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Deciphering molecular relapse and intra-tumor heterogeneity in non-metastatic resectable head and neck squamous cell carcinoma using circulating tumor DNA
•ctDNA provided complementary information on actionable mutations to tissue biopsy.•ctDNA provided a comprehensive view of mutational landscape dynamics over time.•ctDNA-based molecular relapse detection has high levels of clinical validity. Head and neck squamous cell carcinoma (HNSCC) is character...
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Published in: | Oral oncology 2025-01, Vol.160, p.107111, Article 107111 |
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creator | Marret, Grégoire Lamy, Constance Vacher, Sophie Cabel, Luc Séné, Mathieu Ahmanache, Ladidi Courtois, Laura El Beaino, Zakhia Klijanienko, Jerzy Martinat, Charlotte Servant, Nicolas Kamoun, Choumouss Halladjian, Maral Bronzini, Thierry Balsat, Cédric Laes, Jean-François Prévot, Aubray Sauvage, Sébastien Lienard, Maxime Martin, Emmanuel Genin, Bérengère Badois, Nathalie Lesnik, Maria Dubray-Vautrin, Antoine Choussy, Olivier Ghanem, Wahib Taouachi, Rabah Planchon, Julien Masliah Bièche, Ivan Le Tourneau, Christophe Kamal, Maud |
description | •ctDNA provided complementary information on actionable mutations to tissue biopsy.•ctDNA provided a comprehensive view of mutational landscape dynamics over time.•ctDNA-based molecular relapse detection has high levels of clinical validity.
Head and neck squamous cell carcinoma (HNSCC) is characterized by significant genetic intra-tumor heterogeneity (ITH), which may hinder precision medicine strategies that depend on results from single tumor-biopsy specimens. Treatment response assessment relies on radiologic imaging, which cannot detect minimal residual disease (MRD). We assessed the relevance of circulating tumor DNA (ctDNA) as a biomarker for ITH and MRD in HNSCC.
We recruited 41 non-metastatic resectable HNSCC patients treated with upfront curative-intent surgery in the prospective biobanking SCANDARE study (NCT03017573). Thirty-one patients (76 %) showed recurrent disease at a median follow-up of 41 months. Targeted next-generation sequencing was performed on resected tumor tissues, as well as on serial blood samples obtained at surgery, within 14 weeks after surgery, at six months and at recurrence.
ctDNA was detected in 21/41 patients at surgery (sensitivity: 51 %; 95 % CI, 35–67 %) and 15/22 patients at recurrence (sensitivity: 68 %; 95 % confidence interval [CI], 45–86 %). Among patients with mutations identified in longitudinal plasma samples, additional mutations missed in tumor tissues were reported in 3/21 patients (14 %), while emerging mutations were reported in 9/21 patients (43 %). In the postoperative surveillance setting, ctDNA-based MRD detection anticipated clinical recurrence with a median lead-time of 9.9 months (interquartile range, 8.0–14.5 months) in 17/27 patients (63 %). When detected within 14 weeks after surgery, MRD correlated with disease recurrence after adjusting for classical prognostic variables (HR = 3.0; 95 % CI, 1.1–7.9; p = 0.03).
ctDNA detection is a useful biomarker for ITH and MRD in resectable HNSCC patients. |
doi_str_mv | 10.1016/j.oraloncology.2024.107111 |
format | article |
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Head and neck squamous cell carcinoma (HNSCC) is characterized by significant genetic intra-tumor heterogeneity (ITH), which may hinder precision medicine strategies that depend on results from single tumor-biopsy specimens. Treatment response assessment relies on radiologic imaging, which cannot detect minimal residual disease (MRD). We assessed the relevance of circulating tumor DNA (ctDNA) as a biomarker for ITH and MRD in HNSCC.
