{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,1]],"date-time":"2026-10-01T19:30:35Z","timestamp":1790883035939,"version":"4.1.0"},"reference-count":47,"publisher":"MDPI AG","issue":"5","license":[{"start":{"date-parts":[[2024,3,2]],"date-time":"2024-03-02T00:00:00Z","timestamp":1709337600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["JCM"],"abstract":"<jats:p>Background: Post-COVID-19 syndrome, characterized by persistent symptoms emerging more than 12 weeks after acute infection, displays diverse manifestations. This study aimed to analyze co-existing organ dysfunctions in post-COVID-19 patients and explore their potential association with the acute COVID-19 episode and functional impairment. Methods: Data from 238 patients attending post-COVID-19 outpatient care between 1 March 2021 and 1 March 2022, after previous hospitalization for acute COVID-19, were retrospectively analyzed with 80 having comprehensive mapping of organ involvement. Results: The average time between acute episode and post-COVID-19 care was 149 days. Spirometry indicated significant abnormalities in lung function. Predominant symptoms included respiratory (75%), fatigue (73%), neurological (62.5%), and ear-nose-throat issues (51.25%). Multiorgan dysfunctions were observed in 87.5% of patients, contributing to an 18.33% reduction in health quality compared to pre-acute COVID-19 levels. Subgroup analysis identified four distinct post-COVID-19 syndrome subgroups, highlighting the coexistence of respiratory and neurological disorders as potential indicators and drivers of further organ involvement. Our results reveal that most patients with post-COVID-19 syndrome suffer from multiorgan disorders. Conclusions: The presence of coexisting respiratory and neurological symptoms suggests the involvement of other organ systems as well. The complexity of multiorgan involvement requires further studies to provide insights into the different symptom clusters and identify potential targets for personalized preventive and therapeutic interventions to improve patient outcome.<\/jats:p>","DOI":"10.3390\/jcm13051457","type":"journal-article","created":{"date-parts":[[2024,3,4]],"date-time":"2024-03-04T04:36:21Z","timestamp":1709526981000},"page":"1457","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Co-Morbidity Clusters in Post-COVID-19 Syndrome"],"prefix":"10.3390","volume":"13","author":[{"given":"Anna Ter\u00e9z","family":"S\u00e1rk\u00f6zi","sequence":"first","affiliation":[{"name":"Department of Pulmonology, University of Debrecen, 4032 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-2165-4196","authenticated-orcid":false,"given":"Ilona","family":"Tornyi","sequence":"additional","affiliation":[{"name":"Department of Pulmonology, University of Debrecen, 4032 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Erik","family":"B\u00e9k\u00e9si","sequence":"additional","affiliation":[{"name":"Department of Pulmonology, University of Debrecen, 4032 Debrecen, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ildik\u00f3","family":"Horv\u00e1th","sequence":"additional","affiliation":[{"name":"Department of Pulmonology, University of Debrecen, 4032 Debrecen, Hungary"},{"name":"National Koranyi Institute of Pulmonology, 1121 Budapest, Hungary"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,3,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1038\/s41591-021-01283-z","article-title":"Post-acute COVID-19 syndrome","volume":"27","author":"Nalbandian","year":"2021","journal-title":"Nat. Med."},{"key":"ref_2","unstructured":"World Health Organisation (2023, December 22). Post COVID-19 Condition (Long COVID). Available online: https:\/\/www.who.int\/europe\/news-room\/fact-sheets\/item\/post-covid-19-condition."