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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2024. Future State of Smallpox Medical Countermeasures. Washington, DC: The National Academies Press. doi: 10.17226/27652.
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Below is the uncorrected machine-read text of this chapter, intended to provide our own search engines and external engines with highly rich, chapter-representative searchable text of each book. Because it is UNCORRECTED material, please consider the following text as a useful but insufficient proxy for the authoritative book pages.

Future State of Smallpox Medical Countermeasures Lawrence O. Gostin, Lisa Brown, Shalini Singaravelu, and Matthew Masiello, Editors Committee on the Current State of Research, Development, and Stockpiling of Smallpox Medical Countermeasures Board on Health Sciences Policy Board on Global Health Health and Medicine Division Board on Life Sciences Division on Earth and Life Studies Consensus Study Report

NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 This activity was supported by contracts between the National Academy of Sciences and the Administration for Strategic Preparedness and Response (75A50121C00061). 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: 978-0-309-71737-3 International Standard Book Number-10: 0-309-71737-x Digital Object Identifier: https://doi.org/10.17226/27652 Library of Congress Control Number: 2024937873 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. Future state of smallpox medical countermeasures. Washington, DC: The National Academies Press. https://doi.org/10.17226/27652.

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. iii

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 typi- cally include findings, conclusions, and recommendations based on information gathered by the committee and on 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 con- tained 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.

COMMITTEE ON THE CURRENT STATE OF RESEARCH, DEVELOPMENT, AND STOCKPILING OF SMALLPOX MEDICAL COUNTERMEASURES LAWRENCE GOSTIN (Chair), Distinguished University Professor, O’Neil Chair in Global Health Law, O’Neill Institute for National and Global Health Law, Georgetown University GEORGES BENJAMIN, Executive Director, American Public Health Association NAHID BHADELIA, Director, Boston University Center on Emerging Infectious Diseases, Associate Professor, Boston University School of Medicine INGER DAMON, Adjunct Clinical Faculty, Emory University Department of Medicine ANDREW ENDY, Martin Family University Fellow in Undergraduate Education, Faculty Co-Director of Degree Programs, Hasso Plattner Institute of Design, Core Faculty, Stanford University Center for International, Security and Cooperation, Senior Fellow (courtesy), Hoover Institution DIANE E. GRIFFIN, University Distinguished Service Professor, W. Harry Feinstone Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health NOREEN HYNES, Associate Professor of Medicine (Infectious Diseases) and Public Health (International Health), Director of Research and Associate Medical Director (Infectious Diseases), Johns Hopkins Hospital Biocontainment Unit, Director, Geographic Medicine Center for the Division of Infectious Diseases, Johns Hopkins University School of Medicine, Johns Hopkins Bloomberg School of Public Health, Johns Hopkins Hospital RICHARD KENNEDY, Professor of Medicine, Mayo Clinic and Foundation, Co-Director, Mayo Clinic Vaccine Research Group KENT KESTER, Vice President, Translational Medicine, International AIDS Vaccine Initiative ANNE RIMOIN, Professor, Department of Epidemiology, Gordon Levin Endowed Chair in Infectious Diseases and Public Health, Director, Center for Global and Immigrant Health, Jonathan and Karin Fielding School of Public Health, University of California, Los Angeles OYEWALE TOMORI, Professor of Virology, African Center of Excellence for Genomics of Infectious Diseases HENRY WILLIS, Senior Policy Researcher, Professor, RAND Corporation, Pardee RAND Graduate School v

MATTHEW WYNIA, Director, Center for Bioethics and Humanities, University of Colorado ZHILONG YANG, Associate Professor, Department of Veterinary Pathobiology, School of Veterinary Medicine & Biomedical Sciences, Texas A&M University Study Staff LISA BROWN, Study Director SHALINI SINGARAVELU, Program Officer MATTHEW MASIELLO, Associate Program Officer MARGARET McCARTHY, Research Associate (until December 31, 2023) CLAIRE BIFFL, Research Associate (from January 1, 2024) RAYANE SILVA-CURRAN, Senior Program Assistant KAVITA BERGER, Board Director, Board on Life Sciences JULIE PAVLIN, Senior Board Director, Board on Global Health CLARE STROUD, Senior Board Director, Board on Health Sciences Policy Consultant ELLEN CARLIN, Parapet Science & Policy Consulting vi