We recruited 41 non-metastatic resectable HNSCC patients treated with upfront curative-intent surgery in the prospective biobanking SCANDARE study (NCT03017573). Thirty-one patients (76 %) showed recurrent disease at a median follow-up of 41 months. Targeted next-generation sequencing was performed on resected tumor tissues, as well as on serial blood samples obtained at surgery, within 14 weeks after surgery, at six months and at recurrence.
ctDNA was detected in 21/41 patients at surgery (sensitivity: 51 %; 95 % CI, 35–67 %) and 15/22 patients at recurrence (sensitivity: 68 %; 95 % confidence interval [CI], 45–86 %). Among patients with mutations identified in longitudinal plasma samples, additional mutations missed in tumor tissues were reported in 3/21 patients (14 %), while emerging mutations were reported in 9/21 patients (43 %). In the postoperative surveillance setting, ctDNA-based MRD detection anticipated clinical recurrence with a median lead-time of 9.9 months (interquartile range, 8.0–14.5 months) in 17/27 patients (63 %). When detected within 14 weeks after surgery, MRD correlated with disease recurrence after adjusting for classical prognostic variables (HR = 3.0; 95 % CI, 1.1–7.9; p = 0.03).
ctDNA detection is a useful biomarker for ITH and MRD in resectable HNSCC patients.</description><identifier>ISSN: 1368-8375</identifier><identifier>ISSN: 1879-0593</identifier><identifier>EISSN: 1879-0593</identifier><identifier>DOI: 10.1016/j.oraloncology.2024.107111</identifier><identifier>PMID: 39612700</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Biomarkers ; circulating tumor DNA ; Head and neck squamous cell carcinoma ; Liquid biopsy ; Next-generation sequencing ; Tumor heterogeneity</subject><ispartof>Oral oncology, 2025-01, Vol.160, p.107111, Article 107111</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39612700$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Marret, Grégoire</creatorcontrib><creatorcontrib>Lamy, Constance</creatorcontrib><creatorcontrib>Vacher, Sophie</creatorcontrib><creatorcontrib>Cabel, Luc</creatorcontrib><creatorcontrib>Séné, Mathieu</creatorcontrib><creatorcontrib>Ahmanache, Ladidi</creatorcontrib><creatorcontrib>Courtois, Laura</creatorcontrib><creatorcontrib>El Beaino, Zakhia</creatorcontrib><creatorcontrib>Klijanienko, Jerzy</creatorcontrib><creatorcontrib>Martinat, Charlotte</creatorcontrib><creatorcontrib>Servant, Nicolas</creatorcontrib><creatorcontrib>Kamoun, Choumouss</creatorcontrib><creatorcontrib>Halladjian, Maral</creatorcontrib><creatorcontrib>Bronzini, Thierry</creatorcontrib><creatorcontrib>Balsat, Cédric</creatorcontrib><creatorcontrib>Laes, Jean-François</creatorcontrib><creatorcontrib>Prévot, Aubray</creatorcontrib><creatorcontrib>Sauvage, Sébastien</creatorcontrib><creatorcontrib>Lienard, Maxime</creatorcontrib><creatorcontrib>Martin, Emmanuel</creatorcontrib><creatorcontrib>Genin, Bérengère</creatorcontrib><creatorcontrib>Badois, Nathalie</creatorcontrib><creatorcontrib>Lesnik, Maria</creatorcontrib><creatorcontrib>Dubray-Vautrin, Antoine</creatorcontrib><creatorcontrib>Choussy, Olivier</creatorcontrib><creatorcontrib>Ghanem, Wahib</creatorcontrib><creatorcontrib>Taouachi, Rabah</creatorcontrib><creatorcontrib>Planchon, Julien Masliah</creatorcontrib><creatorcontrib>Bièche, Ivan</creatorcontrib><creatorcontrib>Le Tourneau, Christophe</creatorcontrib><creatorcontrib>Kamal, Maud</creatorcontrib><title>Deciphering molecular relapse and intra-tumor heterogeneity in non-metastatic resectable head and neck squamous cell carcinoma using circulating tumor DNA</title><title>Oral oncology</title><addtitle>Oral Oncol</addtitle><description>•ctDNA provided complementary information on actionable mutations to tissue biopsy.•ctDNA provided a comprehensive view of mutational landscape dynamics over time.•ctDNA-based molecular relapse detection has high levels of clinical validity.
