One hundred and one dysembryoplastic neuroepithelial tumors: An adult epilepsy series with immunohistochemical, molecular genetic, and clinical correlations and a review of the literature

Journal of Neuropathology and Experimental Neurology

Volumn 70, Issue 10, 2011, Pages 859-878

  Thom, Maria ^a   Toma, Ahmed ^b   An, Shu ^a   Martinian, Lillian ^a   Hadjivassiliou, George ^a   Ratilal, Bernardo ^b   Dean, Andrew ^d   McEvoy, Andrew ^a,b   Sisodiya, Sanjay M ^a,c   Brandner, Sebastian ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b Department of Neurosurgery ^*  (United Kingdom)

^c NATIONAL HOSPITAL FOR NEUROLOGY AND NEUROSURGERY   (United Kingdom)

^d ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Dysembryoplastic neuroepithelial tumor; Epilepsy; Molecular genetics; Outcome

Indexed keywords

CALBINDIN; CD34 ANTIGEN; NESTIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ADOLESCENT; ADULT; CELL PROLIFERATION; CHILD; CHROMOSOME 19Q; CHROMOSOME 1P; CHROMOSOME 9Q; CHROMOSOME LOSS; CLINICAL FEATURE; CORRELATION ANALYSIS; CORTICAL DYSPLASIA; EPILEPSY; FOLLOW UP; GENE MUTATION; HUMAN; IMMUNOHISTOCHEMISTRY; IMMUNOPHENOTYPING; MAJOR CLINICAL STUDY; MOLECULAR GENETICS; NEUROEPITHELIOMA; NUCLEAR MAGNETIC RESONANCE IMAGING; ONSET AGE; PRIORITY JOURNAL; REVIEW; SEIZURE; TERATOMA;

ADOLESCENT; ADULT; AGE OF ONSET; AGED; ANTIGENS, CD34; CEREBRAL CORTEX; CHILD; DNA MUTATIONAL ANALYSIS; EPILEPSY; FEMALE; HUMANS; ISOCITRATE DEHYDROGENASE; LONGITUDINAL STUDIES; MAGNETIC RESONANCE IMAGING; MALE; MIDDLE AGED; MUTATION; NEOPLASMS, NEUROEPITHELIAL; NERVE TISSUE PROTEINS; OLIGODENDROGLIA; TOMOGRAPHY, X-RAY COMPUTED; YOUNG ADULT;

EID: 80053356269     PISSN: 00223069     EISSN: 15546578     Source Type: Journal    
DOI: 10.1097/NEN.0b013e3182302475     Document Type: Review

References (72)

