{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T00:28:35Z","timestamp":1791851315670,"version":"4.3.4"},"reference-count":121,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2023,11,15]],"date-time":"2023-11-15T00:00:00Z","timestamp":1700006400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Med."],"abstract":"<jats:p>Despite significant progress in dialysis modalities, intermittent renal replacement therapy remains an \u201cunphysiological\u201d treatment that imperfectly corrects uremic disorders and may lead to low-grade chronic inflammation, neutrophil activation, and oxidative stress due to repetitive blood\/membrane interactions contributing to the \u201cremaining uremic syndrome\u201d and cardiovascular disease burden of hemodialysis patients. Understanding dialysis bioincompatibility pathways still remains a clinical and biochemical challenge. Indeed, surrogate biomarkers of inflammation including C-reactive protein could not discriminate between all components involved in these complex pathways. A few examples may serve to illustrate the case. Cytokine release during dialysis sessions may be underestimated due to their removal using high-flux dialysis or hemodiafiltration modalities. Complement activation is recognized as a key event of bioincompatibility. However, it appears as an early and transient event with anaphylatoxin level normalization at the end of the dialysis session. Complement activation is generally assumed to trigger leukocyte stimulation leading to proinflammatory mediators\u2019 secretion and oxidative burst. In addition to being part of the innate immune response involved in eliminating physically and enzymatically microbes, the formation of Neutrophil Extracellular Traps (NETs), known as NETosis, has been recently identified as a major harmful component in a wide range of pathologies associated with inflammatory processes. NETs result from the neutrophil degranulation induced by reactive oxygen species overproduction via NADPH oxidase and consist of modified chromatin decorated with serine proteases, elastase, bactericidal proteins, and myeloperoxidase (MPO) that produces hypochlorite anion. Currently, NETosis remains poorly investigated as a sensitive and integrated marker of bioincompatibility in dialysis. Only scarce data could be found in the literature. Oxidative burst and NADPH oxidase activation are well-known events in the bioincompatibility phenomenon. NET byproducts such as elastase, MPO, and circulating DNA have been reported to be increased in dialysis patients more specifically during dialysis sessions, and were identified as predictors of poor outcomes. As NETs and MPO could be taken up by endothelium, NETs could be considered as a vascular memory of intermittent bioincompatibility phenomenon. In this working hypothesis article, we summarized the puzzle pieces showing the involvement of NET formation during hemodialysis and postulated that NETosis may act as a disease modifier and may contribute to the comorbid burden associated with dialysis bioincompatibility.<\/jats:p>","DOI":"10.3389\/fmed.2023.1268748","type":"journal-article","created":{"date-parts":[[2023,11,15]],"date-time":"2023-11-15T09:46:38Z","timestamp":1700041598000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":8,"title":["What is the role of the neutrophil extracellular traps in the cardiovascular disease burden associated with hemodialysis bioincompatibility?"],"prefix":"10.3389","volume":"10","author":[{"given":"Jean-Paul","family":"Cristol","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alain R.","family":"Thierry","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anne-Sophie","family":"Bargnoux","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marion","family":"Morena-Carrere","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bernard","family":"Canaud","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2023,11,15]]},"reference":[{"key":"ref1","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1038\/s41581-020-0315-4","article-title":"The current and future landscape of dialysis","volume":"16","author":"Himmelfarb","year":"2020","journal-title":"Nat Rev Nephrol"},{"key":"ref2","doi-asserted-by":"publisher","first-page":"39","DOI":"10.5527\/wjn.v11.i2.39","article-title":"Hidden risks associated with conventional short intermittent hemodialysis: a call for action to mitigate cardiovascular risk and morbidity","volume":"11","author":"Canaud","year":"2022","journal-title":"World J Nephrol"},{"key":"ref3","doi-asserted-by":"publisher","first-page":"1856","DOI":"10.1016\/j.ekir.2020.08.031","article-title":"Dialysis-induced cardiovascular and multiorgan morbidity","volume":"5","author":"Canaud","year":"2020","journal-title":"Kidney Int Rep"},{"key":"ref4","doi-asserted-by":"publisher","first-page":"191","DOI":"10.1159\/000014418","article-title":"Why hemodialysis patients are in a prooxidant state? What could be done to correct the pro\/antioxidant imbalance [in process citation]","volume":"18","author":"Morena","year":"2000","journal-title":"Blood