High-dimensional characterization of post-acute sequelae of COVID-19
Open accessPublished version of a preprint
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.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Post-covid syndrome is characterized by several symptoms affecting quality of life.
“This is typically referred to as a post-covid syndrome, characterized by several symptoms affecting quality of life (1–5).”
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Wang, D., Hu, B., Hu, C., Zhu, F., Liu, X., Zhang, J., Wang, B., Xiang, H., Cheng, Z., Xiong, Y., et al. (2020) · JAMA · doi:10.1001/jama.2020.1585 · Cited by 20,148 · see citing works
La certeza de lo impredecible: Cultura Educación y Sociedad en tiempos de COVID19
Martínez González, M. (2020) · DSPACE System - Metalibrary (University of the Coast) · Cited by 18,463 · see citing works
Vincent, J. L., Moreno, R., Takala, J., Willatts, S., De Mendonça, A., Bruining, H., Reinhart, C. K., Suter, P. M., & Thijs, L. G. (1996) · Intensive Care Medicine · doi:10.1007/bf01709751 · Cited by 11,674 · see citing works
Vincent, J.-L., de Mendonca, A., Cantraine, F., Moreno, R., Takala, J., Suter, P. M., Sprung, C. L., Colardyn, F., & Blecher, S. (1998) · Critical Care Medicine · doi:10.1097/00003246-199811000-00016 · Cited by 3,463 · see citing works
Making Neighborhood-Disadvantage Metrics Accessible — The Neighborhood Atlas
Kind, A. J. H., & Buckingham, W. R. (2018) · New England Journal of Medicine · doi:10.1056/nejmp1802313 · Cited by 3,310 · see citing works
Management of post-acute covid-19 in primary care
Greenhalgh, T., Knight, M., A’Court, C., Buxton, M., & Husain, L. (2020) · BMJ · doi:10.1136/bmj.m3026 · Cited by 1,693 · see citing works
Negative Controls: A Tool for Detecting Confounding and Bias in Observational Studies
Lipsitch, M., Tchetgen Tchetgen, E., & Cohen, T. (2010) · Epidemiology · doi:10.1097/ede.0b013e3181d61eeb · Cited by 1,583 · see citing works
A tutorial on propensity score estimation for multiple treatments using generalized boosted models
McCaffrey, D. F., Griffin, B. A., Almirall, D., Slaughter, M. E., Ramchand, R., & Burgette, L. F. (2013) · Statistics in Medicine · doi:10.1002/sim.5753 · Cited by 1,450 · see citing works
Balancing Covariates via Propensity Score Weighting
Li, F., Morgan, K. L., & Zaslavsky, A. M. (2016) · Journal of the American Statistical Association · doi:10.1080/01621459.2016.1260466 · Cited by 1,033 · see citing works
Thomas (2020) · doi:10.1001/jama.2020.7819 · Cited by 835 · see citing works
Long-term Health Consequences of COVID-19
del Rı́o, C., Collins, L. F., & Malani, P. (2020) · JAMA · doi:10.1001/jama.2020.19719 · Cited by 712 · see citing works
The 2016 global and national burden of diabetes mellitus attributable to PM 2·5 air pollution
Bowe, B., Xie, Y., Li, T., Yan, Y., Xian, H., & Al-Aly, Z. (2018) · The Lancet Planetary Health · doi:10.1016/s2542-5196(18)30140-2 · Cited by 371 · see citing works
Proton Pump Inhibitors and Risk of Incident CKD and Progression to ESRD
Xie, Y., Bowe, B. C., Li, T., Xian, H., Balasubramanian, S., & Al‐Aly, Z. (2016) · Journal of the American Society of Nephrology · doi:10.1681/asn.2015121377 · Cited by 334 · see citing works
Balancing Covariates via Propensity Score WeightingPreprint
Li, F., Lock, K., Alan, M., & Zaslavsky, M. (2014) · Cited by 313 · see citing works
Long-term consequences of COVID-19: research needs
Yelin, D., Wirtheim, E., Vetter, P., Kalil, A. C., Bruchfeld, J., Runold, M., Guaraldi, G., Mussini, C., Gudiol, C., Pujol, M., et al. (2020) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(20)30701-5 · Cited by 311 · see citing works
Wei, Y., Wang, Y., Di, Q., Choirat, C., Wang, Y., Koutrakis, P., Zanobetti, A., Dominici, F., & Schwartz, J. D. (2019) · BMJ · doi:10.1136/bmj.l6258 · Cited by 282 · see citing works
Lancet, T. (2020) · The Lancet · doi:10.1016/s0140-6736(20)32662-3 · Cited by 251 · see citing works
Xie, Y., Bowe, B. C., Li, T., Xian, H., Yan, Y., & Al‐Aly, Z. (2017) · BMJ Open · doi:10.1136/bmjopen-2016-015735 · Cited by 231 · see citing works
Xie, Y., Bowe, B. C., Yan, Y., Xian, H., Li, T., & Al‐Aly, Z. (2019) · BMJ · doi:10.1136/bmj.l1580 · Cited by 226 · see citing works
