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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Increased risk of new-onset diabetes in patients with COVID-19: a systematic review and meta-analysis
Li, J., Li, Y., Wang, Z., Liu, N., He, L., & Zhang, H. (2023) · Frontiers in Public Health · doi:10.3389/fpubh.2023.1170156 · Cited by 45
“5%); (2) Two outpatient or one inpatient ICD-10 codes of E08–E13; or (3) receipt of an initial and one refill prescription of a glucoselowering medication.”
BackgroundMethodInfluential
Long COVID as a functional somatic symptom disorder caused by abnormally precise prior expectations during Bayesian perceptual processing: A new hypothesis and implications for pandemic response
Joffe, A. R., & Elliott, A. (2023) · SAGE Open Medicine · doi:10.1177/20503121231194400 · Cited by 50
Multimodal Molecular Imaging Reveals Tissue-Based T Cell Activation and Viral RNA Persistence for Up to 2 Years Following COVID-19Preprint
Peluso, M. J., Ryder, D., Flavell, R. R., Wang, Y., Levi, J., LaFranchi, B. H., Deveau, T., Buck, A. M., Munter, S. E., Asare, K. A., et al. (2023) · medRxiv · doi:10.1101/2023.07.27.23293177 · Cited by 45
Post-acute sequelae of SARS-CoV-2 with clinical condition definitions and comparison in a matched cohort
Horberg, M. A., Watson, E. S., Bhatia, M., Jefferson, C. R., Certa, J. M., Kim, S., Fathi, L., Althoff, K. N., Williams, C., & Moore, R. (2022) · Nature Communications · doi:10.1038/s41467-022-33573-6 · Cited by 43
“persisted into the 30–120 days period, but not previously identified in the pre-existing conditions time interval, and (3) late time interval new disease diagnoses 30–120 days post-T0, but not previously identified in the pre-existing conditions or acute and persistent time intervals (Fig.”
Background
Long-term symptom profiles after COVID-19 vs other acute respiratory infections: an analysis of data from the COVIDENCE UK study
Vivaldi, G., Pfeffer, P., Talaei, M., Basera, T. J., Shaheen, S. O., & Martineau, A. R. (2023) · EClinicalMedicine · doi:10.1016/j.eclinm.2023.102251 · Cited by 46
“Indeed, retrospective cohort studies have generally found worse post-acute outcomes among patients with SARS-CoV-2 compared with in ﬂ uenza 33,34 and other viral infections 35 ; these studies have largely been restricted to hospitalised patients or electronic health record data, thus representing…”
Background
No Evidence of Long-Term Disruption of Glycometabolic Control After SARS-CoV-2 Infection
Laurenzi, A., Caretto, A., Molinari, C., Mercalli, A., Melzi, R., Nano, R., Tresoldi, C., Rovere, P. Q., Ciceri, F., Lampasona, V., et al. (2021) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgab792 · Cited by 44
“For example, compared to individuals who were hospitalized with seasonal influenza, patients who were hospitalized for COVID-19 did not have a significantly higher burden of type 2 diabetes, while they had a significant trend to a lower burden of type 1 diabetes (48,49).”
Result
Deep Dive into the Long Haul: Analysis of Symptom Clusters and Risk Factors for Post-Acute Sequelae of COVID-19 to Inform Clinical Care
Goldhaber, N. H., Kohn, J. N., Ogan, W. S., Sitapati, A. M., Longhurst, C., Wang, A. Y., Lee, S., Hong, S., & Horton, L. E. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph192416841 · Cited by 43
The Coronavirus pandemic – 2022: Viruses, variants & vaccines
Alexandridi, M., Mazej, J., Palermo, E., & Hiscott, J. B. (2022) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2022.02.002 · Cited by 44
Pathophysiology and clinical management of coronavirus disease (COVID-19): a mini-review
Zhu, Y., Sharma, L., & Chang, D. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1116131 · Cited by 57
“Beyond the acute disease, the chronic consequences of COVID-19 are being documented that include severe life-altering changes such as chronic fatigue, impaired memory, and cognitive functions, among others (10, 11).”