1. Daumas-Duport C, Scheithauer BW, Chodkiewicz JP, et al. Dysembryoplastic neuroepithelial tumor: A surgically curable tumor of young patients with intractable partial seizures. Report of thirty-nine cases. Neurosurgery 1988;23:545-46
2. Cavanagh JB. On certain small tumours encountered in the temporal lobe. Brain 1958;81:389-405
3. Louis DN, World Health Organization, International Agency for Research on Cancer, Deutsches Krebsforschungszentrum Heidelberg. WHO Classification of Tumours of the Central Nervous System. 4th ed. Lyon, France: International Agency for Research on Cancer, 2007
4. Honavar M, Janota I, Polkey CE. Histological heterogeneity of dysembryoplastic neuroepithelial tumour: Identification and differential diagnosis in a series of 74 cases. Histopathology 1999;34:342-56 (Pubitemid 29229989)
5. Daumas-Duport C, Varlet P, Bacha S, et al. Dysembryoplastic neuroepithelial tumors: Nonspecific histological formsVA study of 40 cases. J Neurooncol 1999;41:267-80 (Pubitemid 29209815)
6. Burneo JG, Tellez-Zenteno J, Steven DA, et al. Adult-onset epilepsy associated with dysembryoplastic neuroepithelial tumors. Seizure 2008; 17:498-504
7. Fernandez C, Girard N, Paz Paredes A, et al. The usefulness of MR imaging in the diagnosis of dysembryoplastic neuroepithelial tumor in children: A study of 14 cases. AJNR Am J Neuroradiol 2003;24:829-34 (Pubitemid 36617409)
8. Lee J, Lee BL, Joo EY, et al. Dysembryoplastic neuroepithelial tumors in pediatric patients. Brain Dev 2009;31:671-81
9. Duggal N, Taylor R, Zou GY, et al. Dysembryoplastic neuroepithelial tumours: Clinical, proliferative and apoptotic features. J Clin Pathol 2008;61:127-31 (Pubitemid 351158239)
10. Ray WZ, Blackburn SL, Casavilca-Zambrano S, et al. Clinicopathologic features of recurrent dysembryoplastic neuroepithelial tumor and rare malignant transformation: A report of 5 cases and review of the literature. J Neurooncol 2009;94:283-92
11. Rushing EJ, Thompson LD, Mena H. Malignant transformation of a dysembryoplastic neuroepithelial tumor after radiation and chemotherapy. Ann Diagn Pathol 2003;7:240-44 (Pubitemid 36999492)
12. Schittenhelm J, Mittelbronn M, Wolff M, et al. Multifocal dysembryoplastic neuroepithelial tumor with signs of atypia after regrowth. Neuropathology 2007;27:383-89 (Pubitemid 47063275)
13. Hirose T, Scheithauer BW. Mixed dysembryoplastic neuroepithelial tumor and ganglioglioma. Acta Neuropathol (Berl) 1998;95:649-54
14. Prayson RA. Composite ganglioglioma and dysembryoplastic neuroepithelial tumor. Arch Pathol Lab Med 1999;123:247-50 (Pubitemid 29124916)
15. Shimbo Y, Takahashi H, Hayano M, et al. Temporal lobe lesion demonstrating features of dysembryoplastic neuroepithelial tumor and ganglioglioma: A transitional form? Clin Neuropathol 1997;16:65-68 (Pubitemid 27128102)
16. Josan V, Smith P, Kornberg A, et al. Development of a pilocytic astrocytoma in a dysembryoplastic neuroepithelial tumor. Case report. J Neurosurg 2007;106:509-12
17. Gonzales M, Dale S, Susman M, et al. Dysembryoplastic neuroepithelial tumor (DNT)-like oligodendrogliomas or DNTs evolving into oligodendrogliomas: Two illustrative cases. Neuropathology 2007;27:324-30 (Pubitemid 47063278)
18. Sakuta R, Otsubo H, Nolan MA, et al. Recurrent intractable seizures in children with cortical dysplasia adjacent to dysembryoplastic neuroepithelial tumor. J Child Neurol 2005;20:377-84 (Pubitemid 40766999)
19. Minkin K, Klein O, Mancini J, et al. Surgical strategies and seizure control in pediatric patients with dysembryoplastic neuroepithelial tumors: A single-institution experience. J Neurosurg Pediatr 2008;1: 206-10 (Pubitemid 351346509)
20. Dougherty MJ, Santi M, Brose MS, et al. Activating mutations in BRAF characterize a spectrum of pediatric low-grade gliomas. Neuro Oncol 2010;12:621-30
21. Pasquier B, Peoc HM, Fabre-Bocquentin B, et al. Surgical pathology of drug-resistant partial epilepsy. A 10-year-experience with a series of 327 consecutive resections. Epileptic Disord 2002;4:99-119 (Pubitemid 34760686)
22. Sharma MC, Jain D, Gupta A, et al. Dysembryoplastic neuroepithelial tumor: A clinicopathological study of 32 cases. Neurosurg Rev 2009;32: 161Y69; discussion 169-70
23. Wolf HK, Buslei R, Blumcke I, et al. Neural antigens in oligodendrogliomas and dysembryoplastic neuroepithelial tumors. Acta Neuropathol (Berl) 1997;94:436-43 (Pubitemid 27483207)
24. Wolf HK, Buslei R, Schmidt-Kastner R, et al. NeuN: A useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 1996;44: 1167-71 (Pubitemid 26337294)
