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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.
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“This is typically referred to as a post-covid syndrome, characterized by several symptoms affecting quality of life (1–5).”
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Excess risk and clusters of symptoms after COVID-19 in a large Norwegian cohort
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Gastrointestinal post-acute COVID-19 syndrome
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A multisystem, cardio-renal investigation of post-COVID-19 illness
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Editorial: Long COVID, or Post-COVID Syndrome, and the Global Impact on Health Care
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BackgroundUnderstanding How Post–COVID-19 Condition Affects Adults and Health Care Systems
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BackgroundThe Incidence of Diabetes Among 2,808,106 Veterans With and Without Recent SARS-CoV-2 Infection
Wander, P. L., Lowy, E., Beste, L. A., Tulloch-Palomino, L. G., Korpak, A. M., Peterson, A. C., Kahn, S. E., & Boyko, E. J. (2022) · Diabetes Care · doi:10.2337/dc21-1686 · Cited by 82
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“Previous studies thatcharacterized and evaluated the risk of post-acute sequelae have reported a considerable increase in risk of clinical sequelae involving multiple organ systems 1,2,7,8,10 .”
BackgroundComplexity and Challenges of the Clinical Diagnosis and Management of Long COVID
O’Hare, A. M., Vig, E. K., Iwashyna, T. J., Fox, A., Taylor, J. S., Viglianti, E. M., Butler, C. R., Vranas, K. C., Helfand, M., Tuepker, A., et al. (2022) · JAMA Network Open · doi:10.1001/jamanetworkopen.2022.40332 · Cited by 80
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“18 Moreover, the lack of pre-admission serum creatinine or diagnostic codes to establish if a patient has subclinical CKD in these studies preclude appropriate conclusions drawn about long-term kidney function outcomes in patients with COVID-19-associated AKI.”
Long COVID: long-term effects?
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“Although severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) causes an acute respiratory disease, numerous patients who recovered from COVID-19 subsequently experience a constellation of late heterogeneous symptoms and events lasting for more than 3 months after the onset of the acute infection.(1) After an i…”
BackgroundRisk of long COVID main symptoms after SARS-CoV-2 infection: a systematic review and meta-analysis
Marjenberg, Z. R., Leng, S. X., Tascini, C., Garg, M., Misso, K., Guerche‐Séblain, C. E., & Shaikh, N. (2023) · Scientific Reports · doi:10.1038/s41598-023-42321-9 · Cited by 77
“A higher relative risk was also observed in patients with severe infection compared to non-severe infection, and in and non-hospitalised subgroups compared to all COVID-19 infections (adjusted for prior healthcare use and comorbidities) 15, 16, 38 .”
ResultImpact of Long COVID on health and quality of life
O’Mahony, L., Buwalda, T., Blair, M., Forde, B. M., Lunjani, N., Ambikan, A. T., Neogi, U., Barrett, P., Geary, E., O'Connor, N., et al. (2022) · HRB Open Research · doi:10.12688/hrbopenres.13516.1 · Cited by 76
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“Similar findings were observed in a study conducted on US veterans, in which the risk of a decline in renal function and urinary tract infections were correlated with the severity of the initial COVID-19 infection [45].”
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Long‐term side effects and lingering symptoms post COVID‐19 recovery
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Association of COVID-19 Infection With Incident Diabetes
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COVID-19 Post-acute Sequelae Among Adults: 12 Month Mortality Risk
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“One study suggested that COVID-19 infection carries an increased 6-month mortality risk (15).”
BackgroundPartinen, M., Holzinger, B., Morin, C. M., Espie, C. A., Chung, F. F., Penzel, T., Benedict, C., Bolstad, C. J., Cedernaes, J., Chan, R. N. Y., et al. (2021) · BMJ Open · doi:10.1136/bmjopen-2021-050672 · Cited by 77
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Bridging Knowledge Gaps in the Diagnosis and Management of Neuropsychiatric Sequelae of COVID-19
Frontera, J. A., & Simon, N. M. (2022) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2022.1616 · Cited by 74
Risk of incident diabetes post-COVID-19: A systematic review and meta-analysis
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“Notably, two studies did not find significantly higher adjusted HR for T1DM or other forms of diabetes in post-COVID-19 versus controls, thereby suggesting major contribution of T2DM on excess burden of incident diabetes in post-acute COVID-19 [7,8].”