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: DAVID BLAZES, Bill & Melinda Gates Foundation MIKE BRAY, Georgetown Medical School WILLIAM GREG BUREL, Hamilton Grace, LLC JOHN H. CONNOR, National Emerging Infectious Diseases Laboratories, Boston University Chobanian and Avedisian School of Medicine R. ALTA CHARO, University of Wisconsin–Madison RICHARD HATCHETT, Coalition for Epidemic Preparedness Innovations BERNARD MOSS, National Institutes of Health UMAIR A. SHAH, Washington State Department of Health ERICA SHENOY, Massachusetts General Hospital JILL TAYLOR, Association of Public Health Laboratories CRYSTAL WATSON, Johns Hopkins Bloomberg School of Public Health vii

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 ANN M. ARVIN, Stan- ford University, and LAWRENCE COREY, Fred Hutchinson Cancer Center. They were responsible for making certain that an independent examination of this report was carried out in accordance with the standards of the Na- tional Academies and that all review comments were carefully considered. Responsibility for the final content rests entirely with the authoring com- mittee and the National Academies.

Contents ACRONYMS AND ABBREVIATIONS xvii SUMMARY 1 Study Approach, 2 Overarching Conclusions on Medical Countermeasures Readiness, 3 Overall Conclusions on Systems Readiness, 10 Concluding Remarks, 16 1 INTRODUCTION 19 Rationale and Study Charge, 20 About This Report, 22 Background and Context, 25 Lessons Learned from Responding to COVID-19 and Mpox, 27 Smallpox Emergence and Response Considerations, 32 Overarching Conclusions, 33 References, 36 2 STATE OF SMALLPOX MEDICAL COUNTERMEASURES READINESS 41 Diagnostics, Detection, and Surveillance, 41 Vaccines, 47 Therapeutics, 57 Overarching Conclusions, 63 References, 63 ix

x CONTENTS 3 FACTORS INFLUENCING SMALLPOX READINESS AND RESPONSE 73 Evolving Biothreat Landscape, 74 Evolving Research and Technology Landscape, 84 Operational Considerations for MCM Readiness and Response, 92 Overarching Conclusions, 106 References, 106 4 WAY FORWARD: PRIORITIES FOR RESEARCH, DEVELOPMENT, AND STOCKPILING 117 Smallpox Research Agenda, 117 Stockpiling Considerations, 133 Overarching Conclusions, 141 References, 142 APPENDIXES A STUDY METHODS AND PUBLIC MEETINGS AGENDAS 147 B COMMITTEE AND STAFF BIOGRAPHICAL SKETCHES 159

Boxes, Figures, and Tables BOXES S-1 Considerations for Smallpox MCMs in the SNS, 13 S-2 Summary of Priorities for Improved Smallpox Readiness and Response, 17 1-1 Statement of Task, 21 1-2 Summary of Factors Considered by the Committee, 34 2-1 Smallpox Vaccine Summary and Terminology, 51 3-1 Notable Orthopoxvirus Outbreaks (as of February 2024), 76 3-2 Poxvirus Knowledge Gaps, 85 3-3 Opportunities to Strengthen National Laboratory Systems for Smallpox, 100 4-1 Research Program Using Live Variola Virus, 2020–2023, 125 4-2 Considerations for and Questions about the Smallpox MCMs in the SNS, 139 xi

xii BOXES, FIGURES, AND TABLES FIGURES 1-1 PHEMCE stakeholders and engagement, 23 1-2 Minimum smallpox MCM needs according to containment strategy, 36 3-1 Basic orthopoxvirus lifecycle, 81 4-1 Smallpox research agenda, 122 TABLES S-1 Summary of Smallpox Vaccines and Therapeutics in the U.S. Strategic National Stockpile, 4 2-1 Summary of Smallpox Vaccines in the U.S. Strategic National Stockpile, 49 2-2 Potential Adverse Events Associated with Smallpox Vaccination with Replicating Vaccine, 53 2-3 Summary of Smallpox Therapeutics in the U.S. Strategic National Stockpile, 58 3-1 Poxviruses That Infect Humans, 77 4-1 List of Conclusions from the IOM Reports Assessment of Future Scientific Needs for Live Variola Virus (1999) and Live Variola Virus: Considerations for Continuing Research (2009) and Recommendations from the 2022 ACVVR Report, 119 4-2 Smallpox MCM Readiness as a Function of Live Variola and Non-Variola Viral Research: Opportunities for MCM Improvement, 127

