{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T05:46:17Z","timestamp":1790833577228,"version":"4.1.0"},"reference-count":95,"publisher":"American Chemical Society (ACS)","issue":"6","license":[{"start":{"date-parts":[[2021,5,19]],"date-time":"2021-05-19T00:00:00Z","timestamp":1621382400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by-nc-nd\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100000265","name":"Medical Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000265","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000923","name":"Australian Research Council","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000923","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100011025","name":"Government of Western Australia","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100011025","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100022560","name":"Spinnaker Health Research Foundation","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100022560","id-type":"DOI","asserted-by":"crossref"}]},{"name":"McCusker Foundation"},{"name":"Western Australia State Government"},{"DOI":"10.13039\/501100025520","name":"Medical Research Future Fund","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100025520","id-type":"DOI","asserted-by":"crossref"}]},{"DOI":"10.13039\/501100020578","name":"Department of Jobs, Tourism, Science and Innovation, Government of Western Australia","doi-asserted-by":"crossref","id":[{"id":"10.13039\/501100020578","id-type":"DOI","asserted-by":"crossref"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2021,6,4]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>We present a multivariate metabotyping approach to assess the functional recovery of nonhospitalized COVID-19 patients and the possible biochemical sequelae of \u201cPost-Acute COVID-19 Syndrome\u201d, colloquially known as long-COVID. Blood samples were taken from patients ca. 3 months after acute COVID-19 infection with further assessment of symptoms at 6 months. Some 57% of the patients had one or more persistent symptoms including respiratory-related symptoms like cough, dyspnea, and rhinorrhea or other nonrespiratory symptoms including chronic fatigue, anosmia, myalgia, or joint pain. Plasma samples were quantitatively analyzed for lipoproteins, glycoproteins, amino acids, biogenic amines, and tryptophan pathway intermediates using Nuclear Magnetic Resonance (NMR) spectroscopy and mass spectrometry. Metabolic data for the follow-up patients (n = 27) were compared with controls (n = 41) and hospitalized severe acute respiratory syndrome SARS-CoV-2 positive patients (n = 18, with multiple time-points). Univariate and multivariate statistics revealed variable patterns of functional recovery with many patients exhibiting residual COVID-19 biomarker signatures. Several parameters were persistently perturbed, e.g., elevated taurine (p = 3.6 \u00d7 10\u20133 versus controls) and reduced glutamine\/glutamate ratio (p = 6.95 \u00d7 10\u20138 versus controls), indicative of possible liver and muscle damage and a high energy demand linked to more generalized tissue repair or immune function. Some parameters showed near-complete normalization, e.g., the plasma apolipoprotein B100\/A1 ratio was similar to that of healthy controls but significantly lower (p = 4.2 \u00d7 10\u20133) than post-acute COVID-19 patients, reflecting partial reversion of the metabolic phenotype (phenoreversion) toward the healthy metabolic state. Plasma neopterin was normalized in all follow-up patients, indicative of a reduction in the adaptive immune activity that has been previously detected in active SARS-CoV-2 infection. Other systemic inflammatory biomarkers such as GlycA and the kynurenine\/tryptophan ratio remained elevated in some, but not all, patients. Correlation analysis, principal component analysis (PCA), and orthogonal-partial least-squares discriminant analysis (O-PLS-DA) showed that the follow-up patients were, as a group, metabolically distinct from controls and partially comapped with the acute-phase patients. Significant systematic metabolic differences between asymptomatic and symptomatic follow-up patients were also observed for multiple metabolites. The overall metabolic variance of the symptomatic patients was significantly greater than that of nonsymptomatic patients for multiple parameters (\u03c72p = 0.014). Thus, asymptomatic follow-up patients including those with post-acute COVID-19 Syndrome displayed a spectrum of multiple persistent biochemical pathophysiology, suggesting that the metabolic phenotyping approach may be deployed for multisystem functional assessment of individual post-acute COVID-19 patients.