Association of the immediate perioperative dynamics of circulating DNA levels and neutrophil extracellular traps formation in cancer patients

Association of the immediate perioperative dynamics of circulating DNA levels and neutrophil extracellular traps formation in cancer patients

Objectives Elevated circulating DNA (cirDNA) concentrations were found to be associated with trauma or tissue damage which suggests involvement of inflammation or cell death in post-operative cirDNA release. We carried out the first prospective, multicenter study of the dynamics of cirDNA and neutro...

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Veröffentlicht in:Precision clinical medicine 2024-06, Vol.7 (2), p.pbae008-pbae008
Hauptverfasser: Kudriavtsev, Andrei, Pastor, Brice, Mirandola, Alexia, Pisareva, Ekaterina, Gricourt, Yann, Capdevila, Xavier, Thierry, Alain R, Cuvillon, Philippe
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container_issue 2
container_start_page pbae008
container_title Precision clinical medicine
container_volume 7
creator Kudriavtsev, Andrei
Pastor, Brice
Mirandola, Alexia
Pisareva, Ekaterina
Gricourt, Yann
Capdevila, Xavier
Thierry, Alain R
Cuvillon, Philippe
description Objectives Elevated circulating DNA (cirDNA) concentrations were found to be associated with trauma or tissue damage which suggests involvement of inflammation or cell death in post-operative cirDNA release. We carried out the first prospective, multicenter study of the dynamics of cirDNA and neutrophil extracellular trap (NETs) markers during the perioperative period from 24 h before surgery up to 72 h after curative surgery in cancer patients. Methods We examined the plasma levels of two NETs protein markers [myeloperoxidase (MPO) and neutrophil elastase (NE)], as well as levels of cirDNA of nuclear (cir-nDNA) and mitochondrial (cir-mtDNA) origin in 29 colon, prostate, and breast cancer patients and in 114 healthy individuals (HI). Results The synergistic analytical information provided by these markers revealed that: (i) NETs formation contributes to post-surgery conditions; (ii) post-surgery cir-nDNA levels were highly associated with NE and MPO in colon cancer [r = 0.60 (P 
doi_str_mv 10.1093/pcmedi/pbae008
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We carried out the first prospective, multicenter study of the dynamics of cirDNA and neutrophil extracellular trap (NETs) markers during the perioperative period from 24 h before surgery up to 72 h after curative surgery in cancer patients. Methods We examined the plasma levels of two NETs protein markers [myeloperoxidase (MPO) and neutrophil elastase (NE)], as well as levels of cirDNA of nuclear (cir-nDNA) and mitochondrial (cir-mtDNA) origin in 29 colon, prostate, and breast cancer patients and in 114 healthy individuals (HI). Results The synergistic analytical information provided by these markers revealed that: (i) NETs formation contributes to post-surgery conditions; (ii) post-surgery cir-nDNA levels were highly associated with NE and MPO in colon cancer [r = 0.60 (P &lt; 0.001) and r = 0.53 (P &lt; 0.01), respectively], but not in prostate and breast cancer; (iii) each tumor type shows a specific pattern of cir-nDNA and NETs marker dynamics, but overall the pre- and post-surgery median values of cir-nDNA, NE, and MPO were significantly higher in cancer patients than in HI. Conclusion Taken as a whole, our work reveals the association of NETs formation with the elevated cir-nDNA release during a cancer patient's perioperative period, depending on surgical procedure or cancer type. By contrast, cir-mtDNA is poorly associated with NETs formation in the studied perioperative period, which would appear to indicate a different mechanism of release or suggest mitochondrial dysfunction.</description><identifier>ISSN: 2096-5303</identifier><identifier>EISSN: 2516-1571</identifier><identifier>DOI: 10.1093/pcmedi/pbae008</identifier><identifier>PMID: 38699382</identifier><language>eng</language><publisher>England: Oxford University Press</publisher><ispartof>Precision clinical medicine, 2024-06, Vol.7 (2), p.pbae008-pbae008</ispartof><rights>The Author(s) 2024. Published by Oxford University Press on behalf of the West China School of Medicine &amp; West China Hospital of Sichuan University. 2024</rights><rights>The Author(s) 2024. 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We carried out the first prospective, multicenter study of the dynamics of cirDNA and neutrophil extracellular trap (NETs) markers during the perioperative period from 24 h before surgery up to 72 h after curative surgery in cancer patients. Methods We examined the plasma levels of two NETs protein markers [myeloperoxidase (MPO) and neutrophil elastase (NE)], as well as levels of cirDNA of nuclear (cir-nDNA) and mitochondrial (cir-mtDNA) origin in 29 colon, prostate, and breast cancer patients and in 114 healthy individuals (HI). Results The synergistic analytical information provided by these markers revealed that: (i) NETs formation contributes to post-surgery conditions; (ii) post-surgery cir-nDNA levels were highly associated with NE and MPO in colon cancer [r = 0.60 (P &lt; 0.001) and r = 0.53 (P &lt; 0.01), respectively], but not in prostate and breast cancer; (iii) each tumor type shows a specific pattern of cir-nDNA and NETs marker dynamics, but overall the pre- and post-surgery median values of cir-nDNA, NE, and MPO were significantly higher in cancer patients than in HI. Conclusion Taken as a whole, our work reveals the association of NETs formation with the elevated cir-nDNA release during a cancer patient's perioperative period, depending on surgical procedure or cancer type. By contrast, cir-mtDNA is poorly associated with NETs formation in the studied perioperative period, which would appear to indicate a different mechanism of release or suggest mitochondrial dysfunction.