Childs Nerv Syst DOI 10.1007/s00381-015-2684-8

ORIGINAL PAPER

Conventional and advanced (DTI/SWI) neuroimaging findings in pediatric oligodendroglioma Matthias W. Wagner 1 & Andrea Poretti 1 & Thierry A. G. M. Huisman 1 & Thangamadhan Bosemani 1

Received: 17 February 2015 / Accepted: 16 March 2015 # Springer-Verlag Berlin Heidelberg 2015

Abstract Purpose Oligodendroglioma are rare pediatric brain tumors. The literature about neuroimaging findings is scant. A correct presurgical diagnosis is important to plan the therapeutic approach. Here, we evaluated the conventional and advanced neuroimaging features in our cohort of pediatric oligodendrogliomas and discuss our findings in the context of the current literature. Methods Clinical histories were reviewed for tumor grading, neurologic manifestation, treatment, and clinical status at the last follow-up. Neuroimaging studies were retrospectively evaluated for tumor morphology and characteristics on conventional and advanced magnetic resonance imaging (MRI). Results Five children with oligodendroglioma were included in this study. Four children were diagnosed with a low-grade oligodendroglioma. The location of the tumors included the frontal and temporal lobe in two cases each and the frontoparietal lobe in one. In all oligodendrogliomas, tumor margins appeared sharp. In the high-grade oligodendroglioma, a cystic and partially hemorrhagic component was seen. In all children, the tumor showed a T1-hypointense and T2hyperintense signal. The signal intensity on fluid attenuation inversion recovery (FLAIR) images was hyperintense in four and mixed hypo-hyperintense in one child. The anaplastic oligodendroglioma showed postcontrast

* Thangamadhan Bosemani [email protected] 1

Section of Pediatric Neuroradiology, Division of Pediatric Radiology, Russell H. Morgan Department of Radiology and Radiological Science, The Johns Hopkins University School of Medicine, 1800 Orleans Street, Baltimore, MD 21287-0842, USA

enhancement and decreased diffusion while the lowgrade oligodendrogliomas showed increased diffusion. One low-grade oligodendroglioma showed calcifications on susceptibility weighted imaging. Conclusion Conventional MRI findings of pediatric oligodendrogliomas are nonspecific. Advanced MRI sequences may differentiate (1) low-grade and high-grade pediatric oligodendrogliomas and (2) pediatric oligodendrogliomas and other brain tumors.

Keywords Children . Neuroimaging . Oligodendroglioma . Diffusion tensor imaging . Susceptibility weighted imaging

Introduction Oligodendrogliomas are rare tumors in children and account for about 1 % of pediatric brain tumors and 5–18 % of pediatric gliomas [1, 2]. In contrast to these numbers, Puget et al. reported a higher prevalence of pediatric oligodendroglioma [3]. Twenty-two of 85 pediatric gliomas (26 %) were diagnosed as anaplastic oligodendroglioma according to the WHO guideline or oligodendrogliomas type A and B according to the Sainte-Ann classification [3]. Affected children typically present with focal seizures, while headaches, visual field defects, and corticospinal tract signs are less common. Pediatric oligodendrogliomas are typically low-grade, well-differentiated, and slow growing cerebral hemispheric mass lesions that most commonly occur in the frontal region [4]. High-grade, anaplastic oligodendrogliomas are less common [2, 5]. The literature of pediatric oligodendrogliomas, however, is scant and mostly based on single case reports. Neuroimaging plays a key role in the presurgical diagnosis of oligodendrogliomas. Conventional magnetic

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resonance imaging (MRI) provides essential information about the location, signal characteristics, contrast enhancement, and tumor extent, while advanced sequences such as diffusion tensor imaging (DTI) or susceptibility weighted imaging (SWI) may add important information about the biological, physiological, and metabolic features of the tumors. Awareness of the conventional and advanced neuroimaging findings in pediatric oligodendrogliomas may facilitate a correct presurgical diagnosis. This is important to plan the therapeutic approach, such as more or less aggressive surgery and implementation of adjuvant therapies. Here, we review the experience of our tertiary university children’s hospital in the neuroimaging characteristics of pediatric oligodendroglioma. The goals of our study were to evaluate (1) the conventional and advanced (DTI/SWI) imaging characteristics of pediatric oligodendrogliomas in our patients and (2) discuss our findings in the context of the current literature.

neuroimaging (AP), and a radiology resident (MWW). The following image characteristics were evaluated: (1) tumor location and multifocality, (2) peritumoral edema, (3) scalloping of the calvarium, (4) cystic and/or necrotic component, (5) rim of cerebral cortex on T1-weighted images, which is well demarcated from the tumor, and (6) configuration of the tumor margin (sharp vs indistinct). On T1- and T2-weighted images and FLAIR images, the signal intensity of the tumor was evaluated as (1) hypointense, (2) hyperintense, or (3) isointense compared to the adjacent gray matter. On T1CE images, the tumor was assessed for presence of enhancement. In addition, the diffusion characteristics on DTI were classified as (1) decreased, (2) normal, or (3) increased based on apparent diffusion coefficient (ADC) maps. Finally, minimum intensity projection (mIP)-SWI images were evaluated for the presence of foci of hypointense signal within the tumor.