Sivan, M., & Taylor, S. (2020) · BMJ · doi:10.1136/bmj.m4938 · Cited by 224 · see citing works
High Density Lipoprotein Cholesterol and the Risk of All-Cause Mortality among U.S. Veterans
Bowe, B., Xie, Y., Xian, H., Balasubramanian, S., Zayed, M. A., & Al-Aly, Z. (2016) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.00730116 · Cited by 213 · see citing works
Self-citationXie, Y., Bowe, B. C., Li, T., Xian, H., Yan, Y., & Al‐Aly, Z. (2017) · Kidney International · doi:10.1016/j.kint.2016.12.021 · Cited by 201 · see citing works
Acute Kidney Injury in a National Cohort of Hospitalized US Veterans with COVID-19
Bowe, B. C., Cai, M., Xie, Y., Gibson, A. K., Maddukuri, G. S., & Al‐Aly, Z. (2020) · Clinical Journal of the American Society of Nephrology · doi:10.2215/cjn.09610620 · Cited by 201 · see citing works
Higher blood urea nitrogen is associated with increased risk of incident diabetes mellitus
Xie, Y., Bowe, B. C., Li, T., Xian, H., Yan, Y., & Al‐Aly, Z. (2017) · Kidney International · doi:10.1016/j.kint.2017.08.033 · Cited by 198 · see citing works
A Selective Review of Negative Control Methods in Epidemiology
Shi, X., Miao, W., & Tchetgen, E. T. (2020) · Current Epidemiology Reports · doi:10.1007/s40471-020-00243-4 · Cited by 194 · see citing works
Xie, Y., Bowe, B. C., Maddukuri, G. S., & Al‐Aly, Z. (2020) · BMJ · doi:10.1136/bmj.m4677 · Cited by 183 · see citing works
Greene, M. L., Steinman, M. A., McNicholl, I. R., & Valcour, V. (2014) · Journal of the American Geriatrics Society · doi:10.1111/jgs.12695 · Cited by 171 · see citing works
Propensity score weighting for causal inference with multiple treatments
Li, F., & Fan, L. (2019) · The Annals of Applied Statistics · doi:10.1214/19-aoas1282 · Cited by 170 · see citing works
Xie, Y., Bowe, B. C., Gibson, A. K., McGill, J. B., Maddukuri, G. S., Yan, Y., & Al‐Aly, Z. (2020) · Diabetes Care · doi:10.2337/dc20-1890 · Cited by 155 · see citing works
Long COVID guidelines need to reflect lived experience
Gorna, R., MacDermott, N. E., Rayner, C. R., O’Hara, M. E., Evans, S. E., Agyen, L., Nutland, W., Rogers, N., & Hastie, C. (2020) · The Lancet · doi:10.1016/s0140-6736(20)32705-7 · Cited by 153 · see citing works
Bowe, B. C., Xie, Y., Xian, H., Balasubramanian, S., & Al‐Aly, Z. (2016) · Kidney International · doi:10.1016/j.kint.2015.12.034 · Cited by 150 · see citing works
Knipe, D. W., Evans, H. E. R., Marchant, A. L., Gunnell, D., & John, A. M. (2020) · Wellcome Open Research · doi:10.12688/wellcomeopenres.15870.2 · Cited by 127 · see citing works
Covid-19: Mental health consequences of pandemic need urgent research, paper advises
Mahase, E. (2020) · BMJ · doi:10.1136/bmj.m1515 · Cited by 91 · see citing works
Health Services and Outcomes Research Methodology
(2013) · Health Services and Outcomes Research Methodology · doi:10.1007/10742.1572-9400 · Cited by 83 · see citing works
Raker, E. J., Zacher, M. L., & Lowe, S. R. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006706117 · Cited by 82 · see citing works
Meeting the challenge of long COVID
(2020) · Nature Medicine · doi:10.1038/s41591-020-01177-6 · Cited by 75 · see citing works
Olvey, E. L., Clauschee, S. F., & Malone, D. C. (2009) · Clinical Pharmacology & Therapeutics · doi:10.1038/clpt.2009.198 · Cited by 65 · see citing works
Vincent, J., de Mendonça, A., CANTRAINE, F., MORENO, R., TAKALA, J., SUTER, P., Sprung, C., Colardyn, F., & BLECHER, S. (1998) · Ghent University Academic Bibliography (Ghent University) · Cited by 65 · see citing works
Xie, Y., Bowe, B. C., Gibson, A. K., McGill, J. B., Yan, Y., Maddukuri, G. S., & Al‐Aly, Z. (2020) · Diabetes Care · doi:10.2337/dc20-1231 · Cited by 40 · see citing works
Using Veterans Affairs Corporate Data Warehouse to identify 30-day hospital readmissions
Vincent, B. M., Wiitala, W. L., Burns, J., Iwashyna, T. J., & Prescott, H. C. (2018) · Health Services and Outcomes Research Methodology · doi:10.1007/s10742-018-0178-3 · Cited by 39 · see citing works
Vincent, J., Moreno, R., Takala, J., Willatts, S., de Mendonça, A., Bruining, H., Reinhart, C., Suter, P., & Thijs, L. (1997) · EUR Research Repository (Erasmus University Rotterdam) · Cited by 35 · see citing works
