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Home , Central neurocytoma, Subependymoma

BRAIN ABBREVIATION KEY

DNET ϭ dysembryoplastic neuroepithelial tumor WHO ϭ World Health Organization

Received August 30, 2018; accepted November 19, 2018. Neuroimaging Findings in Septal From the Departments of Neuroradiology (P.P.B., P.D., T.J.E.M., S.H.P., J.H.D.) and Dysembryoplastic Neuroepithelial Pathology (Neuropathology) (M.B.L.), University of Virginia Health System, Charlottesville, Tumor: Why Is It Important to Virginia. Previously presented as electronic Recognize This Entity? educational exhibit at the 56th Annual Meeting of the American Society of Neuroradiology, June P.P. Batchala, P. Darvishi, T.J. Eluvathingal Muttikkal, S.H. Patel, M.B. Lopes, and 2–7, 2018, Vancouver, British J.H. Donahue Columbia, Canada. Disclosures S. Patel—UNRELATED: Grants/grants pending: RSNA, Comments: RSNA scholar grant for ABSTRACT research unrelated to the current A dysembryoplastic neuroepithelial tumor like neoplasm of the septum pellucidum is a rare manuscript. entity that can be easily mistaken for more common pathologies, such as a colloid cyst, Please address correspondence to Prem P. Batchala, MD, Department central , or involving the septum pellucidum. On histopathologic ex- of Neuroradiology, University of amination, these tumors can mimic central neurocytomas, , or oligoden- Virginia Medical Center, 1215 Lee Street, Charlottesville, VA 22908; drogliomas. Here, we describe clinical and imaging findings in 4 patients with dysembryo- e-mail: [email protected]. plastic neuroepithelial tumor like neoplasms arising from the septum pellucidum. A http://dx.doi.org/10.3174/ng.1800044 systematic review of the literature follows.

INTRODUCTION torial extracortical locations of DNET The term “dysembryoplastic neuroepithe- include the third ventricle, basal ganglia, lial tumor (DNET)” was originally coined and septum pellucidum.4,5,7 by Daumas-Duport et al1 in 1988. It was Septal DNETs, like their cortical coun- described as a predominantly supratento- terparts, are World Health Organization rial, cortical-based tumor with multinodu- (WHO) grade I neoplasms. But, unlike lar architecture and cellular heterogeneity cortical DNETs, they mostly present with in 39 patients with medically intractable obstructive symptoms rather than sei- partial complex .1 DNETs typically zures.4 On imaging, septal DNET can have mixed glial and neuronal elements on mimic more common neoplastic and non- .1 Typical imaging findings in- neoplastic entities that can arise from the clude a hypoattenuated lesion on CT that septum pellucidum or the foramen of shows T1-weighted hypointensity, T2- Monro. Neoplastic mimics include central weighted hyperintensity, and a characteris- neurocytomas, subependymomas, intra- tic FLAIR hyperintense peripheral rim.2 ventricular , and low-grade Since the original case review in 1988, our , whereas nonneoplastic mimics in- understanding of DNET has evolved. It has clude parasitic cysts (eg, neurocysticerco- been documented that DNETs can occur sis) and colloid cysts. Herein, we describe elsewhere than the typical cortical loca- the clinical and imaging findings in 4 pa- tion.3-8 DNETs can be multifocal, can in- tients with septal DNET from our institu- crease in size during follow-up imaging, tion with histologic confirmation in 3. In with occasional recurrence after resec- addition, we present a systematic literature tion, and, also, very rarely, can undergo review of septal DNET and describe imag- malignant transformation after radiation ing findings of more common mimics of therapy.9-11 The less common supraten- septal DNET.

212 ͉ Neurographics 2019 May/June;9(3):212–219; www.neurographics.org Fig 1. Surgically proved septal DNET. A 6-year-old girl presented with obstructive . A, Axial CT shows a nearly imperceptible left lateral ventricle hypoattenuated septal DNET (arrow) close to the foramen of Monro, causing left lateral ventricle outflow obstruction. B, Axial T2WI shows the lesion to be homogeneously hyperintense (arrow), blending with the CSF background. C, Axial contrast-enhanced T1WI shows the absence of enhancement in the septal DNET (arrow). D, Axial ADC demonstrates facilitated diffusion in the lesion (arrow). E, Axial FLAIR better delineates the septal lesion (arrow) compared with other MR images and CT.