Purif"},{"key":"ref5","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1053\/j.ajkd.2013.11.010","article-title":"Hemodialysis-induced regional left ventricular systolic dysfunction and inflammation: a cross-sectional study","volume":"64","author":"Assa","year":"2014","journal-title":"Am J Kidney Dis"},{"key":"ref6","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1111\/j.1525-139X.2010.00782.x","article-title":"Recurrent circulatory stress: the dark side of dialysis","volume":"23","author":"McIntyre","year":"2010","journal-title":"Semin Dial"},{"key":"ref7","doi-asserted-by":"publisher","first-page":"414","DOI":"10.1159\/000489829","article-title":"Neutrophil extracellular traps in the second decade","volume":"10","author":"Brinkmann","year":"2018","journal-title":"J Innate Immun"},{"key":"ref8","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1002\/jlb.59.2.229","article-title":"Rapid killing of human neutrophils by the potent activator phorbol 12-myristate 13-acetate (PMA) accompanied by changes different from typical apoptosis or necrosis","volume":"59","author":"Takei","year":"1996","journal-title":"J Leukoc Biol"},{"key":"ref9","doi-asserted-by":"publisher","first-page":"231","DOI":"10.1083\/jcb.200606027","article-title":"Novel cell death program leads to neutrophil extracellular traps","volume":"176","author":"Fuchs","year":"2007","journal-title":"J Cell Biol"},{"key":"ref10","doi-asserted-by":"publisher","first-page":"236","DOI":"10.3390\/cells11020236","article-title":"S100A8\/A9 is a marker for the release of neutrophil extracellular traps and induces neutrophil activation","volume":"11","author":"Sprenkeler","year":"2022","journal-title":"Cells"},{"key":"ref11","doi-asserted-by":"publisher","first-page":"1295","DOI":"10.1042\/cs20200531","article-title":"SARS-CoV2 may evade innate immune response, causing uncontrolled neutrophil extracellular traps formation and multi-organ failure","volume":"134","author":"Thierry","year":"2020","journal-title":"Clin Sci"},{"key":"ref12","doi-asserted-by":"publisher","first-page":"2942","DOI":"10.3390\/jcm9092942","article-title":"Neutrophil extracellular traps and by-products play a Key role in COVID-19: pathogenesis, risk factors, and therapy","volume":"9","author":"Thierry","year":"2020","journal-title":"J Clin Med"},{"key":"ref13","first-page":"646","article-title":"Free DNA in the serum of cancer patients and the effect of therapy","volume":"37","author":"Leon","year":"1977","journal-title":"Cancer Res"},{"key":"ref14","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1038\/nri.2017.21","article-title":"Mitochondrial DNA in innate immune responses and inflammatory pathology","volume":"17","author":"West","year":"2017","journal-title":"Nat Rev Immunol"},{"key":"ref15","doi-asserted-by":"publisher","first-page":"286","DOI":"10.1016\/j.jss.2014.06.003","article-title":"Blood transfusion products contain mitochondrial DNA damage-associated molecular patterns: a potential effector of transfusion-related acute lung injury","volume":"191","author":"Lee","year":"2014","journal-title":"J Surg Res"},{"key":"ref16","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1097\/ta.0000000000001421","article-title":"Potential contribution of mitochondrial DNA damage associated molecular patterns in transfusion products to the development of acute respiratory distress syndrome after multiple transfusions","volume":"82","author":"Simmons","year":"2017","journal-title":"J Trauma Acute Care Surg"},{"key":"ref17","doi-asserted-by":"publisher","first-page":"109","DOI":"10.1046\/j.1523-1755.61.s80.20.x","article-title":"Oxidative stress in hemodialysis patients: is NADPH oxidase complex the culprit?","volume":"61","author":"Morena","year":"2002","journal-title":"Kidney Int"},{"key":"ref18","doi-asserted-by":"publisher","first-page":"36","DOI":"10.1016\/j.cca.2019.02.022","article-title":"Myeloperoxidase - a bridge linking inflammation and oxidative stress with cardiovascular disease","volume":"493","author":"Ndrepepa","year":"2019","journal-title":"Clin Chim Acta"},{"key":"ref19","doi-asserted-by":"publisher","first-page":"107711","DOI":"10.1016\/j.pharmthera.2020.107711","article-title":"Myeloperoxidase: a versatile mediator of endothelial dysfunction and therapeutic target during cardiovascular disease","volume":"221","author":"Maiocchi","year":"2021","journal-title":"Pharmacol Ther"},{"key":"ref20","doi-asserted-by":"publisher","first-page":"231","DOI":"10.3390\/cells9010231","article-title":"Neutrophil extracellular traps and cardiovascular diseases: an update","volume":"9","author":"Bonaventura","year":"2020","journal-title":"Cells"},{"key":"ref21","doi-asserted-by":"publisher","first-page":"633","DOI":"10.1016\/j.freeradbiomed.2021.07.007","article-title":"Role of myeloperoxidase and oxidant formation in the extracellular environment in inflammation-induced tissue damage","volume":"172","author":"Hawkins","year":"2021","journal-title":"Free Radic Biol Med"},{"key":"ref22","doi-asserted-by":"publisher","first-page":"1095","DOI":"10.1016\/j.biocel.2008.01.004","article-title":"Human neutrophil elastase: mediator and therapeutic target in