Background
Do Anxiety and Depression Predict Persistent Physical Symptoms After a Severe COVID-19 Episode? A Prospective Study
Bottemanne, H., Gouraud, C., Hulot, J., Blanchard, A., Ranque, B., Lahlou‐Laforêt, K., Limosin, F., Günther, S., Lebeaux, D., & Lemogne, C. (2021) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2021.757685 · Cited by 42
“This question could therefore represent a major public health concern over the next few years, and supports the urgent need to understand the pathophysiological mechanisms and clinical predictors of these symptoms (8, 9).”
Background
Quality of life and ability to work of patients with Post-COVID syndrome in relation to the number of existing symptoms and the duration since infection up to 12 months: a cross-sectional study
Lemhöfer, C., Sturm, C., Loudovici-Krug, D., Guntenbrunner, C., Bülow, M., Reuken, P. A., Quickert, S., & Best, N. (2023) · Quality of Life Research · doi:10.1007/s11136-023-03369-2 · Cited by 45
Depression and anxiety before and at the beginning of the COVID-19 pandemic and incident persistent symptoms: a prospective population-based cohort study
Matta, J., Robineau, O., Wiernik, E., Carrat, F., Severi, G., Touvier, M., Gouraud, C., Vedrines, C. O., Pitron, V., Ranque, B., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02179-9 · Cited by 41
“Further details regarding covariates are given in Supplemental Methods 1.”
Neutrophil extracellular traps and long COVID
Shafqat, A., Omer, M. H., Albalkhi, I., Razzak, G. A., Abdulkader, H. S., Rab, S. A., Sabbah, B. N., AlKattan, K. M., & Yaqinuddin, A. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1254310 · Cited by 49
Outbreaks of COVID-19 variants in US prisons: a mathematical modelling analysis of vaccination and reopening policies
Ryckman, T. S., Chin, E. T., Prince, L., Leidner, D., Long, E., Studdert, D. M., Salomon, J. A., Alarid‐Escudero, F., Andrews, J. R., & Goldhaber‐Fiebert, J. D. (2021) · The Lancet Public Health · doi:10.1016/s2468-2667(21)00162-6 · Cited by 41
COVID-19: Diabetes Perspective—Pathophysiology and Management
Dallavalasa, S., Tulimilli, S. V., Janhavi, P., Ramachandra, R., Madhunapantula, S. V., & Veeranna, R. P. (2023) · Pathogens · doi:10.3390/pathogens12020184 · Cited by 45
“Recent studies have shown that long-COVID effects involve pulmonary and extra-pulmonary organ manifestations and contribute to the development of various diseases such as diabetes [204].”
Background
Interferon at the crossroads of SARS-CoV-2 infection and COVID-19 disease
Samuel, C. E. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104960 · Cited by 50
Vaccination-Associated Myocarditis and Myocardial Injury
Altman, N. L., Berning, A. A., Mann, S., Quaife, R. A., Gill, E. A., Auerbach, S. R., Campbell, T., & Bristow, M. R. (2023) · Circulation Research · doi:10.1161/circresaha.122.321881 · Cited by 42
Return-to-work with long COVID: An Episodic Disability and Total Worker Health® analysis
Stelson, E., Dash, D., McCorkell, L., Wilson, C., Assaf, G., Re’em, Y., & Wei, H. (2023) · Social Science & Medicine · doi:10.1016/j.socscimed.2023.116336 · Cited by 40
The Cost-Effectiveness of Remdesivir for Hospitalized Patients With COVID-19
Whittington, M. D., Pearson, S. D., Rind, D. M., & Campbell, J. D. (2022) · Value in Health · doi:10.1016/j.jval.2021.11.1378 · Cited by 40
Cost-Effectiveness Analysis of Molnupiravir Versus Best Supportive Care for the Treatment of Outpatient COVID-19 in Adults in the US
Goswami, H., Alsumali, A., Jiang, Y., Schindler, M., Duke, E. R., Cohen, J., Briggs, A. H., & Puenpatom, A. (2022) · PharmacoEconomics · doi:10.1007/s40273-022-01168-0 · Cited by 41
“Evidence on long-term sequelae and readmissions in COVID-19 patients is well established [41, 42]; however these outcomes were not captured in the MOVe-OUT trial.”
