Abstract
Although the classification of insular glioma has been established based on the anatomical location in order to facilitate personalized surgical resection, the diagnosis based on anatomical and functional characteristics becomes more complex when insular tumors extend into either the frontobasal brain region and/or the temporal lobe, as part of the limbic system. Moreover, prognosis of insular tumor resection is still controversial. Further analysis of subgroup characteristics of insular grade II gliomas based on clinical and molecular analysis is required to reliably determine patients’ survival rates. In this retrospective study 20 purely insular grade II gliomas patients and 22 paralimbic grade II gliomas that involved frontal and/or temporal lobes were compared with regard to epidemiological and clinical characteristics. The molecular profiles including Isocitrate dehydrogenase 1 (IDH1), telomerase reverse transcriptase (TERT) promoter, and P53 mutations, 1p19q co-deletion were analyzed, and microRNA profiles were assessed by microarray and bioinformatics analysis. Purely insular grade II gliomas displayed a high frequency of IDH1 mutations with favorable outcome. IDH1 mutated paralimbic glioma shared many parameters with the purely insular glioma in respect to growth patterns, survival, and microRNA profile, but differed significantly from the IDH1 wild type paralimbic gliomas. Our findings suggest that IDH1 mutations can define subpopulations of insular gliomas with distinct disease entities regardless of tumor extension patterns. These findings could be useful to develop a customized treatment strategy for insular glioma patients.
Similar content being viewed by others
References
Shelley BP, Trimble MR (2004) The insular lobe of Reil—its anatamico-functional, behavioural and neuropsychiatric attributes in humans—a review. World J Biol Psychiatry 5:176–200
Ture U, Yasargil DC, Al-Mefty O, Yasargil MG (1999) Topographic anatomy of the insular region. J Neurosurg 90:720–733
Yasargil MG, von Ammon K, Cavazos E, Doczi T, Reeves JD, Roth P (1992) Tumours of the limbic and paralimbic systems. Acta Neurochir (Wien) 118:40–52
Wu AS, Witgert ME, Lang FF, Xiao L, Bekele BN, Meyers CA, Ferson D, Wefel JS (2011) Neurocognitive function before and after surgery for insular gliomas. J Neurosurg 115:1115–1125
Duffau H, Taillandier L, Gatignol P, Capelle L (2006) The insular lobe and brain plasticity: lessons from tumor surgery. Clin Neurol Neurosurg 108:543–548
Duffau H, Capelle L (2004) Preferential brain locations of low-grade gliomas. Cancer 100:2622–2626
Mehrkens JH, Kreth FW, Muacevic A, Ostertag CB (2004) Long term course of WHO grade II astrocytomas of the Insula of Reil after I-125 interstitial irradiation. J Neurol 251:1455–1464
Sanai N, Polley MY, Berger MS (2010) Insular glioma resection: assessment of patient morbidity, survival, and tumor progression. J Neurosurg 112:1–9
Goze C, Mansour L, Rigau V, Duffau H (2013) Distinct IDH1/IDH2 mutation profiles in purely insular versus paralimbic WHO Grade II gliomas. J Neurosurg 118:866–872
Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, Mankoo P, Carter H, Siu IM, Gallia GL, Olivi A, McLendon R, Rasheed BA, Keir S, Nikolskaya T, Nikolsky Y, Busam DA, Tekleab H, Diaz LJ, Hartigan J, Smith DR, Strausberg RL, Marie SK, Shinjo SM, Yan H, Riggins GJ, Bigner DD, Karchin R, Papadopoulos N, Parmigiani G, Vogelstein B, Velculescu VE, Kinzler KW (2008) An integrated genomic analysis of human glioblastoma multiforme. Science 321:1807–1812
Zhang C, Moore LM, Li X, Yung WK, Zhang W (2013) IDH1/2 mutations target a key hallmark of cancer by deregulating cellular metabolism in glioma. Neuro Oncol 15:1114–1126
Chan AK, Yao Y, Zhang Z, Chung NY, Liu JS, Li KK, Shi Z, Chan DT, Poon WS, Zhou L, Ng HK (2015) TERT promoter mutations contribute to subset prognostication of lower-grade gliomas. Mod Pathol 28:177–186
Wang Z, Bao Z, Yan W, You G, Wang Y, Li X, Zhang W (2013) Isocitrate dehydrogenase 1 (IDH1) mutation-specific microRNA signature predicts favorable prognosis in glioblastoma patients with IDH1 wild type. J Exp Clin Cancer Res 32:59
