Delayed Mortality Among Solid Organ Transplant Recipients Hospitalized for COVID-19

doi:10.1093/cid/ciac159

Delayed Mortality Among Solid Organ Transplant Recipients Hospitalized for COVID-19

Surgery

Research output: Contribution to journal › Article › peer-review

4 Scopus citations

Abstract

Background. Most studies of solid organ transplant (SOT) recipients with coronavirus disease 2019 (COVID-19) focus on outcomes within 1 month of illness onset. Delayed mortality in SOT recipients hospitalized for COVID-19 has not been fully examined. Methods. We used data from a multicenter registry to calculate mortality by 90 days following initial acute respiratory syndrome coronavirus 2 (SARS-CoV-2) detection in SOT recipients hospitalized for COVID-19 and developed multivariable Cox proportional hazards models to compare risk factors for death by days 28 and 90. Results. Vital status at day 90 was available for 936 of 1117 (84%) SOT recipients hospitalized for COVID-19; 190 of 936 (20%) died by 28 days, and an additional 56 of 246 deaths (23%) occurred between days 29 and 90. Factors associated with mortality by day 90 included age >65 years (adjusted hazard ratio [aHR], 1.8 [1.3–2.4]; P <.001), lung transplant (vs nonlung transplant; aHR, 1.5 [1.0–2.3]; P = .05), heart failure (aHR, 1.9 [1.2–2.9]; P = .006), chronic lung disease (aHR, 2.3 [1.5–3.6]; P < .001), and body mass index ≥30 kg/m² (aHR, 1.5 [1.1–2.0]; P = .02). These associations were similar for mortality by day 28. Compared with diagnosis during early 2020 (1 March 2020–19 June 2020), diagnosis during late 2020 (20 June 2020–31 December 2020) was associated with lower mortality by day 28 (aHR, 0.7 [0.5–1.0]; P = .04) but not by day 90 (aHR, 0.9 [0.7–1.3]; P = .61). Conclusions. In SOT recipients hospitalized for COVID-19, >20% of deaths occurred between 28 and 90 days following SARSCoV-2 diagnosis. Future investigations should consider extending follow-up duration to 90 days for more complete mortality assessment.

Original language	English
Pages (from-to)	711-718
Number of pages	8
Journal	Clinical Infectious Diseases
Volume	78
Issue number	3
DOIs	https://doi.org/10.1093/cid/ciac159
State	Published - Mar 15 2024

Bibliographical note

Publisher Copyright:
© The Author(s) 2022. Published by Oxford University Press for the Infectious Diseases Society of America. All rights reserved.