Best Definitions of Multimorbidity to Identify Patients With High Health Care Resource Utilization
Aubert, C. E., Schnipper, J. L., Roumet, M., Marques-Vidal, P. M., Stirnemann, J., Auerbach, A. D., Zimlichman, E., Kripalani, S. B., Vasilevskis, E. E., Robinson, E. J., et al. (2020) · Mayo Clinic Proceedings Innovations Quality & Outcomes · doi:10.1016/j.mayocpiqo.2019.09.002 · Cited by 34 · see citing works
COVID-19 policies in the UK and consequences for mental health
Townsend, E. (2020) · The Lancet Psychiatry · doi:10.1016/s2215-0366(20)30457-0 · Cited by 27 · see citing works
Distinguishing between direct and indirect consequences of covid-19
Figueroa, J. D., Brennan, P. M., Τheodoratou, E., Poon, M. T. C., Purshouse, K. R., Din, F. V. N., Jin, K., Mesa‐Eguiagaray, I., Dunlop, M. G., Hall, P. S., et al. (2020) · BMJ · doi:10.1136/bmj.m2377 · Cited by 23 · see citing works
Flagged first, then by citations
2 of the 46 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Characterizing long COVID in an international cohort: 7 months of symptoms and their impact
Davis, H. E., Assaf, G. S., McCorkell, L., Wei, H., Low, R. J., Re'em, Y., Redfield, S., Austin, J. P., & Akrami, A. (2021) · eClinicalMedicine · doi:10.1016/j.eclinm.2021.101019 · Cited by 2,881 · see citing works
Long-term cardiovascular outcomes of COVID-19
Xie, Y., Xu, E., Bowe, B. C., & Al‐Aly, Z. (2022) · Nature Medicine · doi:10.1038/s41591-022-01689-3 · Cited by 2,065 · see citing works
Chen, C., Haupert, S. R., Zimmermann, L., Shi, X., Fritsche, L. G., & Mukherjee, B. (2022) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiac136 · Cited by 1,395 · see citing works
1-year outcomes in hospital survivors with COVID-19: a longitudinal cohort study.
Huang, L., Yao, Q., Gu, X., Wang, Q., Ren, L., Wang, Y., Hu, P., Guo, L., Liu, M., Xu, J., et al. (2021) · The Lancet · doi:10.1016/s0140-6736(21)01755-4 · Cited by 1,101 · see citing works
Symptoms and risk factors for long COVID in non-hospitalized adults
Subramanian, A., Nirantharakumar, K., Hughes, S., Myles, P. R., Williams, T., Gokhale, K. M., Taverner, T., Chandan, J. S., Brown, K. R., Simms-Williams, N., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-01909-w · Cited by 1,060 · see citing works
Short-term and Long-term Rates of Postacute Sequelae of SARS-CoV-2 Infection
Groff, D., Sun, A., Ssentongo, A. E., Ba, D. M., Parsons, N., Poudel, G. R., Lekoubou, A., Oh, J. S., Ericson, J. E., Ssentongo, P., et al. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.28568 · Cited by 974 · see citing works
SARS-CoV-2 infection and persistence in the human body and brain at autopsy
Stein, S. R., Ramelli, S. C., Grazioli, A., Chung, J., Singh, M., Yinda, C. K., Winkler, C. W., Sun, J., Dickey, J. M., Ylaya, K., et al. (2022) · Nature · doi:10.1038/s41586-022-05542-y · Cited by 997 · see citing works
Collaborators, G. B. O. D. L. C., Hanson, S. W., Abbafati, C., Aerts, J. G. J. V., Al‐Aly, Z., Ashbaugh, C., Ballouz, T., Blyuss, O. B., Bobkova, P., Bonsel, G. J., et al. (2022) · JAMA · doi:10.1001/jama.2022.18931 · Cited by 989 · see citing works
Taquet, M., Dercon, Q., Luciano, S., Geddes, J. R., Masud Husain, B., & Harrison, P. J. (2021) · PLoS Medicine · doi:10.1371/journal.pmed.1003773 · Cited by 918 · see citing works
Long COVID after breakthrough SARS-CoV-2 infection
Al-Aly, Z., Bowe, B., & Xie, Y. (2022) · Nature Medicine · doi:10.1038/s41591-022-01840-0 · Cited by 866 · see citing works
Development of a Definition of Postacute Sequelae of SARS-CoV-2 Infection
Thaweethai, T., Jolley, S. E., Karlson, E. W., Levitan, E. B., Levy, B. D., McComsey, G. A., McCorkell, L., Nadkarni, G. N., Parthasarathy, S., Singh, U., et al. (2023) · JAMA · doi:10.1001/jama.2023.8823 · Cited by 841 · see citing works
Persistence of somatic symptoms after COVID-19 in the Netherlands: an observational cohort study
Ballering, A., van Zon, S. K. R., Hartman, T. O., & Rosmalen, J. G. M. (2022) · The Lancet · doi:10.1016/s0140-6736(22)01214-4 · Cited by 833 · see citing works
Distinguishing features of long COVID identified through immune profiling
Klein, J., Wood, J., Jaycox, J. R., Dhodapkar, R. M., Lu, P., Gehlhausen, J. R., Tabachnikova, A., Greene, K., TABACOF, L. R., Malik, A. A., et al. (2023) · Nature · doi:10.1038/s41586-023-06651-y · Cited by 818 · see citing works