atherosclerosis","volume":"40","author":"Henriksen","year":"2008","journal-title":"Int J Biochem Cell Biol"},{"key":"ref23","doi-asserted-by":"publisher","first-page":"103826","DOI":"10.1016\/j.isci.2022.103826","article-title":"Association of neutrophil extracellular traps with the production of circulating DNA in patients with colorectal cancer","volume":"25","author":"Pastor","year":"2022","journal-title":"iScience"},{"key":"ref24","doi-asserted-by":"publisher","first-page":"429","DOI":"10.1124\/mol.113.089821","article-title":"Novel small molecule inhibitors of TLR7 and TLR9: mechanism of action and efficacy in vivo","volume":"85","author":"Lamphier","year":"2014","journal-title":"Mol Pharmacol"},{"key":"ref25","doi-asserted-by":"publisher","first-page":"805","DOI":"10.1002\/art.40452","article-title":"Review: cell death, nucleic acids, and immunity: inflammation beyond the grave","volume":"70","author":"Elkon","year":"2018","journal-title":"Arthritis Rheumatol"},{"key":"ref26","doi-asserted-by":"publisher","first-page":"2661","DOI":"10.1172\/jci61303","article-title":"Platelets induce neutrophil extracellular traps in transfusion-related acute lung injury","volume":"122","author":"Caudrillier","year":"2012","journal-title":"J Clin Invest"},{"key":"ref27","doi-asserted-by":"publisher","first-page":"1846","DOI":"10.1111\/all.14746","article-title":"Elastase and exacerbation of neutrophil innate immunity are involved in multi-visceral manifestations of COVID-19","volume":"76","author":"Gu\u00e9ant","year":"2021","journal-title":"Allergy"},{"key":"ref28","doi-asserted-by":"publisher","first-page":"135","DOI":"10.1186\/s13073-022-01125-8","article-title":"Neutrophil extracellular traps have auto-catabolic activity and produce mononucleosome-associated circulating DNA","volume":"14","author":"Pisareva","year":"2022","journal-title":"Genome Med"},{"key":"ref29","doi-asserted-by":"publisher","first-page":"e28209","DOI":"10.1002\/jmv.28209","article-title":"Persistence of neutrophil extracellular traps and anticardiolipin auto-antibodies in post-acute phase COVID-19 patients","volume":"95","author":"Pisareva","year":"2022","journal-title":"J Med Virol"},{"key":"ref30","doi-asserted-by":"publisher","first-page":"368504221110858","DOI":"10.1177\/00368504221110858","article-title":"Mortality and risk factors for COVID-19 in hemodialysis patients: a systematic review and meta-analysis","volume":"105","author":"Li","year":"2022","journal-title":"Sci Prog"},{"key":"ref31","doi-asserted-by":"publisher","first-page":"81","DOI":"10.1038\/s41581-020-00381-4","article-title":"The COVID-19 pandemic: consequences for nephrology","volume":"17","author":"Bruchfeld","year":"2021","journal-title":"Nat Rev Nephrol"},{"key":"ref32","doi-asserted-by":"publisher","first-page":"1178","DOI":"10.1134\/s0006297920100065","article-title":"NETosis: molecular mechanisms, role in physiology and pathology","volume":"85","author":"Vorobjeva","year":"2020","journal-title":"Biochemistry"},{"key":"ref33","doi-asserted-by":"publisher","first-page":"243","DOI":"10.5301\/jn.5000169","article-title":"Prognostic role of C-reactive protein and interleukin-6 in dialysis patients: a systematic review and meta-analysis","volume":"26","author":"Zhang","year":"2013","journal-title":"J Nephrol"},{"key":"ref34","doi-asserted-by":"publisher","first-page":"844","DOI":"10.3390\/biomedicines10040844","article-title":"Biocompatibility of surface-modified membranes for chronic hemodialysis therapy","volume":"10","author":"Bonomini","year":"2022","journal-title":"Biomedicine"},{"key":"ref35","doi-asserted-by":"publisher","first-page":"24","DOI":"10.1111\/j.1492-7535.2004.00083.x","article-title":"The \u201cunphysiology\u201d of dialysis: a major cause of dialysis side effects?","volume":"8","author":"Kjellstrand","year":"2004","journal-title":"Hemodial Int"},{"key":"ref36","doi-asserted-by":"publisher","first-page":"e0199204","DOI":"10.1371\/journal.pone.0199204","article-title":"Influence of citrate concentration on the activation of blood cells in an in vitro dialysis setup","volume":"13","author":"Gubensek","year":"2018","journal-title":"PLoS One"},{"key":"ref37","doi-asserted-by":"publisher","first-page":"i59","DOI":"10.1093\/ckj\/sfab185","article-title":"Blood-incompatibility in haemodialysis: alleviating inflammation and effects of coagulation","volume":"14","author":"Bowry","year":"2021","journal-title":"Clin Kidney J"},{"key":"ref38","doi-asserted-by":"publisher","first-page":"556","DOI":"10.5301\/jn.5000195","article-title":"Vitamin E-coated polysulfone membrane improved red blood cell antioxidant status in hemodialysis patients","volume":"26","author":"Bargnoux","year":"2013","journal-title":"J Nephrol"},{"key":"ref39","doi-asserted-by":"publisher","first-page":"403","DOI":"10.1111\/j.1542-4758.2010.00494.x","article-title":"Biocompatibility of heparin-grafted hemodialysis membranes: impact on monocyte chemoattractant protein-1 circulating level and oxidative status","volume":"14","author":"Morena","year":"2010","journal-title":"Hemodial Int"},{"key":"ref40","doi-asserted-by":"publisher","first-page":"937","DOI":"10.34067\/kid.0000302021","article-title":"Performance