BackgroundMethodHow methodological pitfalls have created widespread misunderstanding about long COVID
Høeg, T. B., Ladhani, S. N., & Prasad, V. K. (2023) · BMJ Evidence-Based Medicine · doi:10.1136/bmjebm-2023-112338 · Cited by 77
Investigating the possible mechanisms of autonomic dysfunction post-COVID-19
Jammoul, M., Naddour, J., Madi, A., Reslan, M. A., Hatoum, F., Zeineddine, J., Abou-Kheir, W. G., & Lawand, N. (2022) · Autonomic Neuroscience · doi:10.1016/j.autneu.2022.103071 · Cited by 76
“A retrospective study that included 9 patients with PASC showed reduced orthostatic cerebral blood flow velocity with or without orthostatic tachycardia (Novak et al., 2022).”
Canas, L. S., Molteni, E., Deng, J., Sudre, C. H., Murray, B. A. K., Kerfoot, E., Antonelli, M., 陳立遠, Rjoob, K., Pujol, J. C., et al. (2023) · The Lancet Digital Health · doi:10.1016/s2589-7500(23)00056-0 · Cited by 97
Iosef, C., Knauer, M. J., Nicholson, M., Nynatten, L. R. V., Cepinskas, G., Drăghici, S., Han, V. K. M., & Fraser, D. D. (2023) · Journal of Translational Medicine · doi:10.1186/s12967-023-04149-9 · Cited by 70
“The extensive actions of EP/p300 include interactions with SMAD1 to bridge coactivators such as NFκB transcribing IL-6, or it may interact with HIF1α/ VEGFA axis [6, 60] (Additional file 9: Fig S9).”
BackgroundDEVRIES, A. R., Shambhu, S., Sloop, S., & Overhage, J. M. (2023) · JAMA Health Forum · doi:10.1001/jamahealthforum.2023.0010 · Cited by 74
Pathophysiological, immunological, and inflammatory features of long COVID
Böhmwald, K., Diethelm‐Varela, B., Rodríguez‐Guilarte, L., Rivera, T., Riedel, C. A., González, P. A., & Kalergis, A. M. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1341600 · Cited by 80
“SARS-CoV-2 is linked to enduring respiratory issues, such as pulmonary fi brosis, angiogenesis, and vessel remodeling (91, 137 – 140).”
BackgroundInfluentialTleyjeh, I. M., Saddik, B. A., Ramakrishnan, R. K., AlSwaidan, N., Alanazi, A. S., Alhazmi, D., Aloufi, A., AlSumait, F., Berbari, E. F., & Halwani, R. (2021) · Journal of Infection and Public Health · doi:10.1016/j.jiph.2021.11.016 · Cited by 69
Prevalence, trajectory over time, and risk factor of post-COVID-19 fatigue
Mazza, M. G., Palladini, M., Villa, G., LORENZO, R. D., Rovere, P. Q., & Benedetti, F. (2022) · Journal of Psychiatric Research · doi:10.1016/j.jpsychires.2022.08.008 · Cited by 70
“Moreover, the acute COVID-19 severity and the related intensity of care were also associated with increasing risk of post-COVID fatigue respectively from asymptomatic patients, to hospitalized patients, and finally in patients admitted in intensive care unit (ICU) (Al-Aly et al., 2021).”
InfluentialRisk of Newly Diagnosed Diabetes After COVID-19 Infection: A Systematic Review and Meta-Analysis
Lai, H., Yang, M., Sun, M., Pan, B., Wang, Q., Wang, J., Tian, J., Ding, G., Yang, K., Song, X., et al. (2022) · Metabolism · doi:10.1016/j.metabol.2022.155330 · Cited by 71
“In addition, Wander et al. [25] and Al-Aly [26] assessed populations from the same database as that of Xie et al. [27].”
Horwitz, L. I., Thaweethai, T., Brosnahan, S. B., Cicek, M. S., Fitzgerald, M. L., Goldman, J. D., Hess, R., Hodder, S., Jacoby, V. L., Jordan, M. R., et al. (2023) · PLoS ONE · doi:10.1371/journal.pone.0286297 · Cited by 72
“electronic health records or claims data.[53, 58-62] The adaptive nature of the protocol allows for rapid responsiveness to new discoveries and changes in the nature of the pandemic.”
