case. Results Clinical Data From 1950 to 1989, 21 patients underwent surgery. for subependymoma; 13 were operated on since i 975. The series included 14 men and seven women, ranging in age from 32 to 72 years (mean 48.5 years). The duration of preoperative symptoms ranged from 6 months to 5 years (mean 3 years). Headache, the most common presenting symptom (57%), usually preceded other complaints by many months. Other symptoms encountered frequently were gait disturbances, nausea, and vomiting; all occurred early in the course and tended to be episodic. Less frequent symptoms, occurring in 23% of patients, included diplopia, blurred vision, tinnitus, weakness, incoordination, memory dis- FIG. 2. Magnetic resonance images ofa supratentorial subependymoma Left: A well-demarcated isointense septum pellueidum mass is seen on the T~-weighted image. Note an area of minimal dystrophic calcification. Right: On the spindensity image, the lesion appears as a hyperintense area. 584 turbances, slurred speech, and emotional lability. On neurological examination the most frequent findings were related to obstructive hydrocephalus or localized mass effect. The most notable findings were cranial nerve palsies due to either increased intracranial pressure or tumor location in the floor of the fourth ventricle. Neuroradiology Tumor size was expressed as the maximum diameter measured by the intrinsic computer matrix scale on the radiographic image, and ranged from 1.5 to 7.0 cm (mean 4.0 cm). Of the 14 tumors located in the fourth ventricle, I1 originated from the floor, two from the lateral wall, and one from the inferior vermis; in three of these cases, neoplasm extended through the foramen magnum to the C1-2 level. In six instances the lesion was situated in the lateral ventricle; four originated from FIG. 3. Photomicrograph of a subependymoma specimen demonstrating the typical Iobular growth pattern with central cellularity and peripheral skeins of fibrillated cell processes. H&E, J. Neurosurg. / Volume 75 / October. 1991
3 Symptomatic subependymoma the septum pellucidum and two from the thalamus. The remaining tumor arose in the third ventricle and extended through a foramen of Monro into a lateral ventricle. Nine patients underwent modern neuroimaging. Computerized tomography (CT) scanning was performed in eight cases, magnetic resonance (MR) imaging in one, and both CT and MR imaging in four. All tumors appeared slightly lobulated and were well demarcated from surrounding tissue. Little or no vascularity or edema was evident. Of the eight tumors imaged by CT alone (Fig. 1), four demonstrated focal dystrophic or spotty calcification and five showed contrast enhancement (minimal in four cases and marked in one). All of the four cases in which MR imaging was performed (Fig. 2) demonstrated an isointense signal on T~-weighted images and a minimally increased signal on spin-density and T_,-weighted images. No postgadolinium MR images were available for review. Surgical Data The surgical approaches included suboccipital craniectomy in 14 cases, frontal craniotomy in five, and stereotactic frontal craniotomy in two. In patients undergoing subtotal tumor resection, a ventriculoperitoheal shunt was placed in three and a ventriculocisternotomy in one. For the purpose of analyzing surgical results, the patients were divided into two groups: those who underwent surgery between the years 1950 and 1974, and those operated on between 1975 and The first group (1950 to 1974) included eight patients, of whom seven had the tumor located in the fourth ventricle and one had a lateral ventricular lesion. Of these, resection was complete in six and subtotal in two. During surgery, intermittent alteration of vital signs (bradycardia), suggestive of transient brain-stem dysfunction, occurred in five cases. Four of these patients required postoperative tracheostomy. The overall perioperative mortality rate in this group was 25%. The second group consisted of 13 patients operated on between 1975 and In these, five tumors occurred in the lateral, one in the third, and seven in the fourth ventricle. Six patients underwent subtotal tumor resection, and gross total removal was achieved in seven. Intraoperative alteration of vital signs was observed in three patients, two of whom required postoperative tracheostomy. No perioperative deaths occurred in this group. Follow-up review, ranging from 1 to 27 years (mean 6 years) after