Results Methods This retrospective study was approved by our Institutional Review Board. The inclusion criteria for this study were (1) diagnosis of oligodendroglioma confirmed by neuropathology and (2) age at diagnosis of 18 years and younger. Data from eligible children were obtained through an electronic search of our pediatric neuroradiology database covering the period between January 1, 2008 and September 30, 2014. Clinical histories were reviewed for (1) age and gender of the children, (2) neurologic manifestation at the first presentation, (3) treatment, (4) clinical status at the last follow-up presentation, and (5) expression of p53 and presence of 1p and 19q deletions. All MRI studies were performed on a 1.5 or 3T clinical scanner (Siemens, Erlangen, Germany) using our standard departmental protocol including three-dimensional T1- and axial T2-weighted images, axial, coronal, and sagittal T1weighted contrast-enhanced images (T1CE), an axial fluidattenuated inversion recovery (FLAIR) sequence, and a single-shot spin echo, echo planar axial DTI sequence with diffusion gradients along 20 noncollinear directions (a b-value of 1000 s/mm2 was used for each of the 20 diffusion-encoding directions and an additional measurement without diffusion weighting (b=0 s/mm2) was performed). Since January 1, 2010, SWI has been included in the routine protocol for brain tumors. The neuroimaging features were retrospectively assessed by a pediatric neuroradiologist (TB), a pediatric neurologist with experience in pediatric

Five children (three females) with oligodendroglioma were included in our study (Table 1). The median age at time of head MRI was 8.93 years (range 3.08 to 18.66 years). In four children, oligodendroglioma were low-grade (WHO grade II, Fig. 1), and in one child high-grade (WHO grade III, Fig. 2). Four children presented with focal seizures, and one with headaches and signs of increased intracranial pressure. Tumor resection was performed in all children and was total in three and partial in two patients. In addition, the child with WHO grade III oligodendroglioma received adjuvant chemotherapy. At the last follow-up (median age 12.04 years, range 5.06 to 23.86 years), the four patients with low-grade tumors were disease free, while the patient with a high-grade oligodendroglioma had tumor progression despite ongoing therapy. In terms of genetic biomarkers, tumor p53 expression was positive in one of the three tested children, one of five children had a deletion on both 1p36 and 19q13 chromosomes, and one of five children had an isolated 1p deletion. Two tumors were located in the frontal lobe, two in the temporal lobe, and one had a fronto-parietal location (Table 2). One tumor was multifocal. Peritumoral edema was seen in one patient. Two of five tumors showed scalloping of the overlying calvarium. On T1-weighted images, a distinct rim of cerebral cortex overlying the tumor was seen in three of five patients, whereas in two children, the cortex could not be differentiated due to tumor invasion. In all children, the margin of the tumor was well-circumscribed. The WHO grade III oligodendroglioma was partially cystic and had a hemorrhagic component; no tumor demonstrated a necrotic part. All tumors were hypointense on T1- and hyperintense on T2-weighted images compared to the adjacent cerebral cortex (Table 3).

Childs Nerv Syst Table 1

Clinical and molecular information in five pediatric patients with oligodendroglioma

Patient

Age (years)

Gender

WHO grade

Symptoms prior to diagnosis

Treatment

Follow-up time (years)

Current clinical status

p53

1p36 del

19q13 del

1 2 3 4

18.66 7.99 8.93 16.85

female female male male

II II II III

severe headaches seizure seizure seizure

total resection total resection total resection partial resection + adjuvant CTx

5.20 4.05 0.73 2.11

stable stable stable progredient

neg N/A N/A pos

yes no yes no

yes no no no

5

3.08

female

II

seizure

partial resection

1.98

stable

neg

no

no

Neg negative, pos positive, del deletion, Ctx chemotherapy

On FLAIR images, four of five tumors had a hyperintense signal, while one tumor has a mixed hyper-hypointense signal compared to gray matter. Postcontrast enhancement was seen only in one patient. The low-grade tumors showed increased diffusion on ADC maps, while ADC values were low in the WHO grade III oligodendroglioma representing decreased/ restricted diffusion. SWI data was available only in one child and showed a hypointense focus within the tumor, most likely representing calcification.