Taquet, M., Sillett, R., Zhu, L., Mendel, J., Camplisson, I., Dercon, Q., & Harrison, P. J. (2022) · The Lancet Psychiatry · doi:10.1016/s2215-0366(22)00260-7 · Cited by 737 · see citing works
Pathological sequelae of long-haul COVID
Mehandru, S., & Mérad, M. (2022) · Nature Immunology · doi:10.1038/s41590-021-01104-y · Cited by 649 · see citing works
Long COVID: post-acute sequelae of COVID-19 with a cardiovascular focus
Raman, B., Bluemke, D. A., Lüscher, T. F., & Neubauer, S. (2022) · European Heart Journal · doi:10.1093/eurheartj/ehac031 · Cited by 673 · see citing works
Acute and postacute sequelae associated with SARS-CoV-2 reinfection
Bowe, B. C., Xie, Y., & Al‐Aly, Z. (2022) · Nature Medicine · doi:10.1038/s41591-022-02051-3 · Cited by 632 · see citing works
Long COVID burden and risk factors in 10 UK longitudinal studies and electronic health records
Thompson, E. J., Williams, D. M., Walker, A. J., Mitchell, R. E., Niedzwiedz, C. L., Yang, T., Huggins, C. F., Kwong, A. S. F., Silverwood, R. J., Gessa, G. D., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30836-0 · Cited by 605 · see citing works
Swank, Z., Senussi, Y., Manickas-Hill, Z., Yu, X. G., Li, J. Z., Alter, G., & Walt, D. R. (2022) · Clinical Infectious Diseases · doi:10.1093/cid/ciac722 · Cited by 580 · see citing works
Long COVID science, research and policy
Al-Aly, Z., Davis, H., McCorkell, L., Soares, L., Wulf-Hanson, S., Iwasaki, A., & Topol, E. J. (2024) · Nature Medicine · doi:10.1038/s41591-024-03173-6 · Cited by 538 · see citing works
Alkodaymi, M. S., Omrani, O. A., Fawzy, N. A., Shaar, B. A., Almamlouk, R., Riaz, M. A., Obeidat, M. A., Obeidat, Y., Gerberi, D., Taha, R. M., et al. (2022) · Clinical Microbiology and Infection · doi:10.1016/j.cmi.2022.01.014 · Cited by 532 · see citing works
Long-term neurologic outcomes of COVID-19
Xu, E., Xie, Y., & Al-Aly, Z. (2022) · Nature Medicine · doi:10.1038/s41591-022-02001-z · Cited by 530 · see citing works
Self-citationRisks and burdens of incident diabetes in long COVID: a cohort study
Xie, Y., & Al-Aly, Z. (2022) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(22)00044-4 · Cited by 564 · see citing works
Natarajan, A., Zlitni, S., Brooks, E. F., Vance, S. E., Dahlen, A., Hedlin, H., Park, R. M., Han, A., Schmidtke, D. T., Verma, R., et al. (2022) · Med · doi:10.1016/j.medj.2022.04.001 · Cited by 409 · see citing works
Psychiatric and neuropsychiatric sequelae of COVID-19 – A systematic review
Schou, T. M., Joca, S. R. L., Wegener, G., & Bay-Richter, C. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.07.018 · Cited by 406 · see citing works
Gluckman, T. J., Bhave, N. M., Allen, L. A., Chung, E. H., Spatz, E. S., Ammirati, E., Baggish, A. L., Bozkurt, B., Cornwell, W. K., Harmon, K. G., et al. (2022) · Journal of the American College of Cardiology · doi:10.1016/j.jacc.2022.02.003 · Cited by 419 · see citing works
Prevalence and Correlates of Long COVID Symptoms Among US Adults
Perlis, R. H., Santillana, M., Ognyanova, K., Safarpour, A., Trujillo, K. L., Simonson, M. D., Green, J., Quintana, A., Druckman, J. N., Baum, M., et al. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.38804 · Cited by 385 · see citing works
Changes in cognitive functioning after COVID-19: a systematic review and meta-analysis
Crivelli, L., Palmer, K., Calandri, I., Guekht, A., Beghi, E., Carroll, W., Frontera, J., García‐Azorín, D., Westenberg, E., Winkler, A. S., et al. (2022) · Alzheimer's & Dementia · doi:10.1002/alz.12644 · Cited by 374 · see citing works
Comorbidities, multimorbidity and COVID-19
Russell, C. D., Lone, N., & Baillie, J. K. (2023) · Nature Medicine · doi:10.1038/s41591-022-02156-9 · Cited by 373 · see citing works
Serotonin reduction in post-acute sequelae of viral infection
Wong, A. C., Devason, A. S., Umana, I. C., Cox, T. O., Dohnalová, L., Litichevskiy, L., Perla, J., Lundgren, P., Etwebi, Z., Izzo, L., et al. (2023) · Cell · doi:10.1016/j.cell.2023.09.013 · Cited by 359 · see citing works
Bowe, B. C., Xie, Y., Xu, E., & Al-Aly, Z. (2021) · Journal of the American Society of Nephrology · doi:10.1681/asn.2021060734 · Cited by 350 · see citing works