surgery, disclosed three deaths. One patient died 8 years after surgery, of aspiration pneumonia due to lower cranial nerve dysfunction, one died 2 years after surgery, with chronic encephalopathy related to poorly controlled hydrocephalus, and the third died of central respiratory depression 3 years after surgery. In none of these cases was there radiological evidence of tumor recurrence or progression. Overall, two patients died perioperatively and three during the follow-up period, but none succumbed to direct tumor progression. Four others died of unrelated causes. Pathological Data The basic morphological features of subependymoma were observed in all cases and included lobular architecture, overall hypocellularity, and clustering of nuclei surrounded by circumferential skeins of long eosinophilic fibrillar processes (Figs. 3 and 4). Microcysts, present in nine cases, were prominent in three instances (Fig. 4). Cellularity was mildly increased in 10 cases. Obvious astrocytic differentiation was noted in one-half of all tumors. Of the 21 lesions, 16 (76%) were pure subependy- FIG. 4. Photomicrographs of a subependymoma specimen. Left: Monotonous cells, typically clustered and devoid of atypia. Cytological uniformity characterizes the majority of subependymomas. H & E, x! 80. Right: Section showing microcysts, a not uncommon finding. This appearance may be prominent in some examples. H & E, x 70. J. Neurosurg. / Volume 75 / October,
4 D. Lombardi, et al. FttJ. 5. Photomicrographs of subependymoma specimens. Although cytological uniformity characterizes subependymomas, fibrilla~ (k'fu and gemistocytic (cemer) astrocytes are not uncommon. The same is true of foci of cellular atypia (righo. H & E. x 180. moma; five (24%) demonstrated a minor element in which the lobular architecture was obscured or lost and the appearance more closely resembled low-grade ependymoma. The presence of such foci appeared to have no effect upon prognosis. The cytological appearance of the subependymoma cells varied, some showing distinct process formation with fibrillation and others the acquisition of obvious astrocytic features (Fig. 5). Atypia, defined as hyperchromasia and variation in nuclear shape and size, was minimal to mild in all but seven cases; in these seven, it was focally moderate in degree (Fig. 5). Mitoses were absent in 10 specimens, rare in eight, and readily identiffed in three; their presence showed no correlation with prognosis. The vast majority of tumors were hypovascular. Although endothelium was prominent in four cases, actual endothelial hyperplasia was focal at best in only one case. Patchy necrosis was noted twice, once in association with hemorrhage; in both instances it was focal and not accompanied by cellular palisading. Degenerative changes were frequent, particularly in large and presumably long-standing lesions; these changes included vascular sclerosis in 18 cases (extensive in five), vascular thrombosis in 10, hemorrhage in one, hemosiderin deposition in 15 (marked in one), ischemic rarefaction in eight (marked in one), microcalcifications in 10 (abundant in two), Rosenthal fiber formation in five (widespread in one), and foci of chronic inflammation in five. Flow Cytometry In 17 cases paraffin-embedded tissue was available for flow cytometric analysis; all but two yielded interpretable DNA histograms. Of the 15 tumors, one showed abnormal DNA content (DNA aneuploid) and two contained a higher than normal percentage of cells in the G2/M growth phase (DNA tetraploid). Radiotherapeutic Data Seven patients received postoperative megavoltage irradiation. The total doses, calculated to the midplane for opposed fields or to the intersection of field centers for nonopposed fields, were 3310, 3600, 4320, 5000 (three patients), and 5400 cgy, delivered in 150- to 200-cGy daily fractions. One patient, diagnosed at another institution as having positive cerebrospinal fluid (CSF) cytology, received craniospinal axis irradiation (3600 cgy to the whole brain and 3420 cgy to the whole spine). The remaining six patients received radiotherapy to localized fields. Of the 13 patients who underwent gross total removal of tumor, 11 did not receive radiotherapy. Of the 10 postoperative survivors, none had experienced tumor recurrence and none had died of their tumors 1 to 27 years (mean 12 years) after surgery, although three died of causes other than subependymoma. Two patients who underwent gross total tumor