Preface Immediately after the eradication of smallpox, nations around the world mobilized to ensure that future generations would not continue to suffer from this ancient and devastating disease. World Health Assembly resolution 33.4 declared that smallpox had been eradicated and recommended poli- cies on vaccination, case investigation, and the limited retention of variola collections in the event of a future re-emergence. However, rapid societal, political, ecological, and technological changes of the 21st century have shed new light on these historical resolutions and the need to reevaluate public health and health systems capacities against natural and intentional threats. As evidenced by recent public health emergencies of international concern, the U.S. public—and the global community at large—expects the United States and its international partners, including the World Health Organization, to rapidly identify an outbreak and equitably make avail- able safe and effective medical countermeasures (MCMs), such as effective diagnostics, therapeutics, biologics, and vaccines. These expectations hold true regardless of the pathogen causing the disease. The National Academies of Sciences, Engineering, and Medicine’s Com- mittee on the Current State of Research, Development, and Stockpiling of Smallpox Medical Countermeasures was tasked with providing strategic counsel to the federal government and international partners regarding the future of the smallpox MCMs portfolio (including research, development, and stockpiling) to ensure readiness and effective response in the event of a smallpox event. xiii

xiv PREFACE As articulated in this report, the committee envisions a responsive and flexible system to establish research priorities for smallpox MCMs, together with judicious stockpiling and strategic plans for the rapid and equitable distribution of MCMs in the event of a smallpox or other orthopoxvirus outbreak, in the United States or globally. Concurrently, the committee emphasizes the optimal use of governmental resources to achieve effective smallpox preparedness, while recognizing the competing demands placed on the government to also be prepared for other significant threats. This type of system will require U.S. and international partners to plan and respond in the face of multiple scientific, societal, political, and eco- logical uncertainties. These uncertainties—and lessons learned from COVID and mpox—argue for research and stockpiling decisions to be made in anticipation of the next potential threat, with a readiness to shift priorities rapidly in the face of emerging information. It is vital to prioritize research into and the development of safer and more effective MCMs, to make judicious choices about stockpiling, and to have modern, well rehearsed, and adaptable strategic plans in place to respond nationally and globally in the event of a variola or other orthopoxvirus outbreak. These efforts will depend on rapid identification (diagnostics and surveillance), effective containment and response, equitable allocation, and global solidarity. On behalf of the committee and the project staff, I extend my sincere thanks to the many individuals who shared their time and expertise to support the committee’s work and inform its deliberations. The study was sponsored by the Administration for Strategic Preparedness and Response on behalf of the U.S. government, and we thank Margaret Sloane and Julia Limage for their guidance and support. The committee extends great thanks and appreciation to Christy Huston of the U.S. Centers for Disease Control and Prevention and Rosamund Lewis of the World Health Orga- nization Smallpox Secretariat for their technical advice. Our appreciation goes to the reviewers for their invaluable feedback and to the monitor and coordinator who oversaw the report review. The committee acknowledges the many staff within the National Acad- emies who provided support in various ways to this project, including Lisa Brown, Shalini Singaravelu, Matthew Masiello, Margaret McCarthy, Claire Biffl, and Rayane Silva-Curran. The committee also extends their gratitude to Clare Stroud, senior board director of the Board on Health Sciences Policy. Ellen Carlin provided research and writing assistance, Anne Marie Houppert assisted in compiling literature, and the report review, produc- tion, and communications staff all provided valuable guidance to ensure the success of the final product.

PREFACE xv Finally, I would like to deeply thank the committee of experts who vol- unteered their invaluable time to this task. The committee’s contributions to this report are reflective of their career-long dedication and service to epidemic and pandemic preparedness and response. Lawrence O. Gostin, Chair Committee on the Current State of Research, Development, and Stockpiling of Smallpox Medical Countermeasures

Acronyms and Abbreviations ACIP Advisory Committee on Immunization Practices ACVVR Advisory Committee on Variola Virus Research AI artificial intelligence AIDS acquired immunodeficiency syndrome APSV Aventis Pasteur smallpox vaccine ARPA-H Advanced Research Projects Agency for Health ASPR Administration for Strategic Preparedness and Response BARDA Biomedical Advanced Research and Development Authority BioMADE BioIndustrial Manufacturing and Design Ecosystem BioMaP National Biopharmaceutical Manufacturing Partnership CBRN chemical, biological, radiological, and nuclear CDC U.S. Centers for Disease Control and Prevention CDV cidofovir CEPI Coalition for Epidemic Preparedness CIADM Centers for Innovation in Advanced Development and Manufacturing CLIA Clinical Laboratory Improvement Amendments CMS Centers for Medicare & Medicaid Services CMV cytomegalovirus COVID-19 coronavirus disease 2019; the disease caused by the virus SARS-CoV-2 CRISPR clustered regularly interspaced short palindromic repeats xvii

