Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysis

Abstract Background Prostate cancer (PCa) is the second most prevalent cancer in males worldwide, yet detecting PCa and its metastases remains a major challenging task in clinical research setups. The present study aimed to characterize the metabolic changes underlying the PCa progression and invest...

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Main Authors: Xi Zhang, Binbin Xia, Hong Zheng, Jie Ning, Yinjie Zhu, Xiaoguang Shao, Binrui Liu, Baijun Dong, Hongchang Gao
Format: Article
Language:English
Published: BMC 2022-06-01
Series:Journal of Translational Medicine
Subjects:
Online Access:https://doi.org/10.1186/s12967-022-03478-5
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author Xi Zhang
Binbin Xia
Hong Zheng
Jie Ning
Yinjie Zhu
Xiaoguang Shao
Binrui Liu
Baijun Dong
Hongchang Gao
author_facet Xi Zhang
Binbin Xia
Hong Zheng
Jie Ning
Yinjie Zhu
Xiaoguang Shao
Binrui Liu
Baijun Dong
Hongchang Gao
author_sort Xi Zhang
collection DOAJ
description Abstract Background Prostate cancer (PCa) is the second most prevalent cancer in males worldwide, yet detecting PCa and its metastases remains a major challenging task in clinical research setups. The present study aimed to characterize the metabolic changes underlying the PCa progression and investigate the efficacy of related metabolic panels for an accurate PCa assessment. Methods In the present study, 75 PCa subjects, 62 PCa patients with bone metastasis (PCaB), and 50 benign prostatic hyperplasia (BPH) patients were enrolled, and we performed a cross-sectional metabolomics analysis of serum samples collected from these subjects using a 1H nuclear magnetic resonance (NMR)-based metabolomics approach. Results Multivariate analysis revealed that BPH, PCa, and PCaB groups showed distinct metabolic divisions, while univariate statistics integrated with variable importance in the projection (VIP) scores identified a differential metabolite series, which included energy, amino acid, and ketone body metabolism. Herein, we identified a series of characteristic serum metabolic changes, including decreased trends of 3-HB and acetone as well as elevated trends of alanine in PCa patients compared with BPH subjects, while increased levels of 3-HB and acetone as well as decreased levels of alanine in PCaB patients compared with PCa. Additionally, our results also revealed the metabolic panels of discriminant metabolites coupled with the clinical parameters (age and body mass index) for discrimination between PCa and BPH, PCaB and BPH, PCaB and PCa achieved the AUC values of 0.828, 0.917, and 0.872, respectively. Conclusions Overall, our study gave successful discrimination of BPH, PCa and PCaB, and we characterized the potential metabolic alterations involved in the PCa progression and its metastases, including 3-HB, acetone and alanine. The defined biomarker panels could be employed to aid in the diagnosis and classification of PCa in clinical practice.
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spelling doaj.art-c0eacafce4434ef39c59bc7747fd6a6c2022-12-22T00:28:01ZengBMCJournal of Translational Medicine1479-58762022-06-0120111410.1186/s12967-022-03478-5Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysisXi Zhang0Binbin Xia1Hong Zheng2Jie Ning3Yinjie Zhu4Xiaoguang Shao5Binrui Liu6Baijun Dong7Hongchang Gao8School of Pharmaceutical Sciences, Wenzhou Medical UniversityDepartment of Urology, Renji Hospital, School of Medicine, Shanghai Jiao Tong UniversitySchool of Pharmaceutical Sciences, Wenzhou Medical UniversitySchool of Pharmaceutical Sciences, Wenzhou Medical UniversityDepartment of Urology, Renji Hospital, School of Medicine, Shanghai Jiao Tong UniversityDepartment of Urology, Renji Hospital, School of Medicine, Shanghai Jiao Tong UniversitySchool of Pharmaceutical Sciences, Wenzhou Medical UniversityDepartment of Urology, Renji Hospital, School of Medicine, Shanghai Jiao Tong UniversitySchool of Pharmaceutical Sciences, Wenzhou Medical UniversityAbstract Background Prostate cancer (PCa) is the second most prevalent cancer in males worldwide, yet detecting PCa and its metastases remains a major challenging task in clinical research setups. The present study aimed to characterize the metabolic changes underlying the PCa progression and investigate the efficacy of related metabolic panels for an accurate PCa assessment. Methods In the present study, 75 PCa subjects, 62 PCa patients with bone metastasis (PCaB), and 50 benign prostatic hyperplasia (BPH) patients were enrolled, and we performed a cross-sectional metabolomics analysis of serum samples collected from these subjects using a 1H nuclear magnetic resonance (NMR)-based metabolomics approach. Results Multivariate analysis revealed that BPH, PCa, and PCaB groups showed distinct metabolic divisions, while univariate statistics integrated with variable importance in the projection (VIP) scores identified a differential metabolite series, which included energy, amino acid, and ketone body metabolism. Herein, we identified a series of characteristic serum metabolic changes, including decreased trends of 3-HB and acetone as well as elevated trends of alanine in PCa patients compared with BPH subjects, while increased levels of 3-HB and acetone as well as decreased levels of alanine in PCaB patients compared with PCa. Additionally, our results also revealed the metabolic panels of discriminant metabolites coupled with the clinical parameters (age and body mass index) for discrimination between PCa and BPH, PCaB and BPH, PCaB and PCa achieved the AUC values of 0.828, 0.917, and 0.872, respectively. Conclusions Overall, our study gave successful discrimination of BPH, PCa and PCaB, and we characterized the potential metabolic alterations involved in the PCa progression and its metastases, including 3-HB, acetone and alanine. The defined biomarker panels could be employed to aid in the diagnosis and classification of PCa in clinical practice.https://doi.org/10.1186/s12967-022-03478-5Prostate cancerBiomarkerSerumMetabolomicsDiagnosis
spellingShingle Xi Zhang
Binbin Xia
Hong Zheng
Jie Ning
Yinjie Zhu
Xiaoguang Shao
Binrui Liu
Baijun Dong
Hongchang Gao
Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysis
Journal of Translational Medicine
Prostate cancer
Biomarker
Serum
Metabolomics
Diagnosis
title Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysis
title_full Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysis
title_fullStr Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysis
title_full_unstemmed Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysis
title_short Identification of characteristic metabolic panels for different stages of prostate cancer by 1H NMR-based metabolomics analysis
title_sort identification of characteristic metabolic panels for different stages of prostate cancer by 1h nmr based metabolomics analysis
topic Prostate cancer
Biomarker
Serum
Metabolomics
Diagnosis
url https://doi.org/10.1186/s12967-022-03478-5
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