removal received radiotherapy; one patient is alive without evidence of tumor 3 years after surgery, and the other died of a nontumor-related cause. Five patients who underwent subtotal resection of tumors received postoperative irradiation; of the three who did not, one patient died postoperatively. Of these five irradiated patients, three are alive 3 to 6 years (mean 4 years) after surgery and two died of unrelated causes. The two non-irradiated patients are alive without tumor recurrence. Overall, tumor recurrence or progression occurred in two of the three patients receiving radiation doses less than 5000 cgy, compared to one of four receiving doses of 5000 cgy or greater. Postirradiation follow-up CT scans or MR images were obtained in four patients with grossly measurable tumor: no residual tumor was observed in two cases, a mild decrease in the size of the residual tumor was present in one case, and no change in the residual tumor was noted in the fourth. 586 J. Neurosurg. / Volume 75 / October, 1991
5 Symptomatic subependymoma Discussion Subependymomas are common tumors of the ventricular system. Their nature has been the subject of controversy for years.~-~ Scheinked 4 first noted histological similarities between the morphology ofsubependymoma and the glia of the subependymal plate. Such similarities have also been reported at the ultrastructural level. ~ Whether subependymomas are essentially ependymal 2 or astrocytic s in nature remains somewhat of an issue. The ultrastructural studies by Fu, et al., 6 demonstrated coexpression of ependymal and astrocytic features, not a surprising conclusion given the cytological spectrum encountered in this series, The vast majority of subependymomas are not associated with clinical symptoms and thus come to light as incidental autopsy findings. Only a minority produce neurological abnormalities and come to the attention of neurosurgeons. Symptomatic subependymomas have been the subject of several series 7"~'"~'~5"~6 and numerous case reports. Given the considerable variation in the preoperative assessment and management of reported cases, the literature leaves a number of questions unsettled, most of which center upon the natural history and optimal therapy of subependymoma. These uncertainties prompted this elinieopathologieal study. The frequency of subependymomas, both incidental and symptomatic, among intracranial neoplasms was reported by Matsumura, et al., "~ to be 0.7%. In our experience, symptomatic subependymomas represent 0.2% of intracranial neoplasms. Radiological Features In general, the radiological appearance of subependymomas consisted of a'well-demarcated, slightly lobulated tumor appearing isodense with minimal enhancement and frequent dystrophic calcification on CT scans, and isointense on T~-weighted and slightly hyperintense on T2-weighted MR images. Relatively little mass effect or surrounding edema was present. A lesion with these characteristics in the fourth ventricle should suggest the possibility of subependymoma. Most ependymomas and choroid plexus papillomas in this location show more marked contrast enhancement. Astrocytomas often demonstrate more intense signal intensity on T_,-weighted MR images and incite more edema in surrounding tissue. *'9 Medulloblastomas tend to show a uniform hyperdense appearance on nonenhanced CT scans but otherwise may resemble subependymoma. An isointense appearance on Ttweighted MR images and an increased signal on T,.- weighted MR images are features common to meduiloblastomas and subependymomas. Surgical Considerations The reported perioperative mortality rate associated with subependymoma varies considerably, ranging from 12% to 30%/"~~ In the series of Jooma, et al., s which consisted solely of subependymomas of the fourth ventricle, the perioperative mortality rate approximated 42%. In our 40-year experience with supratentorial and infratentorial examples, the total perioperative mortality rate was 9%. Division of the patients into two chronological groups (1950 to 1974 and 1975 to 1989) clearly demonstrated that the introduction of microsurgical techniques has greatly decreased perioperative risk. Whenever possible, complete tumor removal is recommended. Since subependymomas in the lateral ventricle usually arise from the septum pellucidum, complete resection of such tumors is often achieved. In contrast, the more common fourth ventficular subependymoma usually arises from the