Liver injury in hospitalized patients with COVID-19: An International observational cohort study

Bharath Kumar Tirupakuzhi Vijayaraghavan; Saptarshi Bishnu; Joaquin Baruch; Barbara Wanjiru Citarella; Christiana Kartsonaki; Aronrag Meeyai; Zubair Mohamed; Shinichiro Ohshimo; Benjamin Lefèvre; Abdulrahman Al-Fares; Jose A. Calvache; Fabio Silvio Taccone; Piero Olliaro; Laura Merson; Neill K.J. Adhikari; Sheryl Ann Abdukahil; Nurul Najmee Abdulkadir; Ryuzo Abe; Laurent Abel; Amal Abrous; Lara Absil; Andrew Acker; Elisabeth Adam; Diana Adrião; Saleh Al Ageel; Kate Ainscough; Ali Ait Hssain; Younes Ait Tamlihat; Takako Akimoto; Ernita Akmal; Eman Al Qasim; Angela Alberti; Tala Al-Dabbous; Senthilkumar Alegesan; Marta Alessi; Beatrice Alex; Kévin Alexandre; Huda Alfoudri; Imran Ali; Kazali Enagnon Alidjnou; Jeffrey Aliudin; Clotilde Allavena; Nathalie Allou; João Melo Alves; Rita Alves; Joana Alves Cabrita; Maria Amaral; Nur Amira; Phoebe Ampaw; Claire Andrejak; Andrea Angheben; François Angoulvant; Séverine Ansart; Sivanesen Anthonidass; Carlos Alexandre Antunes de Brito; Ardiyan Apriyana; Yaseen Arabi; Irene Aragao; Francisco Arancibia; Carolline Araujo; Antonio Arcadipane; Patrick Archambault; Lukas Arenz; Jean-Benoît Arlet; Christel Arnold-Day; Lovkesh Arora; Rakesh Arora; Elise Artaud-Macari; Diptesh Aryal; Muhammad Ashraf; Namra Asif; Jean Baptiste Assie; Amirul Asyraf; Minahel Atif; Anika Atique; Johann Auchabie; Hugues Aumaitre; Adrien Auvet; Laurène Azemar; Cecile Azoulay; Benjamin Bach; Delphine Bachelet; Claudine Badr; Nadia Baig; J. Kenneth Baillie; Erica Bak; Nazreen Abu Bakar; Andriy Bal; Mohanaprasanth Balakrishnan; Valeria Balan; Firouzé Bani-Sadr; Renata Barbalho; Nicholas Yuri Barbosa; Wendy S. Barclay; Saef Umar Barnett; Michaela Barnikel; Audrey Barrelet; Cleide Barrigoto; Marie Bartoli; Romain Basmaci; Muhammad Fadhli Hassin Basri; Jules Bauer; Diego Fernando Bautista Rincon; Abigail Beane; Alexandra Bedossa; Ker Hong Bee; Husna Begum; Sylvie Behilill; Albertus Beishuizen; Aleksandr Beljantsev; David Bellemare; Anna Beltrame; Beatriz Amorim Beltrão; Marine Beluze; Nicolas Benech; Lionel Eric Benjiman; Dehbia Benkerrou; Suzanne Bennett; Luís Bento; Jan-Erik Berdal; Delphine Bergeaud; Hazel Bergin; Giulia Bertoli; Simon Bessis; Sybille Bevilcaqua; Karine Bezulier; Amar Bhatt; Krishna Bhavsar; Claudia Bianco; Farah Nadiah Bidin; Moirangthem Bikram Singh; Felwa Bin Humaid; Mohd Nazlin Bin Kamarudin; François Bissuel; Patrick Biston; Laurent Bitker; Catherine Blier; Mathieu Blot; Lucille Blumberg; Laetitia Bodenes; Debby Bogaert; Anne-Hélène Boivin; Isabela Bolaños; Pierre-Adrien Bolze; François Bompart; Diogo Borges; Raphaël Borie; Elisabeth Botelho-Nevers; Lila Bouadma; Olivier Bouchaud; Sabelline Bouchez; Dounia Bouhmani; Damien Bouhour; Kévin Bouiller; Laurence Bouillet; Camile Bouisse; Anne-Sophie Boureau; John