Oligodendroglioma with Anaplastic Features, Case Report and Review of the Literature

Keywords

Oligodendrogliomas, Anaplastic, Grade, Molecular, benign

Abstract

Anaplastic oligodendrogliomas (AOD) are rare brain tumors with variable overall survival accounting for approximately 1.3% to 4.4% of brain tumors and about 5% to 10% of the gliocytomas. Anaplastic oligodendrogliomas, or grade III oligodendrogliomas, describe rare primary malignant brain tumors with exceedingly variable overall prognosis. Gliomas originate from neural stem cells or glial progenitor cells that develop or maintain glial characteristics. These tumors occur most frequently in males during the 5th and 6th decade of life often presenting with new onset seizures. The WHO grading system distinguishes two histopathologic grades of Oligodendrogliomas: grade II (low-grade) and grade III (anaplastic oligodendroglioma or AOD). Here we present a case of anaplastic oligodendrogliomas and review the literature.

ABBREVIATION

AOD: Anaplastic oligodendrogliomas,

LOH: loss of heterozygosity,

WHO: World Health Organization,

LGGs: lowgrade gliomas,

PFS: progression-free survival,

OS: overall survival,

pODG: pediatric oligodendrogliomas,

INTRODUCTION

Anaplastic oligodendrogliomas (AOD), or grade III oligodendrogliomas, describe rare primary malignant brain tumors with exceedingly variable overall prognosis (1,2). Oligodendrogliomas represent approximately 1.3% to 4.4% of brain tumors and about 5% to 10% of the gliocytomas (3). Gliomas originate from neural stem cells or glial progenitor cells that develop or maintain glial characteristics (4). Studies showed that the most common location for primary oligodendrogliomas occurs within the frontal lobes of the cerebral hemispheres (5). Structural imaging reveals two main key features of oligodendrogliomas: calcification and corticalsubcortical location. When found infratentorial or in deep nuclei, oligodendroglial tumors historically represent a more aggressive phenotype (6).

Oligodendrogliomas occur most frequently in males during the 5th and 6th decade of life often presenting with new onset seizures (4). AOD almost exclusively presents as a single lesion. Although several case reports of multifocal AOD, leptomeningeal spread, and extraneural metastases exist. These cases are rare and potentially reflect the natural course of a glioma with prolonged survival (5, 6). Patients experiencing generalized tonic–clonic seizures frequently exhibited the greatest lesion load in mesial frontal regions such as the cortex connected to the genu of the corpus callosum. While patients with partial seizures experienced oligodendrogliomas more caudo-laterally in orbitofrontal and temporal lobes, sparring cortex connected to the genu. These findings indicate that the genu of the corpus callosum serves as a major pathway for seizure generalization (4, 7).

Researchers identified that loss of heterozygosity (LOH) of the short arm of chromosome 1 (1p) and the long arm of chromosome 19 (19q, 1p19q LOH) in tumor tissue represents a somatic genetic finding common to oligodendrogliomas (8, 9). The co-deletion of chromosomal arms 1p and 19q serves diagnostic importance as well as provides prognostic and predictive relevance (10). The current standard therapy of oligodendrogliomas includes neurosurgery with radiation and chemotherapy (11-13).

CASE PRESENTATION

A 40-year-old man presented with severe headache, visual disturbance and generalized epileptic seizures. No significant medical history was identified. MRI with gadolinium was performed and a single frontal lobe mass was identified. T1 images demonstrated mixed hypointense and hyperintense mass. T2 images revealed a hyperintense mass with mild surrounding edema. Enhancement was noted with contrast administration. Intratumoral calcification was also noted. Stereotactic biopsy was obtained, the tumor showed diffuse infiltration with moderate cellularity (Figure 1A).

Branching small, chicken wire-like blood vessels and fried egglike cells, with clear cytoplasm and well-defined cell border characteristic of oligodendroglioma were noted (Figure1B). Many areas showed increased nuclear pleomorphism and vascular proliferation (Figure 1C). Some foci showed sheets of pleomorphic oligodendrocytes with hyperchromatic nuclei, clear to eosinophilic cytoplasm, increased mitotic activity (>6 mitotic figures/10 HPF), and necrosis. Sheets of minigemistocytes and lymphocytic infiltrate were also identified. The tumor morphologic features were consistent with anaplastic oligodendrogliomas grade III. FISH analysis failed to demonstrate 1p36 or 19q13 deletions. Extra signals of 1 and 19 chromosomes were observed suggestive of Trisomy/tetrasomy.

