A universal cell‐free DNA approach for response prediction to preoperative chemoradiation in rectal cancer
The standard treatment approach for stage II/III rectal cancer is neoadjuvant chemoradiation therapy (nCRT) followed by surgery. In recent years, new treatment approaches have led to higher rates of complete tumor eradication combined with organ‐preservation strategies. However, better tools are sti...
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creator | Grinshpun, Albert Kustanovich, Anatoli Neiman, Daniel Lehmann‐Werman, Roni Zick, Aviad Meir, Karen Vainer, Elez Granit, Roy Z. Arad, Amit Daskal, Noa Schwartz, Ruth Sapir, Eli Maoz, Myriam Tahover, Esther Moss, Joshua Ben‐Dov, Iddo Z. Peretz, Tamar Hubert, Ayala Shemer, Ruth Dor, Yuval |
description | The standard treatment approach for stage II/III rectal cancer is neoadjuvant chemoradiation therapy (nCRT) followed by surgery. In recent years, new treatment approaches have led to higher rates of complete tumor eradication combined with organ‐preservation strategies. However, better tools are still needed to personalize therapy for the individual patient. In this prospective observational study, we analyzed colon‐derived cell‐free (cf)DNA (c‐cfDNA) using a tissue‐specific DNA methylation signature, and its association with therapy outcomes. Analyzing plasma samples (n = 303) collected during nCRT from 37 patients with locally advanced rectal cancer (LARC), we identified colon‐specific methylation markers that discriminated healthy individuals from patients with untreated LARC (area under the curve, 0.81; 95% confidence interval, 0.70‐0.92; P |
doi_str_mv | 10.1002/ijc.34392 |
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What's new?
The treatment of locally advanced rectal cancer is a rapidly evolving field, involves multidisciplinary decision‐making, and has no predictive biomarkers for optimal treatment selection. Here, we show that cell‐free DNA from colorectal cells can be identified in patients with rectal cancer, using tissue‐specific methylation markers. Furthermore, cell‐free DNA levels and dynamics are correlated with individuals' outcomes in patients undergoing neoadjuvant chemoradiation for locally advanced rectal cancer.</description><identifier>ISSN: 0020-7136</identifier><identifier>EISSN: 1097-0215</identifier><identifier>DOI: 10.1002/ijc.34392</identifier><identifier>PMID: 36468189</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Biopsy ; Cancer ; Cell-Free Nucleic Acids - genetics ; cell‐free DNA ; chemoradiation ; Chemoradiotherapy ; Colon ; Colon cancer ; Colorectal cancer ; DNA methylation ; Eradication ; Humans ; Innovative Tools and Methods ; Medical research ; methylation ; neoadjuvant ; Neoadjuvant Therapy ; Neoplasm Recurrence, Local ; Patients ; rectal cancer ; Rectal Neoplasms - genetics ; Rectal Neoplasms - pathology ; Rectal Neoplasms - therapy ; Rectum ; Rectum - pathology ; Retrospective Studies ; Treatment Outcome ; Tumors</subject><ispartof>International journal of cancer, 2023-04, Vol.152 (7), p.1444-1451</ispartof><rights>2022 The Authors. published by John Wiley & Sons Ltd on behalf of UICC.</rights><rights>2022 The Authors. International Journal of Cancer published by John Wiley & Sons Ltd on behalf of UICC.</rights><rights>2022. This article is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4442-434b55f9891c67e07056c01a81690975e703a7717e6523f735271e4b785a618c3</citedby><cites>FETCH-LOGICAL-c4442-434b55f9891c67e07056c01a81690975e703a7717e6523f735271e4b785a618c3</cites><orcidid>0000-0002-3351-5719</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fijc.34392$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fijc.34392$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36468189$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Grinshpun, Albert</creatorcontrib><creatorcontrib>Kustanovich, Anatoli</creatorcontrib><creatorcontrib>Neiman, Daniel</creatorcontrib><creatorcontrib>Lehmann‐Werman, Roni</creatorcontrib><creatorcontrib>Zick, Aviad</creatorcontrib><creatorcontrib>Meir, Karen</creatorcontrib><creatorcontrib>Vainer, Elez</creatorcontrib><creatorcontrib>Granit, Roy Z.