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"o2232","DOI":"10.1136\/bmj.o2232","article-title":"COVID-19: WHO urges action as 17 million long Covid cases are estimated in Europe","volume":"378","author":"Wise","year":"2022","journal-title":"BMJ"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"101762","DOI":"10.1016\/j.eclinm.2022.101762","article-title":"The prevalence and long-term health effects of Long Covid among hospitalised and non-hospitalised populations: A systematic review and meta-analysis","volume":"55","author":"Routen","year":"2023","journal-title":"eClinicalMedicine"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e1247","DOI":"10.1016\/S2214-109X(22)00286-8","article-title":"Post-COVID-19 condition 3 months after hospitalisation with SARS-CoV-2 in South Africa: A prospective cohort study","volume":"10","author":"Dryden","year":"2022","journal-title":"Lancet Glob. Health"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.ijid.2021.11.020","article-title":"Post-COVID syndrome: The aftershock of SARS-CoV-2","volume":"114","author":"Dotan","year":"2022","journal-title":"Int. J. Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"709","DOI":"10.1016\/S2213-2600(23)00159-5","article-title":"Respiratory sequelae of COVID-19: Pulmonary and extrapulmonary origins, and approaches to clinical care and rehabilitation","volume":"11","author":"Singh","year":"2023","journal-title":"Lancet Respir. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"711616","DOI":"10.3389\/fpubh.2021.711616","article-title":"COVID-19: Pulmonary and extra pulmonary manifestations","volume":"9","author":"Elrobaa","year":"2021","journal-title":"Front. Public Health"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1003","DOI":"10.1016\/S2213-2600(23)00262-X","article-title":"Multiorgan MRI findings after hospitalisation with COVID-19 in the UK (C-MORE): A prospective, multicentre, observational cohort study","volume":"11","author":"Raman","year":"2023","journal-title":"Lancet Respir. Med."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1002\/jmv.27309","article-title":"Post-acute COVID-19 syndrome (PCS) and health-related quality of life (HRQoL)\u2014A systematic review and meta-analysis","volume":"94","author":"Malik","year":"2022","journal-title":"J. Med. Virol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"66","DOI":"10.1007\/s12016-021-08848-3","article-title":"A review of persistent post-COVID syndrome (PPCS)","volume":"64","author":"Oronsky","year":"2023","journal-title":"Clin. Rev. Allergy Immunol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1812","DOI":"10.1038\/s41467-022-29513-z","article-title":"Course of post COVID-19 disease symptoms over time in the ComPaRe long COVID prospective e-cohort","volume":"13","author":"Tran","year":"2022","journal-title":"Nat. Commun."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Wolf, S., Zechmeister-Koss, I., and Erd\u00f6s, J. (2022). Possible long COVID healthcare pathways: A scoping review. BMC Health Serv. Res., 22.","DOI":"10.1186\/s12913-022-08384-6"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2101090","DOI":"10.1183\/13993003.01090-2021","article-title":"Multidisciplinary approach for post-acute COVID-19 syndrome: Time to break down the walls","volume":"58","author":"Montani","year":"2021","journal-title":"Eur. Respir. J."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Jones, P.W., Tabberer, M., and Chen, W.H. (2011). Creating scenarios of the impact of COPD and their relationship to COPD Assessment Test (CAT\u2122) scores. BMC Pulm. Med., 11.","DOI":"10.1186\/1471-2466-11-42"},{"key":"ref_16","unstructured":"GlaxoSmithKline (2023, December 20). COPD Assessment Test (CAT). Available online: https:\/\/www.catestonline.org\/patient-site-test-page-hungarian.html."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1136\/thoraxjnl-2020-215916","article-title":"COPD assessment test for the evaluation of COVID-19 symptoms","volume":"76","author":"Daynes","year":"2020","journal-title":"Thorax"},{"key":"ref_18","unstructured":"GlaxoSmithKline (2024, February 14). COPD Assessment Test (CAT). Available online: https:\/\/www.catestonline.org\/patient-site-test-page-english.html."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1016\/S0277-9536(96)00271-7","article-title":"Mapping visual analogue scale health state valuations onto standard gamble and time trade-off values","volume":"44","author":"Dolan","year":"1997","journal-title":"Soc. Sci. Med."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1186\/1477-7525-3-71","article-title":"The visual analog rating scale of health-related quality of life: An examination of end-digit preferences","volume":"3","author":"Shmueli","year":"2005","journal-title":"Health Qual. Life Outcomes"},{"key":"ref_21","unstructured":"National Institutes of Health (2024, February 20). COVID-19 Treatment Guidelines: Clinical Spectrum of SARS-CoV-2 Infection, Available online: https:\/\/www.covid19treatmentguidelines.nih.gov\/overview\/clinical-spectrum\/."