Figure 1: Pathologic examination of the tumor. 1A: The tumor shows diffuse infiltration with moderate cellularity (H&E stain X20). 1B: Branching small, chicken wire-like blood vessels and fried egg-like cells, with clear cytoplasm and well-defined cell border characteristic of oligodendroglioma were noted (H&E stain X40). 1C: Many areas showed increased nuclear pleomorphism and vascular proliferation (H&E stain X60)

The patient received aggressive multimodal treatment including surgical resection, radiotherapy, and chemotherapy (combination chemotherapy with packed cell volume “PCV” administered every 6 weeks for a total of 6 cycles). The patient was followed with regular MRI scans at 3 months initially and then every 6 months. Despite prolonged response, the patient experienced disease relap.

DISCUSSION

The World Health Organization (WHO) classification divides astrocytoma into four grades (I–IV), separated according to the glial type from which they arise, astrocytoma or oligodendroglioma (14, 15). The WHO classifies diffuse low-grade gliomas (LGGs) as grade II astrocytomas, oligodendrogliomas, and oligoastrocytomas (14-17). Clinicians often classify low-grade gliomas as benign neoplasm, disregarding their association with neurological morbidity and mortality and potential for anaplastic transformation (15, 18). Unfortunately, lack of sufficient data results in unclear optimum management of this tumor and individual clinical judgement with subsequent debate currently drives the decision-making process (15, 19).

Anaplastic oligodendroglial tumors frequently present with additional genetic aberrations, in particular 9p LOH and/or deletion of the CDKN2A gene (p16), PIK3CA mutations, and polysomies (4, 20, 21). Some studies suggest shortened recurrence free survival times or poorer prognosis in patients who developed oligodendroglial tumors with polysomy of 1p and 19q (4, 22, 23). The finding of 1p19q LOH in a glial neoplasm shows predictive value of tumor chemosensitivity and prolonged patient survival (24-27). When defined by strict histological criteria or a unanimous diagnosis by four neuropathologists, 1p19q LOH occurred in over 85% of oligodendrogliomas (8, 27, 28). IDH1 mutations occur mainly in low-grade gliomas (astrocytomas and oligodendrogliomas) and retain during tumour progression. This mutation helps distinguish lowgrade gliomas from other tumour entities where the mutation is absent or uncommon. The presence of an IDH1 mutation also impacts prognosis, with a median survival of 3.8 years for patients with mutated IDH1, versus 1.1 years for patients with wild-type IDH (15, 29). One study evaluated prognostic factors of AOD including surgical, radiographic, and histopathologic analysis of 95 patients diagnosed with AOD for 20 years. They measured progression-free survival (PFS) and overall survival (OS). The researchers performed subgroup analyses in isocitrate dehydrogenase (IDH1/2)-mutant and 1p/19q-codeleted patients. The median PFS and OS lengths were 24.7 months and 50.8 months respectively. Patients with the IDH1/2-mutant and 1p/19q-codeletion yielded median PFS and OS lengths of 54.2 and 57.8 months, respectively. This study concluded that young age, frontal lobe involvement, weak enhancement, gross total resection, low Ki-67 index, 1p/19q-codeletion, and IDH1/2 mutations yielded favorable outcomes (30).

Another study evaluated the overall survival (OS) in pediatric oligodendrogliomas (pODG) and found a mean of 199.6 months. Furthermore, the study concluded that pODG presented with smaller size and lower grade than similar adult tumors. Location, size, grade, use of radiotherapy, and extent of resection represented significant prognostic factors with size and grade displaying stronger prognostic factors in children than adults. pODG is less frequently developed in the frontal lobe compared to adult tumors; however, the tumor more commonly occurred in the temporal lobe and extracortical regions. The study determined no significant difference in outcome between children with highgrade tumors and adults with high-grade tumors (31).

Low-grade oligodendrogliomas display round and uniform nuclei with crisp nuclear membranes, delicate chromatin and small-to-inconspicuous nucleoli. In anaplastic examples, despite maintaining an overall sense of regularity and nuclear roundness, cells frequently show enlarged and epithelioid cell structure with nuclei that often exhibit increased size and pleomorphism, vesicular chromatin pattern, and prominent nucleoli (4, 32, 33). However, the histopathological classification of diffuse glioma remains a subject of criticism and suffers from considerable interobserver variability. In fact, tumors with a similar microscopic appearance may present with significantly different clinical outcomes (34). Roughly only 30% of oligodendroglial tumors display anaplastic characteristics histologically. These findings include: nuclear atypia, increased cellularity, increased proliferation activity, and increased cell mitosis (13, 14).

