EBioMedicine (Sep 2022)
Phenotypes of disease severity in a cohort of hospitalized COVID-19 patients: Results from the IMPACC study
- Al Ozonoff,
- Joanna Schaenman,
- Naresh Doni Jayavelu,
- Carly E. Milliren,
- Carolyn S. Calfee,
- Charles B. Cairns,
- Monica Kraft,
- Lindsey R. Baden,
- Albert C. Shaw,
- Florian Krammer,
- Harm van Bakel,
- Denise A. Esserman,
- Shanshan Liu,
- Ana Fernandez Sesma,
- Viviana Simon,
- David A. Hafler,
- Ruth R. Montgomery,
- Steven H. Kleinstein,
- Ofer Levy,
- Christian Bime,
- Elias K. Haddad,
- David J. Erle,
- Bali Pulendran,
- Kari C. Nadeau,
- Mark M. Davis,
- Catherine L. Hough,
- William B. Messer,
- Nelson I. Agudelo Higuita,
- Jordan P. Metcalf,
- Mark A. Atkinson,
- Scott C. Brakenridge,
- David Corry,
- Farrah Kheradmand,
- Lauren I.R. Ehrlich,
- Esther Melamed,
- Grace A. McComsey,
- Rafick Sekaly,
- Joann Diray-Arce,
- Bjoern Peters,
- Alison D. Augustine,
- Elaine F. Reed,
- Matthew C. Altman,
- Patrice M. Becker,
- Nadine Rouphael,
- Al Ozonoff,
- Joanna Schaenman,
- Naresh Doni Jayavelu,
- Carly E. Milliren,
- Carolyn S. Calfee,
- Charles B. Cairns,
- Monica Kraft,
- Lindsey R. Baden,
- Albert C. Shaw,
- Florian Krammer,
- Harm van Bakel,
- Denise A. Esserman,
- Shanshan Liu,
- Ana Fernandez Sesma,
- Viviana Simon,
- David A. Hafler,
- Ruth R. Montgomery,
- Steven H. Kleinstein,
- Ofer Levy,
- Chris Bime,
- Elias K. Haddad,
- David J. Erle,
- Bali Pulendran,
- Kari C. Nadeau,
- Mark M Davis,
- Catherine L. Hough,
- William B. Messer,
- Nelson I. Agudelo Higuita,
- Jordan P. Metcalf,
- Mark A. Atkinson,
- Scott C. Brakenridge,
- David Corry,
- Farrah Kheradmand,
- Lauren I.R. Ehrlich,
- Esther Melamed,
- Grace A. McComsey,
- Rafick Sekaly,
- Joann Diray-Arce,
- Bjoern Peters,
- Alison D. Augustine,
- Elaine F. Reed,
- Kerry McEnaney,
- Brenda Barton,
- Claudia Lentucci,
- Mehmet Saluvan,
- Ana C. Chang,
- Annmarie Hoch,
- Marisa Albert,
- Tanzia Shaheen,
- Alvin T. Kho,
- Sanya Thomas,
- Jing Chen,
- Maimouna D. Murphy,
- Mitchell Cooney,
- Scott Presnell,
- Gabriela K. Fragiadakis,
- Ravi Patel,
- Leying Guan,
- Jeremy Gygi,
- Shrikant Pawar,
- Anderson Brito,
- Zain Khalil,
- Cole Maguire,
- Slim Fourati,
- James A. Overton,
- Randi Vita,
- Kerstin Westendorf,
- Ramin Salehi-Rad,
- Aleksandra Leligdowicz,
- Michael A. Matthay,
- Jonathan P. Singer,
- Kirsten N. Kangelaris,
- Carolyn M. Hendrickson,
- Matthew F. Krummel,
- Charles R. Langelier,
- Prescott G. Woodruff,
- Debra L. Powell,
- James N. Kim,
- Brent Simmons,
- I. Michael Goonewardene,
- Cecilia M. Smith,
- Mark Martens,
- Jarrod Mosier,
- Hiroki Kimura,
- Amy C. Sherman,
- Stephen R. Walsh,
- Nicolas C. Issa,
- Charles Dela Cruz,
- Shelli Farhadian,
- Akiko Iwasaki,
- Albert I. Ko,
- Sharon Chinthrajah,
- Neera Ahuja,
- Angela J. Rogers,
- Maja Artandi,
- Sarah A.R. Siegel,
- Zhengchun Lu,
- Douglas A. Drevets,
- Brent R. Brown,
- Matthew L. Anderson,
- Faheem W. Guirgis,
- Rama V. Thyagarajan,
- Justin F. Rousseau,
- Dennis Wylie,
- Johanna Busch,
- Saurin Gandhi,
- Todd A. Triplett,
