{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,8,15]],"date-time":"2025-08-15T01:29:37Z","timestamp":1755221377216,"version":"3.43.0"},"reference-count":53,"publisher":"Wiley","issue":"13-14","license":[{"start":{"date-parts":[[2026,6,10]],"date-time":"2026-06-10T00:00:00Z","timestamp":1781049600000},"content-version":"am","delay-in-days":374,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#am"},{"start":{"date-parts":[[2025,6,10]],"date-time":"2025-06-10T00:00:00Z","timestamp":1749513600000},"content-version":"vor","delay-in-days":9,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/100000060","name":"National Institute of Allergy and Infectious Diseases","doi-asserted-by":"publisher","award":["UM1AI068616","UM1AI068632","UM1AI068635","UM1AI106716"],"award-info":[{"award-number":["UM1AI068616","UM1AI068632","UM1AI068635","UM1AI106716"]}],"id":[{"id":"10.13039\/100000060","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"National Science Foundation","doi-asserted-by":"publisher","award":["DGE\u20102140004"],"award-info":[{"award-number":["DGE\u20102140004"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100017973","name":"International Maternal Pediatric Adolescent AIDS Clinical Trials Network","doi-asserted-by":"publisher","award":["U01AI068632"],"award-info":[{"award-number":["U01AI068632"]}],"id":[{"id":"10.13039\/100017973","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Statistics in Medicine"],"published-print":{"date-parts":[[2025,6]]},"abstract":"<jats:title>ABSTRACT<\/jats:title><jats:p>Adjustment for prognostic baseline variables can reduce bias due to covariate imbalance and increase efficiency in randomized trials. While the use of covariate adjustment in late\u2010phase trials is justified by favorable large\u2010sample properties, it is seldom used in small, early\u2010phase studies, due to uncertainty in which variables are prognostic and the potential for precision loss, type I error rate inflation, and undercoverage of confidence intervals. To address this problem, we consider adjustment for a valid negative control outcome (NCO), or an auxiliary post\u2010randomization outcome believed to be completely unaffected by treatment but more highly correlated with the primary outcome than baseline covariates. We articulate the assumptions that permit adjustment for NCOs without producing post\u2010randomization selection bias, and describe plausible data\u2010generating models where NCO adjustment can improve upon adjustment for baseline covariates alone. In numerical experiments, we illustrate performance and provide practical recommendations regarding model selection and finite\u2010sample variance corrections. We apply our methods to the reanalysis of two early\u2010phase vaccine trials in HIV exposed uninfected (HEU) infants, where we demonstrate that adjustment for auxiliary post\u2010baseline immunological parameters can enhance the precision of vaccine effect estimates relative to standard approaches that avoid adjustment or adjust for baseline covariates alone.<\/jats:p>","DOI":"10.1002\/sim.70142","type":"journal-article","created":{"date-parts":[[2025,6,10]],"date-time":"2025-06-10T09:09:26Z","timestamp":1749546566000},"update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Negative Control Outcome Adjustment in Early\u2010Phase Randomized Trials: Estimating Vaccine Effects on Immune Responses in HIV Exposed Uninfected Infants"],"prefix":"10.1002","volume":"44","author":[{"ORCID":"https:\/\/orcid.org\/0009-0001-3713-4489","authenticated-orcid":false,"given":"Ethan","family":"Ashby","sequence":"first","affiliation":[{"name":"Department of Biostatistics University of Washington  Seattle WA USA"},{"name":"Vaccine and Infectious Disease Division Fred Hutchinson Cancer Research Center  Seattle WA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4381-1124","authenticated-orcid":false,"given":"Bo","family":"Zhang","sequence":"additional","affiliation":[{"name":"Vaccine