Background
T cell responses to SARS-CoV-2 in people with and without neurologic symptoms of long COVIDPreprint
Visvabharathy, L., Hanson, B. A., Orban, Z. S., Lim, P. H., Palacio, N. M., Jimenez, M., Clark, J. R., Graham, E. L., Liotta, E. M., Tachas, G., et al. (2021) · medRxiv · doi:10.1101/2021.08.08.21261763 · Cited by 40
“, 2010), as well as the possibility of persistent SARS-CoV-2 infection in the 271 periphery (Al-Aly et al., 2021).”
Background
Predictive models of long COVID
Antony, B., Blau, H., Casiraghi, E., Loomba, J. J., Callahan, T. J., Laraway, B. J., Wilkins, K. J., Antonescu, C., Valentini, G., Williams, A. E., et al. (2023) · EBioMedicine · doi:10.1016/j.ebiom.2023.104777 · Cited by 39
Association of 2024–2025 Covid-19 Vaccine with Covid-19 Outcomes in U.S. Veterans
Cai, M., Xie, Y., & Al‐Aly, Z. (2025) · New England Journal of Medicine · doi:10.1056/nejmoa2510226 · Cited by 43
Home Garden With Eco-Healing Functions Benefiting Mental Health and Biodiversity During and After the COVID-19 Pandemic: A Scoping Review
Zhang, X., Zhang, Y., & Zhai, J. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2021.740187 · Cited by 46
““Ecological Medicine” Is an Efficient Healing Alternative to Improve Mental Health—Nature Experience as a Determinant of Mental Health To deal with the negative effects of isolation and social distance policies on mental health, a home garden and gardening can be effective approaches for people re-connecting to green…”
Background
Study protocol for the Innovative Support for Patients with SARS-COV-2 Infections Registry (INSPIRE): A longitudinal study of the medium and long-term sequelae of SARS-CoV-2 infection
O’Laughlin, K. N., Thompson, M., Hota, B. N., Gottlieb, M. A., Plumb, I. D., Chang, A. M., Wisk, L. E., Hall, A. J., Wang, R. C., Spatz, E. S., et al. (2022) · PLoS ONE · doi:10.1371/journal.pone.0264260 · Cited by 39
Demographic And Clinical Factors Associated With Long COVID
Song, Z., & Giuriato, M. (2023) · Health Affairs · doi:10.1377/hlthaff.2022.00991 · Cited by 39
Mechanisms and clinical relevance of the bidirectional relationship of viral infections with metabolic diseases
Perakakis, N., Harb, H., Hale, B. G., Varga, Z., Steenblock, C., Kanczkowski, W., Alexaki, V. I., Ludwig, B., Mirtschink, P., Solimena, M., et al. (2023) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(23)00154-7 · Cited by 39
Direct health care costs associated with COVID-19 in the United States
DeMartino, J. K., Swallow, E., Goldschmidt, D., Yang, K., Viola, M., Radtke, T., & Kirson, N. Y. (2022) · Journal of Managed Care & Specialty Pharmacy · doi:10.18553/jmcp.2022.22050 · Cited by 39
Long COVID and its associated factors among COVID survivors in the community from a middle-income country—An online cross-sectional study
Moy, F. M., Hairi, N. N., Lim, E. R. J., & Bulgiba, A. M. (2022) · PLoS ONE · doi:10.1371/journal.pone.0273364 · Cited by 41
“However, some may still experience poorer work performance due to the Long COVID sequalae [4,5].”
