Metabolomic and gut microbiome profiles across the spectrum of community-based COVID and non-COVID disease

Marc F. Österdahl; Ronan Whiston; Carole H. Sudre; Francesco Asnicar; Nathan J. Cheetham; Aitor Blanco Miguez; Vicky Bowyer; Michela Antonelli; Olivia Snell; Liane dos Santos Canas; Christina Hu; Jonathan Wolf; Cristina Menni; Michael Malim; Deborah Hart; Tim Spector; Sarah Berry; Nicola Segata; Katie Doores; Sebastien Ourselin; Emma L. Duncan; Claire J. Steves

doi:10.1038/s41598-023-34598-7

Metabolomic and gut microbiome profiles across the spectrum of community-based COVID and non-COVID disease

Marc F. Österdahl^*, Ronan Whiston, Carole H. Sudre, Francesco Asnicar, Nathan J. Cheetham, Aitor Blanco Miguez, Vicky Bowyer, Michela Antonelli, Olivia Snell, Liane dos Santos Canas, Christina Hu, Jonathan Wolf, Cristina Menni, Michael Malim, Deborah Hart, Tim Spector, Sarah Berry, Nicola Segata, Katie Doores, Sebastien OurselinEmma L. Duncan, Claire J. Steves

^*Corresponding author for this work

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

2 Citations (Scopus)

Abstract

Whilst most individuals with SARS-CoV-2 infection have relatively mild disease, managed in the community, it was noted early in the pandemic that individuals with cardiovascular risk factors were more likely to experience severe acute disease, requiring hospitalisation. As the pandemic has progressed, increasing concern has also developed over long symptom duration in many individuals after SARS-CoV-2 infection, including among the majority who are managed acutely in the community. Risk factors for long symptom duration, including biological variables, are still poorly defined. Here, we examine post-illness metabolomic profiles, using nuclear magnetic resonance (Nightingale Health Oyj), and gut-microbiome profiles, using shotgun metagenomic sequencing (Illumina Inc), in 2561 community-dwelling participants with SARS-CoV-2. Illness duration ranged from asymptomatic (n = 307) to Post-COVID Syndrome (n = 180), and included participants with prolonged non-COVID-19 illnesses (n = 287). We also assess a pre-established metabolomic biomarker score, previously associated with hospitalisation for both acute pneumonia and severe acute COVID-19 illness, for its association with illness duration. We found an atherogenic-dyslipidaemic metabolic profile, including biomarkers such as fatty acids and cholesterol, was associated with longer duration of illness, both in individuals with and without SARS-CoV-2 infection. Greater values of a pre-existing metabolomic biomarker score also associated with longer duration of illness, regardless of SARS-CoV-2 infection. We found no association between illness duration and gut microbiome profiles in convalescence. This highlights the potential role of cardiometabolic dysfunction in relation to the experience of long duration symptoms after symptoms of acute infection, both COVID-19 as well as other illnesses.

Original language	English
Article number	10407
Journal	Scientific Reports
Volume	13
Issue number	1
Early online date	27 Jun 2023
DOIs	https://doi.org/10.1038/s41598-023-34598-7
Publication status	Published - 27 Jun 2023

Keywords

Humans
COVID-19
SARS-CoV-2
Gastrointestinal Microbiome
Pneumonia
Hospitalization

UN SDGs

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

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10.1038/s41598-023-34598-7

Cite this

Österdahl, M. F., Whiston, R., Sudre, C. H., Asnicar, F., Cheetham, N. J., Blanco Miguez, A., Bowyer, V., Antonelli, M., Snell, O., dos Santos Canas, L., Hu, C., Wolf, J., Menni, C., Malim, M., Hart, D., Spector, T., Berry, S., Segata, N., Doores, K., ... Steves, C. J. (2023). Metabolomic and gut microbiome profiles across the spectrum of community-based COVID and non-COVID disease. Scientific Reports, 13(1), Article 10407. https://doi.org/10.1038/s41598-023-34598-7

