Circulating tumor DNA status and dynamics predict recurrence in patients with resected extrahepatic cholangiocarcinoma
Surgery is the only curative therapeutic option for resectable extrahepatic cholangiocarcinoma, but recurrence is common, and prognosis is poor. There is an unmet clinical need for improved decision-making regarding adjuvant chemotherapy (ACT). Herein, we evaluated the usefulness of monitoring longi...
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| Published in: | Journal of hepatology Vol. 82; no. 5; pp. 861 - 870 |
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| Main Authors: | , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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Elsevier B.V
01.05.2025
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| ISSN: | 0168-8278, 1600-0641, 1600-0641 |
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| Abstract | Surgery is the only curative therapeutic option for resectable extrahepatic cholangiocarcinoma, but recurrence is common, and prognosis is poor. There is an unmet clinical need for improved decision-making regarding adjuvant chemotherapy (ACT). Herein, we evaluated the usefulness of monitoring longitudinal circulating tumor DNA (ctDNA) for molecular residual disease (MRD) in patients from the STAMP trial, which compared the efficacy of adjuvant capecitabine (CAP) vs. gemcitabine plus cisplatin (GemCis).
Between July 2017 and November 2020, 101 patients were randomized 1:1 to receive GemCis (n = 50) or CAP (n = 51). Efficacy outcomes were analyzed with an extended follow-up of 19 months from the previous report. From a biomarker cohort of 89 patients, longitudinal plasma samples (n = 254) were prospectively collected post-surgery before ACT, and on-ACT at 12 and 24 weeks from cycle 1 day 1 (C1D1). ctDNA was evaluated using a personalized, tumor-informed, 16-plex PCR next-generation sequencing assay and was correlated with clinical outcomes.
In the extended follow-up analysis, median disease-free survival (DFS) and overall survival did not significantly differ between the CAP and GemCis groups. Significantly inferior DFS was associated with ctDNA positivity before ACT (hazard ratio [HR] 1.8; p = 0.029), on-ACT at 12 weeks from C1D1 (HR 7.72; p <0.001), on-ACT at 24 weeks from C1D1 (HR 5.24; p <0.001), and anytime post-surgery (HR 3.81; p <0.001). Analysis of pre-treatment to on-treatment ctDNA dynamics revealed that serially ctDNA-negative patients exhibited a significantly longer DFS compared to those with sustained ctDNA positivity (HR 6.7; p <0.001) or those who turned ctDNA positive (HR 5.8; p <0.001).
In patients with resected extrahepatic cholangiocarcinoma, ctDNA status and dynamics predicted recurrence during adjuvant therapy, and may help optimize clinical decision-making.
The findings from this study highlight the critical role of ctDNA as a prognostic biomarker and monitoring tool for patients with resected extrahepatic cholangiocarcinoma. By demonstrating the superiority of ctDNA to predict disease recurrence compared to conventional biomarkers such as cancer antigen 19-9 and carcinoembryonic antigen, this study underscores its potential in guiding decision-making during adjuvant chemotherapy. These results may be crucial to refine post-surgical treatment strategies and improve patient outcomes. The practical application of ctDNA monitoring could lead to more personalized treatment approaches, enabling timely interventions based on molecular residual disease status.
NCT03079427.
[Display omitted]
•No DFS or OS difference between adjuvant CAP and GemCis in resected LN+ eCCA.•Tumor-informed ctDNA status predicts recurrence in patients with resected eCCA.•ctDNA status outperforms CA 19-9 and CEA in predicting survival outcomes.•Personalized ctDNA monitoring helps optimize adjuvant therapy decision-making. |
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| AbstractList | Surgery is the only curative therapeutic option for resectable extrahepatic cholangiocarcinoma, but recurrence is common, and prognosis is poor. There is an unmet clinical need for improved decision-making regarding adjuvant chemotherapy (ACT). Herein, we evaluated the usefulness of monitoring longitudinal circulating tumor DNA (ctDNA) for molecular residual disease (MRD) in patients from the STAMP trial, which compared the efficacy of adjuvant capecitabine (CAP) vs. gemcitabine plus cisplatin (GemCis).