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"e2231790","DOI":"10.1001\/jamanetworkopen.2022.31790","article-title":"Two-year health outcomes in hospitalized COVID-19 survivors in China","volume":"5","author":"Yang","year":"2022","journal-title":"JAMA Netw. Open"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1016\/j.pulmoe.2020.10.013","article-title":"Respiratory function in patients post-infection by COVID-19: A systematic review and meta-analysis","volume":"27","author":"Burgos","year":"2021","journal-title":"Pulmonology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1604","DOI":"10.1001\/jama.2022.18931","article-title":"Estimated global proportions of individuals with persistent fatigue, cognitive, and respiratory symptom clusters following symptomatic COVID-19 in 2020 and 2021","volume":"328","author":"Hanson","year":"2022","journal-title":"JAMA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1016\/j.cmi.2022.01.014","article-title":"Prevalence of post-acute COVID-19 syndrome symptoms at different follow-up periods: A systematic review and meta-analysis","volume":"28","author":"Alkodaymi","year":"2022","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"702635","DOI":"10.3389\/fmed.2021.702635","article-title":"Follow-ups on persistent symptoms and pulmonary function among post-acute COVID-19 patients: A systematic review and meta-analysis","volume":"8","author":"Long","year":"2021","journal-title":"Front. Med."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Mocanu, A., Lazureanu, V.E., Laza, R., Marinescu, A.R., Cut, T.G., Sincaru, S.V., Marza, A.M., Popescu, I.M., Herlo, L.F., and Nelson-Twakor, A. (2023). Laboratory Findings and Clinical Outcomes of ICU-Admitted COVID-19 Patients: A Retrospective Assessment of Particularities Identified among Romanian Minorities. J. Pers. Med., 13.","DOI":"10.3390\/jpm13020195"},{"key":"ref_28","first-page":"1305","article-title":"Risk of COVID-19 Severe Outcomes and Mortality in Migrants and Ethnic Minorities Compared to the General Population in the European WHO Region: A Systematic Review","volume":"24","author":"Mazzalai","year":"2023","journal-title":"J. Int. Migr. Integr."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1194754","DOI":"10.3389\/fmed.2023.1194754","article-title":"Fighting Post-COVID and ME\/CFS\u2013development of curative therapies","volume":"10","author":"Scheibenbogen","year":"2023","journal-title":"Front. Med."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1038\/s41590-021-01104-y","article-title":"Pathological sequelae of long-haul COVID","volume":"23","author":"Mehandru","year":"2022","journal-title":"Nat. Immunol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1186\/s12967-022-03346-2","article-title":"Endothelial dysfunction and altered endothelial biomarkers in patients with post-COVID-19 syndrome and chronic fatigue syndrome (ME\/CFS)","volume":"20","author":"Haffke","year":"2022","journal-title":"J. Transl. Med."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.jare.2021.11.013","article-title":"Analysis of post COVID-19 condition and its overlap with myalgic encephalomyelitis\/chronic fatigue syndrome","volume":"40","author":"Sukocheva","year":"2022","journal-title":"J. Adv. Res."},{"key":"ref_33","first-page":"2200970","article-title":"Circulating anti-nuclear autoantibodies in COVID-19 survivors predict long COVID symptoms","volume":"61","author":"Son","year":"2023","journal-title":"Eur. Respir. J."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2202226","DOI":"10.1183\/13993003.02226-2022","article-title":"Monocyte migration profiles define disease severity in acute COVID-19 and unique features of long COVID","volume":"61","author":"Scott","year":"2023","journal-title":"Eur. Respir. J."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"2300409","DOI":"10.1183\/13993003.00409-2023","article-title":"Long COVID: Clues about causes","volume":"61","author":"Liew","year":"2023","journal-title":"Eur. Respir. J."