</creatorcontrib><creatorcontrib>Arad, Amit</creatorcontrib><creatorcontrib>Daskal, Noa</creatorcontrib><creatorcontrib>Schwartz, Ruth</creatorcontrib><creatorcontrib>Sapir, Eli</creatorcontrib><creatorcontrib>Maoz, Myriam</creatorcontrib><creatorcontrib>Tahover, Esther</creatorcontrib><creatorcontrib>Moss, Joshua</creatorcontrib><creatorcontrib>Ben‐Dov, Iddo Z.</creatorcontrib><creatorcontrib>Peretz, Tamar</creatorcontrib><creatorcontrib>Hubert, Ayala</creatorcontrib><creatorcontrib>Shemer, Ruth</creatorcontrib><creatorcontrib>Dor, Yuval</creatorcontrib><title>A universal cell‐free DNA approach for response prediction to preoperative chemoradiation in rectal cancer</title><title>International journal of cancer</title><addtitle>Int J Cancer</addtitle><description>The standard treatment approach for stage II/III rectal cancer is neoadjuvant chemoradiation therapy (nCRT) followed by surgery. In recent years, new treatment approaches have led to higher rates of complete tumor eradication combined with organ‐preservation strategies. However, better tools are still needed to personalize therapy for the individual patient. In this prospective observational study, we analyzed colon‐derived cell‐free (cf)DNA (c‐cfDNA) using a tissue‐specific DNA methylation signature, and its association with therapy outcomes. Analyzing plasma samples (n = 303) collected during nCRT from 37 patients with locally advanced rectal cancer (LARC), we identified colon‐specific methylation markers that discriminated healthy individuals from patients with untreated LARC (area under the curve, 0.81; 95% confidence interval, 0.70‐0.92; P < .0001). Baseline c‐cfDNA predicted tumor response, with increased levels linked to larger residual cancer. c‐cfDNA measured after the first week of therapy identified patients with maximal response and complete cancer eradication, who had significantly lower c‐cfDNA compared with those who had residual disease (8.6 vs 57.7 average copies/ml, respectively; P = .013). Increased c‐cfDNA after 1 week of therapy was also associated with disease recurrence. Methylation‐based liquid biopsy can predict nCRT outcomes and facilitate patient selection for escalation and de‐escalation strategies.
What's new?
The treatment of locally advanced rectal cancer is a rapidly evolving field, involves multidisciplinary decision‐making, and has no predictive biomarkers for optimal treatment selection. Here, we show that cell‐free DNA from colorectal cells can be identified in patients with rectal cancer, using tissue‐specific methylation markers. Furthermore, cell‐free DNA levels and dynamics are correlated with individuals' outcomes in patients undergoing neoadjuvant chemoradiation for locally advanced rectal cancer.</description><subject>Biopsy</subject><subject>Cancer</subject><subject>Cell-Free Nucleic Acids - genetics</subject><subject>cell‐free DNA</subject><subject>chemoradiation</subject><subject>Chemoradiotherapy</subject><subject>Colon</subject><subject>Colon cancer</subject><subject>Colorectal cancer</subject><subject>DNA methylation</subject><subject>Eradication</subject><subject>Humans</subject><subject>Innovative Tools and Methods</subject><subject>Medical research</subject><subject>methylation</subject><subject>neoadjuvant</subject><subject>Neoadjuvant Therapy</subject><subject>Neoplasm Recurrence, Local</subject><subject>Patients</subject><subject>rectal cancer</subject><subject>Rectal Neoplasms - genetics</subject><subject>Rectal Neoplasms - pathology</subject><subject>Rectal Neoplasms - therapy</subject><subject>Rectum</subject><subject>Rectum - pathology</subject><subject>Retrospective Studies</subject><subject>Treatment