</description><issn>2096-5303</issn><issn>2516-1571</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><recordid>eNqFkU9P3DAQxa2qVUGUa4-Vj-0hMI7z94RWUKASai_t2XLsMesqsY2drOBD8J3rVbaInnqxRzM_v-fRI-QjgzMGPT8PakJtz8MgEaB7Q47LmjUFq1v2NtfQN0XNgR-R05R-A0DJqqrq4D054l3T97wrj8nzJiWvrJytd9QbOm-R2mkvK2ekAaP1-cjjHVL95ORkVdpzyka1jLnv7unV9w0dcYdjotJp6nCZow9bO1J8nKNUOI4ZjTTXIVHj47TaWUeVdAojDbmBbk4fyDsjx4Snh_uE_Lr--vPytrj7cfPtcnNXKF7BXFS9QS6xVaVuupZzbdiQbVjLhoE3Q12iMZ1mwJSuNZjMNW1peMt1XVXANT8hF6tuWIa8q8reUY4iRDvJ-CS8tOLfibNbce93gjFoSijbrPD5oBD9w4JpFpNN-02lQ78kwaHOCdUVQEbPVlRFn1JE8-LDQOxzFGuO4pBjfvDp9e9e8L-pZeDLCvgl_E_sDwagrro</recordid><startdate>20240601</startdate><enddate>20240601</enddate><creator>Kudriavtsev, Andrei</creator><creator>Pastor, Brice</creator><creator>Mirandola, Alexia</creator><creator>Pisareva, Ekaterina</creator><creator>Gricourt, Yann</creator><creator>Capdevila, Xavier</creator><creator>Thierry, Alain R</creator><creator>Cuvillon, Philippe</creator><general>Oxford University Press</general><scope>TOX</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-0537-1460</orcidid></search><sort><creationdate>20240601</creationdate><title>Association of the immediate perioperative dynamics of circulating DNA levels and neutrophil extracellular traps formation in cancer patients</title><author>Kudriavtsev, Andrei ; Pastor, Brice ; Mirandola, Alexia ; Pisareva, Ekaterina ; Gricourt, Yann ; Capdevila, Xavier ; Thierry, Alain R ; Cuvillon, Philippe</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c340t-49fe3ae7c2d68733df1bace171bb36b52eff8d101cd5d0f7c2672f373d54403d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kudriavtsev, Andrei</creatorcontrib><creatorcontrib>Pastor, Brice</creatorcontrib><creatorcontrib>Mirandola, Alexia</creatorcontrib><creatorcontrib>Pisareva, Ekaterina</creatorcontrib><creatorcontrib>Gricourt, Yann</creatorcontrib><creatorcontrib>Capdevila, Xavier</creatorcontrib><creatorcontrib>Thierry, Alain R</creatorcontrib><creatorcontrib>Cuvillon, Philippe</creatorcontrib><collection>Oxford Journals Open Access Collection</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Precision clinical medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kudriavtsev, Andrei</au><au>Pastor, Brice</au><au>Mirandola, Alexia</au><au>Pisareva, Ekaterina</au><au>Gricourt, Yann</au><au>Capdevila, Xavier</au><au>Thierry, Alain R</au><au>Cuvillon, Philippe</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Association of the immediate perioperative dynamics of circulating DNA levels and neutrophil extracellular traps formation in cancer patients</atitle><jtitle>Precision clinical medicine</jtitle><addtitle>Precis Clin Med</addtitle><date>2024-06-01</date><risdate>2024</risdate><volume>7</volume><issue>2</issue><spage>pbae008</spage><epage>pbae008</epage><pages>pbae008-pbae008</pages><issn>2096-5303</issn><eissn>2516-1571</eissn><abstract>Objectives Elevated circulating DNA (cirDNA) concentrations were found to be associated with trauma or tissue damage which suggests involvement of inflammation or cell death in post-operative cirDNA release. We carried out the first prospective, multicenter study of the dynamics of cirDNA and neutrophil extracellular trap (NETs) markers during the perioperative period from 24 h before surgery up to 72 h after curative surgery in cancer patients. Methods We examined the plasma levels of two NETs protein markers [myeloperoxidase (MPO) and neutrophil elastase (NE)], as well as levels of cirDNA of nuclear (cir-nDNA) and mitochondrial (cir-mtDNA) origin in 29 colon, prostate, and breast cancer patients and in 114 healthy individuals (HI). Results The synergistic analytical information provided by these markers revealed that: (i) NETs formation contributes to post-surgery conditions; (ii) post-surgery cir-nDNA levels were highly associated with NE and MPO in colon cancer [r = 0.60 (P &lt; 0.001) and r = 0.53 (P &lt; 0.01), respectively], but not in prostate and breast cancer; (iii) each tumor type shows a specific pattern of cir-nDNA and NETs marker dynamics, but overall the pre- and post-surgery median values of cir-nDNA, NE, and MPO were significantly higher in cancer patients than in HI. Conclusion Taken as a whole, our work reveals the association of NETs formation with the elevated cir-nDNA release during a cancer patient's perioperative period, depending on surgical procedure or cancer type. By contrast, cir-mtDNA is poorly associated with NETs formation in the studied perioperative period, which would appear to indicate a different mechanism of release or suggest mitochondrial dysfunction.</abstract><cop>England</cop><pub>Oxford University Press</pub><pmid>38699382</pmid><doi>10.1093/pcmedi/pbae008</doi><orcidid>https://orcid.org/0000-0003-0537-1460</orcidid><oa>free_for_read</oa></addata></record>
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title Association of the immediate perioperative dynamics of circulating DNA levels and neutrophil extracellular traps formation in cancer patients
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