and hemocompatibility of a novel polysulfone dialyzer: a randomized controlled trial","volume":"2","author":"Ehlerding","year":"2021","journal-title":"Kidney"},{"key":"ref41","doi-asserted-by":"publisher","first-page":"363","DOI":"10.1161\/01.cir.0000053730.47739.3c","article-title":"Clinical application of C-reactive protein for cardiovascular disease detection and prevention","volume":"107","author":"Ridker","year":"2003","journal-title":"Circulation"},{"key":"ref42","doi-asserted-by":"publisher","first-page":"840","DOI":"10.1111\/j.1532-5415.2008.01677.x","article-title":"Biomarkers of inflammation and malnutrition associated with early death in healthy elderly people","volume":"56","author":"Carriere","year":"2008","journal-title":"J Am Geriatr Soc"},{"key":"ref43","doi-asserted-by":"publisher","first-page":"766","DOI":"10.1111\/j.1523-1755.2005.00455.x","article-title":"C-reactive protein and albumin as predictors of all-cause and cardiovascular mortality in chronic kidney disease","volume":"68","author":"Menon","year":"2005","journal-title":"Kidney Int"},{"key":"ref44","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1111\/j.1492-7535.2005.01127.x","article-title":"Association between novel indices of malnutrition-inflammation complex syndrome and cardiovascular disease in hemodialysis patients","volume":"9","author":"Terrier","year":"2005","journal-title":"Hemodial Int"},{"key":"ref45","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1161\/01.cir.0000042700.48769.59","article-title":"Elevations of inflammatory and procoagulant biomarkers in elderly persons with renal insufficiency","volume":"107","author":"Shlipak","year":"2003","journal-title":"Circulation"},{"key":"ref46","doi-asserted-by":"publisher","first-page":"6651367","DOI":"10.1155\/2021\/6651367","article-title":"Uremic toxins, oxidative stress, atherosclerosis in chronic kidney disease, and kidney transplantation","volume":"2021","author":"Wojtaszek","year":"2021","journal-title":"Oxidative Med Cell Longev"},{"key":"ref47","doi-asserted-by":"publisher","first-page":"481","DOI":"10.5301\/ijao.2011.8466","article-title":"Role of the hemodialysis vascular access type in inflammation status and monocyte activation","volume":"34","author":"Col\u00ec","year":"2011","journal-title":"Int J Artif Organs"},{"key":"ref48","doi-asserted-by":"publisher","first-page":"3805","DOI":"10.3390\/ijms20153805","article-title":"Periodontal disease in patients receiving dialysis","volume":"20","author":"Miyata","year":"2019","journal-title":"Int J Mol Sci"},{"key":"ref49","doi-asserted-by":"publisher","first-page":"423","DOI":"10.2215\/CJN.02010507","article-title":"Fine-tuning of the prediction of mortality in hemodialysis patients by use of cytokine proteomic determination","volume":"3","author":"Badiou","year":"2008","journal-title":"Clin J Am Soc Nephrol"},{"key":"ref50","doi-asserted-by":"publisher","first-page":"1495","DOI":"10.1016\/j.kint.2017.01.013","article-title":"Treatment tolerance and patient-reported outcomes favor online hemodiafiltration compared to high-flux hemodialysis in the elderly","volume":"91","author":"Morena","year":"2017","journal-title":"Kidney Int"},{"key":"ref52","doi-asserted-by":"publisher","first-page":"1972","DOI":"10.1046\/j.1523-1755.2001.00009.x","article-title":"Role of contact system activation in hemodialyzer-induced thrombogenicity","volume":"60","author":"Frank","year":"2001","journal-title":"Kidney Int"},{"key":"ref53","doi-asserted-by":"publisher","first-page":"607","DOI":"10.1016\/j.xkme.2021.04.006","article-title":"Hemodialysis-related complement and contact pathway activation and cardiovascular risk: a narrative review","volume":"3","author":"Skinner","year":"2021","journal-title":"Kidney Med"},{"key":"ref54","doi-asserted-by":"publisher","DOI":"10.26402\/jpp.2020.2.12","article-title":"The activation of complement system in different types of renal replacement therapy","volume":"71","author":"Stepniewska","year":"2020","journal-title":"J Physiol Pharmacol: Polish Physiol Society"},{"key":"ref51","doi-asserted-by":"publisher","first-page":"1155","DOI":"10.3390\/antiox10071155","article-title":"Oxidative stress in patients with advanced CKD and renal replacement therapy: the Key role of peripheral blood leukocytes","volume":"10","author":"Vida","year":"2021","journal-title":"Antioxidants"},{"key":"ref55","doi-asserted-by":"publisher","first-page":"388","DOI":"10.1111\/sdi.12686","article-title":"Does inflammation affect outcomes in dialysis patients?","volume":"31","author":"Nowak","year":"2018","journal-title":"Semin Dial"},{"key":"ref56","doi-asserted-by":"publisher","first-page":"569","DOI":"10.1111\/1744-9987.12454","article-title":"A prospective multicenter randomized controlled study on Interleukin-6 removal and induction by a new Hemodialyzer with improved biocompatibility in hemodialysis patients: a pilot study","volume":"20","author":"Kakuta","year":"2016","journal-title":"Ther Apher Dial"},{"key":"ref57","doi-asserted-by":"publisher","first-page":"1697","DOI":"10.1681\/ASN.V591697","article-title":"Polymorphonuclear leukocyte oxidative