Cited by 1,518Long-Term Effects of COVID-19COVID-19 Clinical Research StudiesSARS-CoV-2 and COVID-19 Research

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High-dimensional characterization of post-acute sequelae of COVID-19

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Al-Aly, Ziyad, Xie, Yan, Bowe, Benjamin·2021·Nature

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Abstract

The acute clinical manifestations of COVID-19 have been well characterized 1,2, but the post-acute sequelae of this disease have not been comprehensively described. Here we use the national healthcare databases of the US Department of Veterans Affairs to systematically and comprehensively identify 6-month incident sequelae-including diagnoses, medication use and laboratory abnormalities-in patients with COVID-19 who survived for at least 30 days after diagnosis. We show that beyond the first 30 days of illness, people with COVID-19 exhibit a higher risk of death and use of health resources. Our high-dimensional approach identifies incident sequelae in the respiratory system, as well as several other sequelae that include nervous system and neurocognitive disorders, mental health disorders, metabolic disorders, cardiovascular disorders, gastrointestinal disorders, malaise, fatigue, musculoskeletal pain and anaemia. We show increased incident use of several therapeutic agents-including pain medications (opioids and non-opioids) as well as antidepressant, anxiolytic, antihypertensive and oral hypoglycaemic agents-as well as evidence of laboratory abnormalities in several organ systems. Our analysis of an array of prespecified outcomes reveals a risk gradient that increases according to the severity of the acute COVID-19 infection (that is, whether patients were not hospitalized, hospitalized or admitted to intensive care). Our findings show that a substantial burden of health loss that spans pulmonary and several extrapulmonary organ systems is experienced by patients who survive after the acute phase of COVID-19. These results will help to inform health system planning and the development of multidisciplinary care strategies to reduce chronic health loss among individuals with COVID-19.

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Transcriptomic Analysis of HCN-2 Cells Suggests Connection among Oxidative Stress, Senescence, and Neuron Death after SARS-CoV-2 Infection
Valeri, A., Chiricosta, L., Calcaterra, V., Biasin, M., Cappelletti, G., Carelli, S., Zuccotti, G., Bramanti, P., Pelizzo, G., Mazzon, E., et al. (2021) · Cells · doi:10.3390/cells10092189 · Cited by 18
“The so-called “brain-fog”, loss of smell and taste, depression and anxiety, and memory problems are clear indications that the nervous system suffers the consequences of SARS-CoV-2 infection [4,5].”
Background
Assessing the impact of the COVID-19 pandemic on pragmatic clinical trial participants
Coleman, B. C., Purcell, N., Geda, M. E., Luther, S. L., Peduzzi, P. N., Kerns, R. D., Seal, K. H., Burgess, D. J., Rosen, M. I., Sellinger, J. J., et al. (2021) · Contemporary Clinical Trials · doi:10.1016/j.cct.2021.106619 · Cited by 18
“It may also be useful in studies aiming to differentiate the indirect effects of COVID-19-related impacts from direct effects of COVID-19 infection on musculoskeletal pain and other post-acute sequelae [6].”
Síndrome post-COVID. El desafío continúa
Boix, V., & Merino, E. (2021) · Medicina clínica (Ed. impresa) · doi:10.1016/j.medcli.2021.10.002 · Cited by 18
The Impact of Initial COVID-19 Episode Inflammation Among Adults on Mortality Within 12 Months Post-hospital Discharge
Mainous, A. G., Rooks, B. J., & Orlando, F. A. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.891375 · Cited by 19
Post-COVID-Syndrom – Fokus Fatigue
Hellwig, S., & Domschke, K. (2022) · Der Nervenarzt · doi:10.1007/s00115-022-01306-1 · Cited by 21
Vivencias e impacto en la calidad de vida de personas con COVID persistente
Tíscar-González, V., Gómez, S. S., Martínez, A. L., Serrano, A. P., López, M. T., Alonso, S. D., Rupérez, M., Portuondo, J., & Zorrilla, E. P. (2022) · Gaceta Sanitaria · doi:10.1016/j.gaceta.2022.102247 · Cited by 19
“…graves Se calcula que apro-ximadamente el 10% de las personas infectadas por SARS-CoV-2 desarrollan síntomas persistentes tras la primera infección aguda, que perduran transcurridas más de 12 semanas 4–8 El perﬁl pre-dominante son mujeres de mediana edad sin problemas de salud importantes previos .”
