Pigmented astrocytoma with suprasellar location: case report and literature review
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1 Acta Neuropathol (2004) 108: DOI /s CASE REPORT Ba rd Kronen Krossnes Æ Olav Mella Æ Knut Wester Sverre Jarl Mørk Pigmented astrocytoma with suprasellar location: case report and literature review Received: 7 April 2004 / Revised: 14 June 2004 / Accepted: 18 June 2004 / Published online: 7 September 2004 Ó Springer-Verlag 2004 Abstract A large suprasellar, partly cystic, contrastenhancing tumor was resected from a 19-year-old woman who presented with bitemporal visual field defects and reduced visual acuity. Grossly, the tumor was brown and located in the subarachnoid space. Histologically, it was composed of spindle and pleomorphic cells, including giant tumor cells, with markedly pleomorphic nuclei. Reticulin fibers surrounded single cells and small groups of cells. Very few mitotic figures were found in the tumor, and no necrosis or microvascular proliferation was seen. The tumor thereby resembled a pleomorphic xanthoastrocytoma. Many of the tumor cells contained a dark-brown intracytoplasmic pigment, shown to be melanosomal melanin by ultrastructural examination. Immunohistochemical examination demonstrated that the pigment was present in glial tumor cells. Only four cases of pigmented astrocytic tumors have been published, none of these were suprasellar. Our patient received fractionated radiotherapy with a total dose of 48.6 Gy 14 months after gross total removal of the tumor. She is alive without relapse after 12-year follow-up. Keywords Astrocytoma Æ Melanin Æ Pleomorphic xanthoastrocytoma Æ Suprasellar tumor B. K. Krossnes (&) Æ S. J. Mørk The Gade Institute, Department of Pathology, Haukeland University Hospital, 5021 Bergen, Norway bkkr@haukeland.no Tel.: Fax: O. Mella Department of Oncology, Institute of Medicine, Haukeland University Hospital, 5021 Bergen, Norway K. Wester Department of Neurosurgery, Institute of Surgical Sciences, Haukeland University Hospital, 5021 Bergen, Norway Introduction Pigmented (melanotic) neoplasms have been reported at various sites in the central and peripheral nervous system. The non-neuroepithelial pigmented intracranial tumors reported in the literature are schwannoma [46], benign and malignant melanocytic lesions arising from the leptomeninges [17] and possibly meningioma [21]. Previous reports on pigmented neuroepithelial tumors include astrocytoma [19, 39, 43], ganglioglioma [41], ependymoma [8, 28, 34], subependymoma [34], choroid plexus papilloma [33, 38, 45], choroid plexus carcinoma [5, 27], primitive pineal tumor [4, 31, 32, 35], medulloblastoma [3, 6, 10, 18, 40], medulloepithelioma [37], and central neurocytoma [30]. Ultrastructurally, some of these tumors contained melanosomal melanin [6, 10, 19, 27, 39, 40], while others contained neuromelanin and/or lipofuscin [5, 8, 30, 33, 43]. There are only four previous reports of melanotic astrocytomas: one case of pigmented pilocytic astrocytoma [43], one case of astrocytoma which resembled a pleomorphic xanthoastrocytoma (PXA) [19], one case of PXA [39], and one cerebral ganglioglioma with PXA as the glioma component [41]. Except for the pilocytic astrocytoma, which contained neuromelanin, the pigment in these tumors was shown to be melanosomal melanin. Here we present a melanotic astrocytoma with remarkable morphology and location. Clinical history The patient developed normally until she was years old. Growth then stopped and she developed some adiposity. She had menarche at the age of 12 years, but developed secondary amenorrhea after her first menstruation. Gynecological examination did not show pathology, but endocrinological examination showed low s-estradiol levels. The patient was given medroksyprogesteronacetate for 5 days four times a year to induce menstruation. At the age of 18, she was submitted
2 462 to hospital after a trauma to her left eye. Half a year later she was referred to an ophthalmologist because of reduced visual acuity on the right eye. Bitemporal visual field defects were then found, most pronounced on the right eye. Further examination by CT revealed a suprasellar, well-circumscribed, partly cystic, contrast-enhancing tumor measuring cm in anteroposterior, mediolateral, and vertical directions, respectively (Fig. 1). There was a slight destruction of the dorsum sellae. The radiological diagnosis was craniopharyngeoma. The pituitary function was normal except for low s-levels of growth hormone. The visual field defects progressed over the next months and at the time of surgery the patient had developed bitemporal hemianopsia. Frontal craniotomy was performed when the patient was 19 years old, disclosing a brown suprasellar tumor