Mechanisms of long COVID and the path toward therapeutics
Peluso, M. J., & Deeks, S. G. (2024) · Cell · doi:10.1016/j.cell.2024.07.054 · Cited by 356 · see citing works
Postacute sequelae of COVID-19 at 2 years
Bowe, B. C., Xie, Y., & Al‐Aly, Z. (2023) · Nature Medicine · doi:10.1038/s41591-023-02521-2 · Cited by 344 · see citing works
Menges, D., Ballouz, T., Anagnostopoulos, A., Aschmann, H. E., Domenghino, A., Fehr, J. S., & Puhan, M. A. (2021) · PLoS ONE · doi:10.1371/journal.pone.0254523 · Cited by 343 · see citing works
Wang, W., Wang, C.-Y., Wang, S., & Wei, J. C. (2022) · EClinicalMedicine · doi:10.1016/j.eclinm.2022.101619 · Cited by 343 · see citing works
COVID-19, Hyperglycemia, and New-Onset Diabetes
Khunti, K. K., Prato, S. D., Mathieu, C., Kahn, S. E., Gabbay, R. A., & Buse, J. B. (2021) · Diabetes Care · doi:10.2337/dc21-1318 · Cited by 331 · see citing works
Risks of mental health outcomes in people with covid-19: cohort study
Xie, Y., Xu, E., & Al-Aly, Z. (2022) · BMJ · doi:10.1136/bmj-2021-068993 · Cited by 333 · see citing works
Komaroff, A. L., & Lipkin, W. I. (2023) · Frontiers in Medicine · doi:10.3389/fmed.2023.1187163 · Cited by 321 · see citing works
Peluso, M. J., Lu, S., Tang, A. F., Durstenfeld, M. S., Ho, H.-E., Goldberg, S. A., Forman, C. A., Munter, S. E., Hoh, R., Tai, V., et al. (2021) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiab490 · Cited by 318 · see citing works
Postacute COVID-19 is Characterized by Gut Viral Antigen Persistence in Inflammatory Bowel Diseases
Zollner, A., Koch, R., Jukic, A., Pfister, A., Meyer, M., Rössler, A., Kimpel, J., Adolph, T. E., & Tilg, H. (2022) · Gastroenterology · doi:10.1053/j.gastro.2022.04.037 · Cited by 313 · see citing works
Association of Treatment With Nirmatrelvir and the Risk of Post–COVID-19 Condition
Xie, Y., Choi, T., & Al‐Aly, Z. (2023) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2023.0743 · Cited by 352 · see citing works
Xie, Y., Bowe, B. C., & Al‐Aly, Z. (2021) · Nature Communications · doi:10.1038/s41467-021-26513-3 · Cited by 293 · see citing works
Epigenetic memory of coronavirus infection in innate immune cells and their progenitors
Cheong, J.-G., Ravishankar, A., Sharma, S., Parkhurst, C. N., Grassmann, S. A., Wingert, C. K., Laurent, P., Ma, S., Paddock, L., Miranda, I. C., et al. (2023) · Cell · doi:10.1016/j.cell.2023.07.019 · Cited by 309 · see citing works
Mapping the effectiveness and risks of GLP-1 receptor agonists
Xie, Y., Choi, T., & Al-Aly, Z. (2025) · Nature Medicine · doi:10.1038/s41591-024-03412-w · Cited by 300 · see citing works
Self-citationBarrett, C. E., Koyama, A. K., Alvarez, P., Chow, W., Lundeen, E. A., Perrine, C. G., Pavkov, M. E., Rolka, D. B., Wiltz, J. L., Bull–Otterson, L., et al. (2022) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm7102e2 · Cited by 293 · see citing works
Koc, H. C., Xiao, J., Liu, W., Li, Y., & Chen, G. (2022) · International Journal of Biological Sciences · doi:10.7150/ijbs.75056 · Cited by 291 · see citing works
Long-term perturbation of the peripheral immune system months after SARS-CoV-2 infection
Ryan, F. J., Hope, C. M., Masavuli, M. G., Lynn, M. A., Mekonnen, Z. A., Yeow, A. E. L., García-Valtanen, P., Al-Delfi, Z., Gummow, J., Ferguson, C. C., et al. (2022) · BMC Medicine · doi:10.1186/s12916-021-02228-6 · Cited by 278 · see citing works
Redox imbalance links COVID-19 and myalgic encephalomyelitis/chronic fatigue syndrome
Paul, B. D., Lemle, M. D., Komaroff, A. L., & Snyder, S. H. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2024358118 · Cited by 271 · see citing works
Postacute Sequelae of SARS-CoV-2 Infection in the Pre-Delta, Delta, and Omicron Eras
Xie, Y., Choi, T., & Al‐Aly, Z. (2024) · New England Journal of Medicine · doi:10.1056/nejmoa2403211 · Cited by 281 · see citing works
Matta, J., Wiernik, E., Robineau, O., Carrat, F., Touvier, M., Severi, G., de Lamballerie, X., Blanché, H., Deleuze, J.-F., Gouraud, C., et al. (2022) · JAMA Internal Medicine · doi:10.1001/jamainternmed.2021.6454 · Cited by 266 · see citing works
Komaroff, A. L., & Lipkin, W. I. (2021) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2021.06.002 · Cited by 266 · see citing works
