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Long-Term Health Effects of COVID-19 Disability and Function Following SARS-CoV-2 Infection Paul A. Volberding, Bernice X. Chu, and Carol Mason Spicer, Editors Committee on the Long-Term Health Effects Stemming from COVID-19 and Implications for the Social Security Administration Board on Health Care Services Health and Medicine Division Consensus Study Report PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 1 5/21/24 10:46 AM

NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 This activity was supported by Contract No. 28321318D00060015 between the National Academy of Sciences and U.S. Social Security Administration. Any opinions, findings, conclusions, or recommendations expressed in this publication do not necessarily reflect the views of any organization or agency that provided support for the project. International Standard Book Number-13: 978-0-309-XXXXX-X International Standard Book Number-10: 0-309-XXXXX-X Digital Object Identifier: https://doi.org/10.17226/27756 This publication is available from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. Copyright 2024 by the National Academy of Sciences. National Academies of Sciences, Engineering, and Medicine and National Academies Press and the graphical logos for each are all trademarks of the National Academy of Sciences. All rights reserved. Printed in the United States of America. Suggested citation: National Academies of Sciences, Engineering, and Medicine. 2024. Long-term health effects of COVID-19: Disability and function following SARS-CoV-2 infection. Washington, DC: The National Academies Press. https:// doi.org/10.17226/27756. PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 2 5/21/24 10:46 AM

The National Academy of Sciences was established in 1863 by an Act of Congress, signed by President Lincoln, as a private, nongovernmental institution to advise the nation on issues related to science and technology. Members are elected by their peers for outstanding contributions to research. Dr. Marcia McNutt is president. The National Academy of Engineering was established in 1964 under the charter of the National Academy of Sciences to bring the practices of engineering to advising the nation. Members are elected by their peers for extraordinary contributions to engineering. Dr. John L. Anderson is president. The National Academy of Medicine (formerly the Institute of Medicine) was established in 1970 under the charter of the National Academy of Sciences to advise the nation on medical and health issues. Members are elected by their peers for distinguished contributions to medicine and health. Dr. Victor J. Dzau is president. The three Academies work together as the National Academies of Sciences, Engineering, and Medicine to provide independent, objective analysis and advice to the nation and conduct other activities to solve complex problems and inform public policy decisions. The National Academies also encourage education and research, recognize outstanding contributions to knowledge, and increase public understanding in matters of science, engineering, and medicine. Learn more about the National Academies of Sciences, Engineering, and Medicine at www.nationalacademies.org. PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 3 5/21/24 10:46 AM

Consensus Study Reports published by the National Academies of Sciences, Engineering, and Medicine document the evidence-based consensus on the study’s statement of task by an authoring committee of experts. Reports typically include findings, conclusions, and recommendations based on information gathered by the committee and the committee’s deliberations. Each report has been subjected to a rigorous and independent peer-review process and it represents the position of the National Academies on the statement of task. Proceedings published by the National Academies of Sciences, Engineering, and Medicine chronicle the presentations and discussions at a workshop, symposium, or other event convened by the National Academies. The statements and opinions contained in proceedings are those of the participants and are not endorsed by other participants, the planning committee, or the National Academies. Rapid Expert Consultations published by the National Academies of Sciences, Engineering, and Medicine are authored by subject-matter experts on narrowly focused topics that can be supported by a body of evidence. The discussions contained in rapid expert consultations are considered those of the authors and do not contain policy recommendations. Rapid expert consultations are reviewed by the institution before release. For information about other products and activities of the National Academies, please visit www.nationalacademies.org/about/whatwedo. PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 4 5/21/24 10:46 AM

