{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,8,31]],"date-time":"2026-08-31T23:09:39Z","timestamp":1788217779736,"version":"build-2803163510"},"reference-count":52,"publisher":"Wiley","issue":"5","license":[{"start":{"date-parts":[[2023,8,5]],"date-time":"2023-08-05T00:00:00Z","timestamp":1691193600000},"content-version":"am","delay-in-days":355,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#am"},{"start":{"date-parts":[[2022,8,15]],"date-time":"2022-08-15T00:00:00Z","timestamp":1660521600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/100000005","name":"U.S. Department of Defense","doi-asserted-by":"publisher","award":["PR170067"],"award-info":[{"award-number":["PR170067"]}],"id":[{"id":"10.13039\/100000005","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000738","name":"U.S. Department of Veterans Affairs","doi-asserted-by":"publisher","award":["1I01BX004281"],"award-info":[{"award-number":["1I01BX004281"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000738","name":"U.S. Department of Veterans Affairs","doi-asserted-by":"publisher","award":["5I01BX005428"],"award-info":[{"award-number":["5I01BX005428"]}],"id":[{"id":"10.13039\/100000738","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000041","name":"American Diabetes Association","doi-asserted-by":"publisher","award":["7\u201020\u2010COVID\u2010149"],"award-info":[{"award-number":["7\u201020\u2010COVID\u2010149"]}],"id":[{"id":"10.13039\/100000041","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["R21AI157909"],"award-info":[{"award-number":["R21AI157909"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000049","name":"National Institute on Aging","doi-asserted-by":"publisher","award":["R15AG069544"],"award-info":[{"award-number":["R15AG069544"]}],"id":[{"id":"10.13039\/100000049","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000049","name":"National Institute on Aging","doi-asserted-by":"publisher","award":["R15AG076370"],"award-info":[{"award-number":["R15AG076370"]}],"id":[{"id":"10.13039\/100000049","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Proteomics Clinical Apps"],"published-print":{"date-parts":[[2022,9]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background<\/jats:title><jats:p>While the majority of COVID\u201019 patients fully recover from the infection and become asymptomatic, a significant proportion of COVID\u201019 survivors experience a broad spectrum of symptoms lasting weeks to months post\u2010infection, a phenomenon termed \u201cpost\u2010acute sequelae of COVID\u201019 (PASC).\u201d The aim of this study is to determine whether inflammatory proteins are dysregulated and can serve as potential biomarkers for systemic inflammation in COVID\u201019 survivors.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We determined the levels of inflammatory proteins in plasma from 22 coronavirus disease 2019 (COVID\u201019) long haulers (COV\u2010LH), 22 COVID\u201019 asymptomatic survivors (COV\u2010AS), and 22 healthy subjects (HS) using an Olink proteomics assay and assessed the results by a beads\u2010based multiplex immunoassay.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>Compared to HS, we found that COVID\u201019 survivors still exhibited systemic inflammation, as evidenced by significant changes in the levels of multiple inflammatory proteins in plasma from both COV\u2010LH and COV\u2010AS. CXCL10 was the only protein that significantly upregulated in COV\u2010LH compared with COV\u2010AS and HS.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>Our results indicate that several inflammatory proteins remain aberrantly dysregulated in COVID\u201019 survivors and CXCL10 might serve as a potential biomarker to typify COV\u2010LH. Further characterization of these signature inflammatory molecules might improve the understanding of the long\u2010term impacts of COVID\u201019 and provide new targets for the diagnosis and treatment of COVID\u201019 survivors with PASC.<\/jats:p><\/jats:sec>","DOI":"10.1002\/prca.202200031","type":"journal-article","created":{"date-parts":[[2022,8,5]],"date-time":"2022-08-05T13:53:32Z","timestamp":1659707612000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":39,"title":["Plasma biomarkers for systemic inflammation in COVID\u201019 survivors"],"prefix":"10.1002","volume":"16","author":[{"given":"Juan","family":"Zhao","sequence":"first","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Madison","family":"Schank","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ling","family":"Wang","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xindi","family":"Dang","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dechao","family":"Cao","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sushant","family":"Khanal","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lam N.T.","family":"Nguyen","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yi","family":"Zhang","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiao Y.","family":"Wu","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"James L.","family":"Adkins","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin J.","family":"Pelton","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jinyu","family":"Zhang","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shunbin","family":"Ning","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed El","family":"Gazzar","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jonathan P.","family":"Moorman","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"},{"name":"Hepatitis (HCV\/HBV) and HIV Programs James H. Quillen VA Medical Center, Department of Veterans Affairs  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-1848-1071","authenticated-orcid":false,"given":"Zhi Q.","family":"Yao","sequence":"additional","affiliation":[{"name":"Center of Excellence for Inflammation Infectious Disease and Immunity James H. Quillen College of Medicine East Tennessee State University  Johnson City Tennessee USA"},{"name":"Division of Infectious Inflammatory and Immunologic Diseases Department of Internal Medicine Quillen College of Medicine ETSU  Johnson City Tennessee USA"},{"name":"Hepatitis (HCV\/HBV) and HIV Programs James H. Quillen VA Medical Center, Department of Veterans Affairs  Johnson City Tennessee USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2022,8,15]]},"reference":[{"key":"e_1_2_10_2_1","unstructured":"World