A case of multinodular high-grade neuroepithelial tumor
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1 Brain Tumor Pathol (2011) 28: DOI /s CASE REPORT A case of multinodular high-grade neuroepithelial tumor with ependymal differentiation Kensaku Kamada Yuko Tanaka Takayuki Matsuo Shiro Baba Kenta Ujifuku Kazuhiko Suyama Yoichi Nakazato Izumi Nagata Received: 4 November 2010 / Accepted: 5 March 2011 / Published online: 8 April 2011 Ó The Japan Society of Brain Tumor Pathology 2011 Abstract We describe a rare case of multinodular cerebral neuroepithelial tumor with ependymal differentiation. A 65-year-old man experienced loss of consciousness with an obscure episode of seizure attack. Magnetic resonance images disclosed a lesion located in the left temporal lobe and the insular cortex. The tumor was partially removed. Histologically, the tumor showed infiltrating multinodular tumor nodules in the cerebrum. Each nodule was well demarcated and composed of clear cells with perinuclear halos, intermingled fibrillary cells, and poorly differentiated neuroepithelial cells with mitotic activity. Immunohistochemically, clear cells showed dot-like positivity for epithelial membrane antigen. Fibrillary cells were positive for vimentin and nestin, whereas only a few glial fibrillary acidic protein-immunopositive cells were seen. We conclude that this tumor, being microscopically characterized by multinodular tumor nodules, was a high-grade neuroepithelial tumor with ependymal differentiation. Keywords Ependymoma Ependymal differentiation Neuroepithelial tumor Epithelial membrane antigen (EMA) Central nervous system primitive neuroectodermal tumors (CNS PNET) K. Kamada (&) T. Matsuo S. Baba K. Ujifuku K. Suyama I. Nagata Department of Neurosurgery, Nagasaki University School of Medicine, Sakamoto, Nagasaki , Japan k-kamada@nagasaki-u.ac.jp Y. Tanaka Y. Nakazato Department of Human Pathology, Gunma University Graduate School of Medicine, Maebashi, Japan Introduction In most instances, brain tumors have some characteristics that impart information for the diagnosis. However, we sometimes encounter rare cases that are difficult to diagnose. We report a case of neuroepithelial tumor in the cerebrum, a high-grade tumor with ependymal differentiation, containing poorly differentiated neuroepithelial cells. The microscopic multinodular pattern is extremely rare, and it is hard to categorize this tumor into defined groups or entities of the World Health Organization (WHO) classification now in use [1]. Clinical summary A 65-year-old man experienced loss of consciousness with an obscure episode of seizure attack. He was then admitted to our institution with no neurological deficit. Magnetic resonance (MR) images disclosed a lesion in the left temporal lobe and the insular cortex. MR images showed hypointense signal on T 1 -weighted MR images, hyperintense signal on T 2 -weighted MR images, and no enhancement on T 1 gadolinium (Gd) image (Fig. 1a d). Functional MR images revealed that the left hemisphere was dominant. Single photon emission computerized tomography showed no uptake of thallium-201. An angiogram demonstrated no tumor stain. We performed awake surgery to achieve maximum tumor excision with no verbal deficit. Although we identified the language area, we could not carry on awake surgery because of the occurrence of epileptic activity in the electroencephalogram. We then removed the left temporal tip lesion partially. Macroscopically, the tumor was soft, yellowish white, nonhemorrhagic, and difficult to
2 254 Brain Tumor Pathol (2011) 28: Fig. 1 Preoperative magnetic resonance imaging (MRI). a, b Axial fluid-attenuated inversion recovery (FLAIR) MRI shows hyperintense signal in the left temporal lobe and the insular cortex. c, d T 1 -weighted images obtained after gadolinium-diethylenetriamine pentaacetic acid (Gd-DTPA) administration show no enhancement Fig. 2 MRI 10 months after operation. No recurrence is seen on FLAIR MRI (a) or T 1 -weighted image with Gd-DTPA (b) distinguish from surrounding normal brain. Subsequently, the patient was administered a total 60 Gy of radiotherapy and prescribed 120-mg temozolomide capsules daily for 42 days. The follow-up MR imaging scan showed an image consistent with no tumor relapse at 10 months after the