Fig 2. Septal DNET recurrence 1 year after gross total resection. A, A high-resolution axial T2 sequence better delineates the walls of the hyperintense intraventricular mucoid recurrent septal tumor (arrow). B, Axial FLAIR sequence, showing a hyperintense rim around the recurrent tumor (arrow), a finding also previously reported with cortical DNET. C, Coronal contrast-enhanced T1WI, revealing the relation of the recurrent tumor to the foramen of Monro (arrow). A small, postsurgical, interhemispheric subdural collection is also present (white star).

PATIENT 1 A 6-year-old girl presented with headaches. An initial CT was suspicious for a septal mass that was causing obstruc- tive hydrocephalus. On MR imaging, a cystic lesion was evident at the foramen of Monro, initially reported as a possible atypical colloid cyst (in view of the absence of typical CT hyperattenuation) or a parasitic or glioependy- mal cyst (Fig 1). The patient underwent gross total resection with histopathology that showed a low-grade glioma. Fol- Fig 3. Surgically proved septal DNET. A 22-year-old woman with ob- structive hydrocephalus. A, Axial T2WI, showing an elliptical, hyperin- low-up imaging after a year demonstrated recurrence (Fig tense septal DNET located between the leaves of the anterior inferior 2). Histopathologic examination of the repeated resection septum (arrow). B, Axial FLAIR sequence reveals a hyperintense rim was characteristic for a septal DNET-like lesion. The pa- around the centrally hypointense septal DNET (arrow). A correct preop- tient’s postoperative course was complicated by pituitary erative diagnosis was made in this case. insufficiency and persistent hydrocephalus that required a ventriculoperitoneal shunt. There was no recurrence in the lucidum. There was no evidence of progression in the 6-year 9-year follow-up after the second resection. follow-up.

PATIENT 2 PATIENT 3 A 22-year-old woman presented with acute-onset severe A 14-year-old girl presented with acute-onset headaches, headaches, nausea, and emesis. MR imaging revealed a sep- nausea, and vomiting. MR imaging revealed an intraven- tal mass that caused obstructive hydrocephalus (Fig 3), tricular mass in the left lateral ventricle along the septum and a preoperative diagnosis of septal DNET was made. pellucidum, which caused obstructive hydrocephalus and The patient underwent subtotal resection with histology was reported as a colloid cyst (Fig 4). The patient under- consistent with a DNET-like neoplasm of the septum pel- went gross total resection with histopathology initially re-

