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1 J Neurosurg 118: , 2013 AANS, 2013 Metachronous, multicentric glioma of pilocytic astrocytoma with oligodendroglioma-like component and oligodendroglioma through distinct genetic aberrations Case report Atsushi Kanoke, M.D., 1 Masayuki Kanamori, M.D., Ph.D., 1 Toshihiro Kumabe, M.D., Ph.D., 1 Ryuta Saito, M.D., Ph.D., 1 Mika Watanabe, M.D., Ph.D., 2 and Teiji Tominaga, M.D., Ph.D. 1 1 Department of Neurosurgery, Tohoku University Graduate School of Medicine; and 2 Department of Pathology, Tohoku University Hospital, Sendai, Miyagi, Japan This patient presented with a rare case of metachronous, multicentric gliomas first manifesting as headache and nausea in 1983 when he was an 8-year-old boy. Computed tomography revealed a cerebellar tumor and the tumor was subtotally resected. The histological diagnosis was pilocytic astrocytoma, and radiation therapy to the posterior fossa and chemotherapy consisting of nimustine hydrochloride and fluorouracil were performed. In 1989, at age 14 years, the patient presented with local recurrence. He underwent gross-total resection of the tumor, and histological examination revealed that the tumor consisted of classic pilocytic astrocytoma with a biphasic pattern and a small oligodendroglioma-like component. In 2011, at age 36 years, he presented with seizure. Magnetic resonance imaging revealed a mass lesion in the right middle frontal gyrus. Gross-total resection of the tumor was performed, and the histological diagnosis was oligodendroglioma. Genetic analyses revealed amplification of the BRAF gene in both the primary cerebellar pilocytic astrocytoma and the recurrent tumor with biphasic features, as well as a BRAF V600E missense mutation in the oligodendroglioma-like component. On the other hand, the IDH1 R132H mutation, instead of aberrations of the BRAF gene, was identified in the oligodendroglioma arising in the right frontal lobe. Different types of aberrations of the BRAF gene in the classic and oligodendroglioma-like component in the recurrent pilocytic astrocytoma suggest that they had different cell origins or that amplification of BRAF was negatively selected under the de novo BRAF V600E mutation. In addition, the aberration profiles of IDH1 and BRAF suggest that the oligodendroglioma arose independent of cerebellar pilocytic astrocytoma. ( Key Words pilocytic astrocytoma oligodendroglioma-like component oligodendroglioma IDH1 BRAF oncology Multicentric gliomas are defined as lesions with widely separated locations in different lobes and can be classified based on the time of occurrence. 2 Metachronous tumors are defined as multiple de novo tumors in different sites, with a long interval between the development of the first and second lesions ranging from 0.5 to 25 years. Multicentric gliomas are a well-recognized entity, but the mechanisms, including the cell of origin and the development pathways, remain unknown. Recently, two distinct and mutually exclusive pivotal pathways for the development of pilocytic astrocytoma and oligodendrocytic and astrocytic tumors have been identified. 1,4,8,15,16,20 Duplication at chromosome band 7q34 containing the BRAF-KIAA1549 gene fusion or Abbreviation used in this paper: FISH = fluorescence in situ hybridization. BRAF gene mutation is found in the majority of cases of pilocytic astrocytoma, whereas somatic mutations in the IDH1 or IDH2 gene are frequently observed in adult astrocytoma or oligodendroglioma. In the present paper we report on a case of pilocytic astrocytoma developing local recurrence with a newly developed oligodendroglioma-like component and an oligodendroglioma presenting as metachronous, multicentric glioma through distinct genetic aberrations. Summary of Presentations Case Report First Presentation. This 8-year-old boy first presented to our hospital in 1983 with headache, nausea, and emesis. He was alert and had truncal ataxia. Computed tomography revealed a cystic tumor at the cerebellar vermis. He 854