25. Blumcke I, Becker AJ, Normann S, et al. Distinct expression pattern of microtubule-associated protein-2 in human oligodendrogliomas and glial precursor cells. J Neuropathol Exp Neurol 2001;60:984-93 (Pubitemid 32924124)
26. Blumcke I, Muller S, Buslei R, et al. Microtubule-associated protein-2 immunoreactivity: A useful tool in the differential diagnosis of low-grade neuroepithelial tumors. Acta Neuropathol (Berl) 2004;108:89-96 (Pubitemid 39136293)
27. Duggal N, Iskander S, Hammond RR. MAP2 and nestin co-expression in dysembryoplastic neuroepithelial tumors. Clin Neuropathol 2003;22: 57-65 (Pubitemid 36336826)
28. Ferrer I, Isamat F, Lopez-Obarrio L, et al. Parvalbumin and calbindin D-28K immunoreactivity in central ganglioglioma and dysplastic gangliocytoma of the cerebellum. Report of two cases. J Neurosurg 1993;78: 133-37 (Pubitemid 23005365)
29. Lopes MB, Altermatt HJ, Scheithauer BW, et al. Immunohistochemical characterization of subependymal giant cell astrocytomas. Acta Neuropathol 1996;91:368-75 (Pubitemid 26088972)
30. Pelc K, Vincent S, Ruchoux MM, et al. Calbindin-d(28k): A marker of recurrence for medulloblastomas. Cancer 2002;95:410-19
31. Blumcke I, Wiestler OD. Gangliogliomas: An intriguing tumor entity associated with focal epilepsies. J Neuropathol Exp Neurol 2002;61: 575-84 (Pubitemid 34727339)
32. Hess DC, Abe T, Hill WD, et al. Hematopoietic origin of microglial and perivascular cells in brain. Exp Neurol 2004;186:134-44 (Pubitemid 38333189)
33. Blumcke I, Giencke K, Wardelmann E, et al. The CD34 epitope is expressed in neoplastic and malformative lesions associated with chronic, focal epilepsies. Acta Neuropathol (Berl) 1999;97:481-90 (Pubitemid 29195111)
34. Fassunke J, Majores M, Ullmann C, et al. In situYRT and immunolaser microdissection for mRNA analysis of individual cells isolated from epilepsy-associated glioneuronal tumors. Lab Invest 2004;84: 1520-25 (Pubitemid 39482169)
35. Deb P, Sharma MC, Tripathi M, et al. Expression of CD34 as a novel marker for glioneuronal lesions associated with chronic intractable epilepsy. Neuropathol Appl Neurobiol 2006;32:461-68 (Pubitemid 44401508)
36. Sung CO, Suh YL. Different pattern of expression of nestin in the non-specific form of dysembryoplastic neuroepithelial tumors compared to the simple and complex forms. J Neurooncol 2009;92:7-13
37. Kuhlmann T, Gutenberg A, Schulten HJ, et al. Nogo-A expression in glial CNS tumors: A tool to differentiate between oligodendrogliomas and other gliomas? Am J Surg Pathol 2008;32:1444-53
38. Chang EF, Christie C, Sullivan JE, et al. Seizure control outcomes after resection of dysembryoplastic neuroepithelial tumor in 50 patients. J Neurosurg Pediatr 2006;5:123-30
39. Lee MC, Kang JY, Seol MB, et al. Clinical features and epileptogenesis of dysembryoplastic neuroepithelial tumor. Childs Nerv Syst 2006;22: 1611-18
40. Nolan MA, Sakuta R, Chuang N, et al. Dysembryoplastic neuroepithelial tumors in childhood: Long-term outcome and prognostic features. Neurology 2004;62:2270-76 (Pubitemid 38787786)
41. Ozlen F, Gunduz A, Asan Z, et al. Dysembryoplastic neuroepithelial tumors and gangliogliomas: Clinical results of 52 patients. Acta Neurochir (Wien) 2010;152:1661-71
42. Takahashi A, Hong SC, Seo DW, et al. Frequent association of cortical dysplasia in dysembryoplastic neuroepithelial tumor treated by epilepsy surgery. Surg Neurol 2005;64:419-27 (Pubitemid 41526127)
43. Palmini A, Najm I, Avanzini G, et al. Terminology and classification of the cortical dysplasias. Neurology 2004;62:S2-S8 (Pubitemid 38419835)
44. Chamberlain WA, Cohen ML, Gyure KA, et al. Interobserver and intraobserver reproducibility in focal cortical dysplasia (malformations of cortical development). Epilepsia 2009;50:2593-98
45. Blumcke I, Thom M, Aronica E, et al. The clinicopathologic spectrum of focal cortical dysplasias: A consensus classification proposed by an ad hoc Task Force of the ILAE Diagnostic Methods Commission. Epilepsia 2011;52:158-74
46. Walker TL, Yasuda T, Adams DJ, et al. The doublecortin-expressing population in the developing and adult brain contains multipotential precursors in addition to neuronal-lineage cells. J Neurosci 2007;27: 3734-42 (Pubitemid 46557670)
47. D'Arcangelo G. The role of the reelin pathway in cortical development. Symp Soc Exp Biol 2001;53:59-73