Background
Subclinical Acute Kidney Injury in COVID-19: Possible Mechanisms and Future Perspectives
Silva-Aguiar, R. P., Teixeira¹, D. E., Peres, R. A. S., Peruchetti, D. B., Gomes, C. P., Schmaier, A. H., Rocco, P. R. M., Pinheiro, A. A. S., & Caruso‐Neves, C. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232214193 · Cited by 18
Association between somatic symptom disorder and symptoms with daily life impairment after SARS-CoV-2 infection - results from a population-based cross-sectional study
Schneider, A., Huber, L., Lohse, J., Linde, K., Greißel, A., Sattel, H. C., Henningsen, P., & Hapfelmeier, A. (2023) · Journal of Psychosomatic Research · doi:10.1016/j.jpsychores.2023.111230 · Cited by 19
“Up to now, diagnostic and therapeutic decision making regarding PCS might have been guided by the major disease clusters of the cardiovascular [38] and pulmonary systems [39] as well as the nervous system [40] that are affected by COVID-19.”
Background
Long-term consequences of COVID-19 on mental health and the impact of a physically active lifestyle: a narrative review
Roever, L., Cavalcante, B. R. R., & Caria, A. C. I. (2023) · Annals of General Psychiatry · doi:10.1186/s12991-023-00448-z · Cited by 23
“Furthermore, people who had COVID-19 presented higher risk of death and sequelae in the respiratory system and CNS that could lead to the development of neurocognitive disorders and mental health disorders 30 days after halting the symptoms of the disease [1, 81].”
Background
Pathophysiological effects of SARS-CoV-2 infection on the cardiovascular system and its clinical manifestations—a mini review
Yugar‐Toledo, J. C., Yugar, L. B. T., Sedenho‐Prado, L. G., Schreiber, R., & Moreno, H. (2023) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2023.1162837 · Cited by 18
“However, a database analysis (103) of cardiovascular outcomes after a 12month follow-up revealed that hospital readmission is associated with a high mortality rate, with multiple organ dysfunction being the primary cause (104).”
Background
Paxlovid reduces the risk of Long COVID in patients six months after hospital discharge
Wang, Y., Zhao, D., Xiao, W., Shi, J., Chen, W., Jia, Q., Zhou, Y., Wang, R., Chen, X., & Feng, L. (2023) · Journal of Medical Virology · doi:10.1002/jmv.29014 · Cited by 17
Acute SARS-CoV-2 Infection and Incidence and Outcomes of Out-of-Hospital Cardiac Arrest
Liu, J., Counts, C. R., Drucker, C. J., Emert, J. M., Murphy, D. L., Schwarcz, L., Kudenchuk, P. J., Sayre, M. R., & Rea, T. D. (2023) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.36992 · Cited by 18
Factors associated with unexplained sudden deaths among adults aged 18-45 years in India – A multicentric matched case–control study
Ponnaiah, M., Bhatnagar, T., Abdulkader, R. S., Elumalai, R., Surya, J., Jeyashree, K., Kumar, M. S., Govindaraju, R., Thangaraj, J. W. V., Aggarwal, H. K., et al. (2023) · International Journal of Microbiology Research · doi:10.4103/ijmr.ijmr_2105_23 · Cited by 18
“Although there is some evidence for the increased risk of death among COVID-19-recovered individuals and among those with breakthrough infections, the evidence for sudden deaths among such individuals is scarce 10-13 .”