Between July 2017 and November 2020, 101 patients were randomized 1:1 to receive GemCis (n = 50) or CAP (n = 51). Efficacy outcomes were analyzed with an extended follow-up of 19 months from the previous report. From a biomarker cohort of 89 patients, longitudinal plasma samples (n = 254) were prospectively collected post-surgery before ACT, and on-ACT at 12 and 24 weeks from cycle 1 day 1 (C1D1). ctDNA was evaluated using a personalized, tumor-informed, 16-plex PCR next-generation sequencing assay and was correlated with clinical outcomes.
In the extended follow-up analysis, median disease-free survival (DFS) and overall survival did not significantly differ between the CAP and GemCis groups. Significantly inferior DFS was associated with ctDNA positivity before ACT (hazard ratio [HR] 1.8; p = 0.029), on-ACT at 12 weeks from C1D1 (HR 7.72; p <0.001), on-ACT at 24 weeks from C1D1 (HR 5.24; p <0.001), and anytime post-surgery (HR 3.81; p <0.001). Analysis of pre-treatment to on-treatment ctDNA dynamics revealed that serially ctDNA-negative patients exhibited a significantly longer DFS compared to those with sustained ctDNA positivity (HR 6.7; p <0.001) or those who turned ctDNA positive (HR 5.8; p <0.001).
In patients with resected extrahepatic cholangiocarcinoma, ctDNA status and dynamics predicted recurrence during adjuvant therapy, and may help optimize clinical decision-making.
The findings from this study highlight the critical role of ctDNA as a prognostic biomarker and monitoring tool for patients with resected extrahepatic cholangiocarcinoma. By demonstrating the superiority of ctDNA to predict disease recurrence compared to conventional biomarkers such as cancer antigen 19-9 and carcinoembryonic antigen, this study underscores its potential in guiding decision-making during adjuvant chemotherapy. These results may be crucial to refine post-surgical treatment strategies and improve patient outcomes. The practical application of ctDNA monitoring could lead to more personalized treatment approaches, enabling timely interventions based on molecular residual disease status.
NCT03079427.
[Display omitted]
•No DFS or OS difference between adjuvant CAP and GemCis in resected LN+ eCCA.•Tumor-informed ctDNA status predicts recurrence in patients with resected eCCA.•ctDNA status outperforms CA 19-9 and CEA in predicting survival outcomes.•Personalized ctDNA monitoring helps optimize adjuvant therapy decision-making. Surgery is the only curative therapeutic option for resectable extrahepatic cholangiocarcinoma, but recurrence is common, and prognosis is poor. There is an unmet clinical need for improved decision-making regarding adjuvant chemotherapy (ACT). Herein, we evaluated the usefulness of monitoring longitudinal circulating tumor DNA (ctDNA) for molecular residual disease (MRD) in patients from the STAMP trial, which compares the efficacy of adjuvant capecitabine (CAP) vs. gemcitabine plus cisplatin (GemCis).BACKGROUND & AIMSSurgery is the only curative therapeutic option for resectable extrahepatic cholangiocarcinoma, but recurrence is common, and prognosis is poor. There is an unmet clinical need for improved decision-making regarding adjuvant chemotherapy (ACT). Herein, we evaluated the usefulness of monitoring longitudinal circulating tumor DNA (ctDNA) for molecular residual disease (MRD) in patients from the STAMP trial, which compares the efficacy of adjuvant capecitabine (CAP) vs. gemcitabine plus cisplatin (GemCis).Between July 2017 and November 2020, 101 patients were randomized 1:1 to receive GemCis (n = 50) or CAP (n = 51). Efficacy outcomes were analyzed with an extended follow-up of 19 months from the previous report. From a biomarker cohort of 89 patients, longitudinal plasma samples (n = 254) were prospectively collected post-surgery before ACT, and on-ACT at 12 and 24 weeks from cycle 1 day 1 (C1D1). ctDNA was evaluated using a personalized, tumor-informed, 16-plex PCR next-generation sequencing assay and was correlated with clinical outcomes.METHODSBetween