COMMITTEE ON THE LONG-TERM HEALTH EFFECTS STEMMING FROM COVID-19 AND IMPLICATIONS FOR THE SOCIAL SECURITY ADMINISTRATION PAUL VOLBERDING (Chair), Professor of Medicine Emeritus, University of California, San Francisco ZIYAD AL-ALY, Director, Clinical Epidemiology Center, Chief of Research and Development Service, VA Saint Louis Health Care System JACQUELINE BECKER, Assistant Professor, Clinical Neuropsychologist, Division of General Internal Medicine, Icahn School of Medicine at Mount Sinai ALFRED BERG, Professor and Chair Emeritus, Department of Family Medicine, University of Washington, Seattle ANDREW BINDMAN, Executive Vice President and Chief Medical Officer, Kaiser Permanente ALUKO HOPE, Associate Professor, Department of Medicine, Oregon Health & Science University LEORA HORWITZ, Director, Center for Healthcare Innovation and Delivery Science, NYU Langone Health CLARION JOHNSON, Former Global Medical Director, ExxonMobil BARBARA KORNBLAU, Retired Professor and Director, Occupational Therapy Program, Idaho State University JOAO PEDRO MATIAS LOPES, Assistant Professor, Case Western Reserve University LAURA MALONE, Assistant Professor, Kennedy Krieger Institute and Johns Hopkins School of Medicine, Departments of Neurology and Physical Medicine and Rehabilitation LOUISE ELAINE VAZ, Associate Professor of Pediatrics, Department of Infectious Disease, Oregon Health & Science University MONICA VERDUZCO-GUTIERREZ, Chair and Professor, Department of Rehabilitation Medicine, Long School of Medicine, University of Texas Health Science Center at San Antonio SARAH WULF-HANSON, Lead Research Scientist of Global Health Metrics, Institute for Health Metrics and Evaluation, University of Washington v PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 5 5/21/24 10:46 AM

Study Staff CAROL MASON SPICER, Senior Program Officer/Study Director BERNICE CHU, Program Officer ELIZABETH FERRÉ, Research Associate BURGESS MANOBAH, Research Associate VIOLET BISHOP, Research Assistant JOSEPH GOODMAN, Senior Program Assistant SHARYL NASS, Senior Board Director, Board on Health Care Services vi PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 6 5/21/24 10:46 AM

Reviewers This Consensus Study Report was reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise. The purpose of this independent review is to provide candid and critical comments that will assist the National Academies of Sciences, Engineering, and Medicine in making each published report as sound as possible and to ensure that it meets the institutional standards for quality, objectivity, evidence, and responsiveness to the study charge. The review comments and draft manu- script remain confidential to protect the integrity of the deliberative process. We thank the following individuals for their review of this report: STEPHEN B. BAYLIN, Sidney Kimmel Comprehensive Cancer Center at Johns Hopkins Medicine TAE HWAN CHUNG, Johns Hopkins University TODD E. DAVENPORT, University of the Pacific & Workwell Foundation ALLEN W. HEINEMANN, Northwestern University ANTHONY L. KOMAROFF, Harvard Medical School and Brigham and Women’s Hospital MONICA KURYLO, University of Kansas Medical Center SINDHU MOHANDAS, Children’s Hospital Los Angeles, Keck School of Medicine, University of Southern California SHARON SAYDAH, Centers for Disease Control and Prevention AMANDA VERMA, Washington University School of Medicine in St. Louis JUAN WISNIVESKY, Icahn School of Medicine at Mount Sinai YONGKANG ZHANG, Weill Cornell Medical College vii PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 7 5/21/24 10:46 AM

viii REVIEWERS Although the reviewers listed above provided many constructive com- ments and suggestions, they were not asked to endorse the conclusions or recommendations of this report nor did they see the final draft before its release. The review of this report was overseen by ROBERT S. LAWRENCE, Johns Hopkins Bloomberg School of Public Health, and ERIC B. LARSON, University of Washington School of Public Health. They were responsible for making certain that an independent examination of this report was car- ried out in accordance with the standards of the National Academies and that all review comments were carefully considered. Responsibility for the final content rests entirely with the authoring committee and the National Academies. PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 8 5/21/24 10:46 AM

Contents SUMMARY 1 Context for This Study, 2 Study Charge and Scope, 2 Study Approach and Scope, 4 The Committee’s Conclusions, 5 1 INTRODUCTION 15 Context for This Study, 16 Study Charge and Scope, 17 Study Approach, 19 Terminology and Definitions, 20 Health Equity, 27 Report Organization, 29 References, 29 2 DIAGNOSIS OF SARS-COV-2 INFECTION 39 Viral Testing, 39 Before Viral Diagnostic Testing, 43 Establishing a History of Prior COVID-19, 47 Diagnosis of Long COVID, 48 Summary and Conclusions, 48 References, 48 ix PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 9 5/21/24 10:46 AM