2 Metachronous, multicentric glioma underwent subtotal resection of the tumor via the suboccipital approach. Postoperative CT scanning showed a residual lesion of the cystic wall (Fig. 1A). Histological examination of the first surgical specimen revealed proliferating neoplastic glial cells with piloid features with long, slender bipolar processes. The cellularity was low with myxoid background. Many Rosenthal fibers with strong eosinophilic club-shaped structures and eosinophilic granular bodies showing hyalinosis globular features were observed. The tumor tissue contained pro liferation of vessels, and some vessels showed microvascular proliferation with a characteristic wickerwork pattern (Fig. 1B). Immunohistochemical examination revealed that the tumor cells were focally positive for GFAP, and 0.5% of the neoplastic cells were positive for the monoclonal antibody for Ki 67. The histological diagnosis was pilocytic astrocytoma (WHO Grade I). The patient underwent radiotherapy (a 50-Gy dose of radiation to the posterior fossa) and chemotherapy consisting of nimustine hydrochloride and fluorouracil. Second Presentation. In 1989, follow-up MRI re vealed enlargement of the cystic portion of the lesion when the patient was age 14 years (Fig. 2A). Gross-total resection of the tumor was performed. Histological examination of the second surgical specimen revealed a typical biphasic pattern consisting of compact areas with piloid, spindled cells and hypocellular loose myxoid areas with microcystic features (Fig. 2B). Eosinophilic Rosenthal fibers were observed, especially in the compact areas. Other portions of the tumor tissue had oligodendroglioma-like features with fried egg shaped tumor cells, as well as microcalcification (Fig. 2E). Immunohistochemical examination revealed that the tumor cells in the compact areas were strongly positive for GFAP, vimentin, and Olig2, and tumor cells in the loose areas and oligodendroglioma-like areas were negative for GFAP, but positive for vimentin and Olig2. Immuno staining with MIB-1 monoclonal antibody to detect Ki 67 antigen showed a labeling index of 0.3%. The histological diagnosis was pilocytic astrocytoma (WHO Grade I), with focal oligodendroglioma-like features. He did not receive any adjuvant therapy. Third Presentation. The patient was lost to follow-up for 22 years after the second surgery. In 2011 he suffered generalized tonic convulsion and visited our hospital at age 36 years. A hyperintense area in the right middle frontal gyrus was demonstrated on T2-weighted MRI (Fig. 3A), outside the previously irradiated field, but there was no recurrence of the cerebellar lesion. The patient underwent gross-total resection of the tumor. Histological examination of the third surgical specimen revealed a proliferation of round to oval neoplastic cells with a perinuclear halo in the cerebral cortex and white matter. These fried egg shaped tumor cells had aggregated and exhibited a honeycomb appearance in some parts. No microvascular proliferation or necrosis (Fig. 3B), and no foci of pilocytic astrocytoma, were detected. Immunohistochemical examination revealed that the tumor cells were negative for GFAP and strongly positive for Olig2. Immunostaining with MIB-1 monoclonal antibody to detect Ki 67 antigen showed a labeling index of 11.6%. The histological diagnosis was oligodendroglioma (WHO Grade II). Genetic Analysis The patient provided informed written consent for molecular analyses of the BRAF and IDH1 genes. Molecular analyses were approved by our institutional review board of Tohoku University Graduate School of Medicine. The tumor specimens were analyzed for mutations in the IDH1 and BRAF genes by direct sequencing, and copy number Fig. 1. First presentation. A: Contrast-enhanced CT scan after first surgery demonstrating the resection cavity and enhanced residual lesion at the posterior wall. B: Photomicrograph demonstrating tumor cells with bipolar and long processes, eosinophilic cytoplasm, Rosenthal fibers (arrows), and vascular wickerwork pattern. H & E, original magnification 400. C: Sequencing analysis showing no nucleotide substitutions in the BRAF gene. D: FISH analysis demonstrating allelic amplification of the BRAF loci. 855