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title = "Metabolomic and gut microbiome profiles across the spectrum of community-based COVID and non-COVID disease",

abstract = "Whilst most individuals with SARS-CoV-2 infection have relatively mild disease, managed in the community, it was noted early in the pandemic that individuals with cardiovascular risk factors were more likely to experience severe acute disease, requiring hospitalisation. As the pandemic has progressed, increasing concern has also developed over long symptom duration in many individuals after SARS-CoV-2 infection, including among the majority who are managed acutely in the community. Risk factors for long symptom duration, including biological variables, are still poorly defined. Here, we examine post-illness metabolomic profiles, using nuclear magnetic resonance (Nightingale Health Oyj), and gut-microbiome profiles, using shotgun metagenomic sequencing (Illumina Inc), in 2561 community-dwelling participants with SARS-CoV-2. Illness duration ranged from asymptomatic (n = 307) to Post-COVID Syndrome (n = 180), and included participants with prolonged non-COVID-19 illnesses (n = 287). We also assess a pre-established metabolomic biomarker score, previously associated with hospitalisation for both acute pneumonia and severe acute COVID-19 illness, for its association with illness duration. We found an atherogenic-dyslipidaemic metabolic profile, including biomarkers such as fatty acids and cholesterol, was associated with longer duration of illness, both in individuals with and without SARS-CoV-2 infection. Greater values of a pre-existing metabolomic biomarker score also associated with longer duration of illness, regardless of SARS-CoV-2 infection. We found no association between illness duration and gut microbiome profiles in convalescence. This highlights the potential role of cardiometabolic dysfunction in relation to the experience of long duration symptoms after symptoms of acute infection, both COVID-19 as well as other illnesses.",

keywords = "Humans, COVID-19, SARS-CoV-2, Gastrointestinal Microbiome, Pneumonia, Hospitalization",

author = "{\"O}sterdahl, {Marc F.} and Ronan Whiston and Sudre, {Carole H.} and Francesco Asnicar and Cheetham, {Nathan J.} and {Blanco Miguez}, Aitor and Vicky Bowyer and Michela Antonelli and Olivia Snell and {dos Santos Canas}, Liane and Christina Hu and Jonathan Wolf and Cristina Menni and Michael Malim and Deborah Hart and Tim Spector and Sarah Berry and Nicola Segata and Katie Doores and Sebastien Ourselin and Duncan, {Emma L.} and Steves, {Claire J.}",

note = "Funding Information: We would like to acknowledge support from the Exetera development team (Benjamin Murray, Liyuan Chen, Jie Deng, Eric Kerfoot), the TwinsUK laboratory and administrative teams (Gulsah Akdag, Andy Anastasiou, Andrei Beleanu, Julia Brown, Maria Paz Garcia, Rachel Horsfall, Genevieve Lachance, Ayrun Nessa, Alyce Sheedy, Dovile Vaitkute, Sam Wadge, Sivasubramaniam Rajan Wignarajah, Darioush Yarand). We are also grateful to the CSS Biobank Volunteer Advisory Group for their input on the development of the biobank, and feedback on the significance of this work for affected individuals and the wider public. Funding Information: The CSS Biobank is supported by the Chronic Disease Research Foundation (Grant: CDRF 22/2020). We are also supported by the Wellcome EPSRC Centre for Medical Engineering at King's College London (WT 203148/Z/16/Z) and the UK Department of Health via the National Institute for Health Research (NIHR) comprehensive Biomedical Research Centre award to Guy's & St Thomas{\textquoteright} NHS Foundation Trust in partnership with King's College London and King's College Hospital NHS Foundation Trust. Investigators also received support from Medical Research Council (MRC) (Grant codes: MC_PC_20059 (CJS, SO), MR/T005351/1 and MR/V038664/1 (SO), MR/W005611/1 and MR/S023747/1 (MM)), British Heart Foundation (BHF), Alzheimer's Society, European Union, NIHR, COVID-19 Driver Relief Fund (CDRF) and the NIHR-funded BioResource, Clinical Research Facility and Biomedical Research Centre (BRC) based at GSTT NHS Foundation Trust in partnership with KCL. SO was supported by the French government, through the 3IA C{\^o}te d'Azur Investments in the Future project managed by the National Research Agency (ANR) with the reference number ANR-19-P3IA-0002. ZOE Limited provided in-kind support for all aspects of building, running and supporting the app and service to all users worldwide. This research was funded in part by the Wellcome Trust [215010/Z/18/Z]. Publisher Copyright: {\textcopyright} 2023, The Author(s).",