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Mikl\u00f3s, Z., and Horv\u00e1th, I. (2023). The Role of Oxidative Stress and Antioxidants in Cardiovascular Comorbidities in COPD. Antioxidants, 12.","DOI":"10.20944\/preprints202305.0028.v1"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"3729","DOI":"10.1007\/s10238-023-01139-5","article-title":"Interactions and clinical implications of serological and respiratory variables 3 months after acute COVID-19","volume":"23","author":"Freund","year":"2023","journal-title":"Clin. Exp. Med."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"107367","DOI":"10.1016\/j.rmed.2023.107367","article-title":"Assessment of a close respiratory follow-up schedule at 3 and 6 months after acute COVID-19 and its related investigations","volume":"217","author":"Freund","year":"2023","journal-title":"Respir. Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2300416","DOI":"10.1183\/13993003.00416-2023","article-title":"Eight lessons from 2 years of use of the Post-COVID-19 Functional Status scale","volume":"61","author":"Le","year":"2023","journal-title":"Eur. Respir. J."},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Trongtrakul, K., Tajarernmuang, P., Limsukon, A., Theerakittikul, T., Niyatiwatchanchai, N., Surasit, K., Glunriangsang, P., Liwsrisakun, C., Bumroongkit, C., and Pothirat, C. (2024). The National Early Warning Score 2 with Age and Body Mass Index (NEWS2 Plus) to Determine Patients with Severe COVID-19 Pneumonia. J. Clin. Med., 13.","DOI":"10.3390\/jcm13010298"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Choi, Y.J., Seo, Y.B., Seo, J.W., Lee, J., Nham, E., Seong, H., Yoon, J.G., Noh, J.Y., Cheong, H.J., and Kim, W.J. (2023). Effectiveness of Antiviral Therapy on Long COVID: A Systematic Review and Meta-Analysis. J. Clin. Med., 12.","DOI":"10.3390\/jcm12237375"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1122141","DOI":"10.3389\/fpubh.2023.1122141","article-title":"Italian good practice recommendations on management of persons with Long-COVID","volume":"11","author":"Giuliano","year":"2023","journal-title":"Front. Public Health"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"2103101","DOI":"10.1183\/13993003.03101-2021","article-title":"Inspiratory muscle training enhances recovery post-COVID-19: A randomised controlled trial","volume":"60","author":"McNarry","year":"2022","journal-title":"Eur. Respir. J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"e28289","DOI":"10.1002\/jmv.28289","article-title":"Clinical trials on the pharmacological treatment of long COVID: A systematic review","volume":"95","author":"Chee","year":"2023","journal-title":"J. Med. Virol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"467","DOI":"10.1080\/23744235.2022.2043560","article-title":"Registered clinical trials investigating treatment of long COVID: A scoping review and recommendations for research","volume":"54","author":"Ceban","year":"2022","journal-title":"Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Notarte, K.I., de Oliveira, M.H., Peligro, P.J., Velasco, J.V., Macaranas, I., Ver, A.T., Pangilinan, F.C., Pastrana, A., Goldrich, N., and Kavteladze, D. (2022). Age, sex and previous comorbidities as risk factors not associated with SARS-CoV-2 infection for long COVID-19: A systematic review and meta-analysis. J. Clin. Med., 11.","DOI":"10.3390\/jcm11247314"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e28909","DOI":"10.1002\/jmv.28909","article-title":"New-onset neurodegenerative diseases as long-term sequelae of SARS-CoV-2 infection: A systematic review and meta-analysis","volume":"95","author":"Rahmati","year":"2023","journal-title":"J. Med. Virol."}],"container-title":["Journal of Clinical Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/5\/1457\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:08:25Z","timestamp":1760105305000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2077-0383\/13\/5\/1457"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,3,2]]},"references-count":47,"journal-issue":{"issue":"5","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["jcm13051457"],"URL":"https:\/\/doi.org\/10.3390\/jcm13051457","relation":{},"ISSN":["2077-0383"],"issn-type":[{"value":"2077-0383","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,3,2]]}}}