located in the subarachnoid space. The tumor was found to grow along, and ventral to, both optic nerves and optic chiasma. Small pigmented spots presumed to represent tumor tissue, on the optic nerves near the entrance to the optic canals and on the anterior/inferior rim of the optic chiasma, were not resected to avoid damaging the optic nerves. The immediate peroperative impression was that the tumor might have originated in the leptomeninges at the diaphragma sellae or the optic nerves/ chiasma. The tumor seemed less likely to have originated from the infundibulum or the hypothalamus, as the tumor mass was easily advanced from under the chiasma, apparently not adherent to the anterior aspects of the hypothalamus/pituitary stalk. Postoperative cerebral magnetic resonance imaging (MRI) confirmed the presence of very small lesions with contrast enhancement along both optic nerves and in a small area in the floor of the third ventricle, regarded as probable residual tumor. The visual field defects continued to progress for 1 year after the operation; after that no further visual impairment was observed. However, MRI could not document further tumor growth. To reduce the danger of blindness, the patient was given radiotherapy to the original tumor area with margins including the posterior orbit, the optic chiasma and the hypophysis. Radiotherapy was started 14 months postoperatively, 27 fractions of 1.8 Gy were given to a total dose of 48.6 Gy. After radiotherapy she needed thyroxin medication and also developed diabetes insipidus, whereas the cortisol production remained normal. The radiological findings have been stable, and completely unchanged, during follow-up, and the visual defects also have stabilized. She was well and free of clinical and radiological signs of relapse at last follow-up 12 years after the operation. Materials and methods The surgical specimen was fixed in 10% buffered formalin, routinely processed, and embedded in paraffin. Five-micrometer-thick sections were cut and the following stains were performed: hematoxylin-eosin, Wilder s reticulin silver impregnation, Masson-Fontana s methenamine silver method, Schmorl s ferric-ferricyanide method for melanin, Perl s Prussian blue, periodic acid-schiff with and without prior treatment with diastase, and acid-fast stain (long Ziehl-Neelsen). For immunohistochemical study, paraffin-embedded sections were stained with primary antibodies against: glial fibrillary acidic protein (GFAP, polyclonal, 1:3,000) with and without prior bleaching (for 2 h) with 0.25% potassium permanganate, S-100 protein (polyclonal, 1:800) with and without prior bleaching with potassium permanganate, synaptophysin (polyclonal, 1:100), chromogranin-a (polyclonal, 1:1,600), neuron-specific enolase (monoclonal, 1:200), melanosome-associated antigen HMB-45 (monoclonal, 1:50), neurofilament protein (monoclonal, 1:400), vimentin (monoclonal, 1:100), desmin (monoclonal, 1:50), laminin (monoclonal, 1:25), epithelial membrane antigen (monoclonal, 1:200), cytokeratin (monoclonal, 1:25 DAKO code no. M0821), Ki-67 (MIB-1, monoclonal, 1:50), and p53 (monoclonal, 1:25). All primary antibodies were from DAKO. Immunohistochemical procedures were performed on the automatic immunostainer DAKO TechMate 500 with the DAKO ChemMate Detection Kit, peroxidase/ DAB (code no. K 5001), which is a detection system based on an indirect streptavidin-biotin method. The Ki- 67 labeling index was expressed as a percentage of the total number of cells after counting 1,000 cells in the area with highest number of stained nuclei. For electron microscopic examination, representative areas were excised from one of the paraffin blocks, washed with phosphate buffer, fixed in McDowell solution, postfixed with 1% osmium tetroxide and embedded in Epon 812. Ultrathin sections were cut and stained with uranyl acetate and lead citrate, and examined with a Philips TEM 410 electron microscope at 60 kv. Fig. 1 CT scans after contrast-injection showing a sharply demarcated, suprasellar, contrast-enhancing tumor. A Transverse section (maximal tumor diameter 3.2 cm). B Coronal section Results The formalin-fixed biopsy specimen showed a tumor composed of large pleomorphic cells with copious
