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Thus, 600 MHz 1H solvent-suppressed single-pulse, spin-echo, and 2D J-resolved spectra were collected on plasma recorded from SARS-CoV-2 rRT-PCR-positive patients (n = 15, with multiple sampling timepoints) and age-matched healthy controls (n = 34, confirmed rRT-PCR negative), together with patients with COVID-19\/influenza-like clinical symptoms who tested SARS-CoV-2 negative (n = 35). We compared the single-pulse NMR spectral data with in vitro diagnostic research (IVDr) information on quantitative lipoprotein profiles (112 parameters) extracted from the raw 1D NMR data. All NMR methods gave highly significant discrimination of SARS-CoV-2 positive patients from controls and SARS-CoV-2 negative patients with individual NMR methods, giving different diagnostic information windows on disease-induced phenoconversion. Longitudinal trajectory analysis in selected patients indicated that metabolic recovery was incomplete in individuals without detectable virus in the recovery phase. We observed four plasma cytokine clusters that expressed complex differential statistical relationships with multiple lipoproteins and metabolites. These included the following: cluster 1, comprising MIP-1\u03b2, SDF-1\u03b1, IL-22, and IL-1\u03b1, which correlated with multiple increased LDL and VLDL subfractions; cluster 2, including IL-10 and IL-17A, which was only weakly linked to the lipoprotein profile; cluster 3, which included IL-8 and MCP-1 and were inversely correlated with multiple lipoproteins. IL-18, IL-6, and IFN-\u03b3 together with IP-10 and RANTES exhibited strong positive correlations with LDL1\u20134 subfractions and negative correlations with multiple HDL subfractions. Collectively, these data show a distinct pattern indicative of a multilevel cellular immune response to SARS CoV-2 infection interacting with the plasma lipoproteome giving a strong and characteristic immunometabolic phenotype of the disease. We observed that some patients in the respiratory recovery phase and testing virus-free were still metabolically highly abnormal, which indicates a new role for these technologies in assessing full systemic recovery.<\/jats:p>","DOI":"10.1021\/acs.jproteome.0c00876","type":"journal-article","created":{"date-parts":[[2021,1,13]],"date-time":"2021-01-13T18:50:12Z","timestamp":1610563812000},"page":"1382-1396","source":"Crossref","is-referenced-by-count":84,"title":["NMR Spectroscopic\nWindows on the Systemic Effects\nof SARS-CoV-2 Infection on Plasma Lipoproteins and Metabolites\nin Relation to Circulating Cytokines"],"prefix":"10.1021","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-9193-0462","authenticated-orcid":true,"given":"Samantha","family":"Lodge","sequence":"first","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Murdoch University , , , ,","place":["Murdoch, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philipp","family":"Nitschke","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7158-9930","authenticated-orcid":true,"given":"Torben","family":"Kimhofer","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Murdoch University , , , ,","place":["Murdoch, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jerome D.","family":"Coudert","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Perron Institute for Neurological and Translational Science , , ,","place":["Nedlands, Western Australia, Australia, 6009"]},{"name":"University of Notre Dame , , , ,","place":["Fremantle, Western Australia, Australia, 6160"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sofina","family":"Begum","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Imperial College London , , ,","place":["London, U.K., SW7 2AZ"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sze-How","family":"Bong","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Toby","family":"Richards","sequence":"additional","affiliation":[{"name":"University of Western Australia , , Harry Perkins Building, Robert Warren Drive , Murdoch, , ,","place":["Perth, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dale","family":"Edgar","sequence":"additional","affiliation":[{"name":"University of Western Australia , , Harry Perkins Building, Robert Warren Drive , Murdoch, , ,","place":["Perth, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Edward","family":"Raby","sequence":"additional","affiliation":[{"name":"PathWest Laboratory Medicine WA , , Murdoch, , ,","place":["Perth, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manfred","family":"Spraul","sequence":"additional","affiliation":[{"name":"Biospin GmbH , Silberstreifen, ,","place":["Ettlingen, Germany, 76275"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hartmut","family":"Schaefer","sequence":"additional","affiliation":[{"name":"Biospin GmbH , Silberstreifen, ,","place":["Ettlingen, Germany, 76275"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0916-6360","authenticated-orcid":true,"given":"John C.","family":"Lindon","sequence":"additional","affiliation":[{"name":"Imperial College