- George Yendewa,
- Olivia Giddings,
- Evan J. Anderson,
- Aneesh K. Mehta,
- Jonathan E. Sevransky,
- Bernard Khor,
- Adeeb Rahman,
- Daniel Stadlbauer,
- Jayeeta Dutta,
- Hui Xie,
- Seunghee Kim-Schulze,
- Ana Silvia Gonzalez-Reiche,
- Adriana van de Guchte,
- Keith Farrugia,
- Zenab Khan,
- Holden T. Maecker,
- David Elashoff,
- Jenny Brook,
- Estefania Ramires-Sanchez,
- Megan Llamas,
- Adreanne Rivera,
- Claudia Perdomo,
- Dawn C. Ward,
- Clara E. Magyar,
- Jennifer A. Fulcher,
- Yumiko Abe-Jones,
- Saurabh Asthana,
- Alexander Beagle,
- Sharvari Bhide,
- Sidney A. Carrillo,
- Suzanna Chak,
- Gabriela K. Fragiadakis,
- Rajani Ghale,
- Ana Gonzalez,
- Alejandra Jauregui,
- Norman Jones,
- Tasha Lea,
- Deanna Lee,
- Raphael Lota,
- Jeff Milush,
- Viet Nguyen,
- Logan Pierce,
- Priya A. Prasad,
- Arjun Rao,
- Bushra Samad,
- Cole Shaw,
- Austin Sigman,
- Pratik Sinha,
- Alyssa Ward,
- Andrew Willmore,
- Jenny Zhan,
- Sadeed Rashid,
- Nicklaus Rodriguez,
- Kevin Tang,
- Luz Torres Altamirano,
- Legna Betancourt,
- Cindy Curiel,
- Nicole Sutter,
- Maria Tercero Paz,
- Gayelan Tietje-Ulrich,
- Carolyn Leroux,
- Jennifer Connors,
- Mariana Bernui,
- Michel A. Kutzler,
- Carolyn Edwards,
- Edward Lee,
- Edward Lin,
- Brett Croen,
- Nicholas C. Semenza,
- Brandon Rogowski,
- Nataliya Melnyk,
- Kyra Woloszczuk,
- Gina Cusimano,
- Mathew R. Bell,
- Sara Furukawa,
- Renee McLin,
- Pamela Marrero,
- Julie Sheidy,
- George P. Tegos,
- Crystal Nagle,
- Nathan Mege,
- Kristen Ulring,
- Vicki Seyfert-Margolis,
- Michelle Conway,
- Dave Francisco,
- Allyson Molzahn,
- Heidi Erickson,
- Connie Cathleen Wilson,
- Ron Schunk,
- Bianca Sierra,
- Trina Hughes,
- Kinga Smolen,
- Michael Desjardins,
- Simon van Haren,
- Xhoi Mitre,
- Jessica Cauley,
- Xiaofang Li,
- Alexandra Tong,
- Bethany Evans,
- Christina Montesano,
- Jose Humberto Licona,
- Jonathan Krauss,
- Jun Bai Park Chang,
- Natalie Izaguirre,
- Omkar Chaudhary,
- Andreas Coppi,
- John Fournier,
- Subhasis Mohanty,
- M. Catherine Muenker,
- Allison Nelson,
- Khadir Raddassi,
- Michael Rainone,
- William E. Ruff,
- Syim Salahuddin,
- Wade L. Schulz,
- Pavithra Vijayakumar,
- Haowei Wang,
- Elsio Wunder Jr.,
- H. Patrick Young,
- Yujiao Zhao,
- Miti Saksena,
- Deena Altman,
- Erna Kojic,
- Komal Srivastava,
- Lily Q. Eaker,
- Maria C. Bermúdez-González,
- Katherine F. Beach,
- Levy A. Sominsky,
- Arman R. Azad,
- Juan Manuel Carreño,
- Gagandeep Singh,
- Ariel Raskin,
- Johnstone Tcheou,
- Dominika Bielak,
- Hisaaki Kawabata,
- Lubbertus CF Mulder,
- Giulio Kleiner,
- Alexandra S. Lee,
- Evan Do Do,
- Andrea Fernandes,
- Monali Manohar,
- Thomas Hagan,
- Catherine A. Blish,
- Hena Naz Din,
- Jonasel Roque,
- Samuel Yang,
- Amanda Brunton,
- Peter E. Sullivan,
- Matthew Strnad,
- Zoe L. Lyski,
- Felicity J. Coulter,
- J. Leland Booth,
- Lauren A. Sinko,
- Lyle L. Moldawer,
- Brittany Borresen,
- Brittney Roth-Manning,
- Li-Zhen Song,
- Ebony Nelson,
- Megan Lewis-Smith,
- Jacob Smith,
- Pablo Guaman Tipan,
- Nadia Siles,
- Sam Bazzi,
- Janelle Geltman,
- Kerin Hurley,