Outcome</subject><subject>Tumors</subject><issn>0020-7136</issn><issn>1097-0215</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNp1kcFu1DAQhi0EokvhwAsgS1zaQ9qZ2I6TE1otBYoquMDZ8nonrFfZONhJUW88As_Ik-B0SwVInCxrvvk0Mz9jzxHOEKA89zt3JqRoygdsgdDoAkpUD9ki16DQKKoj9iSlHQCiAvmYHYlKVjXWzYJ1Sz71_ppish131HU_v_9oIxF__WHJ7TDEYN2WtyHySGkIfSI-RNp4N_rQ8zHMvzBQtGOWcLelfYh24-1t2fe5y42z2faO4lP2qLVdomd37zH7_Obi0-pdcfXx7eVqeVU4KWVZSCHXSrVN3aCrNIEGVTlAW2PV5O0UaRBWa9RUqVK0WqhSI8m1rpWtsHbimL06eIdpvaeNo36MtjND9Hsbb0yw3vxd6f3WfAnXBgGhzlfKhpM7QwxfJ0qj2fs0n8f2FKZkSi01gNRiRl_-g-7CFPu8X6Y0lmqeL1OnB8rFkFKk9n4aBDOHaHKI5jbEzL74c_x78ndqGTg_AN98Rzf_N5nL96uD8hfj3Kad</recordid><startdate>20230401</startdate><enddate>20230401</enddate><creator>Grinshpun, Albert</creator><creator>Kustanovich, Anatoli</creator><creator>Neiman, Daniel</creator><creator>Lehmann‐Werman, Roni</creator><creator>Zick, Aviad</creator><creator>Meir, Karen</creator><creator>Vainer, Elez</creator><creator>Granit, Roy Z.</creator><creator>Arad, Amit</creator><creator>Daskal, Noa</creator><creator>Schwartz, Ruth</creator><creator>Sapir, Eli</creator><creator>Maoz, Myriam</creator><creator>Tahover, Esther</creator><creator>Moss, Joshua</creator><creator>Ben‐Dov, Iddo Z.</creator><creator>Peretz, Tamar</creator><creator>Hubert, Ayala</creator><creator>Shemer, Ruth</creator><creator>Dor, Yuval</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><scope>24P</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7T5</scope><scope>7TO</scope><scope>7U9</scope><scope>H94</scope><scope>K9.</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-3351-5719</orcidid></search><sort><creationdate>20230401</creationdate><title>A universal cell‐free DNA approach for response prediction to preoperative chemoradiation in rectal cancer</title><author>Grinshpun, Albert ; Kustanovich, Anatoli ; Neiman, Daniel ; Lehmann‐Werman, Roni ; Zick, Aviad ; Meir, Karen ; Vainer, Elez ; Granit, Roy Z. ; Arad, Amit ; Daskal, Noa ; Schwartz, Ruth ; Sapir, Eli ; Maoz, Myriam ; Tahover, Esther ; Moss, Joshua ; Ben‐Dov, Iddo Z. ; Peretz, Tamar ; Hubert, Ayala ; Shemer, Ruth ; Dor, Yuval</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4442-434b55f9891c67e07056c01a81690975e703a7717e6523f735271e4b785a618c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Biopsy</topic><topic>Cancer</topic><topic>Cell-Free Nucleic Acids - genetics</topic><topic>cell‐free DNA</topic><topic>chemoradiation</topic><topic>Chemoradiotherapy</topic><topic>Colon</topic><topic>Colon cancer</topic><topic>Colorectal cancer</topic><topic>DNA methylation</topic><topic>Eradication</topic><topic>Humans</topic><topic>Innovative Tools and Methods</topic><topic>Medical research</topic><topic>methylation</topic><topic>neoadjuvant</topic><topic>Neoadjuvant Therapy</topic><topic>Neoplasm Recurrence, Local</topic><topic>Patients</topic><topic>rectal cancer</topic><topic>Rectal Neoplasms - genetics</topic><topic>Rectal Neoplasms - pathology</topic><topic>Rectal Neoplasms - therapy</topic><topic>Rectum</topic><topic>Rectum - pathology</topic><topic>Retrospective Studies</topic><topic>Treatment Outcome</topic><topic>Tumors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Grinshpun, Albert</creatorcontrib><creatorcontrib>Kustanovich, Anatoli</creatorcontrib><creatorcontrib>Neiman, Daniel</creatorcontrib><creatorcontrib>Lehmann‐Werman, Roni</creatorcontrib><creatorcontrib>Zick, Aviad</creatorcontrib><creatorcontrib>Meir, Karen</creatorcontrib><creatorcontrib>Vainer, Elez</creatorcontrib><creatorcontrib>Granit, Roy Z.</creatorcontrib><creatorcontrib>Arad, Amit</creatorcontrib><creatorcontrib>Daskal, Noa</creatorcontrib><creatorcontrib>Schwartz, Ruth</creatorcontrib><creatorcontrib>Sapir, Eli</creatorcontrib><creatorcontrib>Maoz, Myriam</creatorcontrib><creatorcontrib>Tahover, Esther</creatorcontrib><creatorcontrib>Moss, Joshua</creatorcontrib><creatorcontrib>Ben‐Dov, Iddo Z.