COMBATING ANTIMICROBIAL
RESISTANCE AND
PROTECTING THE MIRACLE
OF MODERN MEDICINE
Gillian J. Buckley and Guy H. Palmer, Editors
Committee on the Long-Term Health and Economic Effects of
Antimicrobial Resistance in the United States
Board on Population Health and Public Health Practice
Health and Medicine Division
A Consensus Study Report of
THE NATIONAL ACADEMIES PRESS
Washington, DC
www.nap.edu
THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001
This project has been funded in whole or in part with federal funds from the National Institute of Allergy and Infectious Diseases, National Institutes of Health, Department of Health and Human Services, under Contract No. HHSN263201800029I, Task Order No. 75N98020F00003. 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: 978-0-309-26945-2
International Standard Book Number-10: 0-309-26945-8
Digital Object Identifier: https://doi.org/10.17226/26350
Library of Congress Control Number: 2021949602
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Copyright 2022 by the National Academy of Sciences. All rights reserved.
Printed in the United States of America
Suggested citation: National Academies of Sciences, Engineering, and Medicine. 2022. Combating antimicrobial resistance and protecting the miracle of modern medicine. Washington, DC: The National Academies Press. https://doi.org/10.17226/26350.
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COMMITTEE ON THE LONG-TERM HEALTH AND ECONOMIC EFFECTS OF ANTIMICROBIAL RESISTANCE IN THE UNITED STATES1
GUY H. PALMER (Chair), Regents Professor of Pathology and Infectious Diseases, The Jan and Jack Creighton Endowed Chair, Paul G. Allen School for Global Health, Washington State University; Senior Director of Global Health, Washington State University System
MICHAEL BAYM, Assistant Professor, Biomedical Informatics, Harvard University
CÉSAR DE LA FUENTE-NUNEZ, Presidential Assistant Professor, Perelman School of Medicine, School of Engineering and Applied Science, University of Pennsylvania
JENNIFER DIEN BARD, Director, Clinical Microbiology and Virology Laboratory, Associate Professor of Pathology (Clinical Scholar), Keck School of Medicine, University of Southern California
MARTA GOMEZ-CHIARRI, Professor, Department of Fisheries, Animal, and Veterinary Sciences, College of the Environment and Life Sciences, The University of Rhode Island
GUILLAUME LHERMIE, Associate Professor, Animal Health Economics and Veterinary Public Health, College of Veterinary Medicine; Director, Simpson Centre for Agricultural and Food Innovation and Education, School of Public Policy, University of Calgary, Canada
PREETI MALANI, Chief Health Officer, University of Michigan, Professor of Medicine, Division of Infectious Diseases, University of Michigan School of Medicine
ELEFTHERIOS MYLONAKIS, Charles C.J. Carpenter, MD, Professor of Infectious Diseases, Professor of Medicine, Assistant Dean of Medicine, Professor of Molecular Microbiology and Immunology, Warren Alpert Medical School of Brown University; Director, Rhode Island Hospital and The Miriam Hospital
IRUKA N. OKEKE, Professor, Department of Pharmaceutical Microbiology, Faculty of Pharmacy, University of Ibadan
EMMANUEL OKELLO, Assistant Specialist in Cooperative Extension, Population Health, and Reproduction, School of Veterinary Medicine, University of California, Davis
AYLIN SERTKAYA, Vice President and Senior Economist, Eastern Research Group
___________________
1 See Appendix B, Disclosure of Unavoidable Conflict of Interest.
MICHELLE SOUPIR, Associate Chair for Research and Extension, Equity Advisor, College of Engineering; Professor, Department of Agriculture and Biosystems Engineering, Iowa State University
ANDY STERGACHIS, Professor of Pharmacy and Global Health, Adjunct Professor of Health Metrics Sciences, Epidemiology, and Health Systems and Population Health; Associate Dean of Pharmacy; Director, Global Medicines Program & Biomedical Regulatory Affairs Program, University of Washington Schools of Pharmacy and Public Health
MARY E. WILSON, Clinical Professor of Epidemiology and Biostatistics, School of Medicine, University of California, San Francisco; Adjunct Professor, Global Health and Population, Harvard T.H. Chan School of Public Health
QIJING ZHANG, Clarence Hartley Covault Distinguished Professor, Associate Dean for Research and Graduate Studies, Veterinary Microbiology and Preventive Medicine, College of Veterinary Medicine, Iowa State University
Study Staff
GILLIAN J. BUCKLEY, Study Director
KARA LANEY, Senior Program Officer
ROBERTA WEDGE, Senior Program Officer (from May 2021)
AASHAKA SHINDE, Research Associate (from October 2020)
LEILA MEYMAND, Senior Program Assistant (from October 2020)
MISRAK DABI, Finance Business Partner
ROSE MARIE MARTINEZ, Senior Director, Board on Population Health and Public Health Practice
JULIE PAVLIN, Senior Director, Board on Global Health
ROBIN SCHOEN, Director, Board on Agriculture and Natural Resources
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 manuscript remain confidential to protect the integrity of the deliberative process.