Neurosurgery is instrumental for tumor removal and acquisition of neoplastic tissue in order to make a definitive diagnosis. Sophisticated diagnostic preoperative and perioperative methods, magnetic resonance imaging (MRI), use of 5-aminolevulinic acid, MRI tractography, perioperative ultrasound and MRI, awake surgical method, hybrid positron emission tomography (PET) and computed tomography (CT)) and navigated microsurgical techniques serve as integral parts of surgical treatment (12, 13). Non-contrast CT showed coarse calcifications in 90% of oligodendrogliomas (10). Confirming the extent of tumor resection requires a postoperative MRI with 24-72 hours following surgery. Additionally, clinicians reserve targeted-biopsy of the tumor when resection is impossible (13, 35, 36). Patients evaluated early on with modern technology such as 3-D ultrasound, intraoperative MRI, or mapping techniques often achieve safe resections, reducing overall neurological deterioration (18, 37). In AOD patients with LOH at 1p19q, MR single-photon emission computed tomography (SPECT) shows increased thallium-201 uptake irrespective of grade (38).

Researchers retrospectively reviewed Serial MRIs of 27 patients with untreated WHO grade II oligodendrogliomas or mixed gliomas. They examined the kinetics of tumor growth and anaplastic transformation and noticed that untreated lowgrade oligodendrogliomas or mixed gliomas grow continuously during their premalignant phase. Analysis of the mean tumor diameters over time showed constant growth while linear regression found an average slope of 4.1mm per year with a relatively narrow range (Mandonnet, 2003). Due to the slow and often constant growth rate in LGGs (18, 39), reduction of tumor cells capable of undergoing malignant transformation via early resection may provide improved mortality. These researchers found a significant difference in low-grade glioma patients with improved overall survival, and a survival advantage that increased with time in patients with early surgical dissection as opposed to those with biopsy and watchful waiting strategy (18). Additional favorable prognostic factors include young age, good overall medical condition (Karnofsky score), larger extent of tumor resection and combined oncological treatment (13, 40).

Uncontrolled trials found that patients with chemotherapy sensitive recurrent AOD and anaplastic oligoastrocytoma (AOA) responded to procarbazine, lomustine, and vincristine (PCV) in 60% to 70% of cases (16, 41). Triple combination chemotherapy of procarbazine, lomustine and vincristine (PCV) or temozolomide represents the mainstay of treatment (11- 13). In fact, oligodendrogliomas with the 1p/19q co-deletion demonstrate response to early chemotherapy with procarbazine, lomustine and vincristine (1, 2). However, clinical trials illustrate variably prognoses of patients with AOA and low concordance rates in diagnosis of classical AOD. Additionally, clinicians hold ongoing discussions about whether following the removal of AOA with resultant necrotic grade III glioblastoma merits a separate diagnosis (14, 32, 42-46).

AODs are rare brain tumors with variable overall survival. Combined chemotherapy, radiation and neurosurgery are necessary to reduce disease progression and recurrence. We present this case to highlight the spectrum of presentation of this rare tumor and molecular changes. And review the literature to discuss the most recent treatment modalities.

ACKNOWLEDGMENT

Special thanks to Titilopemi Odunlami, Mohamed El-Jammali, and Fareshta Shafaq, MD candidates, American University of the Caribbean for their assistance in reviewing the final manuscript.

REFERENCES

1. Riemenschneider, M. J., Koy, T. H. & Reifenberger, G. Expression of oligodendrocyte lineage genes in oligodendroglial and astrocytic gliomas. Acta Neuropathol. 107, 277–282 (2004).

2. Cairncross, G. et al. Phase III trial of chemoradiotherapy for anaplastic oligodendroglioma: long-term results of RTOG 9402. J. Clin. Oncol. 31, 337–343 (2013).

3. Reifenberger G, Kros JM, Louis DN. Louis DN, Ohgaki H, Wiestler OD, et al. Oligodendroglioma. WHO Classification of Tumors of the Central Nervous System. Lyon: IARC Press; 2007. 54–9.