Funding

Potential conflicts of interest. M. R. H. reports speaking honoraria from Cigna LifeSource and Thermo Fisher Scientific. O. S. K. reports an AST PSECOP PILOT grant outside of the submitted work, speaking honoraria from the Canadian Society of Transplantation and the American Foundation of Donation and Transplantation, a consulting fee from Bennett Jones, LLP, outside of the submitted work and AST ID COP Executive Committee. C. N. K. reports grants or contracts from Regeneron, Beigene, and the Mendez Foundation; consulting fees from Exevir; and is a participant in the data safety monitory board (DSBA) or advisory bord of Beigene. B. D. A. reports consulting fees from Scynexis; served as a site investigator for clinical trials for Scynexis, Cidara, Shire, F2G, Amplyx, and Astellas; royalties or licenses from UpToDate; and is on the Infectious Diseases Society of America (IDSA) Board of Directors. E. A. B. reports research funding from Regeneron for mAb for coronavirus disease 2019 (COVID), Merck letermovir for CMV prophylaxis, Takeda maribavir for CMV treatment, and Hologix for CMV testing unrelated the current work; honoraria from the American Society of Nephrology and UpToDate Section Editor (transplant); served on the DSMB for Ampylx (BK virus treatment); payment or honoraria from WebMD/Medscape for a CMV presentation and ASN for a COVID presentation; and served as American Society of Transplantation Public Policy Chair and American Journal of Transplantation Deputy Editor. M. H.-M. is an NIH T32 Transplant Infectious Diseases Training Grant recipient, funding ended before initiation of this work; served on the scientific review committee for BioNTech for BNT162-17; played an unpaid leadership or fiduciary role for LifeGift (local organ procurement organization) Houston, Texas; and served as a member of the Medical Advisory Committee. M. G. I. reports research support, paid to Northwestern University, from GlaxoSmithKline, Pulmocide, and Regeneron; payments made to self for RIV chapters from UpToDate; is a paid consultant for Adagio, ADMA Biologics, AlloVir, Cidara, Genentech, Roche, Janssen, Shionogi, Takeda, and Viracor Eurofins; and is a paid member of DSMBs for Allovir, CSL Behring, Janssen, Merck, Sequiris, Takeda, and Talaris. D. v. D. reports grants from NIH; personal fees from Achaogen, Allergan, Astellas, Neumedicine, T2biosystems, Roche, Karius, Entasis, Wellspring, Qpex, Pfizer, Utility, Union, and the British Society for Antimicrobial Chemotherapy; and grants and personal fees from Shionogi and Merck outside the submitted work. J. D. G. reports research support from Gilead Sciences, Eli Lilly and Company, Regeneron Pharmaceuticals, NIAID, NIH, BARDA (administered by Merck), and Viracor Eurofins; served as a consultant, speaker, or advisory board member for Gilead Sciences and Eli Lilly and Company; and collaborative services agreements from Labcorp, Monogram Biosciences, and Adaptive Biotechnologies. A. W. reports grants or contracts to their institution from NIH, Sanofi, and GlaxoSmithKline outside of the submitted work; royalties or licenses from UpToDate; travel reimbursement from Innovative Molecules; provision of vaccine for a clinical trial from Merck; consulting fees from Aicuris, Crozet, Auritec, Dxnow, and Gilead; and is a paid member of DSMBs for Merck, X-Vax, and Vir. A. P. L reports grants or contracts from Merck Moderna, Takeda, Allovir, GlaxoSmithKline, Johnson & Johnson, and Novartis outside of the submitted work; royalties or licenses from UpToDate; receipt of consulting fees from Merck, GlaxoSmithKline, Allovir, and Novartis; and served on a DSMB for Novartis. V. H. reports grants or contracts with their institution from Merck outside of the submitted work. E. D. L. reports grants or contracts from the Cystic Fibrosis Foundation outside of the submitted work and served as chair for the OPTN Lung Transplantation Committee and chair for the ISHLT Standards and Guidelines Committee. M. M. reports serving as chair of Digital Strategy Advisory Group for IDSA, Councilor, Transplant Infectious Disease, the Transplantation Society, and Member-at-Large, AST IDCOP Executive Committee. J. M. S. reports receipt of an American Society of Transplantation/CareDx Fellowship grant–research funding for hepatitis C in transplant patients and an NIH NIAID grant outside of the submitted work and has pending patents for gene expression-based classifiers of fungal infection. All remaining authors: No reported conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed. Financial support. This work was supported by the National Institute of Allergy and Infectious Diseases (NIAID; T32AI118690 to M. R. H. and O. S. K.) and the National Heart, Lung, and Blood Institute (HL143050 to C. E. F.) at the NIH. REDCap (Research Electronic Data Capture) at the Institute of Translational Health Sciences at the University of Washington is supported by the National Center for Advancing Translational Sciences of the NIH (UL1 TR002319).

Funders	Funder number
British Society for Antimicrobial Chemotherapy
CareDx Incorporated
National Institutes of Health (NIH)
Canadian Society of Transplantation
Roche Canada
National Institute of Health National Center for Advancing Translational Sciences
American Society for Neural Transplantation and Repair
National Heart, Lung, and Blood Institute (NHLBI)	K23HL143050
National Institute of Allergy and Infectious F32-AI286447 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI168214 Jason W. Rosch Diseases National Institute of Allergy and Infectious P30 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R00-AI166116 Christopher D. Radka Diseases National Institute of Allergy and Infectious T32-AI106700 Cydney N. Johnson Diseases National Institute of Allergy and Infectious R01AI192221 Jason W. Rosch Diseases National Inst...	T32AI118690, T32AI100851
National Center for Advancing Translational Sciences (NCATS)	UL1 TR002319

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 3 Good Health and Well-being