- Gio Gabriele,
- Scott Sieg,
- Tatyana Vaysman,
- Laurel Bristow,
- Laila Hussaini,
- Kieffer Hellmeister,
- Hady Samaha,
- Andrew Cheng,
- Christine Spainhour,
- Erin M. Scherer,
- Brandi Johnson,
- Amer Bechnak,
- Caroline R. Ciric,
- Lauren Hewitt,
- Erin Carter,
- Nina Mcnair,
- Bernadine Panganiban,
- Christopher Huerta,
- Jacob Usher,
- Susan Pereira Ribeiro,
- Matthew C. Altman,
- Patrice M. Becker,
- Nadine Rouphael
Affiliations
- Al Ozonoff
- Clinical & Data Coordinating Center (CDCC); Precision Vaccines Program, Boston Children's Hospital, Boston, MA, United States
- Joanna Schaenman
- David Geffen School of Medicine at the University of California Los Angeles, Los Angeles, CA, United States
- Naresh Doni Jayavelu
- Benaroya Research Institute, Seattle, WA, United States
- Carly E. Milliren
- Clinical & Data Coordinating Center (CDCC); Precision Vaccines Program, Boston Children's Hospital, Boston, MA, United States
- Carolyn S. Calfee
- University of California San Francisco School of Medicine, San Francisco, CA, United States
- Charles B. Cairns
- Drexel University/Tower Health Hospital, Philadelphia, PA, United States
- Monica Kraft
- University of Arizona, Tucson, AZ, United States
- Lindsey R. Baden
- Boston Clinical Site: Precision Vaccines Program, Boston Children's Hospital, Brigham and Women's Hospital, and Harvard Medical School, Boston, MA, United States
- Albert C. Shaw
- Yale School of Medicine, and Yale School of Public Health, New Haven, CT, United States
- Florian Krammer
- Icahn School of Medicine at Mount Sinai, New York, NY, United States
- Harm van Bakel
- Icahn School of Medicine at Mount Sinai, New York, NY, United States
- Denise A. Esserman
- Yale School of Medicine, and Yale School of Public Health, New Haven, CT, United States
- Shanshan Liu
- Clinical & Data Coordinating Center (CDCC); Precision Vaccines Program, Boston Children's Hospital, Boston, MA, United States
- Ana Fernandez Sesma
- Icahn School of Medicine at Mount Sinai, New York, NY, United States
- Viviana Simon
- Icahn School of Medicine at Mount Sinai, New York, NY, United States
- David A. Hafler
- Yale School of Medicine, and Yale School of Public Health, New Haven, CT, United States
- Ruth R. Montgomery
- Yale School of Medicine, and Yale School of Public Health, New Haven, CT, United States
- Steven H. Kleinstein
- Yale School of Medicine, and Yale School of Public Health, New Haven, CT, United States
- Ofer Levy
- Boston Clinical Site: Precision Vaccines Program, Boston Children's Hospital, Brigham and Women's Hospital, and Harvard Medical School, Boston, MA, United States
- Christian Bime
- University of Arizona, Tucson, AZ, United States
- Elias K. Haddad
- Drexel University/Tower Health Hospital, Philadelphia, PA, United States
- David J. Erle
- University of California San Francisco School of Medicine, San Francisco, CA, United States
- Bali Pulendran
- Stanford University, Palo Alto, CA, United States
- Kari C. Nadeau
- Stanford University, Palo Alto, CA, United States
- Mark M. Davis