Background
Anxiety and depression symptoms among patients with long COVID: a retrospective cohort study
Sauer, M. C., Barlow, P. B., Comellas, A. P., & Garg, A. (2024) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-023-01740-5 · Cited by 18
“After the acute illness with SARS-CoV-2, a subgroup of patients experiences persistent symptoms for several months in a syndrome termed Post-Acute Sequelae of SARS-CoV-2 (PASC), also referred to as “Long COVID” [6].”
Depression and fatigue six months post-COVID-19 disease are associated with overlapping symptom constellations: A prospective, multi-center, population-based cohort study
Weiss, M. H., Gutzeit, J., Appel, K. S., Bahmer, T., Beutel, M. E., Deckert, J., Fricke, J., Hanß, S., Hettich-Damm, N., Heuschmann, P. U., et al. (2024) · Journal of Affective Disorders · doi:10.1016/j.jad.2024.02.041 · Cited by 25
Diabetes, Heart Failure, and COVID-19: An Update
Hebbard, C., Lee, B., Katare, R., & Garikipati, V. N. S. (2021) · Frontiers in Physiology · doi:10.3389/fphys.2021.706185 · Cited by 19
“There appears to be an increase in diabetes incidence in patients who have been infected with SARS-CoV-2 (Al-Aly et al., 2021).”
BackgroundInfluential
Incidence and Risk Factors of Long Covid in the Uk: A Single-Centre Observational Study
Nune, A., Durkowski, V., Titman, A., Gupta, L., Hadzhiivanov, M., Ahmed, A., Musat, C., & Sapkota, H. R. (2021) · The Journal of the Royal College of Physicians of Edinburgh · doi:10.4997/jrcpe.2021.405 · Cited by 22
Thromboembolic Disease and Cardiac Thrombotic Complication in COVID-19: A Systematic Review
Nappi, F., Nappi, P., Gambardella, I., & Singh, S. S. A. (2022) · Metabolites · doi:10.3390/metabo12100889 · Cited by 18
Post-COVID condition or “long COVID”, return-to work, and occupational health research
Descatha, A., Evanoff, B., & Fadel, M. (2023) · Scandinavian Journal of Work Environment & Health · doi:10.5271/sjweh.4088 · Cited by 18
Advances in Understanding Long COVID: Pathophysiological Mechanisms and the Role of Omics Technologies in Biomarker Identification
da Silva, M. D., da Silva, T. S., Mendes, C. G., Valbão, M. C. M., Badu-Tawiah, A. K., Laurindo, L. F., Barbalho, S. M., Direito, R., & Miglino, M. A. (2025) · Molecular Diagnosis & Therapy · doi:10.1007/s40291-025-00792-8 · Cited by 20
“This variability remains a significant challenge in deciphering suggesting the influence of genetic and immunological factors [18].”
Overview of acute kidney manifestations and management of patients with COVID-19
Menez, S. P., & Parikh, C. R. (2021) · American Journal of Physiology-Renal Physiology · doi:10.1152/ajprenal.00173.2021 · Cited by 17
Understanding the role of nACE2 in neurogenic hypertension among COVID-19 patients
Kulkarni, P. G., Sakharkar, A. J., & Banerjee, T. (2021) · Hypertension Research · doi:10.1038/s41440-021-00800-4 · Cited by 17
“In yet another study, hypertension was identified as the second most prevalent consequence of COVID-19 [88].”
Background
Diagnostics and Treatments of COVID-19: A Living Systematic Review of Economic Evaluations
Elvidge, J., Summerfield, A., Nicholls, D. A., & Dawoud, D. (2022) · Value in Health · doi:10.1016/j.jval.2022.01.001 · Cited by 19
“Conversely, treatments that prevent symptoms from worsening may be more cost effective if this reduces the likelihood of longterm negative consequences.(43)”
Background
Changes in Serum Liver Function for Patients with COVID-19: A 1-Year Follow-Up Study
Zhu, X., Wang, J., Du, J., Chen, S., Chen, S., Li, J., & Shen, B. (2022) · Infection and Drug Resistance · doi:10.2147/idr.s356181 · Cited by 17
“Acute sequelae of COVID-19 are also a focus of attention today with more and more reports showing organ damage in COVID-19 patients after discharge.(2) Liver injury or abnormalities were reported in COVID-19 patients during and after hospitalization.”