Head and neck squamous cell carcinoma (HNSCC) is characterized by significant genetic intra-tumor heterogeneity (ITH), which may hinder precision medicine strategies that depend on results from single tumor-biopsy specimens. Treatment response assessment relies on radiologic imaging, which cannot detect minimal residual disease (MRD). We assessed the relevance of circulating tumor DNA (ctDNA) as a biomarker for ITH and MRD in HNSCC.
We recruited 41 non-metastatic resectable HNSCC patients treated with upfront curative-intent surgery in the prospective biobanking SCANDARE study (NCT03017573). Thirty-one patients (76 %) showed recurrent disease at a median follow-up of 41 months. Targeted next-generation sequencing was performed on resected tumor tissues, as well as on serial blood samples obtained at surgery, within 14 weeks after surgery, at six months and at recurrence.
ctDNA was detected in 21/41 patients at surgery (sensitivity: 51 %; 95 % CI, 35–67 %) and 15/22 patients at recurrence (sensitivity: 68 %; 95 % confidence interval [CI], 45–86 %). Among patients with mutations identified in longitudinal plasma samples, additional mutations missed in tumor tissues were reported in 3/21 patients (14 %), while emerging mutations were reported in 9/21 patients (43 %). In the postoperative surveillance setting, ctDNA-based MRD detection anticipated clinical recurrence with a median lead-time of 9.9 months (interquartile range, 8.0–14.5 months) in 17/27 patients (63 %). When detected within 14 weeks after surgery, MRD correlated with disease recurrence after adjusting for classical prognostic variables (HR = 3.0; 95 % CI, 1.1–7.9; p = 0.03).
ctDNA detection is a useful biomarker for ITH and MRD in resectable HNSCC patients.</description><subject>Biomarkers</subject><subject>circulating tumor DNA</subject><subject>Head and neck squamous cell carcinoma</subject><subject>Liquid biopsy</subject><subject>Next-generation sequencing</subject><subject>Tumor heterogeneity</subject><issn>1368-8375</issn><issn>1879-0593</issn><issn>1879-0593</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2025</creationdate><recordtype>article</recordtype><recordid>eNpNUctOwzAQtBCIlscvIIsTlxQ7zqtHRHlJFVzgbLn2prg4dms7SP0VvhaHgMRevNLO7oxnELqkZEYJra43M-eFcVY649b7WU7yIg1qSukBmtKmnmeknLPD1LOqyRpWlxN0EsKGEFLSkhyjCZtXNK8JmaKvBUi9fQev7Rp3zoDsjfDYgxHbAFhYhbWNXmSx75zH7xDBuzVY0HGfJtg6m3UQRYgiapn2AsgoVgYSVKiffQvyA4ddLzrXByzBGCyFl9q6TuA-DMRS-4E3Dv1ItHi-OUNHrTABzn_fU_R2f_d6-5gtXx6ebm-WGaSfx6zNoSJN0QLUK1BEyZK1ZZ7P26ZWJaiqKqpVVVNIJVmhWNmqBhqhCKsVoVCwU3Q13t16t-shRN7pMMgUFpJizigrGKPJzAS9-IX2qw4U33rdCb_nf34mwGIEQBL8qcHzIDVYCUr7ZAxXTnNK-BAj3_D_MfIhRj7GyL4BD-eYVA</recordid><startdate>20250101</startdate><enddate>20250101</enddate><creator>Marret, Grégoire</creator><creator>Lamy, Constance</creator><creator>Vacher, Sophie</creator><creator>Cabel, Luc</creator><creator>Séné, Mathieu</creator><creator>Ahmanache, Ladidi</creator><creator>Courtois, Laura</creator><creator>El Beaino, Zakhia</creator><creator>Klijanienko, Jerzy</creator><creator>Martinat, Charlotte</creator><creator>Servant, Nicolas</creator><creator>Kamoun, Choumouss</creator><creator>Halladjian, Maral</creator><creator>Bronzini, Thierry</creator><creator>Balsat, Cédric</creator><creator>Laes, Jean-François</creator><creator>Prévot, Aubray</creator><creator>Sauvage, Sébastien</creator><creator>Lienard, Maxime</creator><creator>Martin, Emmanuel</creator><creator>Genin, Bérengère</creator><creator>Badois, Nathalie</creator><creator>Lesnik, Maria</creator><creator>Dubray-Vautrin, Antoine</creator><creator>Choussy, Olivier</creator><creator>Ghanem, Wahib</creator><creator>Taouachi, Rabah</creator><creator>Planchon, Julien