Fig. 1 Nine-year-old male (patient 3) with focal seizures and a low-grade oligodendroglioma within the left mesial temporal lobe. a Axial T1-weighted image shows a homogenously hypointense tumor (arrow). b Axial T2-weighted image shows a sharply defined, hyperintense tumor (arrow). c Axial FLAIR image shows a solid tumor with mixed hypointense and hyperintense signal (arrow). d Axial postcontrast T1-weighted image does not show tumor enhancement (arrow). e Axial mIP-SWI image shows an intratumoral hypointense focus representing calcification (arrowhead)

Discussion Oligodendrogliomas are rare pediatric brain tumors that are histologically characterized by regular cells with spherical nuclei containing finely granular chromatin surrounded by a halo of cytoplasm [6]. Histologically, high-grade oligodendrogliomas may be differentiated from low-grade oligodendrogliomas by the presence of necrosis, high mitotic activity, increased/high cellularity, nuclear atypia, cellular

Childs Nerv Syst Fig. 2 Seventeen-year-old male (patient 4) with focal seizures and ananaplastic oligodendroglioma within the left fronto-parietal region. a Sagittal T1-weighted image shows a homogenously hypointense tumor (thick arrow). b Sagittal postcontrast T1weighted image shows a hypointense tumor (thick arrow) with peripheral enhancement (short thin arrows). c Axial FLAIR image shows a hyperintense tumor (thick arrow) with medial hypointense component and additional tumor focus in the cingulate gyrus (long thin arrow). d Axial trace of diffusion and e matching ADC map show decreased diffusion (bright on d, dark on e) of the tumor (arrowheads) and additional tumor in the cingulate gyrus (long thin arrows)

pleomorphism, and microvascular proliferation [6]. In adult oligodendrogliomas, the combined presence of 1p36 and 19q13 deletions plays an additional role to the histological tumor grade and in predicting long-term prognosis [7–9]. In pediatric oligodendrogliomas, however, the combined presence of 1p36 and 19q13 deletions does not have any prognostic value [10–12], and the majority of pediatric oligodendrogliomas do not harbor these deletions [10, 13]. Pediatric oligodendroglioma may be located in all parts of the brain, but the majority arises from the white matter of the cerebral hemispheres [7, 10, 14]. Pediatric oligodendrogliomas are most frequently located in the frontal lobes followed by the temporal and parietal lobes as in our patients. Rarely, pediatric oligodendroglioma may occur in the brainstem [15], cerebellopontine angle [16], optic nerve [6], and spinal cord [17]. In pediatric oligodendrogliomas, the location may predict the long-term outcome: centrally located tumors (e.g., thalamus, Table 2

basal ganglia, or mesencephalon) have a poor prognosis whereas hemispheric or cerebellar tumors have an excellent prognosis [7]. On conventional MRI, the appearance of pediatric oligodendroglioma is nonspecific: their margins are most frequently sharply defined and mildly heterogeneous in signal characteristics, with T1-hypointense and T2-/FLAIR-hyperintense signal as in our patients [18–21]. T2- and FLAIR-hyperintense signal indicates edema surrounding tumor cells [20, 22, 23]. Solid parts of the tumor typically enhance moderately after injection of gadolinium-based intravenous contrast agents [21]. Postcontrast enhancement, however, may be minimal. In our study cohort, the anaplastic oligodendroglioma was the only tumor that showed enhancement on T1CE. Advanced MRI sequences provide information about the biological, physiological, and metabolic features of the tumors. On diffusion-weighted imaging (DWI) and DTI, highgrade tumors show low ADC values due to high cellularity

Neuroimaging characteristics of the tumor morphology in five children with oligodendroglioma

Patient

WHO grade

Location

Multifocal

Peritumoral edema

Calvarial scalloping

Cortical rim on T1

Tumor margin

Cystic/necrotic component

1 2 3 4 5

II II II III II

right frontal left temporal left temporal left frontal/parietal left frontal

no no no yes no

no no no no yes

no yes no no yes

yes yes yes no no

sharp sharp sharp sharp sharp

no no no yes no

Childs Nerv Syst Table 3 MRI signal characteristics in five children with oligodendroglioma