Bourke; Maude Bouscambert; Aurore Bousquet; Jason Bouziotis; Bianca Boxma; Marielle Boyer-Besseyre; Maria Boylan; Fernando Augusto Bozza; Axelle Braconnier; Cynthia Braga; Filipa Brás Monteiro; Luca Brazzi; Dorothy Breen; Kathy Brickell; Shaunagh Browne; Marjolein Brusse-Keizer; Petra Bryda; Nina Buchtele; Polina Bugaeva; Marielle Buisson; Erlina Burhan; Aidan Burrell; Ingrid G. Bustos; Denis Butnaru; André Cabie; Eder Caceres; Cyril Cadoz; Rui Caetano Garcês; João Camões; Valentine Campana; Paul Campbell; Cecilia Canepa; Pauline Caraux-Paz; Chiara Simona Cardellino; Filipa Cardoso; Filipe Cardoso; Nelson Cardoso; Sofia Cardoso; Nicolas Carlier; Thierry Carmoi; Gayle Carney; Inês Carqueja; Marie-Christine Carret; François Martin Carrier; Gail Carson; Maire-Laure Casanova; Mariana Cascão; Siobhan Casey; José Casimiro; Bailey Cassandra; Silvia Castañeda; Nidyanara Castanheira; Guylaine Castor-Alexandre; Ivo Castro; François-Xavier Catherine; Paolo Cattaneo; Roberta Cavalin; Alexandros Cavayas; Minerva Cervantes-Gonzalez; Anissa Chair; Catherine Chakveatze; Adrienne Chan; Meera Chand; Christelle Chantalat Auger; Jean-Marc Chapplain; Charlotte Charpentier; Julie Chas; Anjellica Chen; Yih-Sharng Chen; Léo Chenard; Matthew Pellan Cheng; Antoine Cheret; Thibault Chiarabini; Julian Chica; Suresh Kumar Chidambaram; Leong Chin Tho; Catherine Chirouze; Davide Chiumello; Bernard Cholley; Marie-Charlotte Chopin; Ting Soo Chow; Hiu Jian Chua; Jonathan Chua; Jose Pedro Cidade; Anna Ciullo; Emma Clarke; Rolando Claure-Del Granado; Sara Clohisey; Cassidy Codan; Alexandra Coelho; Megan Coles; Gwenhaël Colin; Michael Collins; Sebastiano Maria Colombo; Pamela Combs; Jennifer Connolly; Marie Connor; Anne Conrad; Graham S. Cooke; Mary Copland; Hugues Cordel; Amanda Corley; Sabine Cornelis; Alexander Daniel Cornet; Arianne Joy Corpuz; Andrea Cortegiani; Grégory Corvaisier; Emma Costigan; Camille Couffignal; Sandrine Couffin-Cadiergues; Roxane Courtois; Stéphanie Cousse; Rachel Cregan; Sabine Croonen; Gloria Crowl; Jonathan Crump; Claudina Cruz; Marc Csete; Matthew Cummings; Elodie Curlier; Colleen Curran; Paula Custodio; Ana da Silva Filipe; Charlene Da Silveira; Al-Awwab Dabaliz; Andrew Dagens; Darren Dahly; Heidi Dalton; Jo Dalton; Seamus Daly; Juliana Damas; Nick Daneman; Corinne Daniel; Emmanuelle A. Dankwa; Jorge Dantas; Etienne De Montmollin; Rafael Freitas de Oliveira França; Ana Isabel de Pinho Oliveira; Thushan de Silva; Peter de Vries; David Dean; Alexa Debard; Marie-Pierre Debray; Nathalie DeCastro; William Dechert; Lauren Deconninck; Romain Decours; Eve Defous; Isabelle Delacroix; Eric Delaveuve; Karen Delavigne; Nathalie M. Delfos; Ionna Deligiannis; Dell

doi:10.1371/journal.pone.0277859

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Liver injury in hospitalized patients with COVID-19: An International observational cohort study

