Metabolic and Lipidomic Markers Differentiate COVID-19 From Non-Hospitalized and Other Intensive Care Patients
Coronavirus disease 2019 (COVID-19) is a viral infection affecting multiple organ systems of great significance for metabolic processes. Thus, there is increasing interest in metabolic and lipoprotein signatures of the disease, and early analyses have demonstrated a metabolic pattern typical for ath...
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| Vydané v: | Frontiers in molecular biosciences Ročník 8; s. 737039 |
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Frontiers Media S.A
02.12.2021
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| Abstract | Coronavirus disease 2019 (COVID-19) is a viral infection affecting multiple organ systems of great significance for metabolic processes. Thus, there is increasing interest in metabolic and lipoprotein signatures of the disease, and early analyses have demonstrated a metabolic pattern typical for atherosclerotic and hepatic damage in COVID-19 patients. However, it remains unclear whether this is specific for COVID-19 and whether the observed signature is caused by the disease or rather represents an underlying risk factor. To answer this question, we have analyzed 482 serum samples using nuclear magnetic resonance metabolomics, including longitudinally collected samples from 12 COVID-19 and 20 cardiogenic shock intensive care patients, samples from 18 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibody-positive individuals, and single time point samples from 58 healthy controls. COVID-19 patients showed a distinct metabolic serum profile, including changes typical for severe dyslipidemia and a deeply altered metabolic status compared with healthy controls. Specifically, very-low-density lipoprotein and intermediate-density lipoprotein particles and associated apolipoprotein B and intermediate-density lipoprotein cholesterol were significantly increased, whereas cholesterol and apolipoprotein A2 were decreased. Moreover, a similarly perturbed profile was apparent when compared with other patients with cardiogenic shock who are in the intensive care unit when looking at a 1-week time course, highlighting close links between COVID-19 and lipid metabolism. The metabolic profile of COVID-19 patients distinguishes those from healthy controls and also from patients with cardiogenic shock. In contrast, anti-SARS-CoV-2 antibody-positive individuals without acute COVID-19 did not show a significantly perturbed metabolic profile compared with age- and sex-matched healthy controls, but SARS-CoV-2 antibody-titers correlated significantly with metabolic parameters, including levels of glycine, ApoA2, and small-sized low- and high-density lipoprotein subfractions. Our data suggest that COVID-19 is associated with dyslipidemia, which is not observed in anti-SARS-CoV-2 antibody-positive individuals who have not developed severe courses of the disease. This suggests that lipoprotein profiles may represent a confounding risk factor for COVID-19 with potential for patient stratification. |
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| AbstractList | Coronavirus disease 2019 (COVID-19) is a viral infection affecting multiple organ systems of great significance for metabolic processes. Thus, there is increasing interest in metabolic and lipoprotein signatures of the disease, and early analyses have demonstrated a metabolic pattern typical for atherosclerotic and hepatic damage in COVID-19 patients. However, it remains unclear whether this is specific for COVID-19 and whether the observed signature is caused by the disease or rather represents an underlying risk factor. To answer this question, we have analyzed 482 serum samples using nuclear magnetic resonance metabolomics, including longitudinally collected samples from 12 COVID-19 and 20 cardiogenic shock intensive care patients, samples from 18 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibody-positive individuals, and single time point samples from 58 healthy controls. COVID-19 patients