Neurographics 2019 May/June;9(3):212–219; www.neurographics.org ͉ 213 Fig 4. Surgically proved septal DNET. A 14-year-old girl presented with Fig 6. Septal DNET. A, Low-magnification (40x) and (B) high-magnifica- obstructive hydrocephalus. A, Axial T2WI, showing a homogeneously tion (100x) images, showing like cells (large arrows) hyperintense, rounded septal DNET in the left lateral ventricle attached aligned in columns in a background of mucoid matrix with floating neu- to the anterior-inferior aspect of the septum pellucidum (arrow). B, Axial rons (small arrow) (H&E). Cortical DNET shows similar findings. FLAIR sequence reveals a homogeneously hypointense tumor (arrow). There is no hyperintense FLAIR rim in this patient. The initial histopatho- logic diagnosis was low-grade glioma in this patient, and a local recur- septum pellucidum is a relatively preferred site. The other rence (not shown) after 2 years was treated by gamma knife. A retro- reported sites are the basal ganglia, third ventricle, brain spective review of the histopathology was consistent with a DNET-like 5,7,8 neoplasm of the septum pellucidum. stem, and cerebellum. A systematic review of the Eng- lish literature conducted using PubMed and internet search identified 11 peer-reviewed publications that detailed 30 patients with DNET that involved the septum pellucidum near the foramen of Monro, which, in conjunction with our 4 reported patients, yielded a total of 34 patients (Table 1).3-5,9,12-19 In a large series of 51 DNETs, only 2 patients had lesions that occurred within the ventricles.9 Baisden et al4 reported the single largest series of septal DNET in the English literature to date, with 10 patients. In contradistinction to cortical DNETs, patients with Fig 5. MRI, suggestive of a septal DNET. A 62-year-old woman with head- septal lesions overwhelmingly presented with headache or ache. A, Axial T2WI, showing a homogeneous T2-hyperintense tumor splaying the septal leaves (arrow), an appearance similar to the patient other obstructive symptoms, with only 3 patients who pre- illustrated in Fig 3. B, A hyperintense rim is present around the tumor in sented with and 3 tumors identified incidentally. this axial FLAIR image (arrow). The tumor remained stable for 6 months, The mean age of diagnosis was 22.6 years (range, 3–62 and the patient remains on a serial follow-up protocol. years) and the male-to-female ratio was 10 to 23. The mean imaging follow-up among the 17 patients for whom fol- ported as a low-grade glioma ( versus low-up was reported was 4.1 years, during which time 3 ). However, there was no isocitrate dehydro- patients demonstrated tumor progression (the mean time to genase (IDH) mutation or 1p/19q codeletion on molecular progression was 1.5 years). Daghistani et al9 reported a analysis. Approximately 2 years later, follow-up imaging dem- patient with multiple intraventicular recurrences distant onstrated recurrence (Fig 5). Gamma knife stereotactic radio- from the primary septal tumor site at 0.9–3.3 years after surgery was performed with subsequent lesion regression and subtotal resection. Two other lesions demonstrated local no progression during a 5-year follow-up. A retrospective re- recurrence after gross total resection at 1 and 2 years. view of the histopathology was consistent with a DNET-like On histologic examination, septal DNETs are very sim- neoplasm of the septum pellucidum. ilar to their cortical counterparts. Oligodendrocyte like cells are aligned in a columnar fashion along axons and small PATIENT 4 vessels, which form the so-called specific glioneuronal ele- A 62-year-old woman presented for an evaluation of head- ment, and floating in a mucoid background are aches. CT examination revealed a hypoattenuated lesion at characteristic findings (Fig 6). Yet histology of a septal the foramen of Monro thought to be an atypical colloid cyst DNET on surgical specimens can still pose a challenge or . Follow-up MR imaging revealed a cys- due to close histopathologic features with oligodendro- tic lesion with MR imaging findings compatible with a sep- gliomas or central neurocytomas in piecemeal surgical tal DNET (Fig 6). There was no hydrocephalus. A 6-month specimens.4 In our series, the final histologic diagnosis follow-up revealed a stable lesion, with no developing hy- was made only after retrospective review in 2 of the 3 drocephalus. The patient is currently being observed with patients, with the initial diagnosis being a low-grade gli- serial MR imaging scans. oma in both instances. From an imaging standpoint, a septal DNET is typically DISCUSSION located in the anterior-inferior aspect of the septum pellu- Although uncommon, it is important to be aware that cidum close to the foramen of Monro. The tumor is usually DNET can occur in extracortical locations and that the seen attached to the septum pellucidum or can be found