July 2017 and November 2020, 101 patients were randomized 1:1 to receive GemCis (n = 50) or CAP (n = 51). Efficacy outcomes were analyzed with an extended follow-up of 19 months from the previous report. From a biomarker cohort of 89 patients, longitudinal plasma samples (n = 254) were prospectively collected post-surgery before ACT, and on-ACT at 12 and 24 weeks from cycle 1 day 1 (C1D1). ctDNA was evaluated using a personalized, tumor-informed, 16-plex PCR next-generation sequencing assay and was correlated with clinical outcomes.In the extended follow-up analysis, median disease-free survival (DFS) and overall survival did not significantly differ between the CAP and GemCis groups. Significantly inferior DFS was associated with ctDNA positivity before ACT (hazard ratio [HR] 1.8; p = 0.029), on-ACT at 12 weeks from C1D1 (HR 7.72; p <0.001), on-ACT at 24 weeks from C1D1 (HR 5.24; p <0.001), and anytime post-surgery (HR 3.81; p <0.001). Analysis of pre-treatment to on-treatment ctDNA dynamics revealed that serially ctDNA-negative patients exhibited a significantly longer DFS compared to those with sustained ctDNA positivity (HR 6.7; p <0.001) or those who turned ctDNA positive (HR 5.8; p <0.001).RESULTSIn the extended follow-up analysis, median disease-free survival (DFS) and overall survival did not significantly differ between the CAP and GemCis groups. Significantly inferior DFS was associated with ctDNA positivity before ACT (hazard ratio [HR] 1.8; p = 0.029), on-ACT at 12 weeks from C1D1 (HR 7.72; p <0.001), on-ACT at 24 weeks from C1D1 (HR 5.24; p <0.001), and anytime post-surgery (HR 3.81; p <0.001). Analysis of pre-treatment to on-treatment ctDNA dynamics revealed that serially ctDNA-negative patients exhibited a significantly longer DFS compared to those with sustained ctDNA positivity (HR 6.7; p <0.001) or those who turned ctDNA positive (HR 5.8; p <0.001).In patients with resected extrahepatic cholangiocarcinoma, ctDNA status and dynamics predicted recurrence during adjuvant therapy, and may help optimize clinical decision-making.CONCLUSIONIn patients with resected extrahepatic cholangiocarcinoma, ctDNA status and dynamics predicted recurrence during adjuvant therapy, and may help optimize clinical decision-making.The findings from this study highlight the critical role of ctDNA as a prognostic biomarker and monitoring tool for patients with resected extrahepatic cholangiocarcinoma. By demonstrating the superiority of ctDNA to predict disease recurrence compared to conventional biomarkers such as cancer antigen 19-9 and carcinoembryonic antigen, this study underscores its potential in guiding decision-making during adjuvant chemotherapy. These results may be crucial to refine post-surgical treatment strategies and improve patient outcomes. The practical application of ctDNA monitoring could lead to more personalized treatment approaches, enabling timely interventions based on molecular residual disease status.IMPACT AND IMPLICATIONSThe findings from this study highlight the critical role of ctDNA as a prognostic biomarker and monitoring tool for patients with resected extrahepatic cholangiocarcinoma. By demonstrating the superiority of ctDNA to predict disease recurrence compared to conventional biomarkers such as cancer antigen 19-9 and carcinoembryonic antigen, this study underscores its potential in guiding decision-making during adjuvant chemotherapy. These results may be crucial to refine post-surgical treatment strategies and improve patient outcomes. The practical application of ctDNA monitoring could lead to more personalized treatment approaches, enabling timely interventions based on molecular residual disease status.NCT03079427.CLINICAL TRIAL REGISTRATION NUMBERNCT03079427. Surgery is the only curative therapeutic option for resectable extrahepatic cholangiocarcinoma, but recurrence is common, and prognosis is poor. There is an unmet clinical need for improved decision-making regarding adjuvant chemotherapy (ACT). Herein, we evaluated the usefulness of