showed a distinct metabolic serum profile, including changes typical for severe dyslipidemia and a deeply altered metabolic status compared with healthy controls. Specifically, very-low-density lipoprotein and intermediate-density lipoprotein particles and associated apolipoprotein B and intermediate-density lipoprotein cholesterol were significantly increased, whereas cholesterol and apolipoprotein A2 were decreased. Moreover, a similarly perturbed profile was apparent when compared with other patients with cardiogenic shock who are in the intensive care unit when looking at a 1-week time course, highlighting close links between COVID-19 and lipid metabolism. The metabolic profile of COVID-19 patients distinguishes those from healthy controls and also from patients with cardiogenic shock. In contrast, anti-SARS-CoV-2 antibody-positive individuals without acute COVID-19 did not show a significantly perturbed metabolic profile compared with age- and sex-matched healthy controls, but SARS-CoV-2 antibody-titers correlated significantly with metabolic parameters, including levels of glycine, ApoA2, and small-sized low- and high-density lipoprotein subfractions. Our data suggest that COVID-19 is associated with dyslipidemia, which is not observed in anti-SARS-CoV-2 antibody-positive individuals who have not developed severe courses of the disease. This suggests that lipoprotein profiles may represent a confounding risk factor for COVID-19 with potential for patient stratification. Coronavirus disease 2019 (COVID-19) is a viral infection affecting multiple organ systems of great significance for metabolic processes. Thus, there is increasing interest in metabolic and lipoprotein signatures of the disease, and early analyses have demonstrated a metabolic pattern typical for atherosclerotic and hepatic damage in COVID-19 patients. However, it remains unclear whether this is specific for COVID-19 and whether the observed signature is caused by the disease or rather represents an underlying risk factor. To answer this question, we have analyzed 482 serum samples using nuclear magnetic resonance metabolomics, including longitudinally collected samples from 12 COVID-19 and 20 cardiogenic shock intensive care patients, samples from 18 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibody-positive individuals, and single time point samples from 58 healthy controls. COVID-19 patients showed a distinct metabolic serum profile, including changes typical for severe dyslipidemia and a deeply altered metabolic status compared with healthy controls. Specifically, very-low-density lipoprotein and intermediate-density lipoprotein particles and associated apolipoprotein B and intermediate-density lipoprotein cholesterol were significantly increased, whereas cholesterol and apolipoprotein A2 were decreased. Moreover, a similarly perturbed profile was apparent when compared with other patients with cardiogenic shock who are in the intensive care unit when looking at a 1-week time course, highlighting close links between COVID-19 and lipid metabolism. The metabolic profile of COVID-19 patients distinguishes those from healthy controls and also from patients with cardiogenic shock. In contrast, anti-SARS-CoV-2 antibody-positive individuals without acute COVID-19 did not show a significantly perturbed metabolic profile compared with age- and sex-matched healthy controls, but SARS-CoV-2 antibody-titers correlated significantly with metabolic parameters, including levels of glycine, ApoA2, and small-sized low- and high-density lipoprotein subfractions. Our data suggest that COVID-19 is associated with dyslipidemia, which is not observed in anti-SARS-CoV-2 antibody-positive individuals who have not developed severe courses of the disease. This suggests that lipoprotein profiles may represent a confounding risk factor for COVID-19 with potential for patient stratification.Coronavirus disease 2019 (COVID-19) is a viral infection affecting multiple organ systems of great significance for metabolic processes. Thus, there is increasing interest in