4. Wesseling P, van den Bent M, Perry A. Oligodendroglioma: pathology, molecular mechanisms and markers. Acta Neuropathol. 2015;129(6):809-827. doi:10.1007/s00401-015-1424-1

5. Mork SJ, Lindegaard KF, Halvorsen TB, et al. Oligodendroglioma: incidence and biological behaviour in a defined population. J Neurosurg 1985;63:881–9.

6. van den Bent MJ. Anaplastic oligodendroglioma and oligoastrocytoma. Neurol Clin. 2007 Nov;25(4):1089-109, ix-x. doi: 10.1016/j. ncl.2007.07.013. PMID: 17964027.

7. Wieshmann UC, Milinis K, Paniker J, Das K, Jenkinson MD, Brodbelt A, Crooks D, Keller SS. The role of the corpus callosum in seizure spread: MRI lesion mapping in oligodendrogliomas. Epilepsy Res. 2015 Jan;109:126-33. doi: 10.1016/j.eplepsyres.2014.10.023. Epub 2014 Nov 8. PMID: 25524852.  

8. Burger PC, Minn AY, Smith JS, Borell TJ, Jedlicka AE, et al. Losses of chromosomal arms 1p and 19q in the diagnosis of oligodendroglioma. A study of paraffin-embedded sections. Mod Pathol. 2001 Sep;14(9):842-53. doi: 10.1038/modpathol.3880400. PMID: 11557779.

9. Reifenberger J, Reifenberger G, Liu L, James CD, Wechsler W, et al. Molecular genetic analysis of oligodendroglial tumors shows preferential allelic deletions on 19q and 1p. Am J Pathol. 1994 Nov;145(5):1175-90. PMID: 7977648; PMCID: PMC1887413.

10.Smits M. Imaging of oligodendroglioma. Br J Radiol. 2016;89(1060):20150857. doi: 10.1259/bjr.20150857. Epub 2016 Feb 5. PMID: 26849038; PMCID: PMC4846213.

11.Weller M, Stupp R, Hegi ME, van den Bent M, Tonn JC, Sanson M, et al. Personalized care in neuro-oncology coming of age: why we need MGMT and 1p/19q testing for malignant glioma patients in clinical practice. Neuro Oncol. 2012 Sep;14 Suppl 4(Suppl 4):iv100-8. doi: 10.1093/neuonc/nos206. PMID: 23095825; PMCID: PMC3480248.

12.Roth P, Wick W, Weller M. Anaplastic oligodendroglioma: a new treatment paradigm and current controversies. Curr Treat Options Oncol. 2013 Dec;14(4):505-13. doi: 10.1007/s11864-013-0251-7. PMID: 23907441.

13.Polivka J Jr, Polivka J, Rohan V, Topolcan O. New treatment paradigm for patients with anaplastic oligodendroglial tumors. Anticancer Res. 2014 Apr;34(4):1587-94. PMID: 24692686.

14.Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007 Aug;114(2):97-109. doi: 10.1007/ s00401-007-0243-4. Epub 2007 Jul 6. Erratum in: Acta Neuropathol. 2007 Nov;114(5):547. PMID: 17618441; PMCID: PMC1929165.

15.Garcia Pulido P, Neal J, Halpin S, Hamandi K. Multicentric oligodendroglioma: case report and review of the literature. Seizure. 2013 Jul;22(6):480-2. doi: 10.1016/j.seizure.2013.02.018. Epub 2013 Mar 23. PMID: 23528979.

16.van den Bent MJ, Kros JM, Heimans J, et al: Response rate and prognostic factors of recurrent oligodendroglioma treated with procarbazine, CCNU and vincristine chemotherapy: Dutch NeuroOncology Group. Neurology 51:1140-1145, 1998.

17.Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, et al. Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA. 2012 Nov 14;308(18):1881-8. doi: 10.1001/jama.2012.12807. PMID: 23099483.

18.Jakola AS, Myrmel KS, Kloster R, Torp SH, Lindal S, et al. Comparison of a strategy favoring early surgical resection vs a strategy favoring watchful waiting in low-grade gliomas. JAMA. 2012 Nov 14;308(18):1881-8. doi: 10.1001/jama.2012.12807. PMID: 23099483.

19.Whittle IR. The dilemma of low grade glioma. J Neurol Neurosurg Psychiatry. 2004 Jun;75 Suppl 2(Suppl 2):ii31-6. doi: 10.1136/ jnnp.2004.040501. PMID: 15146037; PMCID: PMC1765658.