year = "2023",

month = jun,

day = "27",

doi = "10.1038/s41598-023-34598-7",

language = "English",

volume = "13",

journal = "Scientific Reports",

issn = "2045-2322",

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Österdahl, MF , Whiston, R , Sudre, CH, Asnicar, F, Cheetham, NJ, Blanco Miguez, A, Bowyer, V, Antonelli, M, Snell, O, dos Santos Canas, L, Hu, C, Wolf, J, Menni, C , Malim, M , Hart, D , Spector, T , Berry, S, Segata, N, Doores, K , Ourselin, S , Duncan, EL & Steves, CJ 2023, 'Metabolomic and gut microbiome profiles across the spectrum of community-based COVID and non-COVID disease', Scientific Reports, vol. 13, no. 1, 10407. https://doi.org/10.1038/s41598-023-34598-7

TY - JOUR

T1 - Metabolomic and gut microbiome profiles across the spectrum of community-based COVID and non-COVID disease

AU - Österdahl, Marc F.

AU - Whiston, Ronan

AU - Sudre, Carole H.

AU - Asnicar, Francesco

AU - Cheetham, Nathan J.

AU - Blanco Miguez, Aitor

AU - Bowyer, Vicky

AU - Antonelli, Michela

AU - Snell, Olivia

AU - dos Santos Canas, Liane

AU - Hu, Christina

AU - Wolf, Jonathan

AU - Menni, Cristina

AU - Malim, Michael

AU - Hart, Deborah

AU - Spector, Tim

AU - Berry, Sarah

AU - Segata, Nicola

AU - Doores, Katie

AU - Ourselin, Sebastien

AU - Duncan, Emma L.

AU - Steves, Claire J.

N1 - Funding Information: We would like to acknowledge support from the Exetera development team (Benjamin Murray, Liyuan Chen, Jie Deng, Eric Kerfoot), the TwinsUK laboratory and administrative teams (Gulsah Akdag, Andy Anastasiou, Andrei Beleanu, Julia Brown, Maria Paz Garcia, Rachel Horsfall, Genevieve Lachance, Ayrun Nessa, Alyce Sheedy, Dovile Vaitkute, Sam Wadge, Sivasubramaniam Rajan Wignarajah, Darioush Yarand). We are also grateful to the CSS Biobank Volunteer Advisory Group for their input on the development of the biobank, and feedback on the significance of this work for affected individuals and the wider public. Funding Information: The CSS Biobank is supported by the Chronic Disease Research Foundation (Grant: CDRF 22/2020). We are also supported by the Wellcome EPSRC Centre for Medical Engineering at King's College London (WT 203148/Z/16/Z) and the UK Department of Health via the National Institute for Health Research (NIHR) comprehensive Biomedical Research Centre award to Guy's & St Thomas’ NHS Foundation Trust in partnership with King's College London and King's College Hospital NHS Foundation Trust. Investigators also received support from Medical Research Council (MRC) (Grant codes: MC_PC_20059 (CJS, SO), MR/T005351/1 and MR/V038664/1 (SO), MR/W005611/1 and MR/S023747/1 (MM)), British Heart Foundation (BHF), Alzheimer's Society, European Union, NIHR, COVID-19 Driver Relief Fund (CDRF) and the NIHR-funded BioResource, Clinical Research Facility and Biomedical Research Centre (BRC) based at GSTT NHS Foundation Trust in partnership with KCL. SO was supported by the French government, through the 3IA Côte d'Azur Investments in the Future project managed by the National Research Agency (ANR) with the reference number ANR-19-P3IA-0002. ZOE Limited provided in-kind support for all aspects of building, running and supporting the app and service to all users worldwide. This research was funded in part by the Wellcome Trust [215010/Z/18/Z]. Publisher Copyright: © 2023, The Author(s).