and Infectious Disease Division Fred Hutchinson Cancer Research Center  Seattle WA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0009-0005-8094-9332","authenticated-orcid":false,"given":"Genevieve G.","family":"Fouda","sequence":"additional","affiliation":[{"name":"Department of Pediatrics Weill Cornell Medicine  New York NY USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4230-6863","authenticated-orcid":false,"given":"Youyi","family":"Fong","sequence":"additional","affiliation":[{"name":"Vaccine and Infectious Disease Division Fred Hutchinson Cancer Research Center  Seattle WA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3237-984X","authenticated-orcid":false,"given":"Holly","family":"Janes","sequence":"additional","affiliation":[{"name":"Vaccine and Infectious Disease Division Fred Hutchinson Cancer Research Center  Seattle WA USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"311","published-online":{"date-parts":[[2025,6,10]]},"reference":[{"key":"e_1_2_12_2_1","unstructured":"Joint United Nations Programme on HIV and AIDS (UNAIDS) \u201cFact Sheet 2024 \u2010 Latest Global and Regional HIV Statistics on the Status of the AIDS Epidemic \u201d(2024) accessed June 3 2025 https:\/\/www.unaids.org\/sites\/default\/files\/media_asset\/UNAIDS_FactSheet_en.pdf."},{"key":"e_1_2_12_3_1","doi-asserted-by":"publisher","DOI":"10.1001\/jama.282.8.744"},{"key":"e_1_2_12_4_1","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/174.4.722"},{"key":"e_1_2_12_5_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1008983"},{"key":"e_1_2_12_6_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2019.11.011"},{"key":"e_1_2_12_7_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cell.2016.05.055"},{"key":"e_1_2_12_8_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1541-0420.2006.00569.x"},{"key":"e_1_2_12_9_1","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jiu444"},{"key":"e_1_2_12_10_1","doi-asserted-by":"publisher","DOI":"10.1002\/sim.3113"},{"key":"e_1_2_12_11_1","doi-asserted-by":"publisher","DOI":"10.1080\/01621459.2022.2049278"},{"key":"e_1_2_12_12_1","doi-asserted-by":"publisher","DOI":"10.1186\/s13063-022-06967-6"},{"key":"e_1_2_12_13_1","doi-asserted-by":"publisher","DOI":"10.1186\/1745\u20106215\u201015\u2010139"},{"key":"e_1_2_12_14_1","doi-asserted-by":"publisher","DOI":"10.1177\/1740774524125156"},{"key":"e_1_2_12_15_1","unstructured":"US Food and Drug Administration (FDA) \u201cAdjusting for Covariates in Randomized Clinical Trials for Drugs and Biological Products: Guidance for Industry\u201d(2023)."},{"key":"e_1_2_12_16_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2016.09.053"},{"key":"e_1_2_12_17_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.ebiom.2022.104271"},{"key":"e_1_2_12_18_1","doi-asserted-by":"publisher","DOI":"10.3390\/v16091365"},{"key":"e_1_2_12_19_1","doi-asserted-by":"publisher","DOI":"10.1186\/s12879\u2010019\u20104049\u20105"},{"key":"e_1_2_12_20_1","doi-asserted-by":"publisher","DOI":"10.1093\/infdis\/jiu279"},{"issue":"5","key":"e_1_2_12_21_1","first-page":"656","article-title":"The Consequences of Adjustment for a Concomitant Variable That has Been Affected by the Treatment","volume":"147","author":"Rosenbaum P.","year":"1984","journal-title":"Journal of the Royal Statistical Society. Series B, Statistical Methodology"},{"key":"e_1_2_12_22_1","doi-asserted-by":"publisher","DOI":"10.1097\/EDE.0b013e3181d61eeb"},{"key":"e_1_2_12_23_1","doi-asserted-by":"publisher","DOI":"10.1007\/s40471\u2010020\u201000243\u20104"},{"key":"e_1_2_12_24_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1541-0420.2007.00976.x"},{"key":"e_1_2_12_25_1","doi-asserted-by":"publisher","DOI":"10.2307\/2287653"},{"key":"e_1_2_12_26_1","doi-asserted-by":"publisher","DOI":"10.1093\/oxfordjournals.epirev.a017990"},{"key":"e_1_2_12_27_1","doi-asserted-by":"publisher","DOI":"10.1093\/biomet\/70.1.41"},{"key":"e_1_2_12_28_1","doi-asserted-by":"publisher","DOI":"10.1214\/aos\/1176344064"},{"key":"e_1_2_12_29_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.vaccine.2018.07.048"},{"key":"e_1_2_12_30_1","doi-asserted-by":"publisher","DOI":"10.1080\/14760584.2020.1749597"},{"key":"e_1_2_12_31_1","doi-asserted-by":"publisher","DOI":"10.1093\/biomet\/asad036"},{"key":"e_1_2_12_32_1","doi-asserted-by":"crossref","unstructured":"M.Bannick