BackgroundWang, K., Khoramjoo, M., Srinivasan, K. K., Gordon, P. M. K., Mandal, R., Jackson, D., Sligl, W., Grant, M. B., Penninger, J. M., Borchers, C. H., et al. (2023) · Cell Reports Medicine · doi:10.1016/j.xcrm.2023.101254 · Cited by 71
Magge, S. N., Wolf, R. M., Pyle, L. L., Brown, E. A., Benavides, V. C., Bianco, M. E., Chao, L. C., Cymbaluk, A., Balikcioglu, P. G., Halpin, K. L., et al. (2022) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2022.08.010 · Cited by 67
Long-term Gastrointestinal Sequelae Following COVID-19: A Prospective Follow-up Cohort Study
Golla, R., Vuyyuru, S. K., Kante, B., Kumar, P., Thomas, D. M., Makharia, G. K., Kedia, S., & Ahuja, V. (2022) · Clinical Gastroenterology and Hepatology · doi:10.1016/j.cgh.2022.10.015 · Cited by 68
Corbett, A., Williams, G. H., Creese, B., Hampshire, A., Hayman, V., Palmer, A., Filakovszky, A., Mills, K., Cummings, J. L., Aarsland, D., et al. (2023) · The Lancet Healthy Longevity · doi:10.1016/s2666-7568(23)00187-3 · Cited by 70
Long COVID: long-term health outcomes and implications for policy and research
Al‐Aly, Z., Agarwal, A., Alwan, N. A., & Luyckx, V. A. (2022) · Nature Reviews Nephrology · doi:10.1038/s41581-022-00652-2 · Cited by 67
Post COVID-19 irritable bowel syndrome
Marasco, G., Cremon, C., Barbaro, M. R., Cacciari, G., Falangone, F., Валерьевна, К. А., Bordin, D. S., Drug, V. L., Miftode, E. G., Fusaroli, P., et al. (2022) · Gut · doi:10.1136/gutjnl-2022-328483 · Cited by 70
Pisareva, E., Badiou, S., Mihalovičová, L., Mirandola, A., Pastor, B., Kudriavtsev, A., Berger, M., Roubille, C., Fesler, P., Klouche, K., et al. (2022) · Journal of Medical Virology · doi:10.1002/jmv.28209 · Cited by 65
“In addition, the PAP patients studied may have had symptoms of different origins: (i), being secondary to COVID‐ 19–induced damage to the lung, heart, skeletal muscle, kidneys, or brain; (ii) persistent debilitating symptoms (post‐COVID syndrome or “long COVID‐19” illness) in patients with no apparent organ damage; or…”
BackgroundLong COVID: Clinical characteristics, proposed pathogenesis and potential therapeutic targets
Kenny, G., Townsend, L., Savinelli, S., & Mallon, P. W. G. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1157651 · Cited by 72
Review of organ damage from COVID and Long COVID: a disease with a spectrum of pathology
Ewing, A. G., Šalamon, Š., Pretorius, E., Joffe, D., Fox, G., Bilodeau, S., & Yaneer Bar-yam, A. (2024) · Medical Review · doi:10.1515/mr-2024-0030 · Cited by 65
Eberst, G., Claudé, F., Laurent, L., Meurisse, A., Roux-Claudé, P., Barnig, C., Vernerey, D., Paget‐Bailly, S., Bouiller, K., Chirouze, C., et al. (2022) · Annals of Intensive Care · doi:10.1186/s13613-022-00997-8 · Cited by 66
“Other studies have demonstrated a higher rate of thromboembolic events in survivors of COVID-19 at 6 months follow-up, raising the question of the number of undiagnosed cases of segmental or subsegmental pulmonary embolism [18, 19].”
ResultXie, Y., Bowe, B. C., & Al‐Aly, Z. (2023) · BMJ · doi:10.1136/bmj-2022-072705 · Cited by 63
Xie, Y., Bowe, B. C., & Al‐Aly, Z. (2023) · BMJ · doi:10.1136/bmj-2022-073312 · Cited by 65
Wang, L., Foer, D., MacPhaul, E., Lo, Y.-C., Bates, D. W., & Zhou, L. (2021) · Journal of Biomedical Informatics · doi:10.1016/j.jbi.2021.103951 · Cited by 61
“This is distinct from prior studies that have used other EHR-based data elements such as billing/diagnosis codes, laboratory results, or medications [14,19,37].”
Abel, K. M., Carr, M., Ashcroft, D. M., Chalder, T., Chew-Graham, C. A., Hope, H. F., Kapur, N., McManus, S., Steeg, S., Webb, R. T., et al. (2021) · JAMA Network Open · doi:10.1001/jamanetworkopen.2021.34803 · Cited by 61
Bhaskaran, K., Rentsch, C. T., Hickman, G., Hulme, W. J., Schultze, A., Curtis, H. J., Wing, K., Warren‐Gash, C., Tomlinson, L. A., Bates, C. J., et al. (2022) · PLoS Medicine · doi:10.1371/journal.pmed.1003871 · Cited by 63
Marques, K. C., Silva, C. C., Trindade, S. D. S., Santos, M. C. D. S., Rocha, R. S. B., Vasconcelos, P. F. D. C., Quaresma, J. A. S., & Falcão, L. F. M. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.862001 · Cited by 63
“(22) studied patients with COVID-19, who recovered at least 30 days after their diagnosis for 6 months.”