<\/jats:p>","DOI":"10.1021\/acs.jproteome.1c00224","type":"journal-article","created":{"date-parts":[[2021,5,19]],"date-time":"2021-05-19T14:03:15Z","timestamp":1621432995000},"page":"3315-3329","source":"Crossref","is-referenced-by-count":121,"title":["Incomplete Systemic\nRecovery and Metabolic Phenoreversion\nin Post-Acute-Phase Nonhospitalized COVID-19 Patients: Implications\nfor Assessment of Post-Acute COVID-19 Syndrome"],"prefix":"10.1021","volume":"20","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0556-8389","authenticated-orcid":true,"given":"Elaine","family":"Holmes","sequence":"first","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin 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,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9193-0462","authenticated-orcid":true,"given":"Samantha","family":"Lodge","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]},{"name":"Murdoch University , , 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Philipp","family":"Nitschke","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, 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, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]},{"name":"Murdoch University , , 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"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 , , 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sofina","family":"Begum","sequence":"additional","affiliation":[{"name":"Imperial College London , , Sir Alexander Fleming Building , South Kensington, ,","place":["London, U.K., SW7 2AZ"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6342-9814","authenticated-orcid":true,"given":"Berin","family":"Boughton","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]},{"name":"Murdoch University , , 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rongchang","family":"Yang","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aude-Claire","family":"Morillon","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sung-Tong","family":"Chin","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Drew","family":"Hall","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Monique","family":"Ryan","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3313-5097","authenticated-orcid":true,"given":"Sze-How","family":"Bong","sequence":"additional","affiliation":[{"name":"Murdoch University , , Harry Perkins Building, 5 Robin Warren Drive , , ,","place":["Perth, WA, Australia, 6150"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Melvin","family":"Gay","sequence":"additional","affiliation":[{"name":"Bruker Pty. 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Persistent Symptoms in Patients After Acute COVID-19","volume":"324","author":"Carfi\u0300","year":"2020","journal-title":"JAMA"},{"key":"2026081415105024700_cit3","doi-asserted-by":"publisher","first-page":"00542","DOI":"10.1183\/23120541.00542-2020","article-title":"Persistent\nSymptoms 3 Months after a SARS-CoV-2 Infection: The Post-COVID-19\nSyndrome?","volume":"6","author":"Goe\u0308rtz","year":"2020","journal-title":"ERJ Open Res."},{"key":"2026081415105024700_cit4","doi-asserted-by":"publisher","DOI":"10.1016\/j.eclinm.2020.100683","article-title":"Medium-Term Effects\nof SARS-CoV-2 Infection on Multiple Vital Organs, Exercise Capacity,\nCognition, Quality of Life and Mental Health, Post-Hospital Discharge","volume":"31","author":"Raman","year":"2021","journal-title":"EClinicalMedicine"},{"key":"2026081415105024700_cit5","doi-asserted-by":"publisher","first-page":"396","DOI":"10.1136\/thoraxjnl-2020-215818","article-title":"\u201cLong-COVID\u201d:\nA Cross-Sectional Study of Persisting Symptoms, Biomarker and Imaging\nAbnormalities Following Hospitalisation for COVID-19","volume":"76","author":"Mandal","year":"2021","journal-title":"Thorax"},{"key":"2026081415105024700_cit6","doi-asserted-by":"publisher","DOI":"10.1093\/braincomms\/fcaa205","article-title":"Frequent Neurocognitive Deficits\nafter Recovery from Mild COVID-19","volume":"2","author":"Woo","year":"2020","journal-title":"Brain Commun."},{"key":"2026081415105024700_cit7","doi-asserted-by":"publisher","first-page":"1095","DOI":"10.1002\/lary.29383","article-title":"COVID-19: Recovery\nfrom Chemosensory\nDysfunction. A Multicentre Study on Smell and Taste","volume":"131","author":"Niklassen","year":"2021","journal-title":"Laryngoscope"},{"key":"2026081415105024700_cit8","doi-asserted-by":"publisher","first-page":"1265","DOI":"10.1001\/jamacardio.2020.3557","article-title":"Outcomes of Cardiovascular\nMagnetic Resonance Imaging in Patients Recently Recovered From Coronavirus\nDisease 2019 (COVID-19)","volume":"5","author":"Puntmann","year":"2020","journal-title":"JAMA Cardiol."