J.Shao J.Liu Y.Du Y.Yi andT.Ye \u201cA General Form of Covariate Adjustment in Randomized Clinical Trials \u201d2023.","DOI":"10.32614\/CRAN.package.RobinCar"},{"key":"e_1_2_12_33_1","doi-asserted-by":"publisher","DOI":"10.1016\/0304-4076(85)90158-7"},{"key":"e_1_2_12_34_1","doi-asserted-by":"publisher","DOI":"10.1093\/jnci\/djz222"},{"key":"e_1_2_12_35_1","doi-asserted-by":"publisher","DOI":"10.1001\/jamanetworkopen.2025.12763"},{"key":"e_1_2_12_36_1","doi-asserted-by":"publisher","DOI":"10.1086\/498163"},{"key":"e_1_2_12_37_1","doi-asserted-by":"publisher","DOI":"10.1097\/01.aids.0000237363.33994.45"},{"key":"e_1_2_12_38_1","doi-asserted-by":"publisher","DOI":"10.3389\/fimmu.2019.02806"},{"key":"e_1_2_12_39_1","doi-asserted-by":"publisher","DOI":"10.1093\/jrsssb\/qkad080"},{"key":"e_1_2_12_40_1","first-page":"465","article-title":"Sur Les Applications de la Theorie des Probabilites Aux Experiences Agricoles: Essai des Principes","volume":"5","author":"Neyman J.","year":"1921","journal-title":"Statistical Science"},{"key":"e_1_2_12_41_1","doi-asserted-by":"publisher","DOI":"10.1214\/12-AOAS583"},{"key":"e_1_2_12_42_1","doi-asserted-by":"publisher","DOI":"10.1214\/ss\/1042727942"},{"key":"e_1_2_12_43_1","doi-asserted-by":"publisher","DOI":"10.1016\/0197-2456(93)90225-3"},{"key":"e_1_2_12_44_1","doi-asserted-by":"publisher","DOI":"10.1093\/biomet\/75.1.57"},{"key":"e_1_2_12_45_1","doi-asserted-by":"publisher","DOI":"10.1080\/01621459.1990.10475316"},{"key":"e_1_2_12_46_1","doi-asserted-by":"publisher","DOI":"10.1214\/13-AOAS679"},{"key":"e_1_2_12_47_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.jeconom.2021.04.007"},{"key":"e_1_2_12_48_1","doi-asserted-by":"publisher","DOI":"10.1097\/01.qai.0000435600.65845.31"},{"key":"e_1_2_12_49_1","doi-asserted-by":"publisher","DOI":"10.1056\/NEJMoa0908492"},{"key":"e_1_2_12_50_1","doi-asserted-by":"publisher","DOI":"10.1086\/323994"},{"key":"e_1_2_12_51_1","doi-asserted-by":"publisher","DOI":"10.1111\/rssa.12915"},{"key":"e_1_2_12_52_1","unstructured":"K.Van Lancker I.D\u00edaz andS.Vansteelandt \u201cAutomated Efficient and Model\u2010Free Inference for Randomized Clinical Trials via Data\u2010Driven Covariate Adjustment. Version Number: 1 \u201d2024."},{"key":"e_1_2_12_53_1","doi-asserted-by":"publisher","DOI":"10.1515\/scid-2024-0001"},{"key":"e_1_2_12_54_1","doi-asserted-by":"publisher","DOI":"10.1111\/biom.13663"}],"container-title":["Statistics in Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/am-pdf\/10.1002\/sim.70142","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1002\/sim.70142","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,8,8]],"date-time":"2025-08-08T16:47:00Z","timestamp":1754671620000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1002\/sim.70142"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,6]]},"references-count":53,"journal-issue":{"issue":"13-14","published-print":{"date-parts":[[2025,6]]}},"alternative-id":["10.1002\/sim.70142"],"URL":"https:\/\/doi.org\/10.1002\/sim.70142","archive":["Portico"],"relation":{},"ISSN":["0277-6715","1097-0258"],"issn-type":[{"type":"print","value":"0277-6715"},{"type":"electronic","value":"1097-0258"}],"subject":[],"published":{"date-parts":[[2025,6]]},"assertion":[{"value":"2024-10-01","order":0,"name":"received","label":"Received","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-05-16","order":2,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2025-06-10","order":3,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}],"article-number":"e70142"}}