ASJC Scopus subject areas

Microbiology (medical)
Infectious Diseases

Access to Document

10.1093/cid/ciac159

Cite this

@article{28acef8b2941441abc26f477ef93146d,

title = "Delayed Mortality Among Solid Organ Transplant Recipients Hospitalized for COVID-19",

abstract = "Background. Most studies of solid organ transplant (SOT) recipients with coronavirus disease 2019 (COVID-19) focus on outcomes within 1 month of illness onset. Delayed mortality in SOT recipients hospitalized for COVID-19 has not been fully examined. Methods. We used data from a multicenter registry to calculate mortality by 90 days following initial acute respiratory syndrome coronavirus 2 (SARS-CoV-2) detection in SOT recipients hospitalized for COVID-19 and developed multivariable Cox proportional hazards models to compare risk factors for death by days 28 and 90. Results. Vital status at day 90 was available for 936 of 1117 (84\%) SOT recipients hospitalized for COVID-19; 190 of 936 (20\%) died by 28 days, and an additional 56 of 246 deaths (23\%) occurred between days 29 and 90. Factors associated with mortality by day 90 included age >65 years (adjusted hazard ratio [aHR], 1.8 [1.3–2.4]; P <.001), lung transplant (vs nonlung transplant; aHR, 1.5 [1.0–2.3]; P = .05), heart failure (aHR, 1.9 [1.2–2.9]; P = .006), chronic lung disease (aHR, 2.3 [1.5–3.6]; P < .001), and body mass index ≥30 kg/m2 (aHR, 1.5 [1.1–2.0]; P = .02). These associations were similar for mortality by day 28. Compared with diagnosis during early 2020 (1 March 2020–19 June 2020), diagnosis during late 2020 (20 June 2020–31 December 2020) was associated with lower mortality by day 28 (aHR, 0.7 [0.5–1.0]; P = .04) but not by day 90 (aHR, 0.9 [0.7–1.3]; P = .61). Conclusions. In SOT recipients hospitalized for COVID-19, >20\% of deaths occurred between 28 and 90 days following SARSCoV-2 diagnosis. Future investigations should consider extending follow-up duration to 90 days for more complete mortality assessment.",

author = "Heldman, \{Madeleine R.\} and Kates, \{Olivia S.\} and Kassem Safa and Kotton, \{Camille N.\} and Ashrit Multani and Georgia, \{Sarah J.\} and Steinbrink, \{Julie M.\} and Alexander, \{Barbara D.\} and Blumberg, \{Emily A.\} and Brandy Haydel and Vagish Hemmige and Marion Hemmersbach-Miller and \{La Hoz\}, \{Ricardo M.\} and Lisset Moni and Yesabeli Condor and Sandra Flores and Munoz, \{Carlos G.\} and Juan Guitierrez and Diaz, \{Esther I.\} and Daniela Diaz and Rodrigo Vianna and Giselle Guerra and Matthias Loebe and Yabu, \{Julie M.\} and Kramer, \{Kailey Hughes\} and Tanna, \{Sajal D.\} and Ison, \{Michael G.\} and Rakita, \{Robert M.\} and Maricar Malinis and Azar, \{Marwan M.\} and McCort, \{Margaret E.\} and Singh, \{Pooja P.\} and Arzu Velioglu and Mehta, \{Sapna A.\} and \{van Duin\}, David and Goldman, \{Jason D.\} and Lease, \{Erika D.\} and Anna Wald and Limaye, \{Ajit P.\} and Fisher, \{Cynthia E.\}",

year = "2024",

month = mar,

day = "15",

doi = "10.1093/cid/ciac159",

language = "English",

volume = "78",

pages = "711--718",

number = "3",

}

TY - JOUR

T1 - Delayed Mortality Among Solid Organ Transplant Recipients Hospitalized for COVID-19

AU - Heldman, Madeleine R.

AU - Kates, Olivia S.

AU - Safa, Kassem

AU - Kotton, Camille N.

AU - Multani, Ashrit

AU - Georgia, Sarah J.

AU - Steinbrink, Julie M.

AU - Alexander, Barbara D.

AU - Blumberg, Emily A.

AU - Haydel, Brandy

AU - Hemmige, Vagish

AU - Hemmersbach-Miller, Marion

AU - La Hoz, Ricardo M.

AU - Moni, Lisset

AU - Condor, Yesabeli

AU - Flores, Sandra

AU - Munoz, Carlos G.

AU - Guitierrez, Juan

AU - Diaz, Esther I.

AU - Diaz, Daniela

AU - Vianna, Rodrigo

AU - Guerra, Giselle

AU - Loebe, Matthias

AU - Yabu, Julie M.

AU - Kramer, Kailey Hughes

AU - Tanna, Sajal D.

AU - Ison, Michael G.

AU - Rakita, Robert M.

AU - Malinis, Maricar

AU - Azar, Marwan M.

AU - McCort, Margaret E.

AU - Singh, Pooja P.

AU - Velioglu, Arzu

AU - Mehta, Sapna A.

AU - van Duin, David

AU - Goldman, Jason D.

AU - Lease, Erika D.