- Stanford University, Palo Alto, CA, United States
- Catherine L. Hough
- Oregon Health Sciences University, Portland, OR, United States
- William B. Messer
- Oregon Health Sciences University, Portland, OR, United States
- Nelson I. Agudelo Higuita
- Oklahoma University Health Sciences Center, Oklahoma, OK, United States
- Jordan P. Metcalf
- Oklahoma University Health Sciences Center, Oklahoma, OK, United States
- Mark A. Atkinson
- University of Florida, Gainesville and University of South Florida, Tampa, FL, United States
- Scott C. Brakenridge
- University of Florida, Gainesville and University of South Florida, Tampa, FL, United States
- David Corry
- Baylor College of Medicine, and the Center for Translational Research on Inflammatory Diseases, Michael E. DeBakey, Houston, TX, United States
- Farrah Kheradmand
- Baylor College of Medicine, and the Center for Translational Research on Inflammatory Diseases, Michael E. DeBakey, Houston, TX, United States
- Lauren I.R. Ehrlich
- The University of Texas at Austin, Austin, TX, United States
- Esther Melamed
- The University of Texas at Austin, Austin, TX, United States
- Grace A. McComsey
- Case Western Reserve University, Cleveland, OH, United States
- Rafick Sekaly
- Case Western Reserve University, Cleveland, OH, United States
- Joann Diray-Arce
- Clinical & Data Coordinating Center (CDCC); Precision Vaccines Program, Boston Children's Hospital, Boston, MA, United States
- Bjoern Peters
- La Jolla Institute for Immunology, La Jolla, CA, United States
- Alison D. Augustine
- National Institute of Allergy and Infectious Diseases/National Institutes of Health, Bethesda, MD, United States
- Elaine F. Reed
- David Geffen School of Medicine at the University of California Los Angeles, Los Angeles, CA, United States
- Matthew C. Altman
- Benaroya Research Institute, Seattle, WA, United States
- Patrice M. Becker
- National Institute of Allergy and Infectious Diseases/National Institutes of Health, Bethesda, MD, United States
- Nadine Rouphael
- Emory University, Atlanta, GA, United States; Corresponding author.
- Al Ozonoff
- Joanna Schaenman
- Naresh Doni Jayavelu
- Carly E. Milliren
- Carolyn S. Calfee
- Charles B. Cairns
- Monica Kraft
- Lindsey R. Baden
- Albert C. Shaw
- Florian Krammer
- Harm van Bakel
- Denise A. Esserman
- Shanshan Liu
- Ana Fernandez Sesma
- Viviana Simon
- David A. Hafler
- Ruth R. Montgomery
- Steven H. Kleinstein
- Ofer Levy
- Chris Bime
- Elias K. Haddad
- David J. Erle
- Bali Pulendran
- Kari C. Nadeau
- Mark M Davis
- Catherine L. Hough
- William B. Messer
- Nelson I. Agudelo Higuita
- Jordan P. Metcalf
- Mark A. Atkinson
- Scott C. Brakenridge
- David Corry
- Farrah Kheradmand
- Lauren I.R. Ehrlich
- Esther Melamed
- Grace A. McComsey
- Rafick Sekaly
- Joann Diray-Arce
- Bjoern Peters
- Alison D. Augustine
- Elaine F. Reed
- Kerry McEnaney
- Brenda Barton
- Claudia Lentucci
- Mehmet Saluvan
- Ana C. Chang
- Annmarie Hoch
- Marisa Albert
- Tanzia Shaheen
- Alvin T. Kho
- Sanya Thomas
- Jing Chen
- Maimouna D. Murphy