floor, thus making complete resection hazardous due to the likelihood of cranial nerve injury. In these situations, debulking or subtotal resection aimed at improving CSF outflow is advisable. Role ~f Radiation Therapy Most authors consider radiotherapy to be of marginal value in the treatment of pure subependymomas, but useful in cases of mixed subependymoma-ependymoma. '~ The efficacy of postoperative radiotherapy for cases of nearly pure subependymoma, such as those in our series, is unclear. In our series, none of the patients who underwent gross total excision without postoperative irradiation experienced tumor recurrence. Therefore, we do not advise irradiation in this setting. The value of postoperative radiation therapy for patients with subtotal excisions cannot be determined from our series. Since a subgroup of irradiated patients with serial imaging studies was shown to have a radiographic response following treatment, it would be reasonable to recommend postoperative radiation therapy for those patients with symptomatic residual tumor or for patients who develop tumor progression or recurrence. Although the numbers of irradiated patients were small, control appeared better with doses of 5000 cgy or greater. Pathology and Prognosis The significance of histological features and of tumor grade, factors known to be of paramount prognostic importance in ordinary infiltrative gliomas, ~ seems to be overshadowed in the subependymoma by the effect of tumor location and surgical considerations. The prognostic utility of flow cytometry, although capable of identifying aggressive lesions in our series, remains unsettled. Acknowledgment Dr. Lombardi is indebted to Professor P. Paoletti, chairman of the Department of Neurosurgery, University of Pavia, Italy, for his support. J. Neurosurg. / Volume 75/October,
6 D. Lombardi, et al. References 1. Artico M, Bardella L, Ciappetta P, et al: Surgical treatment of subependymomas of the central nervous system. Report of 8 cases and review of the literature. Aeta Neurochir 98:25-3 l, Boykin FC, Cowen D, lannucci CA J, et al: Subependymal glomerate astroc.vtomas. J Neuropathol Exp Neural 12: 30-49, Daumas-Duport C, Scheithauer B, O'Fallon J, el al: Grading of astrocytomas. A simple and reproducible method. Cancer 62: , Earnest F IV, Kelly P J, Scheithauer BW, et al: Cerebral astrocytomas: histopathologic correlation of MR and CT contrast enhancement with stereolactic biopsy. Radiology 166: , French JD, Bucy PC: Tumors of the septum pellucidum. J Neurosurg 5: , Fu YS, Chen ATL, Kay S, et al: Is subependymoma (subependymal glomerate astrocytoma) an astrocytoma or ependymoma? A comparative ultrastructural and tissue culture study. Cancer 34: , Hedley DW: How cytometry using paraffin-embedded tissue: five years on. Cytometry 10: , Jooma R, Torrens M J, Bradshaw J, et ai: Subependymomas of the fourth ventricle. Surgical treatment in 12 cases. J Neurosurg 62: , Just M, Thelen M: Tissue characterization with TI, T2, and proton density values: results in 160 patients with brain tumors. Radiology 169: , Matsumura A, Ahyai A, Hori A, et al: Intracerebral subependymomas. Clinical and neuropathological analy- ses with special reference to the possible existence of a less benign variant. Acta Neurochir 96:15-25, 1989 I1. Moss TH: Observations on the nature of subependymama: an electron microscopic study. Neuropathol Appl Neurobiol 10: Rubinstein L J: Tumors of the Central Nervous System. Atlas of Tumor Pathology, Series 2, Fascicle 6. Washington, DC: Armed Forces Institute of Pathology, 1972, pp Russell DS. Rubinstein LJ: Pathology of Tumours of the Nervous System, ed 5. Baltimore: Williams & Wilkins, 1989, pp Scheinker IM: Subependymoma: a newly recongized tumor of subependymal derivation. J Neurosurg 2: , Scheithauer BW: Symptomatic subependymoma. Report of 21 cases with review of the literature. J Neurosurg 49: , Vaquero J, Herrero J, Cabezudo JM, et al: Symptomatic subependymomas of the lateral ventricles. Acta Neuroehir 53:99-105, Vindelov LL, Christensen IJ, Nissen NI: A detergenttrypsin method for the preparation of nuclei for flow cytometric DNA analysis. Cytometry 3: , 1983 Manuscript received June 27, Accepted in final form April l, Address reprint requests to: Bernd W. Scheithauer, M.D., Surgical Pathology, Mayo Clinic, 200 First Street S.W., Rochester, Minnesota J. Neurosurg. / Volume 75 / October, 1991
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