Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoids

Abstract Background Patient-derived organoids (PDOs) represent a promising approach for replicating the characteristics of original tumors and facilitating drug testing for personalized treatments across diverse cancer types. However, clinical evidence regarding their application to esophageal cance...

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Main Authors: Suya Shen, Bing Liu, Wenyan Guan, Ziyao Liu, Yuqing Han, Yingzhe Hu, Yiqiang Chen, Siyuan Liu, Jian He, Zhiwen Li, Weifeng Tang, Pengju Zhang, Wei Ren, Yudong Qiu, Hongping Zheng, Jingjing Li
Format: Article
Language:English
Published: BMC 2024-12-01
Series:Journal of Translational Medicine
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Online Access:https://doi.org/10.1186/s12967-024-05967-1
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author Suya Shen
Bing Liu
Wenyan Guan
Ziyao Liu
Yuqing Han
Yingzhe Hu
Yiqiang Chen
Siyuan Liu
Jian He
Zhiwen Li
Weifeng Tang
Pengju Zhang
Wei Ren
Yudong Qiu
Hongping Zheng
Jingjing Li
author_facet Suya Shen
Bing Liu
Wenyan Guan
Ziyao Liu
Yuqing Han
Yingzhe Hu
Yiqiang Chen
Siyuan Liu
Jian He
Zhiwen Li
Weifeng Tang
Pengju Zhang
Wei Ren
Yudong Qiu
Hongping Zheng
Jingjing Li
author_sort Suya Shen
collection DOAJ
description Abstract Background Patient-derived organoids (PDOs) represent a promising approach for replicating the characteristics of original tumors and facilitating drug testing for personalized treatments across diverse cancer types. However, clinical evidence regarding their application to esophageal cancer remains limited. This study aims to evaluate the efficacy of implementing PDOs in clinical practice to benefit patients with esophageal squamous cell carcinoma (ESCC). Methods Fresh surgical biopsies were obtained from patients with esophageal cancer for the establishment of PDOs. These PDOs were subsequently characterized through histological analysis. A customized drug panel, based on standard-of-care chemotherapy regimens, was applied to the PDOs. The resulting drug sensitivity profiles were then correlated with the clinical responses observed in individual patients undergoing actual treatment. Results A total of 34 PDOs were successfully established with a 61.8% success rate. The classification method based on chemotherapy sensitivity closely corresponded to clinical responses. The paclitaxel plus cisplatin (TP)-sensitive group demonstrated significantly longer progression-free survival (PFS) compared to the resistant groups, Hazard ratio (HR), 5.12; 95% confidence intervals (CI 0.58–44.71; p < 0.05), thus illustrating the potential of this approach for guiding personalized treatment strategies. Conclusion Organoid biobanks were established across multiple institutes to facilitate PDOs-based functional precision medicine. The findings demonstrate that this framework offers robust predictive value in clinical settings, enhances precision therapeutics, and advances drug discovery for esophageal cancer. Graphical Abstract
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spelling doaj-art-9fabfcee71734ba48d1db02be08636e42025-01-05T12:44:23ZengBMCJournal of Translational Medicine1479-58762024-12-0122111610.1186/s12967-024-05967-1Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoidsSuya Shen0Bing Liu1Wenyan Guan2Ziyao Liu3Yuqing Han4Yingzhe Hu5Yiqiang Chen6Siyuan Liu7Jian He8Zhiwen Li9Weifeng Tang10Pengju Zhang11Wei Ren12Yudong Qiu13Hongping Zheng14Jingjing Li15Department of Pancreatic and Metabolic Surgery, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing UniversityKey Laboratory of Carcinogenesis and Translational Research (Ministry of Education/Beijing), Department of Thoracic Surgery II, Peking University Cancer Hospital & InstituteDepartment of Pathology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical SchoolDepartment of Precision Medicine, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical SchoolDepartment of Pancreatic and Metabolic Surgery, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing UniversityDepartment of Pancreatic and Metabolic Surgery, Nanjing Drum Tower Hospital Clinical College of Nanjing University of Chinese MedicineDepartment of Precision Medicine, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical SchoolDepartment of Precision Medicine, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical SchoolDepartment of Nuclear Medicine, Nanjing Drum Tower Hospital, Affiliated Hospital of Nanjing University Medical SchoolDepartment of Pathology, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical SchoolDepartment of Esophageal Surgery, Nanjing Drum Tower Hospital, Affiliated Hospital of Nanjing University Medical SchoolZhejiang Honray Medical Technology Co., LTDThe Comprehensive Cancer Center of Drum Tower Hospital, Medical School of Nanjing University & Clinical Cancer Institute of Nanjing UniversityDepartment of Pancreatic and Metabolic Surgery, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical School, Nanjing UniversityZhejiang Honray Medical Technology Co., LTDDepartment of Precision Medicine, Nanjing Drum Tower Hospital, The Affiliated Hospital of Nanjing University Medical SchoolAbstract Background Patient-derived organoids (PDOs) represent a promising approach for replicating the characteristics of original tumors and facilitating drug testing for personalized treatments across diverse cancer types. However, clinical evidence regarding their application to esophageal cancer remains limited. This study aims to evaluate the efficacy of implementing PDOs in clinical practice to benefit patients with esophageal squamous cell carcinoma (ESCC). Methods Fresh surgical biopsies were obtained from patients with esophageal cancer for the establishment of PDOs. These PDOs were subsequently characterized through histological analysis. A customized drug panel, based on standard-of-care chemotherapy regimens, was applied to the PDOs. The resulting drug sensitivity profiles were then correlated with the clinical responses observed in individual patients undergoing actual treatment. Results A total of 34 PDOs were successfully established with a 61.8% success rate. The classification method based on chemotherapy sensitivity closely corresponded to clinical responses. The paclitaxel plus cisplatin (TP)-sensitive group demonstrated significantly longer progression-free survival (PFS) compared to the resistant groups, Hazard ratio (HR), 5.12; 95% confidence intervals (CI 0.58–44.71; p < 0.05), thus illustrating the potential of this approach for guiding personalized treatment strategies. Conclusion Organoid biobanks were established across multiple institutes to facilitate PDOs-based functional precision medicine. The findings demonstrate that this framework offers robust predictive value in clinical settings, enhances precision therapeutics, and advances drug discovery for esophageal cancer. Graphical Abstracthttps://doi.org/10.1186/s12967-024-05967-1Esophageal squamous cell carcinomaOrganoidsChemotherapyPrecision medicine
spellingShingle Suya Shen
Bing Liu
Wenyan Guan
Ziyao Liu
Yuqing Han
Yingzhe Hu
Yiqiang Chen
Siyuan Liu
Jian He
Zhiwen Li
Weifeng Tang
Pengju Zhang
Wei Ren
Yudong Qiu
Hongping Zheng
Jingjing Li
Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoids
Journal of Translational Medicine
Esophageal squamous cell carcinoma
Organoids
Chemotherapy
Precision medicine
title Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoids
title_full Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoids
title_fullStr Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoids
title_full_unstemmed Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoids
title_short Advancing precision medicine in esophageal squamous cell carcinoma using patient-derived organoids
title_sort advancing precision medicine in esophageal squamous cell carcinoma using patient derived organoids
topic Esophageal squamous cell carcinoma
Organoids
Chemotherapy
Precision medicine
url https://doi.org/10.1186/s12967-024-05967-1
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