Masliah</creator><creator>Bièche, Ivan</creator><creator>Le Tourneau, Christophe</creator><creator>Kamal, Maud</creator><general>Elsevier Ltd</general><scope>NPM</scope><scope>7X8</scope></search><sort><creationdate>20250101</creationdate><title>Deciphering molecular relapse and intra-tumor heterogeneity in non-metastatic resectable head and neck squamous cell carcinoma using circulating tumor DNA</title><author>Marret, Grégoire ; Lamy, Constance ; Vacher, Sophie ; Cabel, Luc ; Séné, Mathieu ; Ahmanache, Ladidi ; Courtois, Laura ; El Beaino, Zakhia ; Klijanienko, Jerzy ; Martinat, Charlotte ; Servant, Nicolas ; Kamoun, Choumouss ; Halladjian, Maral ; Bronzini, Thierry ; Balsat, Cédric ; Laes, Jean-François ; Prévot, Aubray ; Sauvage, Sébastien ; Lienard, Maxime ; Martin, Emmanuel ; Genin, Bérengère ; Badois, Nathalie ; Lesnik, Maria ; Dubray-Vautrin, Antoine ; Choussy, Olivier ; Ghanem, Wahib ; Taouachi, Rabah ; Planchon, Julien Masliah ; Bièche, Ivan ; Le Tourneau, Christophe ; Kamal, Maud</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-e202t-f2e6084fee7bed0dc53f5229f87d5ed6646b671eeeec34d35fd8e8ad037d01e43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2025</creationdate><topic>Biomarkers</topic><topic>circulating tumor DNA</topic><topic>Head and neck squamous cell carcinoma</topic><topic>Liquid biopsy</topic><topic>Next-generation sequencing</topic><topic>Tumor heterogeneity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Marret, Grégoire</creatorcontrib><creatorcontrib>Lamy, Constance</creatorcontrib><creatorcontrib>Vacher, Sophie</creatorcontrib><creatorcontrib>Cabel, Luc</creatorcontrib><creatorcontrib>Séné, Mathieu</creatorcontrib><creatorcontrib>Ahmanache, Ladidi</creatorcontrib><creatorcontrib>Courtois, Laura</creatorcontrib><creatorcontrib>El Beaino, Zakhia</creatorcontrib><creatorcontrib>Klijanienko, Jerzy</creatorcontrib><creatorcontrib>Martinat, Charlotte</creatorcontrib><creatorcontrib>Servant, Nicolas</creatorcontrib><creatorcontrib>Kamoun, Choumouss</creatorcontrib><creatorcontrib>Halladjian, Maral</creatorcontrib><creatorcontrib>Bronzini, Thierry</creatorcontrib><creatorcontrib>Balsat, Cédric</creatorcontrib><creatorcontrib>Laes, Jean-François</creatorcontrib><creatorcontrib>Prévot, Aubray</creatorcontrib><creatorcontrib>Sauvage, Sébastien</creatorcontrib><creatorcontrib>Lienard, Maxime</creatorcontrib><creatorcontrib>Martin, Emmanuel</creatorcontrib><creatorcontrib>Genin, Bérengère</creatorcontrib><creatorcontrib>Badois, Nathalie</creatorcontrib><creatorcontrib>Lesnik, Maria</creatorcontrib><creatorcontrib>Dubray-Vautrin, Antoine</creatorcontrib><creatorcontrib>Choussy, Olivier</creatorcontrib><creatorcontrib>Ghanem, Wahib</creatorcontrib><creatorcontrib>Taouachi, Rabah</creatorcontrib><creatorcontrib>Planchon, Julien Masliah</creatorcontrib><creatorcontrib>Bièche, Ivan</creatorcontrib><creatorcontrib>Le Tourneau, Christophe</creatorcontrib><creatorcontrib>Kamal, Maud</creatorcontrib><collection>PubMed</collection><collection>MEDLINE - Academic</collection><jtitle>Oral oncology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Marret, Grégoire</au><au>Lamy, Constance</au><au>Vacher, Sophie</au><au>Cabel, Luc</au><au>Séné, Mathieu</au><au>Ahmanache, Ladidi</au><au>Courtois, Laura</au><au>El