214 ͉ Neurographics 2019 May/June;9(3):212–219; www.neurographics.org Table 1: Literature review of septum pellucidum DNET and summary of clinical features Presenting Progression - Yes (Y) or No (N) Follow-up Case No. Age (y) Gender Symptoms Intervention Time to Progression - y (in years) (in years) Study 1 26 F HA Biopsy N 3 Cervera-Pierot et al,5 1997 2 17 M SZ Biopsy N 12 Cervera-Pierot et al,5 1997 3 22 F SZ Biopsy, N 8 Cervera-Pierot et al,5 1997 radiotherapy 4 21 F HA, SZ Biopsy — — Cervera-Pierot et al,5 1997 5 20 M Incidental Autopsy — — Baisden et al,4 2001 6 35 F HA, VD GTR N 7 Baisden et al,4 2001 7 20 F HA, VD GTR N 0.4 Baisden et al,4 2001 8 13 M HA, SZ GTR N 1.7 Baisden et al,4 2001 9 6 F SZ, personality change GTR N 1.3 Baisden et al,4 2001 10 19 M Hydrocephalus GTR — — Baisden et al,4 2001 11 26 F HA STR — — Baisden et al,4 2001 12 35 M HA, N, V GTR — — Baisden et al,4 2001 13 17 M HA, N, V STR N 0.5 Baisden et al,4 2001 14 24 F HA GTR N 1.2 Baisden et al,4 2001 15 21 F HA GTR — — Onguru et al,19 2003 16 21 M Incidental Resection — — Ashalatha et al,13 2005 17 12 F HA GTR — — Harter et al,15 2006 18 57 F HA, N/V GTR N 7 Wang et al,12 2007 19 42 F HA, DZ STR N 4 Saito et al,16 2008 20 20 M HA, DZ STR N 2 Saito et al,16 2008 21 15 F Incidental GTR N 0.75 Yuan et al,18 2011 22 25 F HA Resection — — Emmez et al,17 2012 23 — — — STR Y; intraventricular recurrence — Daghistani et al,9 2013 ϫ3 times at 0.9, 1.5, 3.3 y 24–29 range, 3–34; 4 F, 3 M HA Resection — — Gessi et al,14 2016 mean, 16.7 30 29 F HA, N, V, SZ GTR — — Stark et al,3 2018 31 6 F HA GTR Y; 1 y 9 Batchala et al,XX 2018 32 22 F HA, N, V STR N 6 Batchala et al,XX 2018 33 14 F HA, N, V GTR; GKRS Y; 2 y 5 Batchala et al,XX 2018 34 62 F HA Observation N 0.5 Batchala et al,XX 2018 Note:—HA indicates headache; SZ, seizure; VD, visual disturbance; GTR, gross total resection; N, nausea; V, vomiting; STR, subtotal resection; N/V, nausea/vomiting; DZ, dizziness; GKRS, gamma knife ; xx, current study. between the leaves of the septum. It is usually less than 3 cm T2-weighted sequences. Significant heterogeneity, calcifica- in size, with a round or oval shape and mild, smooth lobu- tions, perilesional edema, and solid areas of enhancement lations. The MR imaging signal intensity characteristics re- within the tumor should raise suspicion for other neo- semble those of a cortical DNET and reflect the cystic or plasms, such as , oligodendrogli- mucoid nature of the tumor. Homogeneous T2-weighted oma, intraventricular , subependymal giant hyperintensity, facilitated diffusion, and central T1-weighted cell , or . The identification of a and FLAIR hypointensity with a peripheral rim of FLAIR hy- mural nodule or scolex on high-resolution T2-weighted se- perintensity are typical findings. quences can help in differentiating a septal DNET from Also, we observed that, when the tumor is small, it can be neurocysticercosis at this location. Atypical iso- to hypoat- difficult to perceive against the CSF background on CT and tenuated colloid cysts, subependymomas, or low-grade as- routine T1-weighted and T2-weighted sequences. The tu- trocytomas can sometimes be indistinguishable from septal mor is better appreciated on FLAIR and high-resolution DNETs.

Neurographics 2019 May/June;9(3):212–219; www.neurographics.org ͉ 215 Table 2: Differential diagnosis of septum pellucidum lesions Differential Diagnosis for Septum Pellucidum Lesions Characteristic Imaging Findingsa Colloid cyst Location: typically in the roof of third ventricle, close to the foramen of Monro, splaying forniceal pillars Rounded morphology Hyperdense on CT (2/3rd of cases) Variable MRI signal; hyperintense on T1-weighted sequences (2/3rd of cases) Central neurocytoma Location: in the body of the lateral ventricle; 50% attached to the septum pellucidum Lobulated morphology “Soap bubble” appearance on T2-weighted sequences Calcification common (Ͼ50%) Heterogeneous enhancement Subependymoma Location: can be seen in the third ventricle or attached to the septum pellucidum (but more commonly in the inferior fourth ventricle) Lobulated morphology Typically homogeneous MRI signal, hyperintense on T2-weighted sequences; unlike DNET, homogeneously hyperintense on FLAIR No or only mild enhancement Lower-grade glioma Location: rarely isolated septum pellucidum involvement Variable morphology: circumscribed to infiltrative Variable MRI signal intensity, depending on astrocytic or oligodendroglial lineage; heterogeneity and calcification common in oligodendroglial lineage; astrocytic lineage can be indistinguishable Variable enhancement Higher-grade glioma Infiltrative morphology Heterogeneous enhancement; restricted diffusion, hyperperfusion Subependymal giant cell astrocytoma Location: foramen of Monro Lobulated morphology Heterogeneous enhancement Calcification may be present Tuberous sclerosis stigmata: tubers, subependymal nodules Meningioma, intraventricular Location: rarely in the third ventricle or septum pellucidum; more common in atrium of lateral ventricle Lobulated morphology Homogeneous intense enhancement Calcification is common Septal DNET Location: between leaves of septum pellucidum Rounded, elliptical, or lobulated morphology Homogeneously hypointense on T1-weighted sequences, hyperintense on T2-weighted sequences, and hypointense on FLAIR with peripheral hyperintense rim No enhancement Neurocysticercosis (vesicular stage) Location: variable; lesions elsewhere Rounded morphology Homogeneously hyperintense on T2 in “vesicular stage” with, typically, an eccentric hypointense scolex Note:—a Imaging clues are italicized.

