A Prospective Analysis of Circulating Plasma Metabolites Associated with Ovarian Cancer Risk

Cancer Res. 2020 Mar 15;80(6):1357-1367. doi: 10.1158/0008-5472.CAN-19-2567. Epub 2020 Jan 22.

Abstract

Ovarian cancer has few known risk factors, hampering identification of high-risk women. We assessed the association of prediagnostic plasma metabolites (N = 420) with risk of epithelial ovarian cancer, including both borderline and invasive tumors. A total of 252 cases and 252 matched controls from the Nurses' Health Studies were included. Multivariable logistic regression was used to estimate ORs and 95% confidence intervals (CI), comparing the 90th-10th percentile in metabolite levels, using the permutation-based Westfall and Young approach to account for testing multiple correlated hypotheses. Weighted gene coexpression network analysis (WGCNA; n = 10 metabolite modules) and metabolite set enrichment analysis (n = 23 metabolite classes) were also evaluated. An increase in pseudouridine levels from the 10th to the 90th percentile was associated with a 2.5-fold increased risk of overall ovarian cancer (OR = 2.56; 95% CI, 1.48-4.45; P = 0.001/adjusted P = 0.15); a similar risk estimate was observed for serous/poorly differentiated tumors (n = 176 cases; comparable OR = 2.38; 95% CI, 1.33-4.32; P = 0.004/adjusted P = 0.55). For nonserous tumors (n = 34 cases), pseudouridine and C36:2 phosphatidylcholine plasmalogen had the strongest statistical associations (OR = 9.84; 95% CI, 2.89-37.82; P < 0.001/adjusted P = 0.07; and OR = 0.11; 95% CI, 0.03-0.35; P < 0.001/adjusted P = 0.06, respectively). Five WGCNA modules and 9 classes were associated with risk overall at FDR ≤ 0.20. Triacylglycerols (TAG) showed heterogeneity by tumor aggressiveness (case-only heterogeneity P < 0.0001). The TAG association with risk overall and serous tumors differed by acyl carbon content and saturation. In summary, this study suggests that pseudouridine may be a novel risk factor for ovarian cancer and that TAGs may also be important, particularly for rapidly fatal tumors, with associations differing by structural features. SIGNIFICANCE: Pseudouridine represents a potential novel risk factor for ovarian cancer and triglycerides may be important particularly in rapidly fatal ovarian tumors.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Adult
  • Aged
  • Biomarkers, Tumor / blood*
  • Biomarkers, Tumor / metabolism
  • Carcinoma, Ovarian Epithelial / blood
  • Carcinoma, Ovarian Epithelial / diagnosis
  • Carcinoma, Ovarian Epithelial / epidemiology*
  • Carcinoma, Ovarian Epithelial / metabolism
  • Case-Control Studies
  • Female
  • Follow-Up Studies
  • Gene Expression Profiling
  • Humans
  • Metabolomics
  • Middle Aged
  • Ovarian Neoplasms / blood
  • Ovarian Neoplasms / diagnosis
  • Ovarian Neoplasms / epidemiology*
  • Ovarian Neoplasms / metabolism
  • Prospective Studies
  • Pseudouridine / blood*
  • Pseudouridine / metabolism
  • Risk Assessment / methods
  • Risk Factors
  • Triglycerides / blood*
  • Triglycerides / metabolism

Substances

  • Biomarkers, Tumor
  • Triglycerides
  • Pseudouridine