{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,2,21]],"date-time":"2025-02-21T14:05:54Z","timestamp":1740146754024,"version":"3.37.3"},"reference-count":45,"publisher":"Public Library of Science (PLoS)","issue":"4","license":[{"start":{"date-parts":[[2021,4,15]],"date-time":"2021-04-15T00:00:00Z","timestamp":1618444800000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Ascend Clinical"},{"DOI":"10.13039\/100000062","name":"National Institute of Diabetes and Digestive and Kidney Diseases","doi-asserted-by":"publisher","award":["5K23DK101826"],"award-info":[{"award-number":["5K23DK101826"]}],"id":[{"id":"10.13039\/100000062","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"abstract":"<jats:p>Patients on dialysis are at high risk for death due to COVID-19, yet a significant proportion do survive as evidenced by presence of SARS-CoV-2 antibodies in 8% of patients in the U.S. in July 2020. It is unclear whether patients with seropositivity represent the subgroup with robust health status, who would be more likely to mount a durable antibody response. Using data from a July 2020 sample of 28,503 patients receiving dialysis, we evaluated the cross-sectional association of SARS-CoV-2 seropositivity with laboratory surrogates of patient health. In separate logistic regression models, we assessed the association of SARS-CoV-2 seropositivity with seven laboratory-based covariates (albumin, creatinine, hemoglobin, sodium, potassium, phosphate, and parathyroid hormone), across the entire range of the laboratory and in comparison to a referent value. Models accounted for age, sex, region, race and ethnicity, and county-level COVID-19 deaths per 100,000. Odds of seropositivity for albumin 3 and 3.5 g\/dL were 2.1 (95% CI 1.9\u20132.3) and 1.3 (1.2\u20131.4) respectively, compared with 4 g\/dL. Odds of seropositivity for serum creatinine 5 and 8 mg\/dL were 1.8 (1.6\u20132.0) and 1.3 (1.2\u20131.4) respectively, compared with 12.5 mg\/dL. Lower values of hemoglobin, sodium, potassium, phosphate, and parathyroid hormone were associated with higher odds of seropositivity. Laboratory values associated with poorer health status and higher risk for mortality were also associated with higher likelihood of SARS-CoV-2 antibodies in patients receiving dialysis.<\/jats:p>","DOI":"10.1371\/journal.pone.0249466","type":"journal-article","created":{"date-parts":[[2021,4,15]],"date-time":"2021-04-15T19:02:21Z","timestamp":1618513341000},"page":"e0249466","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":1,"title":["Laboratory correlates of SARS-CoV-2 seropositivity in a nationwide sample of patients on dialysis in the U.S."],"prefix":"10.1371","volume":"16","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9892-8477","authenticated-orcid":true,"given":"Shuchi","family":"Anand","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria E.","family":"Montez-Rath","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5731-8974","authenticated-orcid":true,"given":"Jialin","family":"Han","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8482-8192","authenticated-orcid":true,"given":"Pablo","family":"Garcia","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julie","family":"Bozeman","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Russell","family":"Kerschmann","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Paul","family":"Beyer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Julie","family":"Parsonnet","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7599-0534","authenticated-orcid":true,"given":"Glenn M.","family":"Chertow","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2021,4,15]]},"reference":[{"key":"pone.0249466.ref001","unstructured":"Center for Medicare and Medicaid Services. Preliminary Medicare Covid-19 Data Snapshot. https:\/\/wwwcmsgov\/files\/document\/medicare-covid-19-data-snapshot-fact-sheetpdf. 2020. Epub July 17, 2020."},{"key":"pone.0249466.ref002","article-title":"COVID-19: Clinical course and outcomes of 36 maintenance hemodialysis patients from a single center in Spain","author":"M Goicoechea","year":"2020","journal-title":"Kidney Int"},{"key":"pone.0249466.ref003","article-title":"Risk Factors Associated With Mortality Among Patients With COVID-19 in Intensive Care Units in Lombardy","author":"G Grasselli","year":"2020","journal-title":"Italy. JAMA Intern Med"},{"key":"pone.0249466.ref004","doi-asserted-by":"crossref","unstructured":"Jager KJ, Kramer A, Chesnaye NC, Couchoud C, S\u00e1nchez-\u00c1lvarez JE, Garneata L, et al. 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Management of hemodialysis patients with suspected or confirmed COVID-19 infection: perspective from the Spanish Nephrology. 2020."},{"key":"pone.0249466.ref006","article-title":"Coronavirus Disease 2019 in Patients with End-Stage Kidney Disease on Hemodialysis in Guatemala","author":"R Sosa","year":"2021","journal-title":"Kidney International Reports"},{"key":"pone.0249466.ref007","article-title":"Outcomes of patients with end-stage kidney disease hospitalized with COVID-19","author":"JH Ng","year":"2020","journal-title":"Kidney Int"},{"key":"pone.0249466.ref008","article-title":"Characteristics and Outcomes of Individuals With Pre-existing Kidney Disease and COVID-19 Admitted to Intensive Care Units in the United States","author":"JE Flythe","year":"2020","journal-title":"Am J Kidney Dis"},{"key":"pone.0249466.ref009","article-title":"A report from the Brescia Renal COVID Task Force on the clinical characteristics and short-term outcome of hemodialysis patients with SARS-CoV-2 infection","author":"F Alberici","year":"2020","journal-title":"Kidney Int"},{"issue":"10247","key":"pone.0249466.ref010","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/S0140-6736(20)31304-0","article-title":"Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a population-based study","volume":"396","author":"S Stringhini","year":"2020","journal-title":"Lancet"},{"key":"pone.0249466.ref011","unstructured":"Centers for Disease Control and Prevention. 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EUA Authorized Serology Test Performance. https:\/\/wwwfdagov\/medical-devices\/coronavirus-disease-2019-covid-19-emergency-use-authorizations-medical-devices\/eua-authorized-serology-test-performance. 2020."},{"issue":"8","key":"pone.0249466.ref024","doi-asserted-by":"crossref","first-page":"2208","DOI":"10.1097\/01.ASN.0000133041.27682.A2","article-title":"Mineral metabolism, mortality, and morbidity in maintenance hemodialysis","volume":"15","author":"GA Block","year":"2004","journal-title":"J Am Soc Nephrol"},{"issue":"6","key":"pone.0249466.ref025","doi-asserted-by":"crossref","first-page":"997","DOI":"10.1053\/ajkd.1998.v31.pm9631845","article-title":"Simple nutritional indicators as independent predictors of mortality in hemodialysis patients","volume":"31","author":"SF Leavey","year":"1998","journal-title":"Am J Kidney Dis"},{"issue":"14","key":"pone.0249466.ref026","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1056\/NEJM199309303291404","article-title":"The urea 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