Usefulness of positron emission tomography for differentiating gliomas according to the 2016 World Health Organization classification of tumors of the central nervous system

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OBJECTIVE

Positron emission tomography (PET) is important in the noninvasive diagnostic imaging of gliomas. There are many PET studies on glioma diagnosis based on the 2007 WHO classification; however, there are no studies on glioma diagnosis using the new classification (the 2016 WHO classification). Here, the authors investigated the relationship between uptake of 11C-methionine (MET), 11C-choline (CHO), and 18F-fluorodeoxyglucose (FDG) on PET imaging and isocitrate dehydrogenase (IDH) status (wild-type [IDH-wt] or mutant [IDH-mut]) in astrocytic and oligodendroglial tumors according to the 2016 WHO classification.

METHODS

In total, 105 patients with newly diagnosed cerebral gliomas (6 diffuse astrocytomas [DAs] with IDH-wt, 6 DAs with IDH-mut, 7 anaplastic astrocytomas [AAs] with IDH-wt, 24 AAs with IDH-mut, 26 glioblastomas [GBMs] with IDH-wt, 5 GBMs with IDH-mut, 19 oligodendrogliomas [ODs], and 12 anaplastic oligodendrogliomas [AOs]) were included. All OD and AO patients had both IDH-mut and 1p/19q codeletion. The maximum standardized uptake value (SUV) of the tumor/mean SUV of normal cortex (T/N) ratios for MET, CHO, and FDG were calculated, and the mean T/N ratios of DA, AA, and GBM with IDH-wt and IDH-mut were compared. The diagnostic accuracy for distinguishing gliomas with IDH-wt from those with IDH-mut was assessed using receiver operating characteristic (ROC) curve analysis of the mean T/N ratios for the 3 PET tracers.

RESULTS

There were significant differences in the mean T/N ratios for all 3 PET tracers between the IDH-wt and IDH-mut groups of all histological classifications (p < 0.001). Among the 27 gliomas with mean T/N ratios higher than the cutoff values for all 3 PET tracers, 23 (85.2%) were classified into the IDH-wt group using ROC analysis. In DA, there were no significant differences in the T/N ratios for MET, CHO, and FDG between the IDH-wt and IDH-mut groups. In AA, the mean T/N ratios of all 3 PET tracers in the IDH-wt group were significantly higher than those in the IDH-mut group (p < 0.01). In GBM, the mean T/N ratio in the IDH-wt group was significantly higher than that in the IDH-mut group for both MET (p = 0.034) and CHO (p = 0.01). However, there was no significant difference in the ratio for FDG.

CONCLUSIONS

PET imaging using MET, CHO, and FDG was suggested to be informative for preoperatively differentiating gliomas according to the 2016 WHO classification, particularly for differentiating IDH-wt and IDH-mut tumors.

ABBREVIATIONS AA = anaplastic astrocytoma; AO = anaplastic oligodendroglioma; AUC = area under the curve; CHO = 11C-choline; DA = diffuse astrocytoma; DOR = diagnostic odds ratio; FDG = 18F-fluorodeoxyglucose; GBM = glioblastoma; IDH = isocitrate dehydrogenase; IDH-mut = mutant IDH; IDH-wt = wild-type IDH; MET = 11C-methionine; OD = oligodendroglioma; PET = positron emission tomography; R-2HG = R-2-hydroxyglutarate; ROC = receiver operating characteristic; ROI = region of interest; SUV = standardized uptake value; T/N = tumor maximal SUV/normal brain cortex mean SUV.

Article Information

Correspondence Hiroaki Takei: Chubu Medical Center for Prolonged Traumatic Brain Dysfunction, Kizawa Memorial Hospital, Gifu, Japan. gfwgc34@gmail.com.

INCLUDE WHEN CITING Published online August 16, 2019; DOI: 10.3171/2019.5.JNS19780.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    A and B: Box plots showing the T/N ratios of MET (A), CHO (B), and FDG (C) for each histopathological classification. D and E: Box plots showing comparison of the mean T/N ratios for MET in DA and OD (p = 0.028; D), and those in AA and AO (p = 0.06; E). Lines within the boxes indicate the median, boxes represent the IQR, whiskers denote minimum–maximum, dots within the whiskers indicate the mean, and dots outside the whiskers indicate outliers.

  • View in gallery

    A–C: Box plots showing the T/N ratios of the IDH-wt and the IDH-mut groups in all gliomas. The IDH-wt group contains DA with IDH-wt, AA with IDH-wt, and GBM with IDH-wt. The IDH-mut group contains DA with IDH-mut, AA with IDH-mut, GBM with IDH-mut, OD, and AO. MET (p < 0.001; A), CHO (p < 0.001; B), and FDG (p < 0.001; C). D–F: ROC curves for the 3 tracers (MET [D], CHO [E], and FDG [F]) for distinguishing IDH-wt from IDH-mut for all histopathological classifications. The values within the graph are presented as the cutoff (specificity, sensitivity).

  • View in gallery

    Graphs showing the proportions of patients in the IDH-wt and IDH-mut groups categorized by how many tracers were over the cutoff value; 0/3 indicates that all the mean T/N ratios for the 3 tracers were under the cutoff value, 1/3 indicates that one of the mean T/N ratios for the 3 tracers was over the cutoff value, 2/3 indicates that 2 of the 3 tracers’ mean T/N ratios were over the cutoff value, and 3/3 indicates that all the mean T/N ratios for all 3 tracers were over the cutoff value. Analyses of all patients (n = 105; A), patients with contrast-enhanced lesions on MRI (n = 35; B), patients with non–contrast-enhanced lesions on MRI (n = 68; C).

  • View in gallery

    A–C: Box plots showing comparisons of the mean T/N ratios for MET (A), CHO (B), and FDG (C) in WHO grade II gliomas for DA with IDH-wt, OD, and DA with IDH-mut. There was a significant difference in the mean T/N ratio for MET between DA with IDH-mut and OD (p = 0.041). D–F: Box plots showing comparisons of the mean T/N ratios for MET (D), CHO (E), and FDG (F) in WHO grade III gliomas, including AA with IDH-wt, AO, and AA with IDH-mut. There were significant differences in the mean T/N ratios for all 3 PET tracers between AA with IDH-mut and AA with IDH-wt (p = 0.002 in MET, p = 0.001 in CHO, and p < 0.001 in FDG). There were significant differences in the mean T/N ratios for MET between AA with IDH-wt and AO (p = 0.01) and for FDG between AO and AA with IDH-wt (p = 0.026). G–I: Box plots showing comparisons of the mean T/N ratios for MET (G), CHO (H), and FDG (I) between GBM with IDH-wt and GBM with IDH-mut. There were significant differences in the mean T/N ratios for MET (p = 0.034) and CHO (p = 0.01).

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