BackgroundPersistent symptoms and lab abnormalities in patients who recovered from COVID-19
Varghese, J., Sandmann, S., Ochs, K., Schrempf, I. M., Frömmel, C., Dugas, M., Schmidt, H., Vollenberg, R., & Tepasse, P. (2021) · Scientific Reports · doi:10.1038/s41598-021-91270-8 · Cited by 68
COVID-19 Survival and its impact on chronic kidney disease
Long, J. D., Strohbehn, I. A., Sawtell, R., Bhattacharyya, R. P., & Sise, M. E. (2021) · Translational research · doi:10.1016/j.trsl.2021.11.003 · Cited by 69
“A study that used electronic health records from the Veterans Health Administration to conduct a high-dimensional assessment of long COVID reported increased risk of adverse kidney manifestations, including AKI, CKD, and urinary system infections that occurred even after the first 30 days following diagnosis of COVID-…”
CROMER, S. J., Colling, C., Schatoff, D., Leary, M., Stamou, M. I., Selen, D. J., Putman, M. S., & Wexler, D. J. (2022) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2022.108145 · Cited by 68
Microbiota and COVID-19: Long-term and complex influencing factors
Gang, J., Wang, H., Xue, X., & Zhang, S. J. (2022) · Frontiers in Microbiology · doi:10.3389/fmicb.2022.963488 · Cited by 62
“Long COVID affects multiple systems and has many adverse effects on the physical and mental health (Del Rio et al., 2020; Al-Aly et al., 2021) of survivors.”
BackgroundCD147 contributes to SARS-CoV-2-induced pulmonary fibrosis
Wu, J., Chen, L., Qin, C., Huo, F., Liang, X., Yang, X., Zhang, K., Lin, P., Liu, J., Feng, Z., et al. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01230-5 · Cited by 65
“Given the severe clinical impact of COVID-19 compared to previous pandemic diseases such as SARS and MERS, the global health care system has already been challenged by patients with sequelae of long COVID.(38,39) In a study to assess the sequelae of COVID-19 with a particular focus on the recovery of patients with non…”
BackgroundInfluentialLong-Term Mortality Following COVID-19 Infection: A National Cohort Study From Estonia
Uusküla, A., Jürgenson, T., Pisarev, H., Kolde, R., Meister, T., Tisler, A., Suija, K., Kalda, R., Piirsoo, M., & Fischer, K. (2022) · The Lancet Regional Health - Europe · doi:10.1016/j.lanepe.2022.100394 · Cited by 60
Neurological post‐acute sequelae of SARS‐CoV ‐2 infection
Takao, M., & Ohira, M. (2022) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.13481 · Cited by 66
Oral GS-441524 derivatives: Next-generation inhibitors of SARS‐CoV‐2 RNA‐dependent RNA polymerase
Wang, Z., Yang, L., & Song, X.-Q. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1015355 · Cited by 65
Distinct tissue niches direct lung immunopathology via CCL18 and CCL21 in severe COVID-19
Mothes, R., Reguant, A. P., Koehler, R., Liebeskind, J., Liebheit, A., Bauherr, S., Philipsen, L., Dittmayer, C., Laue, M. M., von Manitius, R., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36333-2 · Cited by 62
Cardiac Arrhythmias in Post-COVID Syndrome: Prevalence, Pathology, Diagnosis, and Treatment
Huseynov, A., Akın, İ., Duerschmied, D., & Scharf, R. E. (2023) · Viruses · doi:10.3390/v15020389 · Cited by 68
Trajectories of the Evolution of Post COVID-19 Condition, Up to Two Years after Symptoms Onset
Servier, C., Porcher, R., Pane, I., Ravaud, P., & Tran, V.-T. (2022) · International Journal of Infectious Diseases · doi:10.1016/j.ijid.2023.05.007 · Cited by 63
“, organ injury from the acute disease or its treatment [13-15]; post viral fatigue syndrome [16]; prolonged viral shedding or presence of a viral reservoir [17 18]; autoimmune mechanisms [19 20], or mental factors [21]) most longitudinal studies have focused on describing the prevalence of patients with one or more sy…”
Lim, J. T., Wee, L. E., Tay, A. T., Pang, D., Chiew, C. J., Ong, B., Lye, D. C., & Tan, K. B. (2023) · Clinical Infectious Diseases · doi:10.1093/cid/ciad469 · Cited by 64
Epidemiologic Features of Recovery From SARS-CoV-2 Infection
Oelsner, E. C., Sun, Y., Balte, P., Allen, N. B., Andrews, H., Carson, A. P., Cole, S. A., Coresh, J., Couper, D. J., Cushman, M., et al. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2024.17440 · Cited by 58
Metadata
- 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
- 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 › 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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