metabolic and lipoprotein signatures of the disease, and early analyses have demonstrated a metabolic pattern typical for atherosclerotic and hepatic damage in COVID-19 patients. However, it remains unclear whether this is specific for COVID-19 and whether the observed signature is caused by the disease or rather represents an underlying risk factor. To answer this question, we have analyzed 482 serum samples using nuclear magnetic resonance metabolomics, including longitudinally collected samples from 12 COVID-19 and 20 cardiogenic shock intensive care patients, samples from 18 severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) antibody-positive individuals, and single time point samples from 58 healthy controls. COVID-19 patients showed a distinct metabolic serum profile, including changes typical for severe dyslipidemia and a deeply altered metabolic status compared with healthy controls. Specifically, very-low-density lipoprotein and intermediate-density lipoprotein particles and associated apolipoprotein B and intermediate-density lipoprotein cholesterol were significantly increased, whereas cholesterol and apolipoprotein A2 were decreased. Moreover, a similarly perturbed profile was apparent when compared with other patients with cardiogenic shock who are in the intensive care unit when looking at a 1-week time course, highlighting close links between COVID-19 and lipid metabolism. The metabolic profile of COVID-19 patients distinguishes those from healthy controls and also from patients with cardiogenic shock. In contrast, anti-SARS-CoV-2 antibody-positive individuals without acute COVID-19 did not show a significantly perturbed metabolic profile compared with age- and sex-matched healthy controls, but SARS-CoV-2 antibody-titers correlated significantly with metabolic parameters, including levels of glycine, ApoA2, and small-sized low- and high-density lipoprotein subfractions. Our data suggest that COVID-19 is associated with dyslipidemia, which is not observed in anti-SARS-CoV-2 antibody-positive individuals who have not developed severe courses of the disease. This suggests that lipoprotein profiles may represent a confounding risk factor for COVID-19 with potential for patient stratification. |
| Author | Ragab, Mohab Eitel, Ingo Ehlers, Marc Meyer-Saraei, Roza Lixenfeld, Anne Sophie Martin, Emily Graf, Tobias Sina, Christian Lehrian, Selina Künsting, Inga Käding, Nadja von Kopylow, Vera Föh, Bandik Taube, Stefan Kreutzmann, Fabian Mallagaray, Alvaro Rahmöller, Johann Günther, Ulrich L. Schmelter, Franziska Jantzen, Eckard |
| AuthorAffiliation | 2 Research and Development Department, GALAB Laboratories GmbH, Hamburg , Germany 3 Medical Department I, University Hospital Schleswig-Holstein, Lübeck , Germany 9 Department of Infectious Diseases and Microbiology, University of Lübeck, Lübeck , Germany 8 Institute of Virology and Cell Biology, University of Lübeck, Lübeck , Germany 1 Institute of Nutritional Medicine, University of Lübeck, Lübeck , Germany 6 Department of Cardiology, Angiology and Intensive Care Medicine, University Heart Center Lübeck, Lübeck , Germany 5 Department of Anesthesiology and Intensive Care, University Medical Center Schleswig-Holstein, Lübeck , Germany 7 German Centre for Cardiovascular Research (DZHK), Partner Site Hamburg/Kiel/Lübeck, Lübeck , Germany 4 Institute of Chemistry and Metabolomics, University of Lübeck, Lübeck , Germany |
| AuthorAffiliation_xml | – name: 1 Institute of Nutritional Medicine, University of Lübeck, Lübeck , Germany – name: 6 Department of Cardiology, Angiology and Intensive Care Medicine, University Heart Center Lübeck, Lübeck , Germany – name: 3 Medical Department I, University Hospital Schleswig-Holstein, Lübeck , Germany – name: 5 Department of Anesthesiology and Intensive Care, University Medical Center Schleswig-Holstein, Lübeck , Germany – name: 9 Department of Infectious Diseases and Microbiology, University of Lübeck, Lübeck , Germany – name: 4 Institute of Chemistry and Metabolomics, University of Lübeck, Lübeck , Germany – name: 7 German Centre for Cardiovascular Research (DZHK), Partner Site Hamburg/Kiel/Lübeck, Lübeck , Germany – name: 2 Research and Development Department, GALAB Laboratories GmbH, Hamburg , Germany – name: 8 Institute of Virology and Cell Biology, University of Lübeck, Lübeck , Germany |