- Mitchell Cooney
- Scott Presnell
- Gabriela K. Fragiadakis
- Ravi Patel
- Leying Guan
- Jeremy Gygi
- Shrikant Pawar
- Anderson Brito
- Zain Khalil
- Cole Maguire
- Slim Fourati
- James A. Overton
- Randi Vita
- Kerstin Westendorf
- Ramin Salehi-Rad
- Aleksandra Leligdowicz
- Michael A. Matthay
- Jonathan P. Singer
- Kirsten N. Kangelaris
- Carolyn M. Hendrickson
- Matthew F. Krummel
- Charles R. Langelier
- Prescott G. Woodruff
- Debra L. Powell
- James N. Kim
- Brent Simmons
- I. Michael Goonewardene
- Cecilia M. Smith
- Mark Martens
- Jarrod Mosier
- Hiroki Kimura
- Amy C. Sherman
- Stephen R. Walsh
- Nicolas C. Issa
- Charles Dela Cruz
- Shelli Farhadian
- Akiko Iwasaki
- Albert I. Ko
- Sharon Chinthrajah
- Neera Ahuja
- Angela J. Rogers
- Maja Artandi
- Sarah A.R. Siegel
- Zhengchun Lu
- Douglas A. Drevets
- Brent R. Brown
- Matthew L. Anderson
- Faheem W. Guirgis
- Rama V. Thyagarajan
- Justin F. Rousseau
- Dennis Wylie
- Johanna Busch
- Saurin Gandhi
- Todd A. Triplett
- George Yendewa
- Olivia Giddings
- Evan J. Anderson
- Aneesh K. Mehta
- Jonathan E. Sevransky
- Bernard Khor
- Adeeb Rahman
- Daniel Stadlbauer
- Jayeeta Dutta
- Hui Xie
- Seunghee Kim-Schulze
- Ana Silvia Gonzalez-Reiche
- Adriana van de Guchte
- Keith Farrugia
- Zenab Khan
- Holden T. Maecker
- David Elashoff
- Jenny Brook
- Estefania Ramires-Sanchez
- Megan Llamas
- Adreanne Rivera
- Claudia Perdomo
- Dawn C. Ward
- Clara E. Magyar
- Jennifer A. Fulcher
- Yumiko Abe-Jones
- Saurabh Asthana
- Alexander Beagle
- Sharvari Bhide
- Sidney A. Carrillo
- Suzanna Chak
- Gabriela K. Fragiadakis
- Rajani Ghale
- Ana Gonzalez
- Alejandra Jauregui
- Norman Jones
- Tasha Lea
- Deanna Lee
- Raphael Lota
- Jeff Milush
- Viet Nguyen
- Logan Pierce
- Priya A. Prasad
- Arjun Rao
- Bushra Samad
- Cole Shaw
- Austin Sigman
- Pratik Sinha
- Alyssa Ward
- Andrew Willmore
- Jenny Zhan
- Sadeed Rashid
- Nicklaus Rodriguez
- Kevin Tang
- Luz Torres Altamirano
- Legna Betancourt
- Cindy Curiel
- Nicole Sutter
- Maria Tercero Paz
- Gayelan Tietje-Ulrich
- Carolyn Leroux
- Jennifer Connors
- Mariana Bernui
- Michel A. Kutzler
- Carolyn Edwards
- Edward Lee
- Edward Lin
- Brett Croen
- Nicholas C. Semenza
- Brandon Rogowski
- Nataliya Melnyk
- Kyra Woloszczuk
- Gina Cusimano
- Mathew R. Bell
- Sara Furukawa
- Renee McLin
- Pamela Marrero
- Julie Sheidy
- George P. Tegos
- Crystal Nagle
- Nathan Mege
- Kristen Ulring
- Vicki Seyfert-Margolis
- Michelle Conway
- Dave Francisco
- Allyson Molzahn
- Heidi Erickson
- Connie Cathleen Wilson
- Ron Schunk
- Bianca Sierra
- Trina Hughes
- Kinga Smolen
- Michael Desjardins
- Simon van Haren
- Xhoi Mitre
- Jessica Cauley
- Xiaofang Li
- Alexandra Tong
- Bethany Evans
- Christina Montesano
- Jose Humberto Licona
- Jonathan Krauss
- Jun Bai Park Chang
- Natalie Izaguirre
- Omkar Chaudhary
- Andreas Coppi
- John Fournier
- Subhasis Mohanty
- M. Catherine Muenker
- Allison Nelson
- Khadir Raddassi
- Michael Rainone
- William E. Ruff
- Syim Salahuddin
- Wade L. Schulz
- Pavithra Vijayakumar
- Haowei Wang
- Elsio Wunder Jr.
