Real-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancer

Abstract HER2-targeted therapies have improved outcomes in metastatic gastric cancer (mGC), yet assessment of HER2 status in tumor tissues remains limited by heterogeneity and temporal changes. This study aimed to evaluate real-time HER2 expression on circulating tumor cells (CTCs) using the On-chip...

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Main Authors: Yasuaki Kimura, Koichi Suzuki, Sawako Tamaki, Iku Abe, Yuhei Endo, Kosuke Ichida, Yuta Muto, Fumiaki Watanabe, Masaaki Saito, Kazuo Takeda, Toshiki Rikiyama
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-06913-x
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author Yasuaki Kimura
Koichi Suzuki
Sawako Tamaki
Iku Abe
Yuhei Endo
Kosuke Ichida
Yuta Muto
Fumiaki Watanabe
Masaaki Saito
Kazuo Takeda
Toshiki Rikiyama
author_facet Yasuaki Kimura
Koichi Suzuki
Sawako Tamaki
Iku Abe
Yuhei Endo
Kosuke Ichida
Yuta Muto
Fumiaki Watanabe
Masaaki Saito
Kazuo Takeda
Toshiki Rikiyama
author_sort Yasuaki Kimura
collection DOAJ
description Abstract HER2-targeted therapies have improved outcomes in metastatic gastric cancer (mGC), yet assessment of HER2 status in tumor tissues remains limited by heterogeneity and temporal changes. This study aimed to evaluate real-time HER2 expression on circulating tumor cells (CTCs) using the On-chip Sort system. CTCs were enriched from blood samples of 27 mGC patients, identified by cytokeratin staining, and assessed for HER2 expression via fluorescent labeling. The epithelial-mesenchymal transition (EMT) index was calculated based on co-expression of vimentin and cytokeratin. CTCs also underwent whole-genome amplification and targeted sequencing using a cancer gene panel. Patients were stratified into three groups: Group A (n = 13), HER2-positive in tissue; Group B (n = 8), tissue HER2-negative but CTC HER2-positive; and Group C (n = 6), HER2-negative in both tissue and CTCs. All patients received cytotoxic chemotherapy; only Group A received additional HER2-targeted therapy. Group B showed the poorest progression-free survival (PFS: 7.0 months), compared to Group A (15.7 months) and Group C (not reached). CTC HER2 expression correlated with EMT index; Groups A and B also exhibited higher EMT indices and shared EMT-related mutations. These findings suggest that CTC-based HER2 monitoring reflects tumor aggressiveness and may help identify patients who could benefit from HER2-targeted therapy despite negative tissue HER2 status.
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spelling doaj-art-e9f1f99520a14a1ba6256498a69459772025-08-20T03:45:24ZengNature PortfolioScientific Reports2045-23222025-07-0115111510.1038/s41598-025-06913-xReal-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancerYasuaki Kimura0Koichi Suzuki1Sawako Tamaki2Iku Abe3Yuhei Endo4Kosuke Ichida5Yuta Muto6Fumiaki Watanabe7Masaaki Saito8Kazuo Takeda9Toshiki Rikiyama10Department of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityOn-chip Biotechnologies Co., LtdDepartment of Surgery, Saitama Medical Center, Jichi Medical UniversityAbstract HER2-targeted therapies have improved outcomes in metastatic gastric cancer (mGC), yet assessment of HER2 status in tumor tissues remains limited by heterogeneity and temporal changes. This study aimed to evaluate real-time HER2 expression on circulating tumor cells (CTCs) using the On-chip Sort system. CTCs were enriched from blood samples of 27 mGC patients, identified by cytokeratin staining, and assessed for HER2 expression via fluorescent labeling. The epithelial-mesenchymal transition (EMT) index was calculated based on co-expression of vimentin and cytokeratin. CTCs also underwent whole-genome amplification and targeted sequencing using a cancer gene panel. Patients were stratified into three groups: Group A (n = 13), HER2-positive in tissue; Group B (n = 8), tissue HER2-negative but CTC HER2-positive; and Group C (n = 6), HER2-negative in both tissue and CTCs. All patients received cytotoxic chemotherapy; only Group A received additional HER2-targeted therapy. Group B showed the poorest progression-free survival (PFS: 7.0 months), compared to Group A (15.7 months) and Group C (not reached). CTC HER2 expression correlated with EMT index; Groups A and B also exhibited higher EMT indices and shared EMT-related mutations. These findings suggest that CTC-based HER2 monitoring reflects tumor aggressiveness and may help identify patients who could benefit from HER2-targeted therapy despite negative tissue HER2 status.https://doi.org/10.1038/s41598-025-06913-xAdvanced gastric cancerCirculating tumor cellsHER2Liquid biopsy
spellingShingle Yasuaki Kimura
Koichi Suzuki
Sawako Tamaki
Iku Abe
Yuhei Endo
Kosuke Ichida
Yuta Muto
Fumiaki Watanabe
Masaaki Saito
Kazuo Takeda
Toshiki Rikiyama
Real-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancer
Scientific Reports
Advanced gastric cancer
Circulating tumor cells
HER2
Liquid biopsy
title Real-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancer
title_full Real-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancer
title_fullStr Real-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancer
title_full_unstemmed Real-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancer
title_short Real-time assessment of circulating tumor cells refines the indication for HER2-targeted therapy in metastatic gastric cancer
title_sort real time assessment of circulating tumor cells refines the indication for her2 targeted therapy in metastatic gastric cancer
topic Advanced gastric cancer
Circulating tumor cells
HER2
Liquid biopsy
url https://doi.org/10.1038/s41598-025-06913-x
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