3 A. Kanoke et al. Fig. 2. Second presentation. A: Axial Gd-DTPA T1-weighted MR image before second surgery demonstrating the cystic lesion with enhancement of the cyst wall. B D: Investigation of the classic pilocytic astrocytoma component. B: Photomicrograph revealing that the tumor consists of a biphasic pattern of compact areas with Rosenthal fibers and hypocellular areas with microcysts. H & E, original magnification 200. C and D: Sequencing analysis (C) showing no mutations in the BRAF gene, and FISH analysis (D) showing duplication of the BRAF loci. E G: Investigation of the oligodendroglioma-like component. E: Photomicrograph demonstrating the honeycomb feature and calcification in a small area of the tumor. H & E, original magnification 400. F and G: Sequencing analysis (F) showing heterozygous nucleotide substitutions (arrow) causing missense mutations (V600E) in the BRAF gene, and FISH analysis (G) showing no copy number changes of BRAF loci. changes of BRAF loci by FISH using Vysis LSI BRAF SpectrumGold Probe (Abbott). DNA of the recurrent pilocytic astrocytoma was extracted from laser microdissected paraffin-embedded sections, and DNA of oligodendroglioma from the third surgery was extracted from snapfrozen tissue. Amplification of BRAF loci was detected in the primary cerebellar pilocytic astrocytoma and biphasic pilocytic astrocytoma component of the recurrent pilocytic astrocytoma (Figs. 1D and 2D), whereas there were no mutations in IDH1 and BRAF (Figs. 1C and 2C) in this lesion. In contrast, IDH1 R132H mutation (Fig. 3C), but no mutation or amplification (Fig. 3D) of the BRAF gene, was found in the oligodendroglioma from the third surgery. The recurrent pilocytic astrocytoma contained an oligodendro- Fig. 3. Third presentation. A: Axial Gd-DTPA T1-weighted MR image and T2-weighted MR image before third surgery demonstrating diffuse lesion without enhancement in the right middle frontal gyrus. B: Photomicrograph demonstrating that the tumor consists of small round cells with clear cytoplasm in fibrous matrix without microvascular proliferation or necrosis. H & E, original magnification 400. C and D: Sequencing analysis (D) showing heterozygous nucleotide substitutions (arrow) causing missense mutations (R132H) in the IDH1 gene, and FISH analysis (D) of the BRAF loci. 856
4 Metachronous, multicentric glioma glioma-like component, which was further investigated to clarify the relationship between pilocytic astrocytoma and oligodendroglioma. The oligodendroglioma-like component was analyzed for copy number changes of BRAF loci with FISH, and for mutations of IDH1 and BRAF in the DNA extracted from microdissected tissue. Interestingly, the oligodendroglioma-like lesion carried a BRAF V600E mutation without amplification of the BRAF gene or mutation in the IDH1 gene (Fig. 2F and G). The results of these analyses are summarized in Table 1. Discussion Pilocytic astrocytomas correspond to WHO Grade I tumors, 10,11 and overall survival rates are 95.8% 100% at 10 years. 3,13 The pattern of failure is local recurrence within 8 years, and the extent of resection is a strong prognostic factor. 13 Disseminated lesions are very common in hypothalamic pilocytic astrocytoma, 12 but distant recurrences are rare in cerebellar pilocytic astrocytoma. Moreover, the histology of these distant recurrences is the same as that of the primary lesion, 12 and, to our knowledge, no previous case of cerebellar pilocytic astrocytoma has involved histologically different tumors occurring distant from the primary site during long-term follow-up. The present case fulfills the clinical, radiological, and histological criteria for metachronous, multicentric gliomas. 2 The largest reported series of 25 cases with multicentric glioma demonstrated several clinical and histological features. 19 First, the most common histological feature was multicentric glioblastoma, and most cases had high-grade glioma. In contrast, only 2 of 25 cases involved low-grade glioma and glioblastoma, and no cases had multicentric low-grade glioma. Second, metachronous, multicentric gliomas were relatively rare compared with synchronous gliomas. 12 Only one case of multicentric low-grade glioma has been reported with simultaneous oligodendroglioma and pilocytic astrocytoma. 5 The present case represents the extremely rare entity of a metachronous low-grade glioma with long-term latency. Across long intervals, our patient had 3 histologically distinct lesions, including classic pilocytic astrocytoma at first and second presentations, an oligodendroglioma-like component of pilocytic astrocytoma at second presentation, and an oligodendroglioma at third presentation. Genetic aberrations may provide interesting indications to elucidate their mechanism of development. First, this case had a local recurrence of pilocytic astrocytoma, consisting of the classic component having BRAF amplification and the oligodendroglial component having a BRAF V600E mutation. It has been reported that either amplification or mutation of the BRAF gene was frequently found in pilocytic astrocytoma in mutually exclusive fashion. 