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. 2024 Aug 19;6(1):vdae143.
doi: 10.1093/noajnl/vdae143. eCollection 2024 Jan-Dec.

Oligodendroglioma patient survival is associated with circulating B-cells and age

Jennie W Taylor  1   2   3 , Gayathri Warrier  3 , Helen M Hansen  3 , Lucie McCoy  3 , Terri Rice  3 , Geno Guerra  3 , Stephen S Francis  4   1   3 , Jennifer L Clarke  1   2   3 , Paige M Bracci  4 , Sara Hadad  3 , Karl T Kelsey  5 , Margaret Wrensch  3 , Annette M Molinaro  4   1   3 , John K Wiencke  4   3
Affiliations

Oligodendroglioma patient survival is associated with circulating B-cells and age

Jennie W Taylor et al. Neurooncol Adv. .

Abstract

Background: Variations in survival among patients with oligodendroglioma are unexplained by known prognostic factors. To assess the impact of peripheral immune profiles on prognosis, we applied immunomethylomics analyses-DNA methylation of archived whole blood samples, to characterize immune cells.

Methods: We compared the proportions of immune cells from patients with oligodendroglioma to other glioma subtypes and controls. We used recursive partitioning analysis (RPA) within the oligodendrogliomas to correlate with survival.

Results: Patients with oligodendrogliomas (141) were median age at diagnosis of 44 years; 57% male; 75% White; 60% prior chemotherapy; and 25% on dexamethasone at sample collection. Patients with oligodendrogliomas had immune profiles more similar to controls than other glioma subtypes, though with notably lower B-cells. RPA of patients with oligodendrogliomas delineated 2 survival groups based on an interaction between age and B-naïve cells. Patients with longer survival (median 24.2 years) were ≤42 years of age with higher B-naïve cells versus worse survival (median 16.9 years) who were ≤42 years of age with lower B-naïve cells or >42 years of age (P = .00032). Patients with worse survival also had lower CD4- and CD8-naïve T-cells. Similar immune profiles were observed in an independent cohort of oligodendroglioma patients prior to surgery.

Conclusions: Peripheral blood immune profiles in oligodendroglioma suggested that younger patients with lower B-naïve cells experienced shorter survival. Though our findings lack of validation cohort and use a heterogenous patient population, they suggest peripheral blood immune profiles may be prognostic for patients with glioma and warrant further investigation.

Keywords: epigenetics; glioma; immune factors; immunomethylomics; oligodendroglioma.

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Conflict of interest statement

J.K.W. and K.T.K. are cofounders of Cellintec, which played no role in the current study. The remaining authors declare no competing interests. J.W.T. has received institutional grant support from Servier Pharmaceuticals and Bristol Myers Squibb; advisory board support from Servier Pharmaceuticals. J.L.C. has received institutional grant support from Servier Pharmaceuticals.

Figures

Figure 1.
Figure 1.
Study schema: (A) Participants enrolled in the AGS underwent blood sampling after diagnosis. Immunomethylomic arrays were run on archived blood samples to generate proportions of 12 immune cell subtypes. (B) Immune profiles from patients with oligodendrogliomas were combined with key clinical variables (ie, age at diagnosis), ratios generated from immune cell subtypes, including NDMI, and analyzed for survival using RPA. AGS, Adult Glioma Study; Treg, -regulatory cells; NK, natural killer cells; NDMI, neutrophil dexamethasone methylation index; RPA, recursive partitioning analysis.
Figure 2.
Figure 2.
Clinical and immune profiles RPA delineates 2 survival groups for patients with oligodendrogliomas based on an interaction between age at diagnosis and B naïve cell proportions. (A) Clinical variables and immune profiles RPA from 141 patients with oligodendrogliomas, identified primary node as age and B-naïve cell proportion as secondary node. Patients fell into 2 survival groups. Part 1 were patients with worse outcome, and included patients ≤42 years of age with a lower proportion of B-naïve cells or patients >42 years of age. Part 2 were patients with better outcome included patients who were ≤42 years of age with a higher proportion of B-naïve cells (>1.91). (B) Kaplan–Meier curves are shown for Part 1 and Part 2 (P = .00032). (C) Table of median overall survival, age, and B-naïve cell proportion for the 2 parts.
Figure 3:
Figure 3:
Clinical and immune profiles RPA distinguishing the younger patients by B-naïve cell proportions identifying 3 survival groups for patients with oligodendrogliomas. (A) Clinical variables and immune profiles RPA from 141 patients with oligodendrogliomas, identified primary node as age and B-naïve cell proportion as secondary node. Part 1a were younger patients with worse outcome and included 28 patients ≤42 years of age with a lower proportion of B-naïve cells (≤1.91). Part 1b were older patients with worse outcome and included 76 patients >42 years of age. Part 2 were patients with better outcome included 37 patients who were ≤42 years of age with a higher proportion of B-naïve cells (>1.91). (B) Kaplan–Meier curves are shown for Part 1a, Part 1b, and Part 2 (P = .0013). (C) Table of median overall survival, age, and B-naïve cell proportion for the 3 parts.
Figure 4.
Figure 4.
Comparisons of immune cell proportions (A) B-naïve cell proportions from 141 patients with oligodendrogliomas compared to 308 patients with other glioma subtypes and 454 controls. (B) B-naïve cell proportions from patients with oligodendrogliomas by 2 parts and (C) by 3 parts. (D-F) Cell proportions by 3 parts for other naïve subtypes including CD4 (D), CD8 (E), and total (F).
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