monitoring longitudinal circulating tumor DNA (ctDNA) for molecular residual disease (MRD) in patients from the STAMP trial, which compared the efficacy of adjuvant capecitabine (CAP) vs. gemcitabine plus cisplatin (GemCis). Between July 2017 and November 2020, 101 patients were randomized 1:1 to receive GemCis (n = 50) or CAP (n = 51). Efficacy outcomes were analyzed with an extended follow-up of 19 months from the previous report. From a biomarker cohort of 89 patients, longitudinal plasma samples (n = 254) were prospectively collected post-surgery before ACT, and on-ACT at 12 and 24 weeks from cycle 1 day 1 (C1D1). ctDNA was evaluated using a personalized, tumor-informed, 16-plex PCR next-generation sequencing assay and was correlated with clinical outcomes. In the extended follow-up analysis, median disease-free survival (DFS) and overall survival did not significantly differ between the CAP and GemCis groups. Significantly inferior DFS was associated with ctDNA positivity before ACT (hazard ratio [HR] 1.8; p = 0.029), on-ACT at 12 weeks from C1D1 (HR 7.72; p <0.001), on-ACT at 24 weeks from C1D1 (HR 5.24; p <0.001), and anytime post-surgery (HR 3.81; p <0.001). Analysis of pre-treatment to on-treatment ctDNA dynamics revealed that serially ctDNA-negative patients exhibited a significantly longer DFS compared to those with sustained ctDNA positivity (HR 6.7; p <0.001) or those who turned ctDNA positive (HR 5.8; p <0.001). In patients with resected extrahepatic cholangiocarcinoma, ctDNA status and dynamics predicted recurrence during adjuvant therapy, and may help optimize clinical decision-making. The findings from this study highlight the critical role of ctDNA as a prognostic biomarker and monitoring tool for patients with resected extrahepatic cholangiocarcinoma. By demonstrating the superiority of ctDNA to predict disease recurrence compared to conventional biomarkers such as cancer antigen 19-9 and carcinoembryonic antigen, this study underscores its potential in guiding decision-making during adjuvant chemotherapy. These results may be crucial to refine post-surgical treatment strategies and improve patient outcomes. The practical application of ctDNA monitoring could lead to more personalized treatment approaches, enabling timely interventions based on molecular residual disease status. NCT03079427. |
| Author | Ryoo, Baek-Yeol Lee, Ji Sung Jeong, Jae Ho Hwang, Dae Wook Lee, Sang Soo Jurdi, Adham Yoo, Changhoon Chon, Hong Jae Sharma, Shruti Moon, Deog-Bog Spickard, Erik Liu, Minetta C. Palsuledesai, Charuta C. Song, Tae Jun Kim, Ki-Hun Renner, Derrick Dutta, Punashi Kim, Kyu-pyo Oh, Dongwook Malhotra, Meenakshi Lee, Seonmin Lee, Jae Hoon Rivero-Hinojosa, Samuel Lee, Myung Ah Jeong, Hyehyun Laliotis, George |
| Author_xml | – sequence: 1 givenname: Changhoon orcidid: 0000-0002-1451-8455 surname: Yoo fullname: Yoo, Changhoon email: yooc@amc.seoul.kr organization: Department of Oncology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 2 givenname: Hyehyun surname: Jeong fullname: Jeong, Hyehyun organization: Department of Oncology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 3 givenname: Jae Ho surname: Jeong fullname: Jeong, Jae Ho organization: Department of Oncology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 4 givenname: Kyu-pyo surname: Kim fullname: Kim, Kyu-pyo organization: Department of Oncology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 5 givenname: Seonmin surname: Lee fullname: Lee, Seonmin organization: University of Ulsan Digestive Disease Research Center, Seoul, Korea – sequence: 6 givenname: Baek-Yeol orcidid: 0000-0002-9052-833X surname: Ryoo fullname: Ryoo, Baek-Yeol organization: Department of Oncology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 7 givenname: Dae Wook orcidid: 0000-0002-1749-038X surname: Hwang fullname: Hwang, Dae Wook organization: Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea – sequence: 8 givenname: Jae Hoon surname: Lee fullname: Lee, Jae Hoon organization: Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea – sequence: 9 givenname: Deog-Bog surname: Moon fullname: Moon, Deog-Bog organization: Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea – sequence: 10 givenname: Ki-Hun surname: Kim fullname: Kim, Ki-Hun organization: Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea – sequence: 11 givenname: Sang Soo orcidid: 0000-0002-2762-9066 surname: Lee fullname: Lee, Sang Soo organization: Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 12 givenname: Tae Jun surname: Song fullname: Song, Tae Jun organization: Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 13 givenname: Dongwook surname: Oh fullname: Oh, Dongwook organization: Department of Gastroenterology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 14 givenname: Myung Ah orcidid: 0000-0002-1204-0574 surname: Lee fullname: Lee, Myung Ah organization: Department of Internal Medicine, College of Medicine, Seoul St. Mary’s Hospital, The Catholic University of Korea, Seoul, Republic of Korea – sequence: 15 givenname: Hong Jae orcidid: 0000-0002-6979-5812 surname: Chon fullname: Chon, Hong Jae organization: Department of Medical Oncology, CHA Bundang Medical Center, CHA University, Seongnam, Republic of Korea – sequence: 16 givenname: Ji Sung surname: Lee fullname: Lee, Ji Sung organization: Department of Clinical Research Center, Asan Institute for Life Sciences, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Republic of Korea – sequence: 17 givenname: George orcidid: 0000-0001-9205-8258 surname: Laliotis fullname: Laliotis, George organization: Natera, Inc., Austin, TX, USA – sequence: 18 givenname: Samuel surname: Rivero-Hinojosa fullname: Rivero-Hinojosa, Samuel organization: Natera, Inc., Austin, TX, USA – sequence: 19 givenname: Erik orcidid: 0000-0002-5024-3559 surname: Spickard fullname: Spickard, Erik organization: Natera, Inc., Austin, TX, USA – sequence: 20 givenname: Derrick orcidid: 0000-0002-1349-8050 surname: Renner fullname: Renner, Derrick organization: Natera, Inc., Austin, TX, USA – sequence: 21 givenname: Punashi surname: Dutta fullname: Dutta, Punashi organization: Natera, Inc., Austin, TX, USA – sequence: 22 givenname: Charuta C. surname: Palsuledesai fullname: Palsuledesai, Charuta C. organization: Natera, Inc., Austin, TX, USA – sequence: 23 givenname: Shruti surname: Sharma fullname: Sharma, Shruti organization: Natera, Inc., Austin, TX, USA – sequence: 24 givenname: Meenakshi surname: Malhotra fullname: Malhotra, Meenakshi organization: Natera, Inc., Austin, TX, USA – sequence: 25 givenname: Adham orcidid: 0000-0002-2985-3053 surname: Jurdi fullname: Jurdi, Adham organization: Natera, Inc., Austin, TX, USA – sequence: 26 givenname: Minetta C. orcidid: 0000-0002-8206-5232 surname: Liu fullname: Liu, Minetta C. organization: Natera, Inc., Austin, TX, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/39532185$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | adjuvant capecitabine Adult Aged Antineoplastic Combined Chemotherapy Protocols - therapeutic use Bile Duct Neoplasms - blood Bile Duct Neoplasms - drug therapy Bile Duct Neoplasms - surgery Biomarkers, Tumor - blood Capecitabine - administration & dosage Capecitabine - therapeutic use Chemotherapy, Adjuvant - methods Cholangiocarcinoma - blood Cholangiocarcinoma - drug therapy Cholangiocarcinoma - genetics Cholangiocarcinoma - mortality Cholangiocarcinoma - surgery Circulating Tumor DNA - blood Cisplatin - administration & dosage Cisplatin - therapeutic use ctDNA Deoxycytidine - administration & dosage Deoxycytidine - analogs & derivatives Deoxycytidine - therapeutic use Disease-Free Survival extrahepatic cholangiocarcinoma Female Gemcitabine gemcitabine plus cisplatin Humans Male Middle Aged Neoplasm Recurrence, Local - blood Neoplasm Recurrence, Local - diagnosis Neoplasm, Residual Prognosis prognostic biomarker |
| Title | Circulating tumor DNA status and dynamics predict recurrence in patients with resected extrahepatic cholangiocarcinoma |
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