</creatorcontrib><creatorcontrib>Peretz, Tamar</creatorcontrib><creatorcontrib>Hubert, Ayala</creatorcontrib><creatorcontrib>Shemer, Ruth</creatorcontrib><creatorcontrib>Dor, Yuval</creatorcontrib><collection>Wiley Online Library Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Immunology Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>International journal of cancer</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Grinshpun, Albert</au><au>Kustanovich, Anatoli</au><au>Neiman, Daniel</au><au>Lehmann‐Werman, Roni</au><au>Zick, Aviad</au><au>Meir, Karen</au><au>Vainer, Elez</au><au>Granit, Roy Z.</au><au>Arad, Amit</au><au>Daskal, Noa</au><au>Schwartz, Ruth</au><au>Sapir, Eli</au><au>Maoz, Myriam</au><au>Tahover, Esther</au><au>Moss, Joshua</au><au>Ben‐Dov, Iddo Z.</au><au>Peretz, Tamar</au><au>Hubert, Ayala</au><au>Shemer, Ruth</au><au>Dor, Yuval</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A universal cell‐free DNA approach for response prediction to preoperative chemoradiation in rectal cancer</atitle><jtitle>International journal of cancer</jtitle><addtitle>Int J Cancer</addtitle><date>2023-04-01</date><risdate>2023</risdate><volume>152</volume><issue>7</issue><spage>1444</spage><epage>1451</epage><pages>1444-1451</pages><issn>0020-7136</issn><eissn>1097-0215</eissn><abstract>The standard treatment approach for stage II/III rectal cancer is neoadjuvant chemoradiation therapy (nCRT) followed by surgery. In recent years, new treatment approaches have led to higher rates of complete tumor eradication combined with organ‐preservation strategies. However, better tools are still needed to personalize therapy for the individual patient. In this prospective observational study, we analyzed colon‐derived cell‐free (cf)DNA (c‐cfDNA) using a tissue‐specific DNA methylation signature, and its association with therapy outcomes. Analyzing plasma samples (n = 303) collected during nCRT from 37 patients with locally advanced rectal cancer (LARC), we identified colon‐specific methylation markers that discriminated healthy individuals from patients with untreated LARC (area under the curve, 0.81; 95% confidence interval, 0.70‐0.92; P < .0001). Baseline c‐cfDNA predicted tumor response, with increased levels linked to larger residual cancer. c‐cfDNA measured after the first week of therapy identified patients with maximal response and complete cancer eradication, who had significantly lower c‐cfDNA compared with those who had residual disease (8.6 vs 57.7 average copies/ml, respectively; P = .013). Increased c‐cfDNA after 1 week of therapy was also associated with disease recurrence. Methylation‐based liquid biopsy can predict nCRT outcomes and facilitate patient selection for escalation and de‐escalation strategies.
What's new?
The treatment of locally advanced rectal cancer is a rapidly evolving field, involves multidisciplinary decision‐making, and has no predictive biomarkers for optimal treatment selection. Here, we show that cell‐free DNA from colorectal cells can be identified in patients with rectal cancer, using tissue‐specific methylation markers. Furthermore, cell‐free DNA levels and dynamics are correlated with individuals' outcomes in patients undergoing neoadjuvant chemoradiation for locally advanced rectal cancer.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>36468189</pmid><doi>10.1002/ijc.34392</doi><tpages>8</tpages><orcidid>https://orcid.org/0000-0002-3351-5719</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Biopsy Cancer Cell-Free Nucleic Acids - genetics cell‐free DNA chemoradiation Chemoradiotherapy Colon Colon cancer Colorectal cancer DNA methylation Eradication Humans Innovative Tools and Methods Medical research methylation neoadjuvant Neoadjuvant Therapy Neoplasm Recurrence, Local Patients rectal cancer Rectal Neoplasms - genetics Rectal Neoplasms - pathology Rectal Neoplasms - therapy Rectum Rectum - pathology Retrospective Studies Treatment Outcome Tumors |
title | A universal cell‐free DNA approach for response prediction to preoperative chemoradiation in rectal cancer |
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