Beaino, Zakhia</au><au>Klijanienko, Jerzy</au><au>Martinat, Charlotte</au><au>Servant, Nicolas</au><au>Kamoun, Choumouss</au><au>Halladjian, Maral</au><au>Bronzini, Thierry</au><au>Balsat, Cédric</au><au>Laes, Jean-François</au><au>Prévot, Aubray</au><au>Sauvage, Sébastien</au><au>Lienard, Maxime</au><au>Martin, Emmanuel</au><au>Genin, Bérengère</au><au>Badois, Nathalie</au><au>Lesnik, Maria</au><au>Dubray-Vautrin, Antoine</au><au>Choussy, Olivier</au><au>Ghanem, Wahib</au><au>Taouachi, Rabah</au><au>Planchon, Julien Masliah</au><au>Bièche, Ivan</au><au>Le Tourneau, Christophe</au><au>Kamal, Maud</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Deciphering molecular relapse and intra-tumor heterogeneity in non-metastatic resectable head and neck squamous cell carcinoma using circulating tumor DNA</atitle><jtitle>Oral oncology</jtitle><addtitle>Oral Oncol</addtitle><date>2025-01-01</date><risdate>2025</risdate><volume>160</volume><spage>107111</spage><pages>107111-</pages><artnum>107111</artnum><issn>1368-8375</issn><issn>1879-0593</issn><eissn>1879-0593</eissn><abstract>•ctDNA provided complementary information on actionable mutations to tissue biopsy.•ctDNA provided a comprehensive view of mutational landscape dynamics over time.•ctDNA-based molecular relapse detection has high levels of clinical validity.
Head and neck squamous cell carcinoma (HNSCC) is characterized by significant genetic intra-tumor heterogeneity (ITH), which may hinder precision medicine strategies that depend on results from single tumor-biopsy specimens. Treatment response assessment relies on radiologic imaging, which cannot detect minimal residual disease (MRD). We assessed the relevance of circulating tumor DNA (ctDNA) as a biomarker for ITH and MRD in HNSCC.
We recruited 41 non-metastatic resectable HNSCC patients treated with upfront curative-intent surgery in the prospective biobanking SCANDARE study (NCT03017573). Thirty-one patients (76 %) showed recurrent disease at a median follow-up of 41 months. Targeted next-generation sequencing was performed on resected tumor tissues, as well as on serial blood samples obtained at surgery, within 14 weeks after surgery, at six months and at recurrence.
ctDNA was detected in 21/41 patients at surgery (sensitivity: 51 %; 95 % CI, 35–67 %) and 15/22 patients at recurrence (sensitivity: 68 %; 95 % confidence interval [CI], 45–86 %). Among patients with mutations identified in longitudinal plasma samples, additional mutations missed in tumor tissues were reported in 3/21 patients (14 %), while emerging mutations were reported in 9/21 patients (43 %). In the postoperative surveillance setting, ctDNA-based MRD detection anticipated clinical recurrence with a median lead-time of 9.9 months (interquartile range, 8.0–14.5 months) in 17/27 patients (63 %). When detected within 14 weeks after surgery, MRD correlated with disease recurrence after adjusting for classical prognostic variables (HR = 3.0; 95 % CI, 1.1–7.9; p = 0.03).
ctDNA detection is a useful biomarker for ITH and MRD in resectable HNSCC patients.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>39612700</pmid><doi>10.1016/j.oraloncology.2024.107111</doi></addata></record> |
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subjects | Biomarkers circulating tumor DNA Head and neck squamous cell carcinoma Liquid biopsy Next-generation sequencing Tumor heterogeneity |
title | Deciphering molecular relapse and intra-tumor heterogeneity in non-metastatic resectable head and neck squamous cell carcinoma using circulating tumor DNA |
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