x CONTENTS 3 SELECTED LONG-TERM HEALTH EFFECTS STEMMING FROM COVID-19 AND FUNCTIONAL IMPLICATIONS 55 Overview of Health Effects Associated with Long COVID, 56 Selected Multisystem Health Effects Associated with Long COVID, 64 Health Effects of Long COVID in Children and Adolescents, 78 Selected Guidance Statements Specific to Long COVID, 84 Overview of Body Systems Potentially Affected in Long COVID, 87 Summary and Conclusions, 93 References, 94 4 GLOBAL FUNCTIONING IN LONG COVID 149 Long-Term Functional Outcomes in Patients Not Hospitalized for COVID-19, 150 Long-Term Functional Outcomes in Patients Hospitalized for COVID-19, 153 Long-Term Functional Outcomes in Patients Receiving Intensive Care for COVID-19, 155 Long-Term Functional Outcomes in Children and Adolescents with COVID-19, 158 Long-Term Functional Outcomes in Other Selected Populations with COVID-19, 159 Effects of Rehabilitation on Functional Trajectories in Individuals With Long COVID, 161 Assessing Global Functioning, 163 Summary and Conclusions, 167 References, 168 5 CHRONIC CONDITIONS SIMILAR TO LONG COVID 183 Case Definitions and Epidemiology, 184 Shared Symptoms and Functional Implications, 185 Common Mechanisms of Action, 187 Prognosis and Progression, 194 Treatment and Management, 195 Summary and Conclusions, 199 References, 201 PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 10 5/21/24 10:46 AM

CONTENTS xi 6 OVERALL CONCLUSIONS 215 Diagnosis of Long COVID, 215 Epidemiology, 216 Health Effects, 217 Functional Impact and Risk of Factors, 217 Long COVID in Children and Adolescents, 218 Disease Management, 220 Disease Course and Prognosis, 220 Health Equity, 221 Similar Chronic Conditions, 222 APPENDIXES A Public Meeting Agendas 225 B Literature Search Strategies 229 C Biographical Sketches of Committee Members 235 PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 11 5/21/24 10:46 AM

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Boxes, Figures, and Tables BOXES S-1 Statement of Task, 3 1-1 Statement of Task, 17 FIGURES 1-1 International Classification of Functioning, Disability and Health Framework, 22 1-2 Social Security Administration’s Adjudication Process for Adults, 25 1-3 Social Security Administration’s Adjudication Process for Children, 26 3-1 Lasting impact of COVID-19, 58 5-1 36-Item Short Form Survey (SF-36) and World Health Organization Disability Assessment Schedule (WHODAS) Scores Among ME/CFS, Long COVID and Control Populations, 187 TABLES 3-1 Research on Clusters of Long COVID Health Effects, 61 3-2 Common Long COVID Symptoms in Children and Adolescents by Body System, 81 3-3 Selected Guidance Statements on Long COVID, 85 xiii PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 13 5/21/24 10:46 AM

xiv BOXES, FIGURES, AND TABLES 4-1 Types of Rehabilitation Programs Used in Long COVID Recovery, 162 4-2 Global Functioning Associated with Long COVID, 164 5-1 Overlap in Common Symptoms among Long COVID, ME/CFS, and Fibromyalgia, 186 5-2 Summary of Potential Biologic Mechanisms of Long COVID, Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS), and Fibromyalgia (FM), 189 ANNEX TABLES Annex Table 1-1 Terminology and Definitions for “Long COVID”, 33 Annex Table 3-1 Selected Respiratory Conditions Associated with Long COVID, 120 Annex Table 3-2 Selected Cardiovascular Conditions Associated with Long COVID, 122 Annex Table 3-3 Selected Neurological Conditions Associated with Long COVID, 124 Annex Table 3-4 Selected Special Senses and Speech Conditions Associated with Long COVID, 130 Annex Table 3-5 Selected Musculoskeletal Conditions Associated with Long COVID, 131 Annex Table 3-6 Selected Endocrine Conditions Associated with Long COVID, 133 Annex Table 3-7 Selected Immune Conditions Associated with Long COVID, 135 Annex Table 3-8 Selected Gastrointestinal Conditions Associated with Long COVID, 136 Annex Table 3-9 Selected Genitourinary Conditions Associated with Long COVID, 139 Annex Table 3-10 Selected Skin Conditions Associated with Long COVID, 141 Annex Table 3-11 Selected Neuropsychiatric Conditions Associated with Long COVID, 142 Annex Table 3-12 Multisystem Conditions Associated with Long COVID, 144 Annex Table 3-13 Physical Activities; Vision, Hearing, and Speech; and Mental Activities, 145 PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 14 5/21/24 10:46 AM