},{"key":"2026081415105024700_cit9","doi-asserted-by":"publisher","first-page":"176","DOI":"10.7150\/ijms.50691","article-title":"Liver Function Recovery\nof COVID-19 Patients after Discharge, a Follow-up Study","volume":"18","author":"An","year":"2021","journal-title":"Int. J. Med. Sci."},{"key":"2026081415105024700_cit10","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/S1473-3099(20)30986-5","article-title":"Long COVID\nin the Skin: A Registry Analysis of COVID-19 Dermatological Duration","volume":"21","author":"McMahon","year":"2021","journal-title":"Lancet Infect. Dis."},{"key":"2026081415105024700_cit11","doi-asserted-by":"publisher","DOI":"10.1016\/j.mehy.2020.110345","article-title":"The Triggering\nof Post-COVID-19 Autoimmunity Phenomena Could Be Associated with Both\nTransient Immunosuppression and an Inappropriate Form of Immune Reconstitution\nin Susceptible Individuals","volume":"145","author":"Can\u0303as","year":"2020","journal-title":"Med. Hypotheses"},{"key":"2026081415105024700_cit12","doi-asserted-by":"publisher","first-page":"789","DOI":"10.1056\/NEJMc2018688","article-title":"New-Onset\nDiabetes in Covid-19","volume":"383","author":"Rubino","year":"2020","journal-title":"N. Engl. J. Med."},{"key":"2026081415105024700_cit13","doi-asserted-by":"publisher","DOI":"10.1016\/j.cyto.2020.155404","article-title":"Cytokine Storm Induced\nby SARS-CoV-2\nInfection: The Spectrum of Its Neurological Manifestations","volume":"138","author":"Thepmankorn","year":"2021","journal-title":"Cytokine"},{"key":"2026081415105024700_cit14","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1016\/j.cytogfr.2020.05.003","article-title":"The Cytokine\nStorm in COVID-19: An Overview of the Involvement of the Chemokine\/chemokine-Receptor\nSystem","volume":"53","author":"Coperchini","year":"2020","journal-title":"Cytokine Growth Factor Rev."},{"key":"2026081415105024700_cit15","first-page":"21","article-title":"Long-Term Sequelae of SARS: Physical,\nNeuropsychiatric,\nand Quality-of-Life Assessment","volume":"15","author":"Hui","year":"2009","journal-title":"Hong Kong Med.\nJ."},{"key":"2026081415105024700_cit16","doi-asserted-by":"publisher","first-page":"e68","DOI":"10.7861\/clinmed.2020-0204","article-title":"Long-Term\nSequelae Following Previous Coronavirus Epidemics","volume":"21","author":"O\u2019Sullivan","year":"2021","journal-title":"Clin. 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Proteome Res."},{"key":"2026081415105024700_cit25","doi-asserted-by":"publisher","first-page":"59.e15","DOI":"10.1016\/j.cell.2020.05.032","article-title":"Proteomic\nand Metabolomic Characterization\nof COVID-19 Patient Sera","volume":"182","author":"Shen","year":"2020","journal-title":"Cell"},{"issue":"5","key":"2026081415105024700_cit26","doi-asserted-by":"publisher","first-page":"2796","DOI":"10.1021\/acs.jproteome.1c00052","article-title":"Systemic\nPerturbations in Amine and\nKynurenine Metabolism Associated with Acute SARS-CoV-2 Infection and\nInflammatory Cytokine Responses","volume":"20","author":"Lawler","year":"2021","journal-title":"J. Proteome\nRes."},{"key":"2026081415105024700_cit27","doi-asserted-by":"publisher","DOI":"10.1016\/j.isci.2020.101645","article-title":"SARS-CoV-2\nInfection Dysregulates the Metabolomic and\nLipidomic Profiles of Serum","volume":"23","author":"Bruzzone","year":"2020","journal-title":"iScience"},{"key":"2026081415105024700_cit28","doi-asserted-by":"publisher","DOI":"10.1371\/journal.ppat.1009243","article-title":"Metabolomic\/lipidomic Profiling of COVID-19 and Individual\nResponse to Tocilizumab","volume":"17","author":"Meoni","year":"2021","journal-title":"PLoS Pathog."},{"key":"2026081415105024700_cit29","doi-asserted-by":"publisher","DOI":"10.1001\/jamanetworkopen.2020.36142","article-title":"Respiratory and Psychophysical Sequelae\nAmong Patients With COVID-19 Four Months After Hospital Discharge","volume":"4","author":"Bellan","year":"2021","journal-title":"JAMA Network Open"},{"key":"2026081415105024700_cit30","doi-asserted-by":"publisher","first-page":"29","DOI":"10.7150\/ijms.49728","article-title":"Longitudinal Clinical and Radiographic Evaluation Reveals Interleukin-6\nas an Indicator of Persistent Pulmonary Injury in COVID-19","volume":"18","author":"Liao","year":"2021","journal-title":"Int. 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