20.Bigner SH, Matthews MR, Rasheed BK, Wiltshire RN, Friedman HS, et al. Molecular genetic aspects of oligodendrogliomas including analysis by comparative genomic hybridization. Am J Pathol. 1999 Aug;155(2):375-86. doi: 10.1016/S0002-9440(10)65134-6. PMID: 10433931; PMCID: PMC1866844.

21.Bettegowda C, Agrawal N, Jiao Y, Sausen M, Wood LD, et al. Mutations in CIC and FUBP1 contribute to human oligodendroglioma. Science. 2011 Sep 9;333(6048):1453-5. doi: 10.1126/science.1210557. Epub 2011 Aug 4. PMID: 21817013; PMCID: PMC3170506.

22.Snuderl M, Eichler AF, Ligon KL, Vu QU, Silver M, et al. Polysomy for chromosomes 1 and 19 predicts earlier recurrence in anaplastic oligodendrogliomas with concurrent 1p/19q loss. Clin Cancer Res. 2009 Oct 15;15(20):6430-7. doi: 10.1158/1078-0432.CCR-09-0867. Epub 2009 Oct 6. PMID: 19808867; PMCID: PMC2818514.

23.Wiens AL, Cheng L, Bertsch EC, Johnson KA, Zhang S, et al. Polysomy of chromosomes 1 and/or 19 is common and associated with less favorable clinical outcome in oligodendrogliomas: fluorescent in situ hybridization analysis of 84 consecutive cases. J Neuropathol Exp Neurol. 2012 Jul;71(7):618-24. doi: 10.1097/NEN.0b013e31825b5f7a. PMID: 22710961.

24.Cairncross JG, Ueki K, Zlatescu MC, Lisle DK, Finkelstein DM, et al. Specific genetic predictors of chemotherapeutic response and survival in patients with anaplastic oligodendrogliomas. J Natl Cancer Inst. 1998;90:1473–1479.

25.Smith JS, Perry A, Borell TJ, Lee HK, O’Fallon J, et al. Alterations of chromosome arms 1p and 19q as predictors of survival in oligodendrogliomas, astrocytomas, and mixed oligoastrocytomas. J Clin Oncol. 2000;18:636–645.

26.Ino Y, Betensky RA, Zlatescu MC, Sasaki H, Macdonald DR, et al. Molecular subtypes of anaplastic oligodendroglioma: implications for patient management at diagnosis. Clin Cancer Res. 2001;7:839–845.

27.Wang M, Murphy KM, Kulesza P, Hatanpaa KJ, Olivi A, et al. Molecular diagnosis of metastasizing oligodendroglioma: a case report. J Mol Diagn. 2004 Feb;6(1):52-7. doi: 10.1016/S1525-1578(10)60491-6. PMID: 14736827; PMCID: PMC1867467.

28.Ueki K, Nishikawa R, Nakazato Y, Hirose T, Hirato J, et al. Correlation of histology and molecular genetic analysis of 1p, 19q, 10q, TP53, EGFR, CDK4, and CDKN2A in 91 astrocytic and oligodendroglial tumors. Clin Cancer Res. 2002;8:196–201

29.Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009 Feb 19;360(8):765- 73. doi: 10.1056/NEJMoa0808710. PMID: 19228619; PMCID: PMC2820383.

30.Shin DW, Lee S, Song SW, Cho YH, Hong SH, et al. Survival outcome and prognostic factors in anaplastic oligodendroglioma: a singleinstitution study of 95 cases. Sci Rep. 2020 Nov 19;10(1):20162. doi: 10.1038/s41598-020-77228-2. PMID: 33214617; PMCID: PMC7677372.

31.Goel NJ, Abdullah KG, Lang SS. Outcomes and Prognostic Factors in Pediatric Oligodendroglioma: A Population-Based Study. Pediatr Neurosurg. 2018;53(1):24-35. doi: 10.1159/000481458. Epub 2017 Nov 2. PMID: 29131101.

32.Miller CR, Dunham CP, Scheithauer BW, Perry A. Significance of necrosis in grading of oligodendroglial neoplasms: a clinicopathologic and genetic study of newly diagnosed high-grade gliomas. J Clin Oncol. 2006 Dec 1;24(34):5419-26. doi: 10.1200/JCO.2006.08.1497. PMID: 17135643.

