Integrating Magnetic Resonance Chemical Shift Imaging for Localized Prostate Cancer Risk Stratification on the Basis of the Impact of Periprostatic Brown Adipocytes Within Tumor Microenvironment.

Abstract

We sought to characterize periprostatic adipose tissue (PPAT) with magnetic resonance imaging (MRI) featuring water-to-oil ratio (R^WO) to detect brown adipocyte (BAT). Between November 2021 and September 2023, 21 localized patients with prostate cancer were studied, categorized as low (n = 4), intermediate (n = 4), and high risk (n = 13). We utilized MRI to analyze the water-only signal and fat-only signal. R^WO was used to predict the risk stratification. Tissue samples, including periprostate fat, were collected during surgery, processed, and stained with hemotoxylin and eosin (H&E) for microscopic analysis. Periprostate adipose cell supernatants were used to treat cancer cells (PC3 and LNCaP) in vitro. We found significantly higher periprostatic adipose tissue R^WO in the high and intermediate risk groups compared with the low risk group (52.12 versus 30.48; p < 0.0001). The receiver operating characteristic curve for distinguishing advanced tumors using PPAT R^WO in MRI imaging yielded an area under the curve of 0.64, which increased to 0.90 after incorporating initial PSA. Immunofluorescence, H&E staining, and immunohistochemistry revealed the presence of brown adipocytes, marked by uncoupling protein 1 expression, in periprostate tumor fat. Results indicate that BAT-related adipokines promote epithelial-mesenchymal transition and invasiveness in human prostate cancer cells. In the study, the chemical shift image of MRI in 21 localized patients with prostate cancer revealed higher periprostatic adipose tissue water-to-oil ratio among patients with high-risk prostate cancer. Adipokines within the tumor-microenvironment attribute to the cancer aggressiveness, and targeting the fat fraction signal in MRI could improve the current risk stratification strategy.