Premortem Skin Biopsy Assessing Microthrombi, Interferon Type I Antiviral and Regulatory Proteins, and Complement Deposition Correlates with Coronavirus Disease 2019 Clinical Stage
Laurence, J. C., Nuovo, G. J., Racine‐Brzostek, S., Seshadri, M., Elhadad, S., CROWSON, A. N., Mulvey, J. J., Harp, J., Ahamed, J., & MAGRO, C. M. J. (2022) · American Journal Of Pathology · doi:10.1016/j.ajpath.2022.05.006 · Cited by 17
“Cutaneous biopsy may also permit exploration of the “long COVID” syndrome, postacute sequelae of SARS-CoV-2 infection, which involves pulmonary and extrapulmonary organ systems.(53) For example, in terms of chronic neurologic sequelae of SARS-CoV-2, magnetic resonance imaging scans, cerebral blood flow studies, and ce…”
Background
The nervous system during COVID ‐19: Caught in the crossfire
Natale, N. R., Lukens, J. R., & Petri, W. A. (2022) · Immunological Reviews · doi:10.1111/imr.13114 · Cited by 19
“As a result, 6 months following hospital discharge, hospitalized COVID-19 patients have an excess burden of ~60 per 1,000 persons with chronic fatigue and an excess burden of ~40 per 1,000 persons with memory problems, compared to PCR negative hospitalized patients 280 .”
Long COVID-19 and Health-Related Quality of Life of Mild Cases in Korea: 3-Months Follow-up of a Single Community Treatment Center
Soh, H. S., & Cho, B. (2022) · Journal of Korean Medical Science · doi:10.3346/jkms.2022.37.e326 · Cited by 18
Time-varying association of acute and post-acute COVID-19 with new-onset diabetes mellitus among hospitalized and non-hospitalized patients
Reges, O., Test, T., Hoshen, M., Cicurel, A., Saliba, W., Greenland, P., Dicker, D., & Lavie, G. (2023) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2022-003052 · Cited by 17
Impact of COVID-19 Infection on Cardiorespiratory Fitness, Sleep, and Psychology of Endurance Athletes—CAESAR Study
Śliż, D., Wiecha, S., Gąsior, J. S., Kasiak, P. S., Ulaszewska, K., Lewandowski, M., Barylski, M., & Mamcarz, A. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12083002 · Cited by 17
“Even non-hospitalized EAs are more likely to develop anxiety, trauma- and stress-related disorders, or fatigue [51].”
Background
Gastrointestinal disorders in post-COVID syndrome. Clinical guidelines
Grinevich, V. B., Лазебник, Л. Б., Kravchuk, Y. A., Радченко, В. Г., Ei, T., Першко, А. М., Seliverstov, P. V., Salikova, S. P., Zhdanov, K. V., Kozlov, K. V., et al. (2023) · Экспериментальная и клиническая гастроэнтерология · doi:10.31146/1682-8658-ecg-208-12-4-68 · Cited by 20
Integrating patient-reported physical, mental, and social impacts to classify long COVID experiences
Vartanian, K. B., Fish, D., Kenton, N. R., Gronowski, B., Wright, B. J., & Robicsek, A. A. (2023) · Scientific Reports · doi:10.1038/s41598-023-43615-8 · Cited by 19
Identifying patterns of reported findings on long-term cardiac complications of COVID-19: a systematic review and meta-analysis
Guo, B., Zhao, C., He, M. Z., Senter, C. C., Zhou, Z., Peng, J., Li, S., Fitzpatrick, A. L., Lindström, S., Stebbins, R. C., et al. (2023) · BMC Medicine · doi:10.1186/s12916-023-03162-5 · Cited by 17
Pituitary–Adrenal Axis and Peripheral Immune Cell Profile in Long COVID