Preface Infection with SARS-CoV-2 can trigger health effects that can continue well after resolution of the initial COVID-19 illness. These effects have protean manifestations, often involving numerous organ systems, that can persist for months or years and may, in some cases, be disabling. Children and adolescents are affected as well as adults. While most aspects of these conditions are poorly understood, concern is real that they may result in an increase in applications for disability received by the Social Security Admin- istration (SSA). Accordingly, SSA commissioned a consensus report from the National Academies of Sciences, Engineering, and Medicine reviewing the long-term health effects of COVID-19 and potential implications for SSA disability. To this end, the National Academies convened an ad hoc commit- tee of experts to provide an overview of this persisting clinical condition, its effects and natural history in a variety of affected populations, and the cur- rent status of treatment and management and of ongoing research efforts. The committee was also charged with reviewing the spectrum of health effects associated with this new condition and their impact on function in both adults and children. Given that the long-term health effects of COVID-19 are complex and that knowledge of those effects is rapidly evolving, the committee convened by the National Academies included experts in the epidemiol- ogy, diagnosis, and clinical management of what has come to be called Long COVID. This committee, including researchers and clinicians, some themselves affected, collected evidence, heard presentations from invited speakers, and deliberated in response to a statement of task from SSA. xv PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 15 5/21/24 10:46 AM

xvi PREFACE This consensus report was prepared with a sense of urgency in light of the rapid evolution of knowledge about the diagnosis of SARS-CoV-2 infection and the long-term health effects and disordered function that may follow COVID-19, against the backdrop of what has been learned about other complex chronic conditions, such as myalgic encephalitis/chronic fatigue syndrome and fibromyalgia, themselves potentially triggered by infections. The committee identified ways in which the diagnosis and management of Long COVID represent unique challenges and raise many remaining questions for the SSA disability program. The committee and I are grateful for the opportunity to point out that the symptoms experienced by these patients are real and should be taken seriously. The committee extends its sincere thanks to the many individuals who shared their time and expertise to support its work and inform its delib- erations. The study was sponsored by SSA, and we thank Brendan Rogak, Vincent Nibali, Megan Butson, and Steve Rollins for their guidance and support. The committee acknowledges Vincent Nibali at SSA for verify- ing the accuracy of relevant technical content pertaining to the disability determination process. The committee also benefited greatly from discus- sions with individuals who presented at the committee’s open sessions: Karin Denault, Lucas Denault, Robert Holman, Akiko Iwasaki, Anthony Komaroff, Avindra Nath, Vincent Nibali, David Putrino, Steve Rollins, Eric Van Gieson, Angela Meriquez Vázquez, and Alexandra Yonts. In addition, the committee’s work benefited from presentations during two concurrent National Academies activities: Symposium on Long COVID: Examining the Working Definition (June 2023), hosted by the Committee on Exam- ining the Working Definition for Long COVID, and Toward a Common Research Agenda in Infection-Associated Chronic Illnesses: A Workshop to Examine Common, Overlapping Clinical and Biological Factors (June 2023), hosted by the Forum on Microbial Threats and the Forum on Neuroscience and Nervous System Disorders. Appreciation goes as well to Sonya Marshall-Gradisnik and Natalie Eaton-Fitch for their work on a paper commissioned by the committee to review chronic conditions similar to Long COVID. The committee thanks the reviewers of this report for their invaluable feedback on an earlier draft and the monitor and coordinator who oversaw the report review. The committee also acknowledges the many staff within the Health and Medicine Division (HMD) who provided support in various ways to this project, including Carol Mason Spicer (study director), Bernice Chu (pro- gram officer), Elizabeth Ferré (research associate), Violet Bishop (research assistant), Burgess Manobah (research associate), Joe Goodman (senior program assistant), Karen Helsing (senior program officer), and Hoda Soltani (former program officer). The committee extends great thanks and PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 16 5/21/24 10:46 AM

PREFACE xvii appreciation to Sharyl Nass, senior director, Board on Health Care Services, who oversaw the project. Greysi Patton (finance business partner), Arzoo Tayyeb (finance business partner), Julie Wiltshire (senior finance business partner), and Ron Brown (deputy director, HMD program finance) over- saw finances for the project; Rebecca Morgan (senior research librarian) provided research assistance, and Anne Marie Houppert (senior librarian) assisted with fact checking; and the report review, production, and com- munications staff all provided valuable guidance to ensure the success of the final product. Rona Briere and her staff provided superb editorial assistance in preparing the final report. Paul Volberding, Chair Committee on the Long-Term Health Effects Stemming from COVID-19 and Implications for the Social Security Administration PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 17 5/21/24 10:46 AM