burst is enhanced in patients with chronic renal insufficiency","volume":"5","author":"Ward","year":"1994","journal-title":"J Am Soc Nephrol"},{"key":"ref58","doi-asserted-by":"publisher","first-page":"21747","DOI":"10.1038\/s41598-020-78742-z","article-title":"Enhanced neutrophil apoptosis accompanying myeloperoxidase release during hemodialysis","volume":"10","author":"Fukushi","year":"2020","journal-title":"Sci Rep"},{"key":"ref59","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1053\/j.ackd.2019.10.001","article-title":"The role of nonenzymatic post-translational protein modifications in uremic vascular calcification","volume":"26","author":"Lim","year":"2019","journal-title":"Adv Chronic Kidney Dis"},{"key":"ref60","doi-asserted-by":"publisher","first-page":"853","DOI":"10.1681\/asn.2012030254","article-title":"Protein carbamylation predicts mortality in ESRD","volume":"24","author":"Koeth","year":"2013","journal-title":"J Am Soc Nephrol"},{"key":"ref61","doi-asserted-by":"publisher","first-page":"228","DOI":"10.1016\/j.jprot.2013.02.015","article-title":"Usefulness of non-enzymatic post-translational modification derived products (PTMDPs) as biomarkers of chronic diseases","volume":"92","author":"Gillery","year":"2013","journal-title":"J Proteome"},{"key":"ref62","doi-asserted-by":"publisher","first-page":"574","DOI":"10.3390\/ijms23010574","article-title":"Carbamylated proteins in renal disease: aggravating factors or just biomarkers?","volume":"23","author":"Gorisse","year":"2022","journal-title":"Int J Mol Sci"},{"key":"ref63","doi-asserted-by":"publisher","first-page":"4524","DOI":"10.1016\/j.bbagen.2013.05.024","article-title":"The potentiation of myeloperoxidase activity by the glycosaminoglycan-dependent binding of myeloperoxidase to proteins of the extracellular matrix","volume":"1830","author":"Kubala","year":"2013","journal-title":"Biochim Biophys Acta"},{"key":"ref64","doi-asserted-by":"publisher","first-page":"410","DOI":"10.3390\/toxins10100410","article-title":"Urea memory: transient cell exposure to urea causes persistent mitochondrial ROS production and endothelial dysfunction","volume":"10","author":"d'Apolito","year":"2018","journal-title":"Toxins"},{"key":"ref65","doi-asserted-by":"publisher","first-page":"1595","DOI":"10.1056\/NEJMoa035003","article-title":"Prognostic value of myeloperoxidase in patients with chest pain","volume":"349","author":"Brennan","year":"2003","journal-title":"N Engl J Med"},{"key":"ref66","doi-asserted-by":"publisher","first-page":"59","DOI":"10.1053\/j.ajkd.2006.03.047","article-title":"Serum myeloperoxidase and mortality in maintenance hemodialysis patients","volume":"48","author":"Kalantar-Zadeh","year":"2006","journal-title":"Am J Kidney Dis"},{"key":"ref67","doi-asserted-by":"publisher","first-page":"369","DOI":"10.1007\/s00011-016-1010-6","article-title":"NETosis provides the link between activation of neutrophils on hemodialysis membrane and comorbidities in dialyzed patients","volume":"66","author":"Korabecna","year":"2017","journal-title":"Inflamm Res"},{"key":"ref68","doi-asserted-by":"publisher","first-page":"391","DOI":"10.21037\/atm.2019.07.57","article-title":"The effects of citrate dialysate in hemodialysis on polymorphonuclear elastase interaction with tissue factor and its inhibitor","volume":"7","author":"Li","year":"2019","journal-title":"Ann Transl Med"},{"key":"ref69","doi-asserted-by":"publisher","first-page":"F203","DOI":"10.1152\/ajprenal.00070.2017","article-title":"Free circulating active elastase contributes to chronic inflammation in patients on hemodialysis","volume":"314","author":"Khatib-Massalha","year":"2018","journal-title":"Am J Physiol Renal Physiol"},{"key":"ref70","doi-asserted-by":"publisher","first-page":"26","DOI":"10.1177\/039139880302600105","article-title":"Inflammatory response of a new synthetic dialyzer membrane. A randomised cross-over comparison between polysulfone and helixone","volume":"26","author":"Stefoni","year":"2003","journal-title":"Int J Artif Organs"},{"key":"ref71","doi-asserted-by":"publisher","first-page":"692","DOI":"10.1016\/j.xkme.2020.06.014","article-title":"Neutrophil activation and neutrophil extracellular trap formation in Dialysis patients","volume":"2","author":"Bieber","year":"2020","journal-title":"Kidney Med"},{"key":"ref72","doi-asserted-by":"publisher","first-page":"21439","DOI":"10.1038\/s41598-021-00863-w","article-title":"Uremic serum damages endothelium by provoking excessive neutrophil extracellular trap formation","volume":"11","author":"Lee","year":"2021","journal-title":"Sci Rep"},{"key":"ref73","doi-asserted-by":"publisher","first-page":"8415179","DOI":"10.1155\/2017\/8415179","article-title":"Increased neutrophil extracellular trap formation in uremia is associated with chronic inflammation and prevalent coronary artery disease","volume":"2017","author":"Kim","year":"2017","journal-title":"J Immunol Res"},{"key":"ref74","doi-asserted-by":"publisher","first-page":"364","DOI":"10.1186\/s12916-022-02564-1","article-title":"Neutrophil degranulation and severely impaired extracellular trap formation at the basis of susceptibility