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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Influential
Immune dysregulation in prolonged Long-COVID: lymphocytes emerge as key mediators of persistent inflammation, exhaustion and cytotoxicity
Spriņģe, M. L., Vaivode, K., Saksis, R., Vainšeļbauma, N. M., Ansone, L., Brīvība, M., Niedra, H., & Rovīte, V. (2026) · Journal of Translational Medicine · doi:10.1186/s12967-026-08081-6 · Cited by 7
“Both acute COVID-19 and Long-COVID symptoms manifest across multiple organ systems; notably, pulmonary and cardio-vascular complications pose a serious threat to the life and health span of patients [3, 4, 16].”
Neurological involvement among non-hospitalized adolescents and young adults 6 months after acute COVID-19
Havdal, L. B., Selvakumar, J. P., Berven, L. L., Stiansen-Sonerud, T., Zetterberg, H., Blennow, K., Holmøy, T., & Wyller, V. B. (2024) · Frontiers in Neurology · doi:10.3389/fneur.2024.1345787 · Cited by 4
“However, a substantial portion of individuals experience persistent post-infective symptoms (1–3).”
Background
Longitudinal landscape of immune reconstitution after acute SARS-CoV-2 infection at single-cell resolution
Ren, L., Liu, Y., Wang, Y., Wu, C., Guo, L., Chen, L., Wang, X., Xiao, Y., Huang, L., Zhong, J., et al. (2024) · 中国科学通报：英文版 · doi:10.1016/j.scib.2024.07.011 · Cited by 4
COVID-19 in Veterans: A Narrative Review
Chuang, Y.-C., Tsai, H.-W., Liu, S., Wu, M., & Liu, P. (2022) · Risk Management and Healthcare Policy · doi:10.2147/rmhp.s354814 · Cited by 4
“The extrapulmonary systems that are affected include the cardiovascular, hematologic, endocrine, dermatological, gastrointestinal, renal, and neurological systems, as well as mental health.(9)”
Background
Enfermedad renal en la COVID-19 persistente: un objetivo inmediato para Nefrología
de Francisco, A. M., & Fresnedo, G. F. (2022) · Nefrología · doi:10.1016/j.nefro.2022.04.004 · Cited by 4
“Un estudio de EEUU que utilizó registros de salud electrónicos de la Administración de Salud de Veteranos (VHA) para realizar una evaluación integral del Covid-19 prolongado encontró que el COVID-19 aumentó el riesgo de ERC y que este riesgo fue mayor entre quienes tenían una enfermedad grave [30]”
Background
Strengthening Asset-backed Pension Systems in a Post-COVID World
OECD (2022) · OECD eBooks · doi:10.1787/288cb3cf-en · Cited by 4
Persistent Symptoms and Sequelae After Severe Acute Respiratory Syndrome Coronavirus 2 Infection Not Requiring Hospitalization: Results From Testing Denmark, a Danish Cross-sectional Survey
van Wijhe, M., Fogh, K., Ethelberg, S., Iversen, K. K., Nielsen, H. I., Østergaard, L. J., Andersen, B. S., Bundgaard, H., Jørgensen, C. S., Scharff, B. F. S. S., et al. (2022) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofac679 · Cited by 4
“of initial infection and female sex were strongly related to long-COVID symptoms, but asthma and other respiratory conditions was only a risk factor for worsening of shortness of breath but not for other long-COVID symptoms [4, 6, 12, 14, 15, 26].”
Absence of self-reported neuropsychiatric and somatic symptoms after Omicron variant SARS-CoV-2 breakthrough infections
Woo, M. S., Mayer, C., Brehm, T. T., Andersen, G., Weigel, A., Löwe, B., Lohse, A. W., Addo, M. M., Gerloff, C. P., Knobloch, J. K. ‐., et al. (2023) · Brain Communications · doi:10.1093/braincomms/fcad092 · Cited by 4
“tigue, headaches, shortness of breath, fever or cognitive impairment.(4) Currently, there is no clear consensus regarding the definition of post-acute sequelae.”