3 463 eosinophilic cytoplasm. Spindle-shaped cells forming fascicles dominated, and larger, plumper, often multinucleated cells were interspersed between the spindlefig. 2 Histological features of the tumor. A Fascicles of pleomorphic, spindle-shaped cells with pigmented areas (hematoxylin and eosin). B Pleomorphic glial cells with highly atypical nuclei (hematoxylin and eosin). C Many tumor cells contain melanin pigment granules (green-blue) (Schmorl). D Reticulin fibers surround individual cells and small groups of cells (reticulin silver impregnation). E The tumor cells display GFAP immunoreactivity (red) (immunoperoxidase). F Co-localization of GFAP-immunoreactive fibrils (red) and melanin pigment granules (dark-brown) is seen in the cells in the center (immunoperoxidase). A, D 100; B, C, E 200; F 630 shaped cells. The tumor cells had large, pleomorphic, hyperchromatic nuclei. Coarse chromatin and prominent nucleoli were often seen and nuclear inclusions were common (Fig. 2A, B). Xanthomatous cells were not present. Mitoses were rare (less than 1 per 50 highpower fields). Dark-brown pigment granules were found in many tumor cells, particularly spindle-shaped cells. The pigment was colored green-blue by Schmorl (Fig. 2C), and black with Masson-Fontana. It was negative for Perl s Prussian blue, acid-fast stain, and periodic acid-schiff. The pigment was completely bleached with potassium permanganate. Staining with
4 464 Wilder s reticulin silver impregnation revealed reticulin fibers surrounding individual cells and small groups of cells (Fig. 2D). In one area a few eosinophilic granular bodies were found. The eosinophilic granular bodies were stained red with periodic acid-schiff both with and without prior treatment with diastase. Focally, a slight perivascular infiltration of small lymphocytes was seen. No necrosis or microvascular proliferation was found. Brain tissue was not found in any of the sections. Immunohistochemical examination showed strong positivity for GFAP (Fig. 2E), S-100 protein, and vimentin in the tumor cells. About half of the cells were also positive for neuron-specific enolase. Co-localization of GFAP and pigment granules was found in some tumor cells (Fig. 2F), but generally the GFAP staining was weaker in the pigmented than in the non-pigmented tumor cells. Co-localization of S-100 and pigment granules was also found. The tumor was negative for the following antibodies: synaptophysin, chromogranin-a, neurofilament protein, HMB-45, epithelial membrane antigen, cytokeratin, desmin, and p53. No basal lamina surrounding individual cells was found in sections stained for laminin. The MIB-1 labeling index was 3%. Ultrastructural examination revealed large numbers of mature melanosomes and also some stage II and III melanosomes in pigmented tumor cells (Fig. 3). Neuromelanin or lipofuscin granules were not found. Bundles of filaments, probably intermediate filaments, were found in many tumor cells, particularly in long, thin cytoplasmic processes. Condensed fibers were found around several cells, but typical basal lamina was not present. Discussion This tumor was difficult to classify when it was examined in 1991, and was diagnosed as a pleomorphic, possibly anaplastic, astrocytic tumor with melanin pigmentation. Using the current (2000) WHO classification [24] the tumor is probably best regarded as a PXA. This entity Fig. 3 Electron microscopical features of tumor cells. A A tumor cell containing mature melanosomes. B Less mature (stage II and III) melanosomes are found in some cells. A 32,000; B 60,000 was first described by Kepes et al. in 1979 [22], but was not included in the WHO classification of CNS tumors before 1993 [25]. The fascicular arrangement of neoplastic cells, great cellular pleomorphism, low mitotic activity, prominent pericellular reticulin network, perivascular lymphocytes, subarachnoidal location of the tumor (without brain invasion), and CT findings (a discrete, contrast-enhancing and cystic tumor), are consistent with the diagnosis PXA [23]. On the other hand, the tumor lacks xanthomatous cells typical for PXA and contains only scarce eosinopilic granular bodies. This diagnosis, however, does not depend on the presence of xanthomatous cells [7, 16]. The proliferation rate as evaluated by the MIB-1 labeling index (3%) is somewhat higher in the present case than generally reported in this entity (lower than 1%) [23]. However, it is well known that comparison of labeling indexes reported from different institutions using different Ki-67 antibodies must be done with caution [42]. PXA is most often located superficially in the cerebral hemispheres. The suprasellar location of the present case is therefore rare for PXA, but a case of PXA with a similar location (just above the sella turcica) has been reported by Heyerdal Strøm et al. [14]. This tumor entity has also been described in the thalamus [26], and even an intrasellar PXA is on record [1]. Our patient had growth arrest, adiposity, and secondary amenorrhea from the age of 12 years, symptoms that may have been caused by the suprasellar tumor, indicating a slow tumor growth over several years until she underwent surgery at the age of 19. The long postoperative survival in the present case also indicates that this tumor is a low-grade astrocytoma, as anaplastic astrocytomas, even after radiotherapy, rarely have this long survival. It is interesting to note that the four earlier reported pigmented astrocytomas were low-grade tumors (pilocytic astrocytoma, PXA and ganglioglioma with PXA as the glioma component). These cases were located in the temporal lobe and associated with long-standing epilepsy, as opposed to our patient, where the tumor was located to the suprasellar area, not associated with seizures. Recurrence of the tumor has not been reported in any of the earlier reported pigmented astrocytomas; however, only one report describes a follow-up of more than 2 years after