London , , ,","place":["London, U.K., SW7 2AZ"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5307-5709","authenticated-orcid":true,"given":"Ruey Leng","family":"Loo","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Murdoch University , , , ,","place":["Murdoch, Western Australia, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0556-8389","authenticated-orcid":true,"given":"Elaine","family":"Holmes","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Murdoch University , , , ,","place":["Murdoch, Western Australia, Australia, 6150"]},{"name":"Imperial College London , , ,","place":["London, U.K., SW7 2AZ"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeremy K.","family":"Nicholson","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building , , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Murdoch University , , , ,","place":["Murdoch, Western Australia, Australia, 6150"]},{"name":"University of Western Australia , , Harry Perkins Building, Robert Warren Drive , Murdoch, , ,","place":["Perth, Western Australia, Australia, 6150"]},{"name":"Imperial College London , , Level 1, Faculty Building South Kensington Campus , ,","place":["London, U.K., SW7 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Med."},{"key":"2026090111332024800_cit5","doi-asserted-by":"publisher","DOI":"10.1017\/s0950268820002332","article-title":"Clinical characteristics\nof imported and second-generation coronavirus disease 2019 (COVID-19)\ncases in Shaanxi outside Wuhan, China: a multicentre retrospective\nstudy","volume":"148","author":"Shi","year":"2020","journal-title":"Epidemiol. Infect."},{"key":"2026090111332024800_cit6","doi-asserted-by":"publisher","first-page":"259","DOI":"10.1038\/s41569-020-0360-5","article-title":"COVID-19 and\nthe cardiovascular\nsystem","volume":"17","author":"Zheng","year":"2020","journal-title":"Nat. Rev. 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Chem."},{"key":"2026090111332024800_cit21","doi-asserted-by":"publisher","first-page":"8004","DOI":"10.1021\/acs.analchem.7b01329","article-title":"Toward\nReliable Lipoprotein Particle Predictions from NMR Spectra of Human\nBlood: An Interlaboratory Ring Test","volume":"89","author":"Monsonis Centelles","year":"2017","journal-title":"Anal. Chem."},{"key":"2026090111332024800_cit22","doi-asserted-by":"publisher","first-page":"11962","DOI":"10.1021\/acs.analchem.8b02412","article-title":"Quantitative\nLipoprotein Subclass and Low Molecular Weight Metabolite Analysis\nin Human Serum and Plasma by (1)H NMR Spectroscopy in a Multilaboratory\nTrial","volume":"90","author":"Jime\u0301nez","year":"2018","journal-title":"Anal. 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Hematol."},{"key":"2026090111332024800_cit35","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0223692","article-title":"Elevated serum alpha-1\nantitrypsin is a major component\nof GlycA-associated risk for future morbidity and mortality","volume":"14","author":"Ritchie","year":"2019","journal-title":"PLoS One"},{"key":"2026090111332024800_cit36","doi-asserted-by":"publisher","first-page":"76","DOI":"10.1007\/s11306-020-01695-x","article-title":"GlycA, a novel marker for low grade inflammation, reflects\ngut microbiome diversity and is more accurate than high sensitive\nCRP in reflecting metabolomic profile","volume":"16","author":"Mokkala","year":"2020","journal-title":"Metabolomics"},{"key":"2026090111332024800_cit37","doi-asserted-by":"publisher","first-page":"635","DOI":"10.1021\/acs.jproteome.6b00710","article-title":"Metabolic Phenotype of Obesity in\na Saudi Population","volume":"16","author":"Ahmad","year":"2017","journal-title":"J. Proteome Res."},{"key":"2026090111332024800_cit38","doi-asserted-by":"publisher","first-page":"916","DOI":"10.1373\/clinchem.2006.081166","article-title":"Diagnostic accuracy\nof blood lactate-to-pyruvate molar\nratio in the differential diagnosis of congenital lactic acidosis","volume":"53","author":"Debray","year":"2007","journal-title":"Clin. Chem."},{"key":"2026090111332024800_cit39","doi-asserted-by":"publisher","first-page":"3370","DOI":"10.1021\/ac960426p","article-title":"High-resolution diffusion and relaxation\nedited one- and two-dimensional 1H NMR spectroscopy of biological\nfluids","volume":"68","author":"Liu","year":"1996","journal-title":"Anal. 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Pharmacol."},{"key":"2026090111332024800_cit44","doi-asserted-by":"publisher","first-page":"639","DOI":"10.1021\/tx049869b","article-title":"Metabonomic\ndeconvolution of embedded toxicity: application to thioacetamide hepato-\nand nephrotoxicity","volume":"18","author":"Waters","year":"2005","journal-title":"Chem. Res. Toxicol."},{"key":"2026090111332024800_cit45","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1021\/tx034212w","article-title":"Geometric\ntrajectory analysis of metabolic responses to toxicity can define\ntreatment specific profiles","volume":"17","author":"Keun","year":"2004","journal-title":"Chem. Res. 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