Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective study

Abstract Background Imaging features of colorectal cancers on 2-deoxy-2-[18F]fluoro-d-glucose (FDG) positron emission tomography/computed tomography (PET/CT) have been considered to be affected by tumor characteristics and tumor immune microenvironment. However, the relationship between PET/CT imagi...

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Main Authors: Jeong Won Lee, Hyein Ahn, Ik Dong Yoo, Sun-pyo Hong, Moo-Jun Baek, Dong Hyun Kang, Sang Mi Lee
Format: Article
Language:English
Published: BMC 2024-04-01
Series:Cancer Imaging
Subjects:
Online Access:https://doi.org/10.1186/s40644-024-00698-4
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author Jeong Won Lee
Hyein Ahn
Ik Dong Yoo
Sun-pyo Hong
Moo-Jun Baek
Dong Hyun Kang
Sang Mi Lee
author_facet Jeong Won Lee
Hyein Ahn
Ik Dong Yoo
Sun-pyo Hong
Moo-Jun Baek
Dong Hyun Kang
Sang Mi Lee
author_sort Jeong Won Lee
collection DOAJ
description Abstract Background Imaging features of colorectal cancers on 2-deoxy-2-[18F]fluoro-d-glucose (FDG) positron emission tomography/computed tomography (PET/CT) have been considered to be affected by tumor characteristics and tumor immune microenvironment. However, the relationship between PET/CT imaging features and immune reactions in tumor tissue has not yet been fully evaluated. This study investigated the association of FDG PET/CT imaging features in the tumor, bone marrow, and spleen with immunohistochemical results of cancer tissue and recurrence-free survival (RFS) in patients with colorectal cancer. Methods A total of 119 patients with colorectal cancer who underwent FDG PET/CT for staging work-up and received curative surgical resection were retrospectively enrolled. From PET/CT images, 10 first-order imaging features of primary tumors, including intensity of FDG uptake, volumetric metabolic parameters, and metabolic heterogeneity parameters, as well as FDG uptake in the bone marrow and spleen were measured. The degrees of CD4+, CD8+, and CD163 + cell infiltration and interleukin-6 (IL-6) and matrix metalloproteinase-11 (MMP-11) expression were graded through immunohistochemical analysis of surgical specimens. The relationship between FDG PET/CT imaging features and immunohistochemical results was assessed, and prognostic significance of PET/CT imaging features in predicting RFS was evaluated. Results Correlation analysis with immunohistochemistry findings showed that the degrees of CD4 + and CD163 + cell infiltration and IL-6 and MMP-11 expression were correlated with cancer imaging features on PET/CT. Patients with enhanced inflammatory response in cancer tissue demonstrated increased FDG uptake, volumetric metabolic parameters, and metabolic heterogeneity. FDG uptake in the bone marrow and spleen was positively correlated with the degree of CD163 + cell infiltration and IL-6 expression, respectively. In multivariate survival analysis, the coefficient of variation of FDG uptake in the tumor (p = 0.019; hazard ratio, 0.484 for 0.10 increase) and spleen-to-liver uptake ratio (p = 0.020; hazard ratio, 24.901 for 1.0 increase) were significant independent predictors of RFS. Conclusions The metabolic heterogeneity of tumors and FDG uptake in the spleen were correlated with tumor immune microenvironment and showed prognostic significance in predicting RFS in patients with colorectal cancer.
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spelling doaj.art-e70c622e21d84aa5923e19cd0cd4fd872024-04-21T11:28:50ZengBMCCancer Imaging1470-73302024-04-0124111210.1186/s40644-024-00698-4Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective studyJeong Won Lee0Hyein Ahn1Ik Dong Yoo2Sun-pyo Hong3Moo-Jun Baek4Dong Hyun Kang5Sang Mi Lee6Department of Nuclear Medicine, Soonchunhyang University Cheonan HospitalDepartment of Pathology, CHA Gangnam Medical Center, CHA University School of MedicineDepartment of Nuclear Medicine, Soonchunhyang University Cheonan HospitalDepartment of Nuclear Medicine, Soonchunhyang University Cheonan HospitalDepartment of Surgery, College of Medicine, Soonchunhyang University Cheonan HospitalDepartment of Colorectal surgery, College of Medicine, Soonchunhyang University Cheonan HospitalDepartment of Nuclear Medicine, Soonchunhyang University Cheonan HospitalAbstract Background Imaging features of colorectal cancers on 2-deoxy-2-[18F]fluoro-d-glucose (FDG) positron emission tomography/computed tomography (PET/CT) have been considered to be affected by tumor characteristics and tumor immune microenvironment. However, the relationship between PET/CT imaging features and immune reactions in tumor tissue has not yet been fully evaluated. This study investigated the association of FDG PET/CT imaging features in the tumor, bone marrow, and spleen with immunohistochemical results of cancer tissue and recurrence-free survival (RFS) in patients with colorectal cancer. Methods A total of 119 patients with colorectal cancer who underwent FDG PET/CT for staging work-up and received curative surgical resection were retrospectively enrolled. From PET/CT images, 10 first-order imaging features of primary tumors, including intensity of FDG uptake, volumetric metabolic parameters, and metabolic heterogeneity parameters, as well as FDG uptake in the bone marrow and spleen were measured. The degrees of CD4+, CD8+, and CD163 + cell infiltration and interleukin-6 (IL-6) and matrix metalloproteinase-11 (MMP-11) expression were graded through immunohistochemical analysis of surgical specimens. The relationship between FDG PET/CT imaging features and immunohistochemical results was assessed, and prognostic significance of PET/CT imaging features in predicting RFS was evaluated. Results Correlation analysis with immunohistochemistry findings showed that the degrees of CD4 + and CD163 + cell infiltration and IL-6 and MMP-11 expression were correlated with cancer imaging features on PET/CT. Patients with enhanced inflammatory response in cancer tissue demonstrated increased FDG uptake, volumetric metabolic parameters, and metabolic heterogeneity. FDG uptake in the bone marrow and spleen was positively correlated with the degree of CD163 + cell infiltration and IL-6 expression, respectively. In multivariate survival analysis, the coefficient of variation of FDG uptake in the tumor (p = 0.019; hazard ratio, 0.484 for 0.10 increase) and spleen-to-liver uptake ratio (p = 0.020; hazard ratio, 24.901 for 1.0 increase) were significant independent predictors of RFS. Conclusions The metabolic heterogeneity of tumors and FDG uptake in the spleen were correlated with tumor immune microenvironment and showed prognostic significance in predicting RFS in patients with colorectal cancer.https://doi.org/10.1186/s40644-024-00698-4Colorectal cancerF-18 fluorodeoxyglucoseImmune microenvironmentPositron emission tomographyPrognosis
spellingShingle Jeong Won Lee
Hyein Ahn
Ik Dong Yoo
Sun-pyo Hong
Moo-Jun Baek
Dong Hyun Kang
Sang Mi Lee
Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective study
Cancer Imaging
Colorectal cancer
F-18 fluorodeoxyglucose
Immune microenvironment
Positron emission tomography
Prognosis
title Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective study
title_full Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective study
title_fullStr Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective study
title_full_unstemmed Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective study
title_short Relationship of FDG PET/CT imaging features with tumor immune microenvironment and prognosis in colorectal cancer: a retrospective study
title_sort relationship of fdg pet ct imaging features with tumor immune microenvironment and prognosis in colorectal cancer a retrospective study
topic Colorectal cancer
F-18 fluorodeoxyglucose
Immune microenvironment
Positron emission tomography
Prognosis
url https://doi.org/10.1186/s40644-024-00698-4
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