Journal article

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Liver injury in hospitalized patients with COVID-19: An International observational cohort study

Bharath Kumar Tirupakuzhi Vijayaraghavan, Saptarshi Bishnu, Joaquin Baruch, Barbara Wanjiru Citarella, Christiana Kartsonaki, Aronrag Meeyai, Zubair Mohamed, Shinichiro Ohshimo, Benjamin Lefèvre, Abdulrahman Al-Fares, …

PLoS ONE, Vol.18(9 September)

2023

DOI: https://doi.org/10.1371/journal.pone.0277859

Abstract

Cohort Studies

COVID-19

Humans

Liver

Patients

SARS-CoV-2

alanine aminotransferase

aspartate aminotransferase

bilirubin

liver enzyme

acute kidney failure

adult respiratory distress syndrome

alanine aminotransferase blood level

Article

artificial ventilation

aspartate aminotransferase level

bilirubin blood level

coronavirus disease 2019

hospital mortality

human

hypertension

invasive ventilation

liver injury

mortality

neurological complication

noninvasive ventilation

sensitivity analysis

sepsis

cohort analysis

coronavirus disease 2019

liver

patient

Severe acute respiratory syndrome coronavirus 2

Background Using a large dataset, we evaluated prevalence and severity of alterations in liver enzymes in COVID-19 and association with patient-centred outcomes. Methods We included hospitalized patients with confirmed or suspected SARS-CoV-2 infection from the International Severe Acute Respiratory and emerging Infection Consortium (ISARIC) database. Key exposure was baseline liver enzymes (AST, ALT, bilirubin). Patients were assigned Liver Injury Classification score based on 3 components of enzymes at admission: Normal; Stage I) Liver injury: any component between 1-3x upper limit of normal (ULN); Stage II) Severe liver injury: any component ≥3x ULN. Outcomes were hospital mortality, utilization of selected resources, complications, and durations of hospital and ICU stay. Analyses used logistic regression with associations expressed as adjusted odds ratios (OR) with 95% confidence intervals (CI). Results Of 17,531 included patients, 46.2% (8099) and 8.2% (1430) of patients had stage 1 and 2 liver injury respectively. Compared to normal, stages 1 and 2 were associated with higher odds of mortality (OR 1.53 [1.37-1.71]; OR 2.50 [2.10-2.96]), ICU admission (OR 1.63 [1.48-1.79]; OR 1.90 [1.62-2.23]), and invasive mechanical ventilation (OR 1.43 [1.27-1.70]; OR 1.95 (1.55-2.45). Stages 1 and 2 were also associated with higher odds of developing sepsis (OR 1.38 [1.27-1.50]; OR 1.46 [1.25-1.70]), acute kidney injury (OR 1.13 [1.00-1.27]; OR 1.59 [1.32-1.91]), and acute respiratory distress syndrome (OR 1.38 [1.22-1.55]; OR 1.80 [1.49-2.17]). Conclusions Liver enzyme abnormalities are common among COVID-19 patients and associated with worse outcomes. © 2023 Vijayaraghavan et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Title: Liver injury in hospitalized patients with COVID-19: An International observational cohort study