to infections of hemodialysis patients","volume":"20","author":"Talal","year":"2022","journal-title":"BMC Med"},{"key":"ref75","doi-asserted-by":"publisher","first-page":"1371","DOI":"10.1093\/ckj\/sfaa115","article-title":"Cell-free DNA as a marker for the outcome of end-stage renal disease patients on haemodialysis","volume":"14","author":"Coimbra","year":"2021","journal-title":"Clin Kidney J"},{"key":"ref76","doi-asserted-by":"publisher","first-page":"849","DOI":"10.1159\/000510772","article-title":"NET formation in Dialysis: a valuable, albeit mysterious and enticing predictor of mortality","volume":"51","author":"Goligorsky","year":"2020","journal-title":"Am J Nephrol"},{"key":"ref77","doi-asserted-by":"publisher","first-page":"475","DOI":"10.1080\/08860220902963673","article-title":"Cell-free plasma DNA during hemodialysis","volume":"31","author":"Opatrna","year":"2009","journal-title":"Ren Fail"},{"key":"ref78","doi-asserted-by":"publisher","first-page":"852","DOI":"10.1159\/000510771","article-title":"Elevated circulating cell-free DNA in hemodialysis-treated patients is associated with increased mortality","volume":"51","author":"Einbinder","year":"2020","journal-title":"Am J Nephrol"},{"key":"ref79","doi-asserted-by":"publisher","first-page":"100242","DOI":"10.1016\/j.xgen.2022.100242","article-title":"Circulating DNA fragmentomics and cancer screening","volume":"3","author":"Thierry","year":"2023","journal-title":"Cell Genomics"},{"key":"ref80","doi-asserted-by":"publisher","first-page":"i72","DOI":"10.1093\/ckj\/sfab192","article-title":"Multitargeted interventions to reduce dialysis-induced systemic stress","volume":"14","author":"Canaud","year":"2021","journal-title":"Clin Kidney J"},{"key":"ref81","doi-asserted-by":"publisher","first-page":"218","DOI":"10.1016\/j.thromres.2016.05.017","article-title":"Tissue factor expressed by adherent cells contributes to hemodialysis-membrane thrombogenicity","volume":"144","author":"Lakbakbi","year":"2016","journal-title":"Thromb Res"},{"key":"ref82","doi-asserted-by":"publisher","first-page":"2074","DOI":"10.1111\/jth.12710","article-title":"Activated platelets present high mobility group box 1 to neutrophils, inducing autophagy and promoting the extrusion of neutrophil extracellular traps","volume":"12","author":"Maugeri","year":"2014","journal-title":"J Thromb Haemost"},{"key":"ref83","doi-asserted-by":"publisher","first-page":"1078891","DOI":"10.3389\/fimmu.2022.1078891","article-title":"Impact of neutrophil extracellular traps on fluid properties, blood flow and complement activation","volume":"13","author":"Burmeister","year":"2022","journal-title":"Front Immunol"},{"key":"ref84","doi-asserted-by":"publisher","first-page":"1715","DOI":"10.3390\/diagnostics12071715","article-title":"Neutrophil extracellular traps and neutrophil-derived extracellular vesicles: common players in neutrophil effector functions","volume":"12","author":"Pfister","year":"2022","journal-title":"Diagnostics"},{"key":"ref85","doi-asserted-by":"publisher","first-page":"6438","DOI":"10.1038\/s41598-017-06893-7","article-title":"Tumor-derived exosomes induce the formation of neutrophil extracellular traps: implications for the establishment of Cancer-associated thrombosis","volume":"7","author":"Leal","year":"2017","journal-title":"Sci Rep"},{"key":"ref86","doi-asserted-by":"publisher","first-page":"4302096","DOI":"10.1155\/2018\/4302096","article-title":"Noncoding RNAs carried by extracellular vesicles in endocrine diseases","volume":"2018","author":"Pomatto","year":"2018","journal-title":"Int J Endocrinol"},{"key":"ref87","doi-asserted-by":"publisher","first-page":"11","DOI":"10.1007\/s12020-012-9839-0","article-title":"Extracellular vesicles as an emerging mechanism of cell-to-cell communication","volume":"44","author":"Tetta","year":"2013","journal-title":"Endocrine"},{"key":"ref88","doi-asserted-by":"publisher","first-page":"e13825","DOI":"10.14814\/phy2.13825","article-title":"Exercise during hemodialysis does not affect the phenotype or prothrombotic nature of microparticles but alters their proinflammatory function","volume":"6","author":"Martin","year":"2018","journal-title":"Physiol Rep"},{"key":"ref89","doi-asserted-by":"publisher","first-page":"e72663","DOI":"10.1371\/journal.pone.0072663","article-title":"Elevated levels of procoagulant plasma microvesicles in dialysis patients","volume":"8","author":"Burton","year":"2013","journal-title":"PLoS One"},{"key":"ref90","doi-asserted-by":"publisher","first-page":"64","DOI":"10.1159\/000440974","article-title":"Significance of the DNA-histone complex level as a predictor of major adverse cardiovascular events in hemodialysis patients: the effect of uremic toxin on DNA-histone complex formation","volume":"41","author":"Jeong","year":"2016","journal-title":"Blood Purif"},{"key":"ref91","doi-asserted-by":"publisher","first-page":"e1","DOI":"10.1017\/erm.2017.12","article-title":"Cell-free DNA: the role in pathophysiology and as a biomarker in kidney diseases","volume":"20","author":"Celec","year":"2018","journal-title":"Expert Rev Mol