Patient

WHO grade

T1

T2

FLAIR

Contrast enhancement

Diffusion characteristic

SWI

1 2 3 4 5

II II II III II

-

+ + + + +

+ + -/+ + +

no N/A no yes no

increased increased increased decreased increased

N/A N/A N/A N/A

ADC apparent diffusion coefficient, FLAIR fluid-attenuated inversion recovery, N/A not applicable, SWI susceptibility-weighted imaging, “-” hypointense signal, “+” hyperintense signal

and large nucleus to cytoplasmic ratio [24–26]. In agreement with the literature, only the anaplastic oligodendroglioma in our series showed low ADC values and decreased diffusion. Conversely, high ADC values indicating increased diffusion were found in the low-grade oligodendrogliomas, which have typically a low cell density. SWI is a recently developed 3D gradient-echo sequence that is highly sensitive to blood, blood products, and calcifications [27–30]. Intratumoral calcifications are seen in 50–90 % of oligodendrogliomas, while hemorrhagic foci are present in about 20 % of the tumors [2, 6, 10, 21]. Generally, calcifications are typical of low-grade tumors, whereas hemorrhages and an increased vascularity are common in high-grade tumors. However, in the only adult study that applied SWI to evaluate oligodendroglioma, the presence of calcifications on SWI did not correlate with tumor grade [28]. High-grade oligodendrogliomas most likely result from a malignant transformation of low-grade oligodendrogliomas that show intratumoral calcifications. The malignant transformation does not affect the presence of calcifications. Hence, calcifications may be present in both low- and high-grade oligodendrogliomas. In our cohort of pediatric oligodendroglioma, SWI was acquired only in one lowgrade tumor and detected intratumoral calcifications. Tumor vascularity may be studied using perfusionweighted imaging (PWI) [31]. High vascularity reflects high tumor angiogenesis and is typically associated with high tumor grade. In addition, high vascularity as shown by an increased relative cerebral blood volume may help to differentiate between oligodendrogliomas and low-grade gliomas in adults [32]. 1H-magnetic resonance spectroscopy (MRS) allows noninvasive detection and measurement of normal and abnormal metabolites in brain tumors. Generally, high choline-to-creatine ratio and low N-acetylaspartate-to-creatine ratio as well as the presence of lipid and lactate peaks are seen in rapidly proliferating, high-grade tumors. In oligodendroglioma, high choline peak and the presence of lactate and lipid on 1H-MRS are correlated with high tumor grades [33]. The conventional MRI findings of pediatric oligodendroglioma are nonspecific. Advanced sequences may help to differentiate between oligodendrogliomas and

other tumors. The presence of calcifications favors oligodendroglioma compared to pilocytic astrocytoma or dysembryoplastic neuroepithelial tumors (DNETs). Calcifications are best demonstrated on advanced MRI sequences such as SWI. The presence of a lactate peak on 1H-MRS supports the diagnosis of pilocytic astrocytomas compared to lowgrade oligodendroglioma. It is more difficult to differentiate between low-grade oligodendrogliomas and diffuse fibrillary astrocytoma (WHO grade II). Imaging findings on conventional MRI sequences are similar (both show T1 hypointense and T2/FLAIR hyperintense signal) [34], while the presence of calcifications on SWI may favor oligodendrogliomas. In addition, histology identifies fibrillary astrocytoma based on the chronic fibrillary astrogliosis induced by isolated neoplastic oligodendrocytes [35]. The differentiation between highgrade oligodendrogliomas and glioblastoma multiforme is also challenging. Compared to oligodendrogliomas, glioblastoma multiforme appear irregularly hypointense and isointense on T1-weighted images and have a heterogeneous signal on T2-weighted images that result from areas of necrosis or hemorrhage [7]. Peritumoral vasogenic edema is more prominent in glioblastomas compared to oligodendrogliomas [7]. The presence of calcifications, however, favors oligodendrogliomas. Even more problematic is the differentiation between anaplastic oligodendrogliomas and anaplastic gliomas, which are almost indistinguishable by neuroimaging [21]. Only the presence of calcifications may favor oligodendrogliomas. Differentiation between high-grade oligodendrogliomas and anaplastic gliomas requires careful histologic inspection for classic oligodendroglial morphologies, including minigemistocytes and gliofibrillary oligodendrocytes. Similar neuroimaging findings have been reported between high-grade oligodendrogliomas and anaplastic oligoastrocytomas [5]. The differentiation between these two high-grade tumors by neuropathology is also difficult [36]. In conclusion, oligodendroglioma are rare brain tumors in children. Conventional MRI findings of pediatric oligodendroglioma are nonspecific and similar to those of fibrillary astrocytomas and oligoastrocytomas. Advanced MRI sequences may facilitate differentiation between lowgrade and high-grade pediatric oligodendroglioma. The

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differentiation between high-grade oligodendroglioma and high-grade astrocytoma remains, however, difficult.

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