Creators: Bharath Kumar Tirupakuzhi Vijayaraghavan - George Institute for Global Health
Saptarshi Bishnu - Apollo Hospitals
Joaquin Baruch - University of Oxford
Barbara Wanjiru Citarella - University of Oxford
Christiana Kartsonaki - University of Oxford
Aronrag Meeyai - University of Oxford
Zubair Mohamed - Amrita Vishwa Vidyapeetham
Shinichiro Ohshimo - Hiroshima University
Benjamin Lefèvre - Centre Hospitalier Universitaire de Nancy
Abdulrahman Al-Fares - Ministry of Health
Jose A. Calvache - University of Cauca
Fabio Silvio Taccone - Erasmus Hospital
Piero Olliaro - University of Oxford
Laura Merson - University of Oxford
Neill K.J. Adhikari - Canada Research Chairs
Sheryl Ann Abdukahil
Nurul Najmee Abdulkadir
Ryuzo Abe
Laurent Abel
Amal Abrous
Lara Absil
Andrew Acker
Elisabeth Adam
Diana Adrião
Saleh Al Ageel
Kate Ainscough
Ali Ait Hssain
Younes Ait Tamlihat
Takako Akimoto
Ernita Akmal
Eman Al Qasim
Angela Alberti
Tala Al-Dabbous
Senthilkumar Alegesan
Marta Alessi
Beatrice Alex
Kévin Alexandre
Huda Alfoudri
Imran Ali
Kazali Enagnon Alidjnou
Jeffrey Aliudin
Clotilde Allavena
Nathalie Allou
João Melo Alves
Rita Alves
Joana Alves Cabrita
Maria Amaral
Nur Amira
Phoebe Ampaw
Claire Andrejak
Andrea Angheben
François Angoulvant
Séverine Ansart
Sivanesen Anthonidass
Carlos Alexandre Antunes de Brito
Ardiyan Apriyana
Yaseen Arabi
Irene Aragao
Francisco Arancibia
Carolline Araujo
Antonio Arcadipane
Patrick Archambault
Lukas Arenz
Jean-Benoît Arlet
Christel Arnold-Day
Lovkesh Arora
Rakesh Arora
Elise Artaud-Macari
Diptesh Aryal
Muhammad Ashraf
Namra Asif
Jean Baptiste Assie
Amirul Asyraf
Minahel Atif
Anika Atique
Johann Auchabie
Hugues Aumaitre
Adrien Auvet
Laurène Azemar
Cecile Azoulay
Benjamin Bach
Delphine Bachelet
Claudine Badr
Nadia Baig
J. Kenneth Baillie
Erica Bak
Nazreen Abu Bakar
Andriy Bal
Mohanaprasanth Balakrishnan
Valeria Balan
Firouzé Bani-Sadr
Renata Barbalho
Nicholas Yuri Barbosa
Wendy S. Barclay
Saef Umar Barnett
Michaela Barnikel
Audrey Barrelet
Cleide Barrigoto
Marie Bartoli
Romain Basmaci
Muhammad Fadhli Hassin Basri
Jules Bauer
Diego Fernando Bautista Rincon
Abigail Beane
Alexandra Bedossa
Ker Hong Bee
Husna Begum
Sylvie Behilill
Albertus Beishuizen
Aleksandr Beljantsev
David Bellemare
Anna Beltrame
Beatriz Amorim Beltrão
Marine Beluze
Nicolas Benech
Lionel Eric Benjiman
Dehbia Benkerrou
Suzanne Bennett
Luís Bento
Jan-Erik Berdal
Delphine Bergeaud
Hazel Bergin
Giulia Bertoli
Simon Bessis
Sybille Bevilcaqua
Karine Bezulier
Amar Bhatt
Krishna Bhavsar
Claudia Bianco
Farah Nadiah Bidin
Moirangthem Bikram Singh
Felwa Bin Humaid
Mohd Nazlin Bin Kamarudin
François Bissuel
Patrick Biston
Laurent Bitker
Catherine Blier
Mathieu Blot
Lucille Blumberg
Laetitia Bodenes
Debby Bogaert
Anne-Hélène Boivin
Isabela Bolaños
Pierre-Adrien Bolze
François Bompart
Diogo Borges