Background
Gut Microbiota Disruption in COVID-19 or Post-COVID Illness Association with severity biomarkers: A Possible Role of Pre / Pro-biotics in manipulating microflora
Alharbi, K. S., Singh, Y. P., Almalki, W. H., Rawat, S., Afzal, O., Altamimi, A. S. A., Kazmi, I. A., Al-Abbasi, F. A., Alzarea, S. I., Singh, S. K., et al. (2022) · Chemico-Biological Interactions · doi:10.1016/j.cbi.2022.109898 · Cited by 38
“turbances, among others (Table 1) [30,31].”
What Do We Need to Know About Musculoskeletal Manifestations of COVID-19?
Pires, R. E. S., Reis, I. G. N., Waldolato, G., Pires, D. D., Bidolegui, F., & Giordano, V. (2022) · JBJS Reviews · doi:10.2106/jbjs.rvw.22.00013 · Cited by 40
Remdesivir for the treatment of patients hospitalized with COVID-19 receiving supplemental oxygen: a targeted literature review and meta-analysis
Beckerman, R., Gori, A., Jeyakumar, S., Malin, J. J., Paredes, R., Póvoa, P. M. S. R., Smith, N., & Teixeira-Pinto, A. M. (2022) · Scientific Reports · doi:10.1038/s41598-022-13680-6 · Cited by 37
Reductions in US life expectancy during the COVID-19 pandemic by race and ethnicity: Is 2021 a repetition of 2020?
Andrasfay, T., & Goldman, N. (2022) · PLoS ONE · doi:10.1371/journal.pone.0272973 · Cited by 40
“Apart from direct COVID-19 deaths, there is also evidence that survivors of COVID-19 have increased mortality risks for at least six months following initial recovery [44], and the mortality impact of long COVID is not yet known.”
Background
Post-COVID-19 Syndrome Mechanisms, Prevention and Management
Najafi, M. B., & Javanmard, S. (2023) · International Journal of Preventive Medicine · doi:10.4103/ijpvm.ijpvm_508_21 · Cited by 38
“7 times higher than matched controls in non‐hospitalized survivors at 6‐months follow‐up.[73] Overall it was shown that COVID survivors have a 3 times higher chance to experience a major adverse cardiac event (heart failure, arrhythmias, and myocardial infarction) at 5 months post‐discharge compared to age, sex, and r…”
Background
Systemic antibody responses against human microbiota flagellins are overrepresented in chronic fatigue syndrome patients
Vogl, T. J., Kalka, I. N., Klompus, S., Leviatan, S., Weinberger, A., & Segal, E. (2022) · Science Advances · doi:10.1126/sciadv.abq2422 · Cited by 36
“…corona-virus 2) has also been reported to cause persisting ME/CFS–like symptoms in a subset of recovered patients [termed as long corona-virus disease 2019 (long COVID), post–COVID-19 syndrome, or chronic COVID syndrome] ( 34 – 38 ), with implications for studying “classical” ME/CFS ( 39 ).”
Dissecting the Molecular Mechanisms Surrounding Post-COVID-19 Syndrome and Neurological Features
Mohamed, M. S., Johansson, A., Jonsson, J., & Schiöth, H. B. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084275 · Cited by 37
“Summary of the described manifestations of PCS; (*) represents the most commonly reported symptoms [4,8,18,20,21,24].”
BackgroundInfluential
Anti-nucleocapsid antibody levels and pulmonary comorbid conditions are linked to post–COVID-19 syndrome
Jia, X., Cao, S., Lee, A., Manohar, M., Sindher, S., Ahuja, N. K., Artandi, M. K., Blish, C. A., Blomkalns, A. L., Chang, I., et al. (2022) · JCI Insight · doi:10.1172/jci.insight.156713 · Cited by 35
“Long-term respiratory complications of COVID-19 infection are well documented and include abnormal lung imaging, lung diffusion impairment, and pulmonary fibrosis (24, 25).”
Life stressors significantly impact long-term outcomes and post-acute symptoms 12-months after COVID-19 hospitalization
Frontera, J. A., Sabadia, S. B., Yang, D., de Havenon, A., Yaghi, S. R., Lewis, A. K., Lord, A. S., Melmed, K. R., Thawani, S. P., Balcer, L. J., et al. (2022) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2022.120487 · Cited by 42
“[5] D. Groff, A. Sun, A.E. Ssentongo, et al., Short-term and long-term rates of Postacute sequelae of SARS-CoV-2 infection: a systematic review, JAMA Netw.”