16 Intratumoral genetic heterogeneity occurs in pilocytic astrocytoma, oligoastrocytoma, astrocytoma, and glioblastoma. 17,18,21,25 However, demonstration of an intratumoral heterogeneous type of aberration of a single gene in the tissue of a single tumor is noteworthy, and this finding could lead to a different morphological phenotype in the same tumor. Our observations suggest that the oligodendroglioma-like component had the genetic characteristics of pilocytic astrocytoma but that the mechanism causing the aberrations in the BRAF gene was different from that of classic pilocytic astrocytoma. Because the primary pilocytic astrocytoma did not carry the BRAF V600E mutation, pilocytic astrocytoma and oligodendroglioma-like component in the first recurrent tissue had a different cell origin, or the amplification of BRAF was negatively selected under de novo BRAF V600E mutation. Second, we investigated the mechanism for the occurrence of metachronous, multicentric glioma, based on the analysis for IDH1 and BRAF mutation and BRAF amplification. Previously, differences and similarities in genetic aberrations have been reported in cases of multicentric lesions. 5,7,24 Multicentric spinal ependymomas had the same chromosome aberrations, 24 whereas multicentric gliomas showed different profiles at 1p/19q loci. 5,7 The present analysis showed that the pilocytic astrocytoma and oligodendroglioma had typical aberration profiles frequently observed in sporadic cases. The development of the multicentric pilocytic astrocytoma and oligodendroglioma in the present case was consistent with the idea that a mutation in the IDH1 gene and aberrations in the BRAF gene are mutually exclusive. This finding strongly suggests that these multicentric lesions developed independently through different molecular pathways. In addition, judging from the different genetic aberration profiles found in the oligodendroglioma-like component in the second specimen and in the oligodendroglioma in the third specimen, these 2 histologically similar regions developed from different cells of origin and are most likely the conjunction of rare, random events. Genetic analyses revealed that the multicentric gliomas developed independently in the present case, but the direct cause for multicentric lesions remains unknown. The well-recognized etiologies of glioma are familial tumor syndrome, including neurofibromatosis Type 1, Li- Fraumeni, and Turcot syndromes, prior radiation therapy, and chemotherapy. 6,9,10,11,22 Our patient had no family his- TABLE 1: Summary of genetic aberrations* Presentation Histology Copy No. BRAF Mutation IDH1 Mutation 1st PA (biphasic component) amplification wild-type wild-type 2nd PA (biphasic component) amplification wild-type wild-type 2nd PA (oligodendroglioma-like component) no changes V600E wild-type 3rd oligodendroglioma no changes wild-type R132H * PA = pilocytic astrocytoma. 857
5 A. Kanoke et al. tory or signs of syndrome predisposing to tumor, or a history of right frontal lobe irradiation. The results of genetic analyses in the present case supported that the idea that the metachronous multicentric gliomas developed from different cells of origin independently. Our patient received chemotherapy combining nimustine hydrochloride and fluorouracil, which could have caused the second malignancy, 14,23 and these treatment may be associated with multicentric glioma. Further genetic and population-based investigations could resolve the mechanisms of gliomagenesis. Disclosure The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper. Author contributions to the study and manuscript preparation include the following. Conception and design: Kanamori, Tominaga. Acquisition of data: Kanamori, Kanoke, Kumabe, Saito, Watanabe. Analysis and interpretation of data: Kanamori, Kanoke, Kumabe, Saito, Watanabe. Drafting the article: Kanamori, Kanoke, Kumabe, Tominaga. Critically revising the article: Kanamori, Kanoke, Kumabe, Tominaga. Reviewed submitted version of manuscript: Kanamori, Kanoke, Kumabe. Approved the final version of the manuscript on behalf of all authors: Kanamori. Study supervision: Kanamori, Kumabe. References 1. Balss J, Meyer J, Mueller W, Korshunov A, Hartmann C, von Deimling A: Analysis of the IDH1 codon 132 mutation in brain tumors. Acta Neuropathol 116: , Batzdorf U, Malamud N: The problem of multicentric gliomas. J Neurosurg 20: , Burkhard C, Di Patre PL, Schüler D, Schüler G, Yaşargil MG, Yonekawa Y, et al: A population-based study of the incidence and survival rates in patients with pilocytic astrocytoma. J Neurosurg 98: , Jacob K, Albrecht S, Sollier C, Faury D, Sader E, Montpetit A, et al: Duplication of 7q34 is specific to juvenile pilocytic astrocytomas and a hallmark of cerebellar and optic pathway tumours. Br J Cancer 101: , Kan P, Gottfried O, Blumenthal DT, Townsend JJ, Drozd-Borysiuk E, Brothman AR, et al: Oligodendroglioma and juvenile pilocytic astrocytoma presenting as synchronous primary brain tumors. Case report with histological and molecular differentiation of the tumors and review of the literature. J Neurosurg 100: , Kanamori M, Kon H, Nobukuni T, Nomura S, Sugano K, Mashiyama S, et al: Microsatellite instability and the PTEN1 gene mutation in a subset of early onset gliomas carrying germline mutation or promoter methylation of the hmlh1 gene. Oncogene 19: , Kanamori M, Kumabe T, Watanabe M, Tominaga T: Anaplastic astrocytoma and anaplastic oligodendroglioma occurring 6 years after subtotal resection of a central neurocytoma. Case report. J Neurosurg 107: , Korshunov A, Meyer J, Capper D, Christians A, Remke M, Witt H, et al: Combined molecular analysis of BRAF and IDH1 distinguishes pilocytic astrocytoma from diffuse astrocytoma. Acta Neuropathol 118: , Little MP, de Vathaire F, Shamsaldin A, Oberlin O, Campbell S, Grimaud E, et al: Risks of brain tumour following treatment for cancer in childhood: modification by genetic factors, radiotherapy and chemotherapy. Int J Cancer 78: , Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (eds): Familial tumour syndromes, in WHO Classification of Tumours of the Central Nervous System, ed 4. Lyon: IARC, 2007, pp Louis DN, Ohgaki H, Wiestler OD, Cavenee WK (eds): Pilocytic astrocytoma, in WHO Classification of Tumours of the Central Nervous System, ed 4. Lyon: IARC, 2007, pp Mamelak AN, Prados MD, Obana WG, Cogen PH, Edwards MS: Treatment options and prognosis for multicentric juvenile pilocytic astrocytoma. J Neurosurg 81:24 30, Ogiwara H, Bowman RM, Tomita T: Long-term follow-up of pediatric benign cerebellar astrocytomas. Neurosurgery 70: 40 48, Oshita F, Tamura T, Kojima A, Yamada K, Fukuda M, Nakagawa K, et al: Late toxicities and complications in three-year survivors of small cell lung cancer. Eur J Cancer 27: , Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al: An integrated genomic analysis of human glioblastoma multiforme. Science 321: , Pfister S, Janzarik WG, Remke M, Ernst A, Werft W, Becker N, et al: BRAF gene duplication constitutes a mechanism of MAPK pathway activation in low-grade astrocytomas. J Clin Invest 118: , Qu M, Olofsson T, Sigurdardottir S, You C, Kalimo H, Nistér M, et al: Genetically distinct astrocytic and oligodendroglial components in oligoastrocytomas. Acta Neuropathol 113: , Ren ZP, Olofsson T, Qu M, Hesselager G, Soussi T, Kalimo H, et al: Molecular genetic analysis of p53 intratumoral heterogeneity in human astrocytic brain tumors. 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Hematol Cell Ther 41: , Vural M, Arslantas A, Ciftci E, Artan S, Adapinar B: Multiple intradural-extramedullary ependymomas: proven dissemination by genetic analysis. Case report. J Neurosurg Spine 12: , Wemmert S, Romeike BF, Ketter R, Steudel WI, Zang KD, Urbschat S: Intratumoral genetic heterogeneity in pilocytic astrocytomas revealed by CGH-analysis of microdissected tumor cells and FISH on tumor tissue sections. Int J Oncol 28: , 2006 Manuscript submitted December 29, Accepted September 18, Please include this information when citing this paper: published online October 19, 2012; DOI: / JNS Address correspondence to: Masayuki Kanamori, M.D., Ph.D., Department of Neurosurgery, Tohoku University Graduate School of Medicine, 1-1 Seiryo-machi, Aoba-ku, Sendai , Japan. mkanamori@med.tohoku.ac.jp. 858
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