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Acronyms and Abbreviations AAPRM American Academy of Physical Medicine and Rehabilitation ADL activity of daily living aHR adjusted hazard ratio ARDS acute respiratory distress syndrome BUN blood urea nitrogen CBT cognitive-behavioral therapy CDC Centers for Disease Control and Prevention CFQ Cognitive Failures Questionnaire CI confidence interval CLIA chemiluminescent immunoassays CMR cardio magnetic resonance COMPASS 31 31-question Composite Autonomic Symptom Score COVID-19 coronavirus disease 2019 CPET cardiopulmonary exercise testing CRISPR clustered regularly interspaced short palindromic repeats CRP c-reactive protein CT computed tomography CTPA computed tomography pulmonary angiography CXR chest x-ray DALY disability-adjusted life year DLCO diffusing capacity of the lungs for carbon monoxide xix PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 19 5/21/24 10:46 AM

xx ACRONYMS AND ABBREVIATIONS DM diabetes mellitus DMS-5-TR Diagnostic and Statistical Manual of Mental Disorders, Fifth Edition DSQ DePaul Symptom Questionnaire EBV Epstein-Barr virus ECG electrocardiogram ECog Everyday Cognition Scale EECP enhanced external counterpulsation ELISA enzyme-linked immunosorbent assays ESR erythrocyte sedimentation rate FDA Food and Drug Administration FM fibromyalgia g-AChR ganglionic neuronal nicotinic acetylcholine receptor GET graded exercise therapy GPCR G-protein-coupled receptor GWAS genomic-wide association studies HADS Hospital Anxiety and Depression Scale HIV human immunodeficiency virus IACC infection-associated chronic conditions IADLs instrumental activities of daily living ICD-11 International Classification of Diseases and Related Health Problems, 11th Revision IADL instrumental activity of daily living ICF International Classification of Function, Disability and Health ICU intensive care unit IGRA interferon-γ (IFN-γ) release assay IRR incidence rate ratio LAMP loop-mediated isothermal amplification LFIA lateral flow immunoassays LQBTQI+ lesbian, gay, bisexual, transgender, queer, intersex, or other MCAS mast cell activation syndrome MCI mild cognitive impairment ME/CFS myalgic encephalomyelitis/chronic fatigue syndrome MFI Multidimensional Fatigue Inventory MFIS Modified Fatigue Impact Scale PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 20 5/21/24 10:46 AM

ACRONYMS AND ABBREVIATIONS xxi miRNA microRNA MIS-C multisystem inflammatory syndrome in children NAAT nucleic acid amplification test NASA National Aeronautics and Space Administration NCS neurocardiogenic syncope NICE National Institute for Health and Care Excellence NIH National Institutes of Health OH orthostatic hypotension PAOFI Patient’s Assessment of Own Functioning Inventory PASC post-acute sequelae of COVID-19 PCCI post-COVID-19 cognitive impairment PCR polymerase chain reaction PedsQL Pedatric Quality of Life PEM post-exertional malaise PICS post-intensive care syndrome POTS post orthostatic tachycardia syndrome PROMIS Patient-Reported Outcomes Measurement Information System PTSD posttraumatic stress disorder RECOVER Researching COVID to Enhance Recovery ROS reactive oxygen species RT-PCR real-time reverse transcription PCR SARS-CoV-2 severe acute respiratory syndrome coronavirus 2 SD standard deviation SF-36 36-Item Short Form Survey SSA Social Security Administration SSDI Social Security Disability Insurance SSI Supplemental Security Income SSRI selective serotonin reuptake inhibitor TSH thyroid-stimulating hormone VA U.S Department of Veteran Affairs V˙O2 volume of oxygen consumption VQ ventilation perfusion WHO World Health Organization PREPUBLICATION COPY—Uncorrected Proofs A02506-Long-Term_Health_Effects_of_COVID-19_FM.indd 21 5/21/24 10:46 AM

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Since the onset of the coronavirus disease 2019 (COVID-19) pandemic in early 2020, many individuals infected with the virus that causes COVID-19, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), have continued to experience lingering symptoms for months or even years following infection. Some symptoms can affect a person's ability to work or attend school for an extended period of time. Consequently, in 2022, the Social Security Administration requested that the National Academies convene a committee of relevant experts to investigate and provide an overview of the current status of diagnosis, treatment, and prognosis of long-term health effects related to Long COVID. This report presents the committee conclusions.

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