Three-year outcomes of post-acute sequelae of COVID-19
Cai, M., Xie, Y., Topol, E. J., & Al‐Aly, Z. (2024) · Nature Medicine · doi:10.1038/s41591-024-02987-8 · Cited by 261 · see citing works
COVID-19 and metabolic disease: mechanisms and clinical management
Steenblock, C., Schwarz, P. E. H., Ludwig, B., Linkermann, A., Zimmet, P., Kulebyakin, K. Y., Va, T., Markov, A. G., Lehnert, H., de Angelis, M. H., et al. (2021) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(21)00244-8 · Cited by 248 · see citing works
Sex differences in sequelae from COVID-19 infection and in long COVID syndrome: a review
Sylvester, S. V., Rusu, R., Chan, B., Bellows, M., O’Keefe, C., & Nicholson, S. (2022) · Current Medical Research and Opinion · doi:10.1080/03007995.2022.2081454 · Cited by 280 · see citing works
Taquet, M., Dercon, Q., & Harrison, P. J. (2022) · Brain, Behavior, and Immunity · doi:10.1016/j.bbi.2022.04.013 · Cited by 246 · see citing works
Verlohren, S., Brennecke, S. P., Galindo, A., Karumanchi, S. A., Mirković, L., Schlembach, D., Stepan, H., Vatish, M., Zeisler, H., & Rana, S. (2021) · Pregnancy Hypertension · doi:10.1016/j.preghy.2021.12.003 · Cited by 242 · see citing works
Unraveling the Mystery Surrounding Post-Acute Sequelae of COVID-19
Ramakrishnan, R. K., Kashour, T., Hamid, Q. A., Halwani, R., & Tleyjeh, I. M. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.686029 · Cited by 240 · see citing works
Long COVID and Post-infective Fatigue Syndrome: A Review
Sandler, C. X., Wyller, V. B., Moss-Morris, R. E., Buchwald, D., Crawley, E. M., Hautvast, J. L. A., Katz, B. Z., Knoop, H., Little, P. S., Taylor, R. R., et al. (2021) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofab440 · Cited by 232 · see citing works
Cohen, K., Ren, S., Heath, K., Dasmariñas, M. C., Jubilo, K. G., Guo, Y., Lipsitch, M., & Daugherty, S. E. (2022) · BMJ · doi:10.1136/bmj-2021-068414 · Cited by 219 · see citing works
Incidence and risk factors for persistent symptoms in adults previously hospitalized for COVID‐19
Munblit, D., Bobkova, P., Spiridonova, E., Shikhaleva, A., Gamirova, A., Blyuss, O. B., Nekliudov, N. A., Bugaeva, P., Andreeva, M., DunnGalvin, A., et al. (2021) · Clinical & Experimental Allergy · doi:10.1111/cea.13997 · Cited by 231 · see citing works
DNA binding to TLR9 expressed by red blood cells promotes innate immune activation and anemia
Lam, L., Murphy, S., Kokkinaki, D., Venosa, A., Sherrill-Mix, S. A., Casu, C., Rivella, S., Weiner, A. I., Park, J., Shin, S., et al. (2021) · Science Translational Medicine · doi:10.1126/scitranslmed.abj1008 · Cited by 209 · see citing works
Data-driven identification of post-acute SARS-CoV-2 infection subphenotypes
Zhang, H., Zang, C., Xu, Z., Zhang, Y., Xu, J., Bian, J., Morozyuk, D., Khullar, D., Zhang, Y., Nordvig, A. S., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-02116-3 · Cited by 181 · see citing works
Wang, B., Zhang, L., Wang, Y., Dai, T., Qin, Z., Zhou, F., & Zhang, L. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-00986-0 · Cited by 185 · see citing works
Post-acute sequelae of COVID-19 in a non-hospitalized cohort: Results from the Arizona CoVHORT
Bell, M. L., Catalfamo, C. J., Farland, L. V., Ernst, K. C., Jacobs, E. T., Klimentidis, Y. C., Jehn, M., & Pogreba-Brown, K. (2021) · PLoS ONE · doi:10.1371/journal.pone.0254347 · Cited by 177 · see citing works
Addressing the post-acute sequelae of SARS-CoV-2 infection: a multidisciplinary model of care
Parker, A. M., Brigham, E. P., Connolly, B. A., McPeake, J. M., Agranovich, A. V., Kenes, M. T., Casey, K. S., Reynolds, C., Schmidt, K. F. R., Kim, S. Y., et al. (2021) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(21)00385-4 · Cited by 169 · see citing works
Generalisable long COVID subtypes: findings from the NIH N3C and RECOVER programmes
Reese, J., Blau, H., Casiraghi, E., Bergquist, T. R., Loomba, J. J., Callahan, T. J., Laraway, B. J., Antonescu, C., Coleman, B. D., Gargano, M. A., et al. (2022) · EBioMedicine · doi:10.1016/j.ebiom.2022.104413 · Cited by 169 · see citing works
Reduction in life expectancy in Brazil after COVID-19
Castro, M. C., Gurzenda, S., Turra, C. M., Kim, S., Andrasfay, T., & Goldman, N. (2021) · Nature Medicine · doi:10.1038/s41591-021-01437-z · Cited by 164 · see citing works