Health Organization. (2022).Coronavirus disease (COVID\u20102019) situation reports. Retrieved June 8 2022 fromhttps:\/\/www.who.int\/emergencies\/diseases\/novel\u2010coronavirus\u20102019\/situation\u2010reports"},{"key":"e_1_2_10_3_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41586\u2010021\u201003553\u20109"},{"key":"e_1_2_10_4_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0140\u20106736(20)32662\u20103"},{"key":"e_1_2_10_5_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41591\u2010020\u201001177\u20106"},{"key":"e_1_2_10_6_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pmed.1003773"},{"key":"e_1_2_10_7_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41590\u2010021\u201001104\u2010y"},{"key":"e_1_2_10_8_1","unstructured":"COVID\u201019 rapid guideline: Managing the long\u2010term effects of COVID\u201019. London: National Institute for Health and Care Excellence (NICE); (2020)https:\/\/www.ncbi.nlm.nih.gov\/books\/NBK567261\/"},{"key":"e_1_2_10_9_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41577\u2010020\u20100331\u20104"},{"key":"e_1_2_10_10_1","doi-asserted-by":"publisher","DOI":"10.1002\/jmv.26097"},{"key":"e_1_2_10_11_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41591\u2010020\u20101051\u20109"},{"key":"e_1_2_10_12_1","doi-asserted-by":"publisher","DOI":"10.1093\/ofid\/ofab156"},{"key":"e_1_2_10_13_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.709759"},{"key":"e_1_2_10_14_1","doi-asserted-by":"publisher","DOI":"10.1136\/thoraxjnl\u20102020\u2010215818"},{"key":"e_1_2_10_15_1","doi-asserted-by":"publisher","DOI":"10.3390\/jpm11030227"},{"key":"e_1_2_10_16_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598\u2010021\u201098253\u20109"},{"key":"e_1_2_10_17_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0253894"},{"key":"e_1_2_10_18_1","doi-asserted-by":"publisher","DOI":"10.26508\/lsa.202101099"},{"key":"e_1_2_10_19_1","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jiab181"},{"key":"e_1_2_10_20_1","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jproteome.1c00863"},{"key":"e_1_2_10_21_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.virusres.2021.198508"},{"key":"e_1_2_10_22_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0095192"},{"key":"e_1_2_10_23_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.693462"},{"key":"e_1_2_10_24_1","doi-asserted-by":"publisher","DOI":"10.1002\/eji.202149535"},{"key":"e_1_2_10_25_1","doi-asserted-by":"publisher","DOI":"10.3389\/fpubh.2021.732787"},{"key":"e_1_2_10_26_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.virusres.2021.198508"},{"key":"e_1_2_10_27_1","doi-asserted-by":"publisher","DOI":"10.1021\/acs.jproteome.0c00641"},{"key":"e_1_2_10_28_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598\u2010021\u201001943\u20107"},{"key":"e_1_2_10_29_1","doi-asserted-by":"publisher","DOI":"10.3390\/v13061062"},{"key":"e_1_2_10_30_1","doi-asserted-by":"publisher","DOI":"10.1097\/MD.0000000000024321"},{"key":"e_1_2_10_31_1","doi-asserted-by":"publisher","DOI":"10.1172\/jci.insight.155055"},{"key":"e_1_2_10_32_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598\u2010020\u201077525\u2010w"},{"key":"e_1_2_10_33_1","doi-asserted-by":"publisher","DOI":"10.1165\/rcmb.2021\u20100358OC"},{"key":"e_1_2_10_34_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cellsig.2020.109859"},{"key":"e_1_2_10_35_1","doi-asserted-by":"publisher","DOI":"10.3892\/br.2020.1282"},{"key":"e_1_2_10_36_1","doi-asserted-by":"publisher","DOI":"10.3390\/ijms20010189"},{"key":"e_1_2_10_37_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ajpath.2014.08.025"},{"key":"e_1_2_10_38_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cmet.2020.01.009"},{"key":"e_1_2_10_39_1","doi-asserted-by":"publisher","DOI":"10.1080\/15384101.2016.1151581"},{"key":"e_1_2_10_40_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ebiom.2021.103317"},{"key":"e_1_2_10_41_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41587\u2010020\u20100602\u20104"},{"key":"e_1_2_10_42_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cytogfr.2020.12.005"},{"key":"e_1_2_10_43_1","doi-asserted-by":"publisher","DOI":"10.1186\/s10020\u2010021\u201000390\u20104"},{"key":"e_1_2_10_44_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00705\u2010021\u201005247\u2010z"},{"key":"e_1_2_10_45_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2021.668507"},{"key":"e_1_2_10_46_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cytogfr.2011.06.001"},{"key":"e_1_2_10_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cyto.2018.11.018"},{"key":"e_1_2_10_48_1","doi-asserted-by":"publisher","DOI":"10.1097\/QAD.0000000000000174"},{"key":"e_1_2_10_49_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1005774"},{"key":"e_1_2_10_50_1","doi-asserted-by":"publisher","DOI":"10.1038\/s41598\u2010019\u201054803\u2010w"},{"key":"e_1_2_10_51_1","doi-asserted-by":"publisher","DOI":"10.1097\/TP.0000000000001065"},{"key":"e_1_2_10_52_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0034942"},{"key":"e_1_2_10_53_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jhep.2014.05.026"}],"container-title":["PROTEOMICS \u2013 Clinical Applications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/prca.202200031","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/full-xml\/10.1002\/prca.202200031","content-type":"application\/xml","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/am-pdf\/10.1002\/prca.202200031","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/prca.202200031","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,8,23]],"date-time":"2023-08-23T06:55:34Z","timestamp":1692773734000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/prca.202200031"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,15]]},"references-count":52,"journal-issue":{"issue":"5","published-print":{"date-parts":[[2022,9]]}},"alternative-id":["10.1002\/prca.202200031"],"URL":"https:\/\/doi.org\/10.1002\/prca.202200031","archive":["Portico"],"relation":{},"ISSN":["1862-8346","1862-8354"],"issn-type":[{"value":"1862-8346","type":"print"},{"value":"1862-8354","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,15]]},"assertion":[{"value":"2022-05-17","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-08-03","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2022-08-15","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"2200031"}}