operation (Fig. 2). Pathological findings Histologically, the tumor showed multinodular tumor nodules in the cerebrum (Fig. 3). In the marginal zone of the tumor, nodules were dispersed and infiltrating in the brain parenchyma. Each nodule was well demarcated and separated by a band of cerebral tissue with slight astrocytic gliosis (Fig. 4a, b). Each nodule was composed of clear cells, showing perinuclear haloes (Fig. 4c), and fibrillary spindle cells. These cells had round to oval nuclei with finely speckled chromatin. Fibrillary spindle cells surrounded the clear cell nests, forming background fibrillary stroma containing a rich branching capillary network (Fig. 4d). A perivascular anuclear zone with fibrillary processes was seen (Fig. 4e); however, neither classic perivascular pseudorosettes nor true ependymal rosettes were found. Some nodules were similar to primitive neuroectodermal tumors (PNET), being composed of densely
3 Brain Tumor Pathol (2011) 28: Fig. 3 Low-power view shows multilocular tumor nodules in the cerebrum. Bar 1mm packed cells with carrot-shaped hyperchromatic nuclei and scanty cytoplasm (Fig. 4f), and sometimes arranged in polar spongioblastoma-like fashion. Tumor cells showed increased mitotic activity; on average, as many as 5 mitotic figures were seen per 10 high-power fields. In the highly cellular PNET-like area, as many as 20 mitotic figures per 10 high-power fields were seen, and apoptosis was also prominent. Necrosis and microvascular proliferation were not seen. Immunohistochemically, tumor cells with fibrillary processes were focally positive for glial fibrillary acidic protein (GFAP) (Fig. 5a). Olig2 (Fig. 5b) was completely immunonegative except that immunopositivity was seen for intervening oligodendrocytes. Epithelial membrane antigen (EMA) immunoreactivity had a characteristic dotlike and ring-like appearance (Fig. 5c) in tumor cells. Cytoplasm and processes of fibrillary cells were strongly stained for nestin (Fig. 5d) and partially stained for vimentin. Neuronal antigens, such as neurofilament protein Fig. 4 a Multiple tumor nodules were seen in the cerebrum. b Cortical neurons and neuropils with fibrillary astrocytic gliosis were seen in the internodular spaces. c Clear cells tended to form small nests and mimic oligodendroglioma. d Clear cells and fibrillary cells were intermingled in the fibrillary stroma. e Fibrillary processes were irregularly arranged in the perivascular anuclear zone. f Tumor cells in the primitive neuroectodermal tumor (PNET)-like area showed high nuclear to cytoplasmic ratio with mitotic and apoptotic activity. a 950; b, d, e 9200; c, f 9400
4 256 Brain Tumor Pathol (2011) 28: Fig. 5 a Astrocytes in the cerebral tissue and intratumoral reactive astrocytes (arrows) showed strong GFAP expression and a few tumor cells (arrowhead) showed immunopositivity for tumor cytoplasm and processes. b Olig2 was immunopositive for residual oligodendroglia, but tumor cells showed no expression of this antigen. c Dot-like and ring-like epithelial membrane antigen (EMA) positivity was seen in the tumor cytoplasm or pericellular area. d Cytoplasm and processes of fibrillary spindle cells showed nestin immunoreactivity. e Neurofilament protein was immunonegative for tumor cells. Internodular neuron and entrapped cortical neuron were immunoreactive for neurofilament (NF). f High proliferative activity was demonstrated by MIB-1 antibody; positive cells were especially seen in the PNETlike area. a, b, d, e, f 9200; c 9400 (NF) (Fig. 5e), NeuN, synaptophysin, and class III b tubulin were immunonegative for either clear/fibrillary cells or PNET-like tumor cells. MIB-1 labeling index was 23.7% in the PNET-like area (Fig. 5f). Discussion The poorly defined tumor without Gd enhancement seemed to be low-grade glioma on the MR images. However, histopathology revealed unique characteristics, that is, a multinodular pattern with morphological diversity in the present case. The morphology of clear cells with perinuclear haloes and spindle cells with fibrillary processes suggested glial differentiation of the tumor. Among glial tumors, the formation of a perivascular anuclear zone and the well-demarcated growth pattern of each nodule seemed especially to resemble ependymoma. The presence of clear cells with