Background
An alternative mechanism for skeletal muscle dysfunction in long-term post-viral lung disease
Martin, R. A., Keeler, S. P., Wu, K., Shearon, W. J., Patel, D., Li, J., Hoang, M., Hoffmann, C. M., Hughes, M. E., & Holtzman, M. J. (2023) · American Journal of Physiology-Lung Cellular and Molecular Physiology · doi:10.1152/ajplung.00338.2022 · Cited by 6
Patterns of Opioid and Non-Opioid Analgesic Consumption in Patients with Post-COVID-19 Conditions
Carrasco‐Garrido, P., Palacios‐Ceña, D., Hernández‐Barrera, V., Jiménez‐Trujillo, I., Gallardo-Pino, C., & Fernández‐de‐las‐Peñas, C. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12206586 · Cited by 4
“Al-Aly et al., in an investigation into the characterization of post-acute sequelae of COVID-19, identiﬁed incident sequelae such as musculoskeletal pain and showed an increased incident use of several therapeutic approaches, including pain medications (opioids and non-opioids) [47].”
Background
Potential use of sodium glucose co-transporter 2 inhibitors during acute illness: a systematic review based on COVID-19
Tisch, C., Xourgia, E., Exadaktylos, A. K., & Ziaka, M. (2024) · Endocrine · doi:10.1007/s12020-024-03758-8 · Cited by 4
“In a large veterans ’ study from the U.S. in 2021, Al-Aly et al. [101] showed that even 30 days after the initial diagnosis of COVID-19, there was an increased likelihood that renal function was still impaired [101].”
Background
Salivary biomarkers as pioneering indicators for diagnosis and severity stratification of pediatric long COVID
Tyrkalska, S. D., Pérez-Sánz, F., Franco‐Martínez, L., Rubio, C. P., Tvarijonaviciute, A., Martínez-Subiela, S., Hernández, M. J. M., González-Aumatell, A., Carreras‐Abad, C., Marsal, È. D., et al. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1396263 · Cited by 4
Post-COVID Conditions in US Primary Care: A PRIME Registry Comparison of Patients With COVID-19, Influenza-Like Illness, and Wellness Visits
Velásquez, E. E. M., Kamdar, N. S., Rehkopf, D. H., Saydah, S., Bull–Otterson, L., Hao, S., Vala, A., Chu, I. M., Bazemore, A., Phillips, R. L., et al. (2024) · The Annals of Family Medicine · doi:10.1370/afm.3131 · Cited by 4
Drug Repurposing for COVID-19 by Constructing a Comorbidity Network with Central Nervous System Disorders
Qian, J., Yang, B., Wang, S., Yuan, S., Zhu, W., Zhou, Z., Zhang, Y., & Hu, G. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25168917 · Cited by 5
“However, the post-acute sequelae of SARS-CoV-2 infection—referred to as long COVID—include several long-term neurologic disorders [4,5].”
Background
The negative effects of long COVID-19 on cardiovascular health and implications for the presurgical examination
Stimart, H. L., & Hipkins, B. (2024) · Journal of Osteopathic Medicine · doi:10.1515/jom-2024-0109 · Cited by 4
Blood matters: the hematological signatures of Coronavirus infection
Toro, A. R., Arévalo, A. P., Pereira-Gómez, M., Sabater, A. A., Zizzi, E. A., Perbolianachis, P., Pascual, G., Lage-Vickers, S., Pórfido, J. L., Achinelli, I., et al. (2024) · Cell Death and Disease · doi:10.1038/s41419-024-07247-8 · Cited by 4
“A growing body of evidence links abnormal RBC dynamics to COVID-19, with several studies suggesting that the virus may induce hemolysis [5, 28 – 30].”