Kikkenborg Berg, S., Dam Nielsen, S., Nygaard, U., Bundgaard, H., Palm, P., Rotvig, C., & Vinggaard Christensen, A. (2022) · The Lancet Child & Adolescent Health · doi:10.1016/s2352-4642(22)00004-9 · Cited by 168 · see citing works
Proposed subtypes of post‐COVID‐19 syndrome (or long‐COVID) and their respective potential therapies
Yong, S. J., & Liu, S. (2021) · Reviews in Medical Virology · doi:10.1002/rmv.2315 · Cited by 165 · see citing works
Magnúsdóttir, I., Lovik, A., Unnarsdóttir, A. B., McCartney, D. L., Ask, H., Kõiv, K., Christoffersen, L. A. N., Johnson, S. U., Hauksdóttir, A., Fawns‐Ritchie, C., et al. (2022) · The Lancet Public Health · doi:10.1016/s2468-2667(22)00042-1 · Cited by 158 · see citing works
Acute and chronic neurological disorders in COVID-19: potential mechanisms of disease
Balcom, E. F., Nath, A., & Power, C. (2021) · Brain · doi:10.1093/brain/awab302 · Cited by 161 · see citing works
S1-Leitlinie Post-COVID/Long-COVID
Koczulla, A. R., Ankermann, T., Behrends, U., Berlit, P., Böing, S., Brinkmann, F., Franke, C., Glöckl, R., Gogoll, C., Hummel, T. R., et al. (2021) · Pneumologie · doi:10.1055/a-1551-9734 · Cited by 161 · see citing works
Zhou, Y., Xu, J., Hou, Y., Leverenz, J. B., Kallianpur, A. R., Mehra, R., Liu, Y., Yu, H., Pieper, A. A., Jehi, L. E., et al. (2021) · Alzheimer s Research & Therapy · doi:10.1186/s13195-021-00850-3 · Cited by 160 · see citing works
COVID-19 therapeutics: Challenges and directions for the future
Robinson, P. C., Liew, D. F. L., Tanner, H. L., Grainger, J. R., Dwek, R. A., Reisler, R. B., Steinman, L., Feldmann, M., Ho, L., Hussell, T., et al. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2119893119 · Cited by 156 · see citing works
Kompaniyets, L., Bull–Otterson, L., Boehmer, T. K., Baca, S., Alvarez, P., Hong, K., Hsu, J., Harris, A. M., Gundlapalli, A. V., & Saydah, S. (2022) · MMWR Morbidity and Mortality Weekly Report · doi:10.15585/mmwr.mm7131a3 · Cited by 161 · see citing works
Risk for newly diagnosed diabetes after COVID-19: a systematic review and meta-analysis
Zhang, T., Mei, Q., Zhang, Z., Walline, J. H., Liu, Y., Zhu, H., & Zhang, S. (2022) · BMC Medicine · doi:10.1186/s12916-022-02656-y · Cited by 161 · see citing works
Xie, Y., Choi, T., & Al‐Aly, Z. (2023) · The Lancet Infectious Diseases · doi:10.1016/s1473-3099(23)00684-9 · Cited by 154 · see citing works
Nalbandian, A., Desai, A. D., & Wan, E. Y. (2022) · Annual Review of Medicine · doi:10.1146/annurev-med-043021-030635 · Cited by 163 · see citing works
A Longitudinal Study of COVID-19 Sequelae and Immunity: Baseline Findings
Sneller, M. C., Liang, C., Marques, A. R., Chung, J. Y., Shanbhag, S. M., Fontana, J. R., Raza, H., Okeke, O., Dewar, R. L., Higgins, B. P., et al. (2022) · Annals of Internal Medicine · doi:10.7326/m21-4905 · Cited by 156 · see citing works
Pathogenesis of Respiratory Viral and Fungal Coinfections
Salazar, F., Bignell, E., Brown, G. D., Cook, P. C., & Warris, A. (2021) · Clinical Microbiology Reviews · doi:10.1128/cmr.00094-21 · Cited by 155 · see citing works
Rao, S., Lee, G. M., Razzaghi, H., Lorman, V., Mejías, A., Pajor, N. M., Thacker, D., Webb, R. D., Dickinson, K., Bailey, L. C., et al. (2022) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/jamapediatrics.2022.2800 · Cited by 150 · see citing works
Long-term cardiac pathology in individuals with mild initial COVID-19 illness
Püntmann, V. O., Martin, S. S., Shchendrygina, A., Hoffmann, J., Ka, M. M., Giokoglu, E., Vanchin, B., Holm, N., Karyou, A., Laux, G. S., et al. (2022) · Nature Medicine · doi:10.1038/s41591-022-02000-0 · Cited by 154 · see citing works
Evolving phenotypes of non-hospitalized patients that indicate long COVID
Estiri, H., Strasser, Z. H., Brat, G. A., Semenov, Y. R., Aaron, J. R., Agapito, G., Albayrak, A., ALESSIANI, M., Amendola, D. F., Anthony, L. L. L. J., et al. (2021) · BMC Medicine · doi:10.1186/s12916-021-02115-0 · Cited by 150 · see citing works
Khullar, D., Zhang, Y., Zang, C., Xu, Z., Wang, F., Weiner, M. G., Carton, T. W., Rothman, R. L., Block, J. P., & Kaushal, R. (2023) · Journal of General Internal Medicine · doi:10.1007/s11606-022-07997-1 · Cited by 149 · see citing works