BackgroundInfluential
Severity of COVID-19 and adverse long-term outcomes: a retrospective cohort study based on a US electronic health record database
Jovanoski, N., Chen, X., Becker, U., Zalocusky, K. A., Chawla, D., Tsai, L. W., Borm, M. E. A., Neighbors, M., & Yau, V. (2021) · BMJ Open · doi:10.1136/bmjopen-2021-056284 · Cited by 35
Who Is at Risk of Poor Mental Health Following Coronavirus Disease-19 Outpatient Management?
Hüfner, K., Tymoszuk, P., Ausserhofer, D., Sahanic, S., Pizzini, A., Rass, V., Gálffy, M., Boehm, A., Kurz, K., Sonnweber, T., et al. (2022) · Frontiers in Medicine · doi:10.3389/fmed.2022.792881 · Cited by 33
“In large-scale studies encompassing both in- and outpatients, COVID-19 was identified as an important risk factor for anxiety, stress-related, and depressive adjustment disorders (9) and mental health conditions were ascertained in nearly one-fifth of COVID-19 convalescents (8).”
BackgroundInfluential
Health Care Access and Affordability Among US Adults Aged 18 to 64 Years With Self-reported Post–COVID-19 Condition
Karpman, M., Zuckerman, S., & Morriss, S. (2023) · JAMA Network Open · doi:10.1001/jamanetworkopen.2023.7455 · Cited by 35
Rehabilitative interventions in patients with persistent post COVID-19 symptoms—a review of recent advances and future perspectives
Gloeckl, R., Leitl, D., Schneeberger, T., Jarosch, I., & Koczulla, A. R. (2023) · European Archives of Psychiatry and Clinical Neuroscience · doi:10.1007/s00406-023-01631-9 · Cited by 40
Exploring the Pathophysiology of Long COVID: The Central Role of Low-Grade Inflammation and Multisystem Involvement
Gusev, E., & Sarapultsev, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25126389 · Cited by 39
Accelerated vascular ageing after COVID-19 infection: the CARTESIAN study
Bruno, R. M., Badhwar, S., Abid, L., Agharazii, M., Anastasio, F., Bellien, J., Burghuber, O., Faconti, L., Filipovský, J., Ghiadoni, L., et al. (2025) · European Heart Journal · doi:10.1093/eurheartj/ehaf430 · Cited by 34
Inflammation, immunity, and antigen persistence in post-acute sequelae of SARS-CoV-2 infection
Newell, K. L., & Waickman, A. T. (2022) · Current Opinion in Immunology · doi:10.1016/j.coi.2022.102228 · Cited by 37
STIMULATE-ICP: A pragmatic, multi-centre, cluster randomised trial of an integrated care pathway with a nested, Phase III, open label, adaptive platform randomised drug trial in individuals with Long COVID: A structured protocol
Forshaw, D., Wall, E. C., Prescott, G. J., Dehbi, H., Green, A., Attree, E., Hismeh, L., Strain, W. D., Crooks, M. G., Watkins, C. L., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0272472 · Cited by 34
Untargeted analysis in post-COVID-19 patients reveals dysregulated lipid pathways two years after recovery
López‐Hernández, Y., Oropeza-Valdez, J. J., López, D. A. G., Borrego-Moreno, J. C., Murgu, M., Valdez, J., López, J. A., & Monárrez‐Espino, J. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1100486 · Cited by 38
“In terms of mortality, a large study comprising nearly five million healthy controls and 90,000 COVID-19 patients revealed that the risk of death among COVID-19 survivors in the following 6 months after infection, increased by 60% (Al-Aly et al., 2021).”
BackgroundInfluential
Unmet needs for health care
OECD (2021) · Health at a glance · doi:10.1787/13aff239-en · Cited by 36

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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