33.Miller CR, Perry A. Glioblastoma. Arch Pathol Lab Med. 2007 Mar;131(3):397-406. doi: 10.1043/1543-2165(2007)131[397:G]2.0. CO;2. PMID: 17516742.

34.van den Bent MJ. Interobserver variation of the histopathological diagnosis in clinical trials on glioma: a clinician’s perspective. Acta Neuropathol. 2010;120(3):297–304.

35.Cairncross G, Berkey B, Shaw E, Jenkins R, Scheithauer B, et al. Intergroup Radiation Therapy Oncology Group Trial 9402, Phase III trial of chemotherapy plus radiotherapy compared with radiotherapy alone for pure and mixed anaplastic oligodendroglioma: Intergroup Radiation Therapy Oncology Group Trial 9402. J Clin Oncol. 2006 .

36.van den Bent MJ, Carpentier AF, Brandes AA, Sanson M, Taphoorn MJ, et al. Adjuvant procarbazine, lomustine, and vincristine improves progression-free survival but not overall survival in newly diagnosed anaplastic oligodendrogliomas and oligoastrocytomas: a randomized European Organisation for Research and Treatment of Cancer phase III trial. J Clin Oncol. 2006 Jun 20;24(18):2715-22. doi: 10.1200/ JCO.2005.04.6078. PMID: 16782911.

37.Claus EB, Horlacher A, Hsu L, Schwartz RB, Dello-Iacono D, et al. Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer. 2005 Mar 15;103(6):1227-33. doi: 10.1002/cncr.20867. PMID: 15690327.

38.Walker C, du Plessis DG, Fildes D, Haylock B, Husband D, et al. Correlation of molecular genetics with molecular and morphological imaging in gliomas with an oligodendroglial component. Clin Cancer Res. 2004 Nov 1;10(21):7182-91. doi: 10.1158/1078-0432.CCR-04- 0681. PMID: 15534091.

39.Mandonnet E, Delattre JY, Tanguy ML, Swanson KR, Carpentier AF, et al. Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol. 2003 Apr;53(4):524-8. doi: 10.1002/ana.10528. PMID: 12666121.

40.Gorlia T, Delattre JY, Brandes AA, Kros JM, Taphoorn MJ, et al. New clinical, pathological and molecular prognostic models and calculators in patients with locally diagnosed anaplastic oligodendroglioma or oligoastrocytoma. A prognostic factor analysis of European Organisation for Research and Treatment of Cancer Brain Tumour Group Study 26951. Eur J Cancer. 2013 Nov;49(16):3477-85. doi: 10.1016/j.ejca.2013.06.039. Epub 2013 Jul 26. PMID: 23896377.

41.Cairncross G, Macdonald D, Ludwin S, et al: Chemotherapy for anaplastic oligodendroglioma: National Cancer Institute of Canada Clinical Trials Group. J Clin Oncol 12:2013-2021, 1994.

42.Burger PC. What is an oligodendroglioma? Brain Pathol. 2002;12(2):257–259.

43.Kros JM Gorlia T Kouwenhoven MC et al. Panel review of anaplastic oligodendroglioma from EORTC trial 26951: assessment of consensus in diagnosis, influence of 1p/19q loss and correlations with outcome. J Neuropathol Exp Neurol. 2007;66(6):545–551.

44.Wick W Hartmann C Engel Cet al. NOA-04 randomized phase iii trial of sequential radiochemotherapy of anaplastic glioma with procarbazine, lomustine, and vincristine or temozolomide. J Clin Oncol. 2009;27(35):5874–5880.

45.Giannini C Burger PC Berkey BA et al. Anaplastic oligodendroglial tumors: refining the correlation among histopathology, 1p 19q Deletion and clinical outcome in intergroup radiation therapy oncology group trial 9402. Brain Pathol. 2008;18(3):360–369.

46.Kouwenhoven MC Gorlia T Kros JM et al. Molecular analysis of anaplastic oligodendroglial tumors in a prospective randomized study: a report from EORTC study 26951. Neuro Oncol. 2009;11(6):737–746.

Citation

Mahmoudzadeh S, Parrill A, Tsao T, Eaton K, Sheplay K, et al. (2021) Oligodendroglioma with Anaplastic Features, Case Report and Review of the Literature. SM J Neurol Neurosci 7: 5.