- H. Patrick Young
- Yujiao Zhao
- Miti Saksena
- Deena Altman
- Erna Kojic
- Komal Srivastava
- Lily Q. Eaker
- Maria C. Bermúdez-González
- Katherine F. Beach
- Levy A. Sominsky
- Arman R. Azad
- Juan Manuel Carreño
- Gagandeep Singh
- Ariel Raskin
- Johnstone Tcheou
- Dominika Bielak
- Hisaaki Kawabata
- Lubbertus CF Mulder
- Giulio Kleiner
- Alexandra S. Lee
- Evan Do Do
- Andrea Fernandes
- Monali Manohar
- Thomas Hagan
- Catherine A. Blish
- Hena Naz Din
- Jonasel Roque
- Samuel Yang
- Amanda Brunton
- Peter E. Sullivan
- Matthew Strnad
- Zoe L. Lyski
- Felicity J. Coulter
- J. Leland Booth
- Lauren A. Sinko
- Lyle L. Moldawer
- Brittany Borresen
- Brittney Roth-Manning
- Li-Zhen Song
- Ebony Nelson
- Megan Lewis-Smith
- Jacob Smith
- Pablo Guaman Tipan
- Nadia Siles
- Sam Bazzi
- Janelle Geltman
- Kerin Hurley
- Gio Gabriele
- Scott Sieg
- Tatyana Vaysman
- Laurel Bristow
- Laila Hussaini
- Kieffer Hellmeister
- Hady Samaha
- Andrew Cheng
- Christine Spainhour
- Erin M. Scherer
- Brandi Johnson
- Amer Bechnak
- Caroline R. Ciric
- Lauren Hewitt
- Erin Carter
- Nina Mcnair
- Bernadine Panganiban
- Christopher Huerta
- Jacob Usher
- Susan Pereira Ribeiro
- Matthew C. Altman
- Patrice M. Becker
- Nadine Rouphael
- Journal volume & issue
-
Vol. 83
p. 104208
Abstract
Summary: Background: Better understanding of the association between characteristics of patients hospitalized with coronavirus disease 2019 (COVID-19) and outcome is needed to further improve upon patient management. Methods: Immunophenotyping Assessment in a COVID-19 Cohort (IMPACC) is a prospective, observational study of 1164 patients from 20 hospitals across the United States. Disease severity was assessed using a 7-point ordinal scale based on degree of respiratory illness. Patients were prospectively surveyed for 1 year after discharge for post-acute sequalae of COVID-19 (PASC) through quarterly surveys. Demographics, comorbidities, radiographic findings, clinical laboratory values, SARS-CoV-2 PCR and serology were captured over a 28-day period. Multivariable logistic regression was performed. Findings: The median age was 59 years (interquartile range [IQR] 20); 711 (61%) were men; overall mortality was 14%, and 228 (20%) required invasive mechanical ventilation. Unsupervised clustering of ordinal score over time revealed distinct disease course trajectories. Risk factors associated with prolonged hospitalization or death by day 28 included age ≥ 65 years (odds ratio [OR], 2.01; 95% CI 1.28–3.17), Hispanic ethnicity (OR, 1.71; 95% CI 1.13–2.57), elevated baseline creatinine (OR 2.80; 95% CI 1.63– 4.80) or troponin (OR 1.89; 95% 1.03–3.47), baseline lymphopenia (OR 2.19; 95% CI 1.61–2.97), presence of infiltrate by chest imaging (OR 3.16; 95% CI 1.96–5.10), and high SARS-CoV2 viral load (OR 1.53; 95% CI 1.17–2.00). Fatal cases had the lowest ratio of SARS-CoV-2 antibody to viral load levels compared to other trajectories over time (p=0.001). 589 survivors (51%) completed at least one survey at follow-up with 305 (52%) having at least one symptom consistent with PASC, most commonly dyspnea (56% among symptomatic patients). Female sex was the only associated risk factor for PASC. Interpretation: Integration of PCR cycle threshold, and antibody values with demographics, comorbidities, and laboratory/radiographic findings identified risk factors for 28-day outcome severity, though only female sex was associated with PASC. Longitudinal clinical phenotyping offers important insights, and provides a framework for immunophenotyping for acute and long COVID-19. Funding: NIH.