PY - 2023/6/27

Y1 - 2023/6/27

N2 - Whilst most individuals with SARS-CoV-2 infection have relatively mild disease, managed in the community, it was noted early in the pandemic that individuals with cardiovascular risk factors were more likely to experience severe acute disease, requiring hospitalisation. As the pandemic has progressed, increasing concern has also developed over long symptom duration in many individuals after SARS-CoV-2 infection, including among the majority who are managed acutely in the community. Risk factors for long symptom duration, including biological variables, are still poorly defined. Here, we examine post-illness metabolomic profiles, using nuclear magnetic resonance (Nightingale Health Oyj), and gut-microbiome profiles, using shotgun metagenomic sequencing (Illumina Inc), in 2561 community-dwelling participants with SARS-CoV-2. Illness duration ranged from asymptomatic (n = 307) to Post-COVID Syndrome (n = 180), and included participants with prolonged non-COVID-19 illnesses (n = 287). We also assess a pre-established metabolomic biomarker score, previously associated with hospitalisation for both acute pneumonia and severe acute COVID-19 illness, for its association with illness duration. We found an atherogenic-dyslipidaemic metabolic profile, including biomarkers such as fatty acids and cholesterol, was associated with longer duration of illness, both in individuals with and without SARS-CoV-2 infection. Greater values of a pre-existing metabolomic biomarker score also associated with longer duration of illness, regardless of SARS-CoV-2 infection. We found no association between illness duration and gut microbiome profiles in convalescence. This highlights the potential role of cardiometabolic dysfunction in relation to the experience of long duration symptoms after symptoms of acute infection, both COVID-19 as well as other illnesses.

AB - Whilst most individuals with SARS-CoV-2 infection have relatively mild disease, managed in the community, it was noted early in the pandemic that individuals with cardiovascular risk factors were more likely to experience severe acute disease, requiring hospitalisation. As the pandemic has progressed, increasing concern has also developed over long symptom duration in many individuals after SARS-CoV-2 infection, including among the majority who are managed acutely in the community. Risk factors for long symptom duration, including biological variables, are still poorly defined. Here, we examine post-illness metabolomic profiles, using nuclear magnetic resonance (Nightingale Health Oyj), and gut-microbiome profiles, using shotgun metagenomic sequencing (Illumina Inc), in 2561 community-dwelling participants with SARS-CoV-2. Illness duration ranged from asymptomatic (n = 307) to Post-COVID Syndrome (n = 180), and included participants with prolonged non-COVID-19 illnesses (n = 287). We also assess a pre-established metabolomic biomarker score, previously associated with hospitalisation for both acute pneumonia and severe acute COVID-19 illness, for its association with illness duration. We found an atherogenic-dyslipidaemic metabolic profile, including biomarkers such as fatty acids and cholesterol, was associated with longer duration of illness, both in individuals with and without SARS-CoV-2 infection. Greater values of a pre-existing metabolomic biomarker score also associated with longer duration of illness, regardless of SARS-CoV-2 infection. We found no association between illness duration and gut microbiome profiles in convalescence. This highlights the potential role of cardiometabolic dysfunction in relation to the experience of long duration symptoms after symptoms of acute infection, both COVID-19 as well as other illnesses.

KW - Humans

KW - COVID-19

KW - SARS-CoV-2

KW - Gastrointestinal Microbiome

KW - Pneumonia

KW - Hospitalization

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DO - 10.1038/s41598-023-34598-7

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SN - 2045-2322

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JO - Scientific Reports

JF - Scientific Reports

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M1 - 10407

ER -

Metabolomic and gut microbiome profiles across the spectrum of community-based COVID and non-COVID disease

Abstract

Keywords

UN SDGs

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