Lessons Learned From Characterizing Long COVID Among US Medicare Beneficiaries
Lu, Y., Lindaas, A., Izurieta, H. S., Cozen, M. L., Menis, M. D., Shi, X., Steele, W. R., Wernecke, M., Chillarige, Y., Kelman, J. A., et al. (2025) · Pharmacoepidemiology and Drug Safety · doi:10.1002/pds.70101 · Cited by 4
Wearable data reveals distinct characteristics of individuals with persistent symptoms after a SARS-CoV-2 infection
Ledebur, K., Wiedermann, M., Puta, C., Stefan Thurner, A., Klimek, P., & Brockmann, D. (2025) · npj Digital Medicine · doi:10.1038/s41746-025-01456-x · Cited by 4
“…the high temporalresolutionofthedataanditscoverageoflongperiodsoftimepermitadetailedanalysisofwearabledatasignalsinallphasesofaSARS-CoV-2 infection,i.e.theacutephase(fromtheweekofthepositiveSARS-CoV-2test tofourweeksafterthetest),thesub-acutephase(fourweeksto12weeksafter…”
The implications of somatic symptom disorder on the impairment of daily life are greater in post-COVID syndrome than in asthma or COPD - results of a cross-sectional study in a rehabilitation clinic
Schneider, A., Hapfelmeier, A., Greißel, A., Limbach, M., Schwarzl, G., Ebert, F., Huber, V., & Hayden, M. C. (2025) · Scientific Reports · doi:10.1038/s41598-025-96055-x · Cited by 4
COVID-19 Pandemic–Related Exposures and Cognitive Function in Middle-Aged Women
Wang, S., Menor, A., Chibnik, L. B., Kang, J. H., Vyas, C. M., Blacker, D., Kubzansky, L. D., Koenen, K. C., & Roberts, A. L. (2025) · JAMA Network Open · doi:10.1001/jamanetworkopen.2025.5532 · Cited by 5
On the Utility of Nailfold Capillaroscopy in Detecting the Effects of Fibrinaloid Microclots in Diseases Involving Blood Stasis
Kell, D. B., & Pretorius, E. (2025) · Immune discovery. · doi:10.70322/immune.2025.10011 · Cited by 5
Functional Outcomes of Severe COVID-19 Patients After a Post-Acute Care Hospitalization
Ramos, J. G. R., Laporte, L. R., de Souza, F. R., & de Andrade, L. F. (2021) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2021.09.007 · Cited by 4
The health impact of COVID‑19
Mueller, M., Suzuki, E. M., Paolantonio, G., Hewlett, E., & James, C. D. (2021) · Health at a glance · doi:10.1787/b0118fae-en · Cited by 4
Long-COVID aus Sicht der Anthroposophischen Medizin – Symptome und Behandlungsmöglichkeiten. Empfehlungen einer internationalen Expertenkommission für medizinische Fachkräfte
Szőke, H., Sommer, M., Streit, E., Grah, C., Winkler, M., Busche, P., Pöchtrager, S., Mergelsberg, J., Wullschleger, C., Gerlach, K. L., et al. (2022) · Der Merkurstab · doi:10.14271/dms-21451-de · Cited by 4
Organbezogene Folgeerscheinungen von COVID‑19 bei Erwachsenen
Hennigs, J. K., Oqueka, T., Harbaum, L., & Klose, H. F. E. (2022) · Bundesgesundheitsblatt - Gesundheitsforschung - Gesundheitsschutz · doi:10.1007/s00103-022-03513-2 · Cited by 4
Post-COVID pain syndrome: a review of international observations
Shavlovskaya, O. A., Бокова, И. А., & Shavlovskiy, N. I. (2022) · Neurology neuropsychiatry Psychosomatics · doi:10.14412/2074-2711-2022-2-91-97 · Cited by 4
Impacts of androgen deprivation therapy on the risks and outcomes of SARS-CoV-2 infection in patients with prostate cancer
Huang, Y., Li, W., Sun, M., Duan, X., Wang, Y.-T., Zhang, L.-X., Xin, Z.-H., Yun, Z., Fan, B., & Li, X. (2022) · Asian Journal of Andrology · doi:10.4103/aja202246 · Cited by 4
The comeback effect: How happy are people who have recovered from a COVID-19 infection?