Med"},{"key":"ref92","doi-asserted-by":"publisher","first-page":"1069743","DOI":"10.1155\/2016\/1069743","article-title":"Role of myeloperoxidase in patients with chronic kidney disease","volume":"2016","author":"Kisic","year":"2016","journal-title":"Oxidative Med Cell Longev"},{"key":"ref93","doi-asserted-by":"publisher","first-page":"101080","DOI":"10.1016\/j.cpcardiol.2021.101080","article-title":"Myeloperoxidase is independently associated with incident heart failure in patients with coronary artery disease and kidney disease","volume":"47","author":"Janus","year":"2022","journal-title":"Curr Probl Cardiol"},{"key":"ref94","doi-asserted-by":"publisher","first-page":"189","DOI":"10.1016\/j.clim.2018.10.003","article-title":"The relationship between autophagy, increased neutrophil extracellular traps formation and endothelial dysfunction in chronic kidney disease","volume":"197","author":"Kim","year":"2018","journal-title":"Clin Immunol"},{"key":"ref95","doi-asserted-by":"publisher","first-page":"257","DOI":"10.1016\/j.blre.2015.12.004","article-title":"DAMP and DIC: the role of extracellular DNA and DNA-binding proteins in the pathogenesis of DIC","volume":"30","author":"Liaw","year":"2016","journal-title":"Blood Rev"},{"key":"ref96","doi-asserted-by":"publisher","first-page":"1078","DOI":"10.1055\/s-0038-1641749","article-title":"Neutrophil extracellular traps participate in all different types of thrombotic and haemorrhagic complications of coronary atherosclerosis","volume":"118","author":"Pertiwi","year":"2018","journal-title":"Thromb Haemost"},{"key":"ref97","doi-asserted-by":"publisher","first-page":"1777","DOI":"10.1161\/atvbaha.111.242859","article-title":"Neutrophil extracellular trap (NET) impact on deep vein thrombosis","volume":"32","author":"Fuchs","year":"2012","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"ref98","doi-asserted-by":"publisher","first-page":"14270","DOI":"10.1096\/fj.201901363RRR","article-title":"DNA-bound elastase of neutrophil extracellular traps degrades plasminogen, reduces plasmin formation, and decreases fibrinolysis: proof of concept in septic shock plasma","volume":"33","author":"Cruz","year":"2019","journal-title":"FASEB J"},{"key":"ref99","doi-asserted-by":"publisher","first-page":"105","DOI":"10.1159\/000245634","article-title":"Haemodialysis-induced myocardial stunning in chronic kidney disease - a new aspect of cardiovascular disease","volume":"29","author":"McIntyre","year":"2010","journal-title":"Blood Purif"},{"key":"ref100","doi-asserted-by":"publisher","first-page":"F445","DOI":"10.1152\/ajprenal.00368.2017","article-title":"Effect of isolated ultrafiltration and isovolemic dialysis on myocardial perfusion and left ventricular function assessed with (13) N-NH (3) positron emission tomography and echocardiography","volume":"314","author":"Assa","year":"2018","journal-title":"Am J Physiol Renal Physiol"},{"key":"ref101","doi-asserted-by":"publisher","first-page":"H500","DOI":"10.1152\/ajpheart.00381.2014","article-title":"Neutrophil extracellular traps in ischemia-reperfusion injury-induced myocardial no-reflow: therapeutic potential of DNase-based reperfusion strategy","volume":"308","author":"Ge","year":"2015","journal-title":"Am J Physiol Heart Circ Physiol"},{"key":"ref102","doi-asserted-by":"publisher","first-page":"1182","DOI":"10.1161\/circresaha.116.304944","article-title":"Coronary neutrophil extracellular trap burden and deoxyribonuclease activity in ST-elevation acute coronary syndrome are predictors of ST-segment resolution and infarct size","volume":"116","author":"Mangold","year":"2015","journal-title":"Circ Res"},{"key":"ref103","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1007\/s00395-019-0740-3","article-title":"Neutrophil extracellular traps and fibrocytes in ST-segment elevation myocardial infarction","volume":"114","author":"Hofbauer","year":"2019","journal-title":"Basic Res Cardiol"},{"key":"ref104","doi-asserted-by":"publisher","first-page":"11599","DOI":"10.1038\/s41598-019-47853-7","article-title":"Neutrophil extracellular traps and dsDNA predict outcomes among patients with ST-elevation myocardial infarction","volume":"9","author":"Liu","year":"2019","journal-title":"Sci Rep"},{"key":"ref105","doi-asserted-by":"publisher","first-page":"2032","DOI":"10.1161\/atvbaha.113.301627","article-title":"Elevated levels of circulating DNA and chromatin are independently associated with severe coronary atherosclerosis and a prothrombotic state","volume":"33","author":"Borissoff","year":"2013","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"ref106","doi-asserted-by":"publisher","first-page":"2182358","DOI":"10.1155\/2016\/2182358","article-title":"The time course of markers of neutrophil extracellular traps in patients undergoing revascularisation for acute myocardial infarction or stable angina pectoris","volume":"2016","author":"Helseth","year":"2016","journal-title":"Mediat Inflamm"},{"key":"ref107","doi-asserted-by":"publisher","first-page":"762","DOI":"10.1177\/2047487318760618","article-title":"Markers of neutrophil extracellular traps are associated with adverse clinical outcome in stable coronary artery