Lai A, Kharbanda S, Pope WB, Tran A, Solis OE, Peale F, Forrest WF, Pujara K, Carrillo JA, Pandita A, Ellingson BM, Bowers CW, Soriano RH, Schmidt NO, Mohan S, Yong WH, Seshagiri S, Modrusan Z, Jiang Z, Aldape KD, Mischel PS, Liau LM, Escovedo CJ, Chen W, Nghiemphu PL, James CD, Prados MD, Westphal M, Lamszus K, Cloughesy T, Phillips HS (2011) Evidence for sequenced molecular evolution of IDH1 mutant glioblastoma from a distinct cell of origin. J Clin Oncol 29:4482–4490
Wang Y, Zhang T, Li S, Fan X, Ma J, Wang L, Jiang T (2015) Anatomical localization of isocitrate dehydrogenase 1 mutation: a voxel-based radiographic study of 146 low-grade gliomas. Eur J Neurol 22:348–354
Gilbertson RJ, Gutmann DH (2007) Tumorigenesis in the brain: location, location, location. Cancer Res 67:5579–5582
Duncan CG, Barwick BG, Jin G, Rago C, Kapoor-Vazirani P, Powell DR, Chi JT, Bigner DD, Vertino PM, Yan H (2012) A heterozygous IDH1R132H/WT mutation induces genome-wide alterations in DNA methylation. Genome Res 22:2339–2355
Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, Campos C, Fabius AW, Lu C, Ward PS, Thompson CB, Kaufman A, Guryanova O, Levine R, Heguy A, Viale A, Morris LG, Huse JT, Mellinghoff IK, Chan TA (2012) IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483:479–483
Zhou X, Ruan J, Wang G, Zhang W (2007) Characterization and identification of microRNA core promoters in four model species. PLoS Comput Biol 3:e37
Mandonnet E, Capelle L, Duffau H (2006) Extension of paralimbic low grade gliomas: toward an anatomical classification based on white matter invasion patterns. J Neurooncol 78:179–185
Hu H, Wang Z, Liu Y, Zhang C, Li M, Zhang W, Wang K, Cai J, Cheng W, Huang H, Jiang T (2015) Genome-wide transcriptional analyses of Chinese patients reveal cell migration is attenuated in IDH1-mutant glioblastomas. Cancer Lett 357:566–574
Skrap M, Mondani M, Tomasino B, Weis L, Budai R, Pauletto G, Eleopra R, Fadiga L, Ius T (2012) Surgery of insular nonenhancing gliomas: volumetric analysis of tumoral resection, clinical outcome, and survival in a consecutive series of 66 cases. Neurosurgery 70(1081–1093):1093–1094
Eckel-Passow JE, Lachance DH, Molinaro AM, Walsh KM, Decker PA, Sicotte H, Pekmezci M, Rice T, Kosel ML, Smirnov IV, Sarkar G, Caron AA, Kollmeyer TM, Praska CE, Chada AR, Halder C, Hansen HM, McCoy LS, Bracci PM, Marshall R, Zheng S, Reis GF, Pico AR, O’Neill BP, Buckner JC, Giannini C, Huse JT, Perry A, Tihan T, Berger MS, Chang SM, Prados MD, Wiemels J, Wiencke JK, Wrensch MR, Jenkins RB (2015) Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 372:2499–2508
Skrap M, Mondani M, Tomasino B, Weis L, Budai R, Pauletto G, Eleopra R, Fadiga L, Ius T (2012) Surgery of insular nonenhancing gliomas: volumetric analysis of tumoral resection, clinical outcome, and survival in a consecutive series of 66 cases. Neurosurgery 70(1081–1093):1093–1094
Sanai N, Polley MY, Berger MS (2010) Insular glioma resection: assessment of patient morbidity, survival, and tumor progression. J Neurosurg 112:1–9
Zhang ZY, Chan AK, Ding XJ, Qin ZY, Hong CS, Chen LC, Zhang X, Zhao FP, Wang Y, Wang Y, Zhou LF, Zhuang Z, Ng HK, Yan H, Yao Y, Mao Y (2015) TERT promoter mutations contribute to IDH mutations in predicting differential responses to adjuvant therapies in WHO grade II and III diffuse gliomas. Oncotarget. [Epub ahead of print]
Acknowledgments
This work was supported by grant 13JC1408000 from the Science and Technology Commission of Shanghai Municipality (to Liang-fu Zhou), the Research Special Fund For Public Welfare Industry of Health (No. 201402008) to Yao Yu, the National Key Clinical Specialist Construction Programs of China (Oncology) to Liang-fu Zhou.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors have declared that no competing interests exist.
Rights and permissions
About this article
Cite this article
Tang, C., Zhang, Zy., Chen, Lc. et al. Subgroup characteristics of insular low-grade glioma based on clinical and molecular analysis of 42 cases. J Neurooncol 126, 499–507 (2016). https://doi.org/10.1007/s11060-015-1989-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11060-015-1989-5