Alijotas‐Reig, J., Anunciación-Llunell, A., Esteve‐Valverde, E., Morales-Pérez, S., Rivero-Santana, S., Trapé, J., González-García, L., Ruiz, D., Marques-Soares, J. R., & Miró‐Mur, F. (2024) · Biomedicines · doi:10.3390/biomedicines12030581 · Cited by 19
Post-viral symptoms and conditions are more frequent in COVID-19 than influenza, but not more persistent
Tesch, F., Ehm, F., Loser, F., Bechmann, L., Vivirito, A., Wende, D., Batram, M., Buschmann, T., Menzer, S., Ludwig, M., et al. (2024) · BMC Infectious Diseases · doi:10.1186/s12879-024-10059-y · Cited by 21
“In line with previous studies [17], we included the severity of COVID-19 as a stratification feature and differentiated between (1) individuals with outpatient diagnoses of COVID-19, (2) individuals with a hospitalization with COVID-19, and (3) individuals requiring intensive care and/or mechanical…”
Method
Outpatient Treatment of Severe Acute Respiratory Syndrome Coronavirus 2 Infection to Prevent Coronavirus Disease 2019 Progression
Cohen, M. S., Wohl, D. A., Fischer, W. A., Smith, D. M., & Eron, J. J. (2021) · Clinical Infectious Diseases · doi:10.1093/cid/ciab494 · Cited by 16
Musculoskeletal pain related to COVID-19 survivors after hospitalization: A short review (Dolor musculoesquelético en supervivientes del COVID-19 tras la hospitalización: Una breve revision)
Fiore, E., Corbellini, C., Acucella, L., Gargano, S., Romero, E. A. S., Cotella, D., & Villafañe, J. H. (2022) · Retos · doi:10.47197/retos.v44i0.90361 · Cited by 17
Long-term cardiac surveillance and outcomes of COVID-19 patients
Mitrani, R. D., Dabas, N., Alfadhli, J., Lowery, M. H., Best, T. M., Hare, J. M., Myerburg, R. J., & Goldberger, J. J. (2022) · Trends in Cardiovascular Medicine · doi:10.1016/j.tcm.2022.06.003 · Cited by 17
Inflammation in the COVID-19 airway is due to inhibition of CFTR signaling by the SARS-CoV-2 spike protein
Caohuy, H., Eidelman, O., Chen, T., Mungunsukh, O., Yang, Q., Walton, N. I., Pollard, B. S., Khanal, S., Hentschel, S., Florez, C., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-66473-4 · Cited by 17
SARS-CoV-2-induced cytokine storm drives prolonged testicular injury and functional impairment in mice that are mitigated by dexamethasone
Giannakopoulos, S., Pak, J., Bakse, J., Ward, M. A., Nerurkar, V. R., Tallquist, M. D., & Verma, S. (2025) · PLoS Pathogens · doi:10.1371/journal.ppat.1012804 · Cited by 18
Healthcare utilization patterns before and after a long COVID diagnosis: a case-control study
DeVoss, R., Carlton, E. J., Jolley, S. E., & Perraillon, M. C. (2025) · BMC Public Health · doi:10.1186/s12889-025-21393-4 · Cited by 16
Rates of infection with other pathogens after a positive COVID-19 test versus a negative test in US veterans (November, 2021, to December, 2023): a retrospective cohort study
Cai, M., Xu, E., Xie, Y., & Al‐Aly, Z. (2025) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(24)00831-4 · Cited by 17
The (apparent) antibody paradox in COVID-19
Ameratunga, R., Woon, S., Lea, E., Steele, R. H., Lehnert, K., Leung, E. Y., & Brooks, A. E. S. (2022) · Expert Review of Clinical Immunology · doi:10.1080/1744666x.2022.2044797 · Cited by 16
“symptoms including severe fatigue, chest pain, breathlessness and neurological symptoms including autonomic instability, loss of memory and clarity of thought (brain fog) [66,67].”