AU - Wald, Anna

AU - Limaye, Ajit P.

AU - Fisher, Cynthia E.

PY - 2024/3/15

Y1 - 2024/3/15

N2 - Background. Most studies of solid organ transplant (SOT) recipients with coronavirus disease 2019 (COVID-19) focus on outcomes within 1 month of illness onset. Delayed mortality in SOT recipients hospitalized for COVID-19 has not been fully examined. Methods. We used data from a multicenter registry to calculate mortality by 90 days following initial acute respiratory syndrome coronavirus 2 (SARS-CoV-2) detection in SOT recipients hospitalized for COVID-19 and developed multivariable Cox proportional hazards models to compare risk factors for death by days 28 and 90. Results. Vital status at day 90 was available for 936 of 1117 (84%) SOT recipients hospitalized for COVID-19; 190 of 936 (20%) died by 28 days, and an additional 56 of 246 deaths (23%) occurred between days 29 and 90. Factors associated with mortality by day 90 included age >65 years (adjusted hazard ratio [aHR], 1.8 [1.3–2.4]; P <.001), lung transplant (vs nonlung transplant; aHR, 1.5 [1.0–2.3]; P = .05), heart failure (aHR, 1.9 [1.2–2.9]; P = .006), chronic lung disease (aHR, 2.3 [1.5–3.6]; P < .001), and body mass index ≥30 kg/m2 (aHR, 1.5 [1.1–2.0]; P = .02). These associations were similar for mortality by day 28. Compared with diagnosis during early 2020 (1 March 2020–19 June 2020), diagnosis during late 2020 (20 June 2020–31 December 2020) was associated with lower mortality by day 28 (aHR, 0.7 [0.5–1.0]; P = .04) but not by day 90 (aHR, 0.9 [0.7–1.3]; P = .61). Conclusions. In SOT recipients hospitalized for COVID-19, >20% of deaths occurred between 28 and 90 days following SARSCoV-2 diagnosis. Future investigations should consider extending follow-up duration to 90 days for more complete mortality assessment.

AB - Background. Most studies of solid organ transplant (SOT) recipients with coronavirus disease 2019 (COVID-19) focus on outcomes within 1 month of illness onset. Delayed mortality in SOT recipients hospitalized for COVID-19 has not been fully examined. Methods. We used data from a multicenter registry to calculate mortality by 90 days following initial acute respiratory syndrome coronavirus 2 (SARS-CoV-2) detection in SOT recipients hospitalized for COVID-19 and developed multivariable Cox proportional hazards models to compare risk factors for death by days 28 and 90. Results. Vital status at day 90 was available for 936 of 1117 (84%) SOT recipients hospitalized for COVID-19; 190 of 936 (20%) died by 28 days, and an additional 56 of 246 deaths (23%) occurred between days 29 and 90. Factors associated with mortality by day 90 included age >65 years (adjusted hazard ratio [aHR], 1.8 [1.3–2.4]; P <.001), lung transplant (vs nonlung transplant; aHR, 1.5 [1.0–2.3]; P = .05), heart failure (aHR, 1.9 [1.2–2.9]; P = .006), chronic lung disease (aHR, 2.3 [1.5–3.6]; P < .001), and body mass index ≥30 kg/m2 (aHR, 1.5 [1.1–2.0]; P = .02). These associations were similar for mortality by day 28. Compared with diagnosis during early 2020 (1 March 2020–19 June 2020), diagnosis during late 2020 (20 June 2020–31 December 2020) was associated with lower mortality by day 28 (aHR, 0.7 [0.5–1.0]; P = .04) but not by day 90 (aHR, 0.9 [0.7–1.3]; P = .61). Conclusions. In SOT recipients hospitalized for COVID-19, >20% of deaths occurred between 28 and 90 days following SARSCoV-2 diagnosis. Future investigations should consider extending follow-up duration to 90 days for more complete mortality assessment.

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UR - https://www.scopus.com/pages/publications/85188295900#tab=citedBy

U2 - 10.1093/cid/ciac159

DO - 10.1093/cid/ciac159

M3 - Article

C2 - 35212363

AN - SCOPUS:85188295900

SN - 1058-4838

VL - 78

SP - 711

EP - 718

JO - Clinical Infectious Diseases

JF - Clinical Infectious Diseases

IS - 3

ER -

Delayed Mortality Among Solid Organ Transplant Recipients Hospitalized for COVID-19

Abstract

Bibliographical note

Funding

UN SDGs

ASJC Scopus subject areas

Access to Document

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