5 465 surgery [41]. Our case is thus the first published case where long-term postoperative course without relapse has been documented, indicating that pigmented PXA do not differ from ordinary PXA concerning prognosis. Melanocytes, derived from the neural crest, are normally present in the pia mater of adult human subjects, although they are seldom recognized, except over the ventrolateral surface of the medulla oblongata and upper spinal cord [13]. These cells are the presumed origin of melanotic lesions in the meninges such as melanocytoma and malignant melanoma [17]. Melanin is normally produced in a specialized organelle called the melanosome. This organelle contains the enzyme tyrosinase, which is involved in the oxidation of tyrosine to the pigmented polymers we call melanin [36]. Production of melanosomal melanin in tissues of central neuroepithelial origin is developmentally restricted in humans to the fetal pineal gland [11] and to the pigmented layer of the retina [29]. Astrocytes are not involved in either of these synthetic modalities. Experiments in the OTT-6050 mouse teratoma model have shown that melanosomal melanin may be produced in primitive central neuroepithelial cells [12, 44]. Neuromelanin, which is believed to be a product of auto-oxidation of precursors in catecholamine synthesis, is normally found in certain groups of neurons such as substantia nigra and locus ceruleus. Ultrastructurally, neuromelanin is similar to lipofuscin [15]. Neuromelanin and melanosomal melanin have similar staining qualities in that they both are Schmorl and Masson-Fontana positive, with positivity disappearing after potassium permanganate bleaching [8]. In the present case lack of staining with periodic acid-schiff and acid-fast stain excludes the possibility that the pigment is lipofuscin [2, 8]. Ultrastructurally, the pigment was shown to be melanin by the finding of stage II and III melanosomes (premelanosomes) [9], and no neuromelanin was found. The pigmented cells tended to be spindle shaped, and generally had smaller nuclei than the large plumper tumor cells. Theoretically, the pigmented cells could be entrapped leptomeningeal melanocytes, proliferating in response to the astrocytic tumor. It was difficult to demonstrate positive reaction for GFAP in the pigmented cells by immunohistochemistry, but this may have been related to the intense pigmentation in most of the cells. A few pigmented cells were, however, positive for GFAP (Fig. 2F). Three of the four reported pigmented astrocytomas contained melanosomal melanin, and it was concluded that the pigment was present in neoplastic glia cells [19, 39, 41]. The pigmented cells were negative for HMB-45, which is a monoclonal antibody that detects a glycoconjugate present in immature melanosomes [20]. Negativity for HMB-45 was also found in the three earlier described pigmented astrocytomas with ultrastructurally documented premelanosomes [19, 39, 41]. One pigmented medulloblastoma has been reported to be negative for HMB-45 [3], whereas some of the pigmented cells were positive for HMB-45 in another case [40]. Pigmented schwannomas and the melanocytic lesions of the leptomeninges are most often positive for HMB-45 [24]. These findings indicate that HMB-45 should not be expected to be demonstrable by immunohistochemistry in pigmented gliomas even if melanosomal melanin is found ultrastructurally. We have here presented the fifth published example of a pigmented astrocytoma. This case provides further evidence that not only tumors derived from the neural crest, but also neuroepithelial tumors originating from cells derived from the primitive neural tube, may produce melanosomal melanin. The long postoperative survival indicates that pigmented PXA have a good prognosis. References 1. Arita K, Kurisu K, Tominaga A, Sugiyama K, Sumida M, Hirose T (2002) Intrasellar pleomorphic xanthoastrocytoma: case report. 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monotonous, stippled, round, smoothcontoured nuclei and scanty acidophilic or
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