Dahlén, M., Thorbjørnsen, H., Wågert, P. V. H., Hellström, C., Kerstis, B., Lindberg, D., Stier, J., & Elvén, M. (2022) · International Journal of Wellbeing · doi:10.5502/ijw.v12i2.2019 · Cited by 4
Network analysis between neuron dysfunction and neuroimmune response based on neural single-cell transcriptome of COVID-19 patients
Lin, X., Nie, H., Tang, R., Wang, P., Jin, X., Jiang, Q., Han, F., Chen, N., & Li, Y. (2022) · Computers in Biology and Medicine · doi:10.1016/j.compbiomed.2022.106055 · Cited by 5
“The symptoms were including loss of smell and taste, and some people may later struggle with headaches, fatigue, weakness and confusion(3,5).”
Background
Postcovid Syndrome – The New Reality
Хорева, М. А. (2022) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-022-01286-4 · Cited by 4
Critical role of diagnostic SARS-CoV-2 T cell assays for immunodeficient patients
Ameratunga, R., Woon, S., Steele, R. H., Lehnert, K., Leung, E. Y., & Brooks, A. E. S. (2022) · Journal of Clinical Pathology · doi:10.1136/jcp-2022-208305 · Cited by 4
COVID-19 in Russia: Evolution of Views on the Pandemic. Report II
Стародубов, В. И., Beregovykh, V. V., Акимкин, В. Г., Семененко, Т. А., Викторовна, У. С., Avdeev, S. N., Zykov, K. A., Трофимова, Т. Н., Вачиковна, П. Н., Переходов, С. Н., et al. (2022) · Annals of the Russian academy of medical sciences · doi:10.15690/vramn2122 · Cited by 7
Caractéristiques cliniques et épidémiologiques des décès COVID-19 en Tunisie avant l´émergence des VOCs: mars 2020-février 2021
Dhaouadi, S., Hechaichi, A., Letaief, H., Safer, M., Mziou, E., Talmoudi, K., Borgi, C., Chebbi, H., Somrani, N., Ali, M. B., et al. (2022) · Pan African Medical Journal · doi:10.11604/pamj.2022.43.172.35544 · Cited by 4
“Le RR de décès augmentait progressivement avec l ́âge pour atteindre 74,5 (IC à 95 % [60,8-91,4]) chez les sujets âgés de 75 ans et plus par rapport à ceux âgés entre 40 et 45 ans.”
Posttraumatic Stress Symptoms Among COVID-19 Survivors After Hospitalization
Sobczak, E., Swafford, E. P., Samano, D., Bass, D., Ghamasaee, P., Kottapally, M., Merenda, A., O’Phelan, K. H., Romano, J. G., Sacco, R. L., et al. (2023) · Journal of Neuropsychiatry · doi:10.1176/appi.neuropsych.20220126 · Cited by 4
No Causal Effects Detected in COVID-19 and Myalgic Encephalomyelitis/Chronic Fatigue Syndrome: A Two Sample Mendelian Randomization Study
Xu, W., Cao, Y., & Wu, L. (2023) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph20032437 · Cited by 4
Outcomes in patients with large vessel occlusion strokes undergoing mechanical thrombectomy with concurrent COVID-19: a nationwide retrospective analysis
Ramsay, I. A., Fountain, H. B., Elarjani, T., Govindarajan, V., Silva, M., Abdelsalam, A., Burks, J. D., Starke, R. M., & Luther, E. (2023) · Journal of NeuroInterventional Surgery · doi:10.1136/jnis-2023-020263 · Cited by 4
Post COVID-19 Symptoms Among Infected Vaccinated Individuals: A Cross-Sectional Study in Saudi Arabia
Adly, H. M., Saleh, S. A. K., Garout, M. A., Abdulkhaliq, A. A., Khafagy, A. A., Saati, A. A., AlJahdali, I. A., Alandiyjany, M. N., & Al‐Tawfiq, J. A. (2023) · Journal of Epidemiology and Global Health · doi:10.1007/s44197-023-00146-9 · Cited by 6
“…of 1832 adults, the risk of symptoms > 28 days after SARS-CoV-2 symptoms was higher in unvaccinated at the time of infection [23] while Al-Aly et al. showed that two doses of COVID-19 vaccines would be more effective in reducing post-COVID-19 symptoms with certain vaccines better than others [24].”