Background
Noninterventional studies in the COVID-19 era: methodological considerations for study design and analysis
Butler, A. M., Burcu, M., Christian, J. B., Tian, F., Andersen, K. M., Blumentals, W. A., Maddox, K. E. J., & Alexander, G. C. (2022) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2022.11.011 · Cited by 18
“The ability for COVID-19 infection history or vaccination status to bias treatment effect estimates will be wide-ranging given the substantial COVID-19 burden of acute clinical manifestations and postacute sequelae [85].”
Background
Gastrointestinal and Hepatobiliary Symptoms and Disorders with Long (Chronic) COVID Infection
Rizvi, A., Ziv, Y., Crawford, J. M., & Trindade, A. J. (2023) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2022.09.002 · Cited by 17
“91]).(15) Similarly, in a Danish cohort of patients followed-up to 6months after COVID-19 infection, higher rates of general practitioner and outpatient care utilization were reported and attributed to postacute COVID-19 symptoms.”
BackgroundMethodResultInfluential
Cardiovascular and cerebral vascular health in females with postacute sequelae of COVID-19
Nandadeva, D., Skow, R. J., Stephens, B. Y., Grotle, A., Georgoudiou, S., Barshikar, S., Seo, Y., & Fadel, P. J. (2023) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00018.2023 · Cited by 16
Biomimetic Alveoli System with Vivid Mechanical Response and Cell–Cell Interface
Niu, M., Zhu, Y., Ding, X., Zu, Y., Zhao, Y., & Wang, Y. (2023) · Advanced Healthcare Materials · doi:10.1002/adhm.202300850 · Cited by 16
Individual preferences, government policy, and COVID-19: A game-theoretic epidemiological analysis
Zhou, Y., Rahman, M. M., Khanam, R., & Taylor, B. R. (2023) · Applied Mathematical Modelling · doi:10.1016/j.apm.2023.06.014 · Cited by 16
“Reinfection will significantly increase the probability of COVID-19 sequelae [3-6].”

Authors: Al-Aly, Z., Xie, Y., & Bowe, B.
Affiliations: VA St. Louis Health Care System (US)
ORCID: Al-Aly, Ziyad
Xie, Yan
Bowe, Benjamin
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2021-04-22
Volume: 594
Issue: 7862
Pages: 259-264
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/s41586-021-03553-9
OpenAlex: W3153493739
Cited by: 1,518
References: 46
Citations by year: 2026: 95 · 2025: 170 · 2024: 268 · 2023: 365 · 2022: 391 · 2021: 228
FWCI: 149.17
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.springer.com/tdm (tdm)
www.springer.com/tdm (vor)
Locations: Nature (publishedVersion)
Research Square (acceptedVersion, cc-by)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Funders: U.S. Department of Veterans Affairs
American Society of Nephrology
McDonnell Center for Systems Neuroscience
Topics: Health Sciences › Medicine › Clinical Neurology › Long-Term Effects of COVID-19
Health Sciences › Medicine › Infectious Diseases › COVID-19 Clinical Research Studies
Health Sciences › Medicine › Infectious Diseases › SARS-CoV-2 and COVID-19 Research
Keywords: post-COVID-19 sequelae, long COVID, COVID-19 mortality, health resource utilization, pulmonary sequelae, neurocognitive disorders, mental illness, metabolic disorders, cardiovascular disease, gastrointestinal diseases, fatigue, musculoskeletal pain, anemia, medication use, laboratory abnormalities, disease severity, intensive care unit admission, veterans
MeSH terms: COVID-19, SARS-CoV-2, COVID-19 Drug Treatment, Post-Acute COVID-19 Syndrome, Female, Hospitalization, Humans, Influenza, Human, Male, Outpatients, Risk, Time Factors, United States, United States Department of Veterans Affairs, Cohort Studies, Databases, Factual, Electronic Health Records, Datasets as Topic

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High-dimensional characterization of post-acute sequelae of COVID-19

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