| Author_xml | – sequence: 1 givenname: Franziska surname: Schmelter fullname: Schmelter, Franziska – sequence: 2 givenname: Bandik surname: Föh fullname: Föh, Bandik – sequence: 3 givenname: Alvaro surname: Mallagaray fullname: Mallagaray, Alvaro – sequence: 4 givenname: Johann surname: Rahmöller fullname: Rahmöller, Johann – sequence: 5 givenname: Marc surname: Ehlers fullname: Ehlers, Marc – sequence: 6 givenname: Selina surname: Lehrian fullname: Lehrian, Selina – sequence: 7 givenname: Vera surname: von Kopylow fullname: von Kopylow, Vera – sequence: 8 givenname: Inga surname: Künsting fullname: Künsting, Inga – sequence: 9 givenname: Anne Sophie surname: Lixenfeld fullname: Lixenfeld, Anne Sophie – sequence: 10 givenname: Emily surname: Martin fullname: Martin, Emily – sequence: 11 givenname: Mohab surname: Ragab fullname: Ragab, Mohab – sequence: 12 givenname: Roza surname: Meyer-Saraei fullname: Meyer-Saraei, Roza – sequence: 13 givenname: Fabian surname: Kreutzmann fullname: Kreutzmann, Fabian – sequence: 14 givenname: Ingo surname: Eitel fullname: Eitel, Ingo – sequence: 15 givenname: Stefan surname: Taube fullname: Taube, Stefan – sequence: 16 givenname: Nadja surname: Käding fullname: Käding, Nadja – sequence: 17 givenname: Eckard surname: Jantzen fullname: Jantzen, Eckard – sequence: 18 givenname: Tobias surname: Graf fullname: Graf, Tobias – sequence: 19 givenname: Christian surname: Sina fullname: Sina, Christian – sequence: 20 givenname: Ulrich L. surname: Günther fullname: Günther, Ulrich L. |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/34938772$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | Copyright © 2021 Schmelter, Föh, Mallagaray, Rahmöller, Ehlers, Lehrian, von Kopylow, Künsting, Lixenfeld, Martin, Ragab, Meyer-Saraei, Kreutzmann, Eitel, Taube, Käding, Jantzen, Graf, Sina and Günther. Copyright © 2021 Schmelter, Föh, Mallagaray, Rahmöller, Ehlers, Lehrian, von Kopylow, Künsting, Lixenfeld, Martin, Ragab, Meyer-Saraei, Kreutzmann, Eitel, Taube, Käding, Jantzen, Graf, Sina and Günther. 2021 Schmelter, Föh, Mallagaray, Rahmöller, Ehlers, Lehrian, von Kopylow, Künsting, Lixenfeld, Martin, Ragab, Meyer-Saraei, Kreutzmann, Eitel, Taube, Käding, Jantzen, Graf, Sina and Günther |
| Copyright_xml | – notice: Copyright © 2021 Schmelter, Föh, Mallagaray, Rahmöller, Ehlers, Lehrian, von Kopylow, Künsting, Lixenfeld, Martin, Ragab, Meyer-Saraei, Kreutzmann, Eitel, Taube, Käding, Jantzen, Graf, Sina and Günther. – notice: Copyright © 2021 Schmelter, Föh, Mallagaray, Rahmöller, Ehlers, Lehrian, von Kopylow, Künsting, Lixenfeld, Martin, Ragab, Meyer-Saraei, Kreutzmann, Eitel, Taube, Käding, Jantzen, Graf, Sina and Günther. 2021 Schmelter, Föh, Mallagaray, Rahmöller, Ehlers, Lehrian, von Kopylow, Künsting, Lixenfeld, Martin, Ragab, Meyer-Saraei, Kreutzmann, Eitel, Taube, Käding, Jantzen, Graf, Sina and Günther |
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| Keywords | COVID-19 NMR SARS-CoV-2 metabolomics lipoproteins |
| Language | English |
| License | Copyright © 2021 Schmelter, Föh, Mallagaray, Rahmöller, Ehlers, Lehrian, von Kopylow, Künsting, Lixenfeld, Martin, Ragab, Meyer-Saraei, Kreutzmann, Eitel, Taube, Käding, Jantzen, Graf, Sina and Günther. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Sander Kooijman, Leiden University Medical Center, Netherlands Toby James Athersuch, Imperial College London, United Kingdom These authors have contributed equally to this work and share senior authorship These authors have contributed equally to this work and share first authorship This article was submitted to Metabolomics, a section of the journal Frontiers in Molecular Biosciences Edited by: Emmanuel Mikros, National and Kapodistrian University of Athens, Greece |
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