Systematic Review of the Prevalence of Long COVID
Woodrow, M., Carey, C., Ziauddeen, N., Thomas, R., Akrami, A., Lutje, V., Greenwood, D. C., & Alwan, N. A. (2023) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofad233 · Cited by 146 · see citing works
Solving the puzzle of Long Covid
Al‐Aly, Z., & Topol, E. J. (2024) · Science · doi:10.1126/science.adl0867 · Cited by 142 · see citing works
Incident autoimmune diseases in association with SARS-CoV-2 infection: a matched cohort study
Tesch, F., Ehm, F., Vivirito, A., Wende, D., Batram, M., Loser, F., Menzer, S., Jacob, J., Roessler, M., Seifert, M., et al. (2023) · Clinical Rheumatology · doi:10.1007/s10067-023-06670-0 · Cited by 142 · see citing works
Long COVID: aiming for a consensus
Munblit, D., O’Hara, M. E., Akrami, A., Perego, E., Olliaro, P., & Needham, D. M. (2022) · The Lancet Respiratory Medicine · doi:10.1016/s2213-2600(22)00135-7 · Cited by 138 · see citing works
Long-term gastrointestinal outcomes of COVID-19
Xu, E., Xie, Y., & Al‐Aly, Z. (2023) · Nature Communications · doi:10.1038/s41467-023-36223-7 · Cited by 136 · see citing works
Bajema, K. L., Berry, K., Streja, E., Rajeevan, N., Li, Y., Mutalik, P., Yan, L., Cunningham, F. E., Hynes, D. M., Rowneki, M., et al. (2023) · Annals of Internal Medicine · doi:10.7326/m22-3565 · Cited by 134 · see citing works
Li, J., Zhou, Y., Ma, J., Zhang, Q., Shao, J., Liang, S., Yu, Y., Li, W., & Wang, C. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01640-z · Cited by 139 · see citing works
Cardiometabolic outcomes up to 12 months after COVID-19 infection. A matched cohort study in the UK
Rezel‐Potts, E., Douiri, A., Sun, X., Chowienczyk, P., Shah, A. M., & Gulliford, M. C. (2022) · PLoS Medicine · doi:10.1371/journal.pmed.1004052 · Cited by 135 · see citing works
Warren, C. M., Snow, T. T., Lee, A., Shah, M. M., Heider, A., Blomkalns, A. L., Betts, B. A., Buzzanco, A. S., González, J. C., Chinthrajah, R. S., et al. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.25524 · Cited by 132 · see citing works
Peluso, M. J., Kelly, J. D., Lu, S., Goldberg, S. A., Davidson, M. C., Mathur, S., Durstenfeld, M. S., Spinelli, M. A., Hoh, R., Tai, V., et al. (2021) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofab640 · Cited by 126 · see citing works
Angiotensin-converting enzyme 2—at the heart of the COVID-19 pandemic
Oudit, G. Y., Wang, K., Viveiros, A., Kellner, M. J., & Penninger, J. M. (2023) · Cell · doi:10.1016/j.cell.2023.01.039 · Cited by 131 · see citing works
Gut Microbiome Alterations in COVID-19
Zuo, T., Wu, X., Wen, W., & Lan, P. (2021) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2021.09.004 · Cited by 132 · see citing works
Post-Acute COVID-19 Syndrome and the cardiovascular system: What is known?
Dixit, N. M., Churchill, A., Nsair, A., & Hsu, J. J. (2021) · American Heart Journal Plus Cardiology Research and Practice · doi:10.1016/j.ahjo.2021.100025 · Cited by 129 · see citing works
Risks and burdens of incident dyslipidaemia in long COVID: a cohort study
Xu, E., Xie, Y., & Al‐Aly, Z. (2023) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(22)00355-2 · Cited by 130 · see citing works
Hou, Y., Gu, T., Ni, Z., Shi, X., Ranney, M. L., & Mukherjee, B. (2025) · Open Forum Infectious Diseases · doi:10.1093/ofid/ofaf533 · Cited by 126 · see citing works
Roessler, M., Tesch, F., Batram, M., Jacob, J., Loser, F., Weidinger, O., Wende, D., Vivirito, A., Toepfner, N., Ehm, F., et al. (2022) · PLoS Medicine · doi:10.1371/journal.pmed.1004122 · Cited by 125 · see citing works
- Authors
- Al-Aly, Z., Xie, Y., & Bowe, B.
- Affiliations
- VA St. Louis Health Care System (US)
- Venue
- Nature
- Published
- 2021-04-22
- Volume
- 594
- Issue
- 7862
- Pages
- 259-264
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- OpenAlex
- W3153493739
- Cited by
- 1,518
- References
- 46
- Citations by year
- 2026: 95 · 2025: 170 · 2024: 268 · 2023: 365 · 2022: 391 · 2021: 228 · 2020: 1
- FWCI
- 149.17
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- 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 › 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
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