We thank the following individuals for their review of this report:
Although the reviewers listed above provided many constructive comments 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 JIM E. RIVIERE, North Carolina State University, and ELLEN WRIGHT CLAYTON, Vanderbilt University. They were responsible for making certain that an independent examination of this report was carried 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.
Preface
I was in the lobby of the Fred Hutchinson Cancer Research Center in Seattle, waiting to meet with a colleague, when a wall display of the timeline of successful hematopoietic bone marrow transplants caught my attention. The timeline, in the form of a spiral, starts slowly in the 1970s—successes were few and failures many as scientists strove to understand the basic immunology underlying transplantation and clinicians to establish the optimal procedures and patient care. The successes slowly and then suddenly accelerate, providing life-saving transplants where previously no hope existed. Today, bone marrow transplants are performed in hospitals worldwide. Indeed, it is paradoxical that one of the highest accolades for the incredible achievements in modern medicine over recent decades is that we can take them for granted. The same is true for numerous medical procedures: organ transplants, joint replacements, improved cancer treatment, even safe childbirth. All of us know someone whose lives have been touched by these advances. Underlying this remarkable progress is the reliance on effective antibiotics to prevent and treat infections in patients at their most vulnerable moments. Addressing the challenges of the emergence and spread of resistant microbes; improving laboratory, diagnostics, and surveillance; and catalyzing the development of new classes of medicines is highly complex, cutting across scientific disciplines, medical specialties, institutions, and agencies. However, the goal is clear: preserve the medical advances of the past and allow continued progress, all afforded by and dependent on the availability of effective antibiotics.
Given the complexity of antibiotic resistance and the inherent multidisciplinary and interdisciplinary approaches required to address resistance, and to ensure a robust pipeline of effective medicines, the committee brought together expertise from across human, animal, and environmental health sectors. The committee has endeavored to examine the full range of initiatives and programs incorporated into the National Strategy and Action Plan for Combating Antibiotic-Resistant Bacteria and the progress in meeting the goals of the plan. The responsiveness of the multiple U.S. government agencies engaged in carrying out the plan was deeply appreciated as was the evaluation conducted by the Center for Infectious Disease Research and Policy at the University of Minnesota. Equally, given the need for global solutions to a challenge that knows no borders, the committee benefited from the multiple international organizations engaged in preserving antibiotic effectiveness and appreciates their willingness to share their expertise and perspectives. The committee was respectful of prior reports on antibiotic resistance and endeavored to assess their recommendations in the context of the committee’s statement of task. On behalf of the committee, I want to express my appreciation for the openness of these organizations and agencies and their efforts in working to ensure access to effective antibiotics.
A study of this magnitude requires a tremendous commitment from the committee members. All have sacrificed evenings, weekends, and holidays—without financial compensation—in this commitment and in their desire to bring the best possible science to bear on a challenging issue. Their commitment was all the more impressive as the study took place during the COVID-19 pandemic. Several of our committee members had frontline clinical care responsibilities; others increased commitments in laboratory testing, surveillance, and modeling—all were impacted by the pandemic by increased responsibilities at work and at home. Despite these increased responsibilities and the ability to only meet and work together virtually, the committee, individually and collectively, brought their expertise, experience, and knowledge to the task. I cannot thank them enough.
On behalf of the committee, I would like to express our thanks and appreciation to the National Academies leadership and staff: Rose Marie Martinez, Senior Director of the Board on Population Health and Public Health Practice; Kara Laney, Senior Program Officer; Roberta Wedge, Senior Program Officer; Aashaka Shinde, Research Associate; and Leila Meymand, Senior Program Assistant. A special thank you and deep appreciation to the Study Director, Gillian Buckley, who provided exceptional leadership throughout the study. Without her leadership and the work of the staff in planning, organization, and editing, this report would not have been possible.
The evolutionary basis of antimicrobial resistance dictates that there will be no magic bullets or simple solutions. Ensuring that modern medicine can continue to rely on effective antibiotics will require continual innovation and process improvement. Minimizing the need for antibiotics through preventive health care and improved sanitation, housing, and access to clean water is achievable, as is ensuring that the right antibiotic is available and given at the appropriate dose for the appropriate duration. Achieving those goals is fundamental to meeting the National Academy of Medicine’s vision of “a healthier future for everyone.”
Guy H. Palmer, Chair
Committee on the Long-Term Health and Economic Effects of Antimicrobial Resistance in the United States
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Acknowledgments
This report is a product of the cooperation and contributions of many people. The committee and staff are grateful for the support of the National Academies of Sciences, Engineering, and Medicine’s Health and Medicine Division (HMD) staff who contributed to producing this report. The committee and staff thank Tina Seliber, Lauren Shern, Leslie Sim, and Taryn Young in the HMD Executive Office; Anne Marie Houppert, Christopher Lao-Scott, and Rebecca Morgan in the National Academies Research Center; Sadaf Faraz, Devona Overton, Esther