disease","volume":"25","author":"Langseth","year":"2018","journal-title":"Eur J Prev Cardiol"},{"key":"ref108","doi-asserted-by":"publisher","first-page":"2634","DOI":"10.1046\/j.1523-1755.2000.00124.x","article-title":"Analysis of the effect of hemodialysis on peripheral and central arterial pressure waveforms","volume":"57","author":"Covic","year":"2000","journal-title":"Kidney Int"},{"key":"ref109","doi-asserted-by":"publisher","first-page":"1109","DOI":"10.1038\/ki.2015.62","article-title":"Ischemic brain injury in hemodialysis patients: which is more dangerous, hypertension or intradialytic hypotension?","volume":"87","author":"McIntyre","year":"2015","journal-title":"Kidney Int"},{"key":"ref110","doi-asserted-by":"publisher","first-page":"147","DOI":"10.1681\/asn.2018050462","article-title":"Investigating the relationship between cerebral blood flow and cognitive function in hemodialysis patients","volume":"30","author":"Findlay","year":"2019","journal-title":"J Am Soc Nephrol"},{"key":"ref111","doi-asserted-by":"publisher","first-page":"957","DOI":"10.1681\/asn.2013101086","article-title":"Randomized clinical trial of dialysate cooling and effects on brain white matter","volume":"26","author":"Eldehni","year":"2015","journal-title":"J Am Soc Nephrol"},{"key":"ref112","doi-asserted-by":"publisher","first-page":"e154225","DOI":"10.1172\/jci154225","article-title":"Neutrophil extracellular traps regulate ischemic stroke brain injury","volume":"132","author":"Denorme","year":"2022","journal-title":"J Clin Invest"},{"key":"ref113","doi-asserted-by":"publisher","first-page":"643","DOI":"10.1007\/s12035-021-02635-z","article-title":"Neutrophil extracellular traps exacerbate ischemic brain damage","volume":"59","author":"Li","year":"2022","journal-title":"Mol Neurobiol"},{"key":"ref114","doi-asserted-by":"publisher","first-page":"2488","DOI":"10.1038\/s41467-020-16191-y","article-title":"Neutrophil extracellular traps released by neutrophils impair revascularization and vascular remodeling after stroke","volume":"11","author":"Kang","year":"2020","journal-title":"Nat Commun"},{"key":"ref115","doi-asserted-by":"publisher","first-page":"133","DOI":"10.2215\/cjn.04610510","article-title":"Circulating endotoxemia: a novel factor in systemic inflammation and cardiovascular disease in chronic kidney disease","volume":"6","author":"McIntyre","year":"2011","journal-title":"Clin J Am Soc Nephrol"},{"key":"ref116","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1186\/s12882-020-01803-y","article-title":"Factors of microinflammation in non-diabetic chronic kidney disease: a pilot study","volume":"21","author":"Olivier","year":"2020","journal-title":"BMC Nephrol"},{"key":"ref117","doi-asserted-by":"publisher","first-page":"141","DOI":"10.1159\/000366519","article-title":"Circulating endotoxaemia and frequent haemodialysis schedules","volume":"128","author":"Jefferies","year":"2014","journal-title":"Nephron Clin Pract"},{"key":"ref118","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1186\/s13099-022-00497-x","article-title":"The emerging role of neutrophilic extracellular traps in intestinal disease","volume":"14","author":"Chen","year":"2022","journal-title":"Gut Pathog"},{"key":"ref119","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1002\/jlb.4a0119-009rr","article-title":"Mac-1 triggers neutrophil DNA extracellular trap formation to Aspergillus fumigatus independently of PAD4 histone citrullination","volume":"107","author":"Silva","year":"2020","journal-title":"J Leukoc Biol"},{"key":"ref120","doi-asserted-by":"publisher","first-page":"111482","DOI":"10.1016\/j.biopha.2021.111482","article-title":"Intestinal ischemic reperfusion injury: recommended rats model and comprehensive review for protective strategies","volume":"138","author":"Wang","year":"2021","journal-title":"Biomed Pharmacother"},{"key":"ref121","doi-asserted-by":"publisher","first-page":"1891","DOI":"10.1128\/iai.00050-12","article-title":"Afa\/Dr diffusely adhering Escherichia coli strain C1845 induces neutrophil extracellular traps that kill bacteria and damage human enterocyte-like cells","volume":"80","author":"Marin-Esteban","year":"2012","journal-title":"Infect Immun"}],"updated-by":[{"DOI":"10.3389\/fmed.2024.1393023","type":"corrigendum","label":"Corrigendum","source":"publisher","updated":{"date-parts":[[2024,3,12]],"date-time":"2024-03-12T00:00:00Z","timestamp":1710201600000}}],"container-title":["Frontiers in Medicine"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2023.1268748\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2024,3,12]],"date-time":"2024-03-12T16:20:39Z","timestamp":1710260439000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fmed.2023.1268748\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,15]]},"references-count":121,"alternative-id":["10.3389\/fmed.2023.1268748"],"URL":"https:\/\/doi.org\/10.3389\/fmed.2023.1268748","relation":{"corrigendum":[{"id-type":"doi","id":"10.3389\/fmed.2024.1393023","asserted-by":"object"}]},"ISSN":["2296-858X"],"issn-type":[{"value":"2296-858X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,15]]},"article-number":"1268748"}}