SEPTAL DNET MIMICS ON IMAGING more frequently at this location and have similar imaging Septal DNET mimics on imaging are presented in Table 2. appearances. In our experience, the most common mimics As demonstrated in the aforementioned patients, a septal that we encountered were colloid cysts, central neurocyto- DNET can be confused with pathologic entities that occur mas, subependymomas, and septal gliomas. Colloid cysts

216 ͉ Neurographics 2019 May/June;9(3):212–219; www.neurographics.org Fig 7. Septal DNET mimic: colloid cyst. A, Axial T2-weighted, (B) axial T1-weighted, and (C) coronal contrast-enhanced T1WIs show a colloid cyst typically located at the foramen of Monro (arrows), appearing hypointense on T2WI and hyperintense on T1WI due to proteinaceous contents, with no contrast enhancement.

Fig 8. Septal DNET mimic: central neurocytoma. A, Axial T2-weighted, (B) axial ADC, and (C) axial contrast-enhanced T1WIs show a central neurocy- toma (arrows) arising from the septum pellucidum, with mild T2-weighted heterogeneity, restricted diffusion, and heterogeneous enhancement. A “soap bubble” appearance has been described on T2WI.

Fig 9. Septal DNET mimic: subependymoma. A, Axial T2-weighted, (B) axial FLAIR, and (C) axial contrast-enhanced T1WIs show a subependymoma (arrows) from the septum pellucidum, with a close resemblance to septal DNET MR imaging signal intensity characteristics, though lacking the “FLAIR rim sign” common to DNETs. are benign, mucin-containing lesions that are characteristi- Complete surgical resection is often curative, with chemo- cally found within the roof of the third ventricle near the radiation often reserved for incomplete resections.21 foramen of Monro. Typically, they are rounded, Ͻ3cmin Subependymomas are benign WHO grade I intraventric- size, hyperattenuated on CT, and, on MR imaging, can be ular lesions that most commonly present in middle-age to hyperintense on T1-weighted and hypointense on T2- elderly patients. The fourth ventricle is the most common weighted sequences, depending on the water-to-protein ra- location. Occasionally, they can be found attached to the tio (Fig 7). As with septal DNET, hydrocephalus can be the septum pellucidum. Like DNETs, they can be homoge- initial presentation. Endoscopy-guided complete resection neously T2 hyperintense and are usually nonenhancing. results in a cure.20 However, unlike DNETs, subependymomas more com- Central neurocytomas are WHO grade II intraventricu- monly demonstrate central hyperintensity on FLAIR (Fig lar neuroepithelial neoplasms that usually present in young 9). Complete surgical resection is typically curative, with adults, with Ͼ50% of the tumors attached to the septum the use of adjuvant radiation being controversial.22,23 pellucidum close to the foramen of Monro. A multilobu- Lower-grade gliomas, typically WHO grade II astrocy- lated tumor with punctate calcifications on CT and a “bub- tomas or , that involve the septum can bly” solid-cystic appearance on MR imaging with hetero- easily mimic a septal DNET on imaging. On MR imaging, geneous enhancement is suggestive of this low-grade these tumors show T1-weighted hypointensity and T2- tumor (Fig 8). As with a septal DNET, a central neurocy- weighted/FLAIR hyperintensity, without significant en- toma can closely mimic an oligodendroglioma on histology. hancement. However, oligodendrogliomas tend to be more

Neurographics 2019 May/June;9(3):212–219; www.neurographics.org ͉ 217 Fig 10. Septal DNET mimic: giant cell glioblastoma. A, Axial T2-weighted, (B) axial ADC, and (C) axial contrast-enhanced T1WIs show a glioblastoma (arrows) involving the septum and expanding the third ventricle, with T2-weighted hyperintensity and restricted diffusion. The absence of enhance- ment in this patient is atypical for a glioblastoma. heterogeneous, with calcifications. Higher-grade gliomas or further evidence for a germinal origin. Br J Neurosurg 1999; tend to show a more aggressive appearance 13:508–11 with significant heterogeneous enhancement (Fig 10). 7. Leung SY, Gwi E, Ng HK, et al. Dysembryoplastic neuroepi- Other pathologies that are found close to the foramen of thelial tumor. A tumor with small neuronal cells resembling Monro, such as subependymal giant cell astrocytoma, oligodendroglioma. 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