48. Georgala PA, Manuel M, Price DJ. The generation of superficial cortical layers is regulated by levels of the transcription factor pax6. Cereb Cortex 2011;21:81-94
49. Martinian L, Boer K, Middeldorp J, et al. Expression patterns of glial fibrillary acidic protein (GFAP)-delta in epilepsy-associated lesional pathologies. Neuropathol Appl Neurobiol 2009;35:394-405
50. Sisodiya SM, Fauser S, Cross JH, et al. Focal cortical dysplasia Type II: Biological features and clinical perspectives. Lancet Neurol 2009;8: 830-43
51. Campos AR, Clusmann H, von Lehe M, et al. Simple and complex dysembryoplastic neuroepithelial tumors (DNT) variants: Clinical profile, MRI, and histopathology. Neuroradiology 2009;51:433-43
52. Aldape K, Burger PC, Perry A. Clinicopathologic aspects of 1p/19q loss and the diagnosis of oligodendroglioma. Arch Pathol Lab Med 2007;131: 242-51
53. Cairncross G, Jenkins R. Gliomas with 1p/19q codeletion: A.K.A. oligodendroglioma. Cancer J 2008;14:352-57
54. Bauman GS, Ino Y, Ueki K, et al. Allelic loss of chromosome 1p and radiotherapy plus chemotherapy in patients with oligodendrogliomas. Int J Radiat Oncol Biol Phys 2000;48:825-30
55. van den Bent MJ, Looijenga LH, Langenberg K, et al. Chromosomal anomalies in oligodendroglial tumors are correlated with clinical features. Cancer 2003;97:1276-84 (Pubitemid 36237315)
56. Fujisawa H, Marukawa K, Hasegawa M, et al. Genetic differences between neurocytoma and dysembryoplastic neuroepithelial tumor and oligodendroglial tumors. J Neurosurg 2002;97:1350-55 (Pubitemid 35424290)
57. Johnson MD, Vnencak-Jones CL, Toms SA, et al. Allelic losses in oligodendroglial and oligodendroglioma-like neoplasms: Analysis using microsatellite repeats and polymerase chain reaction. Arch Pathol Lab Med 2003;127:1573-79 (Pubitemid 37517467)
58. Perry A, Fuller CE, Banerjee R, et al. Ancillary FISH analysis for 1p and 19q status: Preliminary observations in 287 gliomas and oligodendroglioma mimics. Front Biosci 2003;8:a1-a9 (Pubitemid 39069937)
59. Prayson RA, Castilla EA, Hartke M, et al. Chromosome 1p allelic loss by fluorescence in situ hybridization is not observed in dysembryoplastic neuroepithelial tumors. Am J Clin Pathol 2002;118:512-17 (Pubitemid 44698507)
60. Yan H, Parsons DW, Jin G, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009;360:765-73
61. Hartmann C, Meyer J, Balss J, et al. Type and frequency of IDH1 and IDH2 mutations are related to astrocytic and oligodendroglial differentiation and age: A study of 1,010 diffuse gliomas. Acta Neuropathol 2009;118:469-74
62. Ichimura K, Pearson DM, Kocialkowski S, et al. IDH1 mutations are present in the majority of common adult gliomas but rare in primary glioblastomas. Neuro Oncol 2009;11:341-47
63. Ohgaki H, Kleihues P. Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci 2009;100:2235-41
64. Bourne TD, Schiff D. Update on molecular findings, management and outcome in low-grade gliomas. Nat Rev Neurol 2010;6:695-701
65. Nakatsuka M, Mizuno S, Kimura T, et al. A case of an unclassified tumor closely resembling dysembryoplastic neuroepithelial tumor with rapid growth. Brain Tumor Pathol 2000;17:41-45
66. Luyken C, Blumcke I, Fimmers R, et al. Supratentorial gangliogliomas: Histopathologic grading and tumor recurrence in 184 patients with a median follow-up of 8 years. Cancer 2004;101:146-55 (Pubitemid 38812434)
67. Luyken C, Blumcke I, Fimmers R, et al. The spectrum of long-term epilepsy-associated tumors: Long-term seizure and tumor outcome and neurosurgical aspects. Epilepsia 2003;44:822-30 (Pubitemid 36754008)
68. Aronica E, Leenstra S, van Veelen CW, et al. Glioneuronal tumors and medically intractable epilepsy: A clinical study with long-term follow-up of seizure outcome after surgery. Epilepsy Res 2001;43:179-91 (Pubitemid 32204444)
69. Ruban D, Byrne RW, Kanner A, et al. Chronic epilepsy associated with temporal tumors: Long-term surgical outcome. Neurosurg Focus 2009; 27:E6
70. Bilginer B, Yalnizoglu D, Soylemezoglu F, et al. Surgery for epilepsy in children with dysembryoplastic neuroepithelial tumor: Clinical spectrum, seizure outcome, neuroradiology, and pathology. Childs Nerv Syst 2009; 25:485-91
71. Jensen RL, Caamano E, Jensen EM, et al. Development of contrast enhancement after long-term observation of a dysembryoplastic neuroepithelial tumor. J Neurooncol 2006;78:59-62 (Pubitemid 43786661)
72. Maher CO, White JB, Scheithauer BW, et al. Recurrence of dysembryoplastic neuroepithelial tumor following resection. Pediatr Neurosurg 2008;44:333-36 (Pubitemid 351931439)