oligodendroglia-like appearance in this tumor urged discrimination among clear cell ependymoma, oligodendroglioma, central neurocytoma, clear cell carcinoma, and hemangioblastoma. The clear cells of this tumor showed a characteristic dot-like and ring-like appearance for EMA immunostaining, which is commonly seen in ependymoma [2]. Additionally, as in this tumor, immunopositivity for vimentin [3] and nestin [4] but immunonegativity for Olig2 [5] in ependymoma have been reported. Scarce immunopositivity for GFAP and immunonegativity for S100 protein [6, 7] as seen in the present case were not typical for ependymoma. The reason those antigens were reduced or disappeared was unclear. One possibility is that this tumor has a malignant potential or immaturity demonstrated by increased mitotic activity and high MIB-1 labeling index, compared to the usual ependymoma [8], and the existence of a poorly differentiated
5 Brain Tumor Pathol (2011) 28: PNET-like area. It has been reported that expression of vimentin and nestin was seen in developing tumors whereas GFAP tended to increase with tumor maturation [9]. In this case, the tumor existed as a cortical ependymoma without attachment to the ventricular system. Miyazawa et al. [10] reported 14 cases of cortical ependymoma, of which, interestingly, half were diagnosed as clear cell ependymoma or anaplastic ependymoma. This tumor showed some pathological similarity to these in its location and the unique pathological findings. Considering the malignant potential of the tumor, the patient underwent radiotherapy and chemotherapy with temozolomide as adjuvant treatment. He has remained free of recurrence for 10 months. We believe that this combination therapy is presently reasonable and appropriate. However, evaluating which procedure is more effective, radiotherapy or chemotherapy, is difficult. In conclusion, we experienced a tumor that resembled clear cell ependymoma but showed anaplasia with a PNETlike embryonal component without necrosis and microvascular proliferation. As it could not be categorized by the WHO classification of tumors of the central nervous system, we regarded this tumor as high-grade neuroepithelial tumor with ependymal differentiation. Its characteristic morphological architecture of well-demarcated multinodular tumor nodules was extremely unusual and has not previously been reported. Acknowledgments This work was supported in part by a Nagasaki University President s Fund Grant. References 1. Louis DN, Ohgaki H, Otmar D et al (2007) WHO classification of tumors of the central nervous system, 4th edn. IARC Press, Lyon 2. Kawano N, Yasui Y, Utsuki S, Oka H et al (2004) Light microscopic demonstration of the microlumen of ependymoma: a study of the usefulness of antigen retrieval for epithelial membrane antigen (EMA) immunostaining. Brain Tumor Pathol 21: Figarella BD, Gambarelli D, Dollo C et al (1991) Infratentorial ependymomas of childhood. Correlation between histological features, immunohistological phenotype, silver nucleolar organizer region staining values and post-operative survival in 16 cases. Acta Neuropathol (Berl) 82(3): Almqvist PM, Mah R, Lendahl U et al (2002) Immunohistochemical detection of nestin in pediatric brain tumors. J Histochem Cytochem 50: Ishizawa K, Komori T, Shimada S, Hirose T (2008) Olig2 and CD99 are useful negative markers for the diagnosis of brain tumors. Clin Neuropathol 27(3): Kimura T, Budka H, Soler FS (1986) An immunocytochemical comparison of the glia-associated proteins glial fibrillary acidic protein (GFAP) and S-100 protein (S100P) in human brain tumors. Clin Neuropathol 5: Gullota F, Schindler F, Schmultzler R et al (1985) GFAP in brain tumor diagnosis: possibilities and limitations. Pathol Res Pract 180: Kurt E, Zheng PP, Hop WC et al (2006) Identification of relevant prognostic histopathologic features in 69 intracranial ependymomas, excluding myxopapillary ependymomas and subependymomas. Cancer (Phila) 106: Engelhard HH, Duncan HA, Del Canto M (1997) Molecular characterization of glioblastoma cell differentiation. Neurosurgery 41(4): Miyazawa T, Hirose T, Nakanishi K et al (2007) Supratentorial ectopic cortical ependymoma occurring with intratumoral hemorrhage. Brain Tumor Pathol 24(1):35 40
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