Background
Daily COVID-19 symptom assessment over 28 days – findings from a daily direct-to-patient registry of COVID-19 positive patients
Brinkley, E., Knuth, K. B., Kwon, T., Mack, C. D., Leister-Tebbe, H. K., Bao, W., Reynolds, M. W., & Dreyer, N. A. (2023) · Journal of Patient-Reported Outcomes · doi:10.1186/s41687-023-00668-7 · Cited by 4
“%) experience symptom resolution within a month [6, 10].”
Background
Risk of Major Adverse Cardiovascular Events After SARS-CoV-2 Infection in British Columbia: A Population-Based Study
García, H. A. V., Wong, S., Jeong, D., Binka, M., Naveed, Z., Wilton, J., Hawkins, N. M., & Janjua, N. Z. (2024) · The American Journal of Medicine · doi:10.1016/j.amjmed.2024.04.010 · Cited by 4
Molecular overlaps of neurological manifestations of COVID-19 and schizophrenia from a proteomic perspective
Antunes, A. S. L. M., Reis‐de‐Oliveira, G., & Martins‐de‐Souza, D. (2024) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-024-01842-8 · Cited by 5
The enduring effect of the COVID-19 pandemic on diabetes
Al‐Aly, Z., & Cao, B. (2024) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(24)00180-3 · Cited by 4
A Practical Approach to Tailor the Term Long COVID for Diagnostics, Therapy and Epidemiological Research for Improved Long COVID Patient Care
Hoffmann, K., Stingl, M., O’Mahony, L., & Untersmayr, E. (2024) · Infectious Diseases and Therapy · doi:10.1007/s40121-024-01025-x · Cited by 4
“To differentiate the first subgroup would additionally make sense in terms of known risk factors for LC, which overlap largely with risk factors for severe acute disease progression [10].”
Background
SARS-CoV-2 in Domestic UK Cats from Alpha to Omicron: Swab Surveillance and Case Reports
Jones, S., Tyson, G. B., Orton, R. J., Smollett, K. L., Manna, F., Kwok, K. T. T., Suárez, N. M., Logan, N. A., McDonald, M., Bowie, A., et al. (2023) · Viruses · doi:10.3390/v15081769 · Cited by 4
“However, research has shown that humans are at an increased risk of acute kidney injury and chronic disease following SARS-CoV-2 infection, even if they were not hospitalised [56], and this cat’s renal disease might therefore also be related to SARS-CoV-2 infection.”
Background
COVID-19 are dangerous to the kidneys in any situation, not only in a pandemic: LONG-COVID-19 and kidney disease
Evrin, T., & Katipoglu, B. (2021) · Cardiology Journal · doi:10.5603/cj.a2021.0163 · Cited by 4
“Even beyond the first 30 days after diagnosis of COVID-19, unfavorable renal symptoms such as urinary tract infections, AKI, and CKD occurred in individuals who required hospitalization [6].”
Background
Clinical coding of long COVID in English primary care: a federated analysis of 58 million patient records in situ using OpenSAFELY
Walker, A. J., MacKenna, B., Inglesby, P., Rentsch, C. T., Curtis, H. J., Morton, C. E., Morley, J., Mehrkar, A., Bacon, S., Hickman, G., et al. (2021) · University of Oxford · doi:10.53764/rpt.3917ab5ac5 · Cited by 4

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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