Raphaël Borie
Elisabeth Botelho-Nevers
Lila Bouadma
Olivier Bouchaud
Sabelline Bouchez
Dounia Bouhmani
Damien Bouhour
Kévin Bouiller
Laurence Bouillet
Camile Bouisse
Anne-Sophie Boureau
John Bourke
Maude Bouscambert
Aurore Bousquet
Jason Bouziotis
Bianca Boxma
Marielle Boyer-Besseyre
Maria Boylan
Fernando Augusto Bozza
Axelle Braconnier
Cynthia Braga
Filipa Brás Monteiro
Luca Brazzi
Dorothy Breen
Kathy Brickell
Shaunagh Browne
Marjolein Brusse-Keizer
Petra Bryda
Nina Buchtele
Polina Bugaeva
Marielle Buisson
Erlina Burhan
Aidan Burrell
Ingrid G. Bustos
Denis Butnaru
André Cabie
Eder Caceres
Cyril Cadoz
Rui Caetano Garcês
João Camões
Valentine Campana
Paul Campbell
Cecilia Canepa
Pauline Caraux-Paz
Chiara Simona Cardellino
Filipa Cardoso
Filipe Cardoso
Nelson Cardoso
Sofia Cardoso
Nicolas Carlier
Thierry Carmoi
Gayle Carney
Inês Carqueja
Marie-Christine Carret
François Martin Carrier
Gail Carson
Maire-Laure Casanova
Mariana Cascão
Siobhan Casey
José Casimiro
Bailey Cassandra
Silvia Castañeda
Nidyanara Castanheira
Guylaine Castor-Alexandre
Ivo Castro
François-Xavier Catherine
Paolo Cattaneo
Roberta Cavalin
Alexandros Cavayas
Minerva Cervantes-Gonzalez
Anissa Chair
Catherine Chakveatze
Adrienne Chan
Meera Chand
Christelle Chantalat Auger
Jean-Marc Chapplain
Charlotte Charpentier
Julie Chas
Anjellica Chen
Yih-Sharng Chen
Léo Chenard
Matthew Pellan Cheng
Antoine Cheret
Thibault Chiarabini
Julian Chica
Suresh Kumar Chidambaram
Leong Chin Tho
Catherine Chirouze
Davide Chiumello
Bernard Cholley
Marie-Charlotte Chopin
Ting Soo Chow
Hiu Jian Chua
Jonathan Chua
Jose Pedro Cidade
Anna Ciullo
Emma Clarke
Rolando Claure-Del Granado
Sara Clohisey
Cassidy Codan
Alexandra Coelho
Megan Coles
Gwenhaël Colin
Michael Collins
Sebastiano Maria Colombo
Pamela Combs
Jennifer Connolly
Marie Connor
Anne Conrad
Graham S. Cooke
Mary Copland
Hugues Cordel
Amanda Corley
Sabine Cornelis
Alexander Daniel Cornet
Arianne Joy Corpuz
Andrea Cortegiani
Grégory Corvaisier
Emma Costigan
Camille Couffignal
Sandrine Couffin-Cadiergues
Roxane Courtois
Stéphanie Cousse
Rachel Cregan
Sabine Croonen
Gloria Crowl
Jonathan Crump
Claudina Cruz
Marc Csete
Matthew Cummings
Elodie Curlier
Colleen Curran
Paula Custodio
Ana da Silva Filipe
Charlene Da Silveira
Al-Awwab Dabaliz
Andrew Dagens
Darren Dahly
Heidi Dalton
Jo Dalton
Seamus Daly
Juliana Damas
Nick Daneman
Corinne Daniel
Emmanuelle A. Dankwa
Jorge Dantas
Etienne De Montmollin
Rafael Freitas de Oliveira França
Ana Isabel de Pinho Oliveira
Thushan de Silva
Peter de Vries
David Dean
Alexa Debard
Marie-Pierre Debray
Nathalie DeCastro
William Dechert
Lauren Deconninck
Romain Decours
Eve Defous
Isabelle Delacroix
Eric Delaveuve
Karen Delavigne
Nathalie M. Delfos
Ionna Deligiannis
Dell
Publication Details: PLoS ONE, Vol.18(9 September)
Publisher: Public Library of Science
Identifiers: 991006163015902656
Language: English
Resource Type: Journal article