xviii ACRONYMS AND ABBREVIATIONS DNA deoxyribonucleic acid DoD Department of Defense EA IND expanded access for an investigational new drug EIND emergency investigational new drug ELISA enzyme-linked immunosorbent assay EM electron microscopy EU European Union EUA Emergency Use Authorization EV enveloped virion FDA U.S. Food and Drug Administration FD&C Food, Drug, and Cosmetic Act FY fiscal year GAO Government Accountability Office GMP good manufacturing practice HERA Health Emergency Preparedness and Response Authority HHS Department of Health and Human Services HIV human immunodeficiency virus IgG immunoglobulin G IgM immunoglobulin M IND investigational new drug IOM Institute of Medicine IR inverted repeat ITAP Independent Test Assessment Program IV intravenous KFF Kaiser Family Foundation LAMP loop mediated isothermal amplification LDT laboratory developed tests LLM large language model LRN Laboratory Response Network mAbs monoclonal antibodies MCM medical countermeasure MERS-CoV Middle East respiratory syndrome coronavirus MPXV monkeypox mRNA messenger ribonucleic acid MV mature virion

ACRONYMS AND ABBREVIATIONS xix MVA modified vaccinia Ankara MVA-BN modified vaccinia Ankara-Bavarian Nordic NIAID National Institute of Allergy and Infectious Diseases NIH National Institutes of Health NYCBOH New York City Board of Health OPXV orthopoxvirus OWS Operation Warp Speed PCR polymerase chain reaction PHEMCE Public Health Emergency Medical Countermeasures Enterprise POC point-of-care PON point-of-need PPE personal protective equipment qPCR quantitative polymerase chain reaction SAGE Strategic Advisory Group of Experts on Immunization SARS severe acute respiratory syndrome SARS-CoV-2 severe acute respiratory syndrome-related coronavirus SCARDA Strategic Center of Biomedical Advanced Vaccine Research and Development for Preparedness and Response SNS U.S. Strategic National Stockpile STOMP Study of Tecovirimat for Human Monkeypox Virus SVES Smallpox Vaccine Emergency Stockpile TPP target product profile VARV variola virus VECTOR State Research Center of Virology and Biotechnology VIG vaccinia immunoglobulin VIGIV vaccinia immune globulin intravenous WHA World Health Assembly WHO World Health Organization

Acknowledgments This Consensus Study Report would not have been possible without the many experts who generously contributed their time and expertise to inform the development of this report. The committee thanks all the speakers (Appendix  A) for their timely participation and expert contri- butions to the public workshops: Steve Adams, Paul Chaplin, Matthew Clark, Gavin Cloherty, John Connor, Nicole Dorsey, Manoj Gandhi, Noel Gerald, Matthew Hepburn, Dennis Hruby, Nathaniel Hupert, Christy Hutson, Stuart Isaacs, Cyrus Javan, Ewa King, Brett Leav, Seth Lederman, Rosamund Lewis, Julia Limage, Karen Martins, Cathryn Mayes, Bernard Moss, Marcus Plescia, Chris Sinclair, Margaret Sloane, Crystal Watson, Daniel Wolfe, and Kevin Yeskey. The committee is deeply appreciative of the following individuals who contributed their expertise on poxvirus research: Jia Liu, Grant McFadden, Stefan Rothenburg, and Yan Xiang. The committee would also like to thank the sponsor of this study. Funds for the committee’s work was provided by the Administration for Strategic Pre- paredness and Response (ASPR). The committee also extends their gratitude to the group of interagency federal experts for informing the committee’s charge. Many others within the National Academies supported this project. The committee thanks the staff of the Health and Medicine Division (HMD) Ex- ecutive Office, Office of Communications, Office of Governmental Affairs, and Research Center. The committee is grateful to Ellen Carlin for her invalu- able contributions to conducting research, report writing, and editing. Finally, Robert Pool is to be credited for his editorial assistance in preparing this report. We are deeply grateful to all those who collaborated on this project for working so diligently under a very short timeline. xxi

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At the request of the Administration for Strategic Preparedness and Response, the National Academies convened a committee to examine lessons learned from the COVID-19 pandemic and mpox multi-country outbreak to inform an evaluation of the state of smallpox research, development, and stockpiling of medical countermeasures (MCM). In the resulting report, the committee presents findings and conclusions that may inform U.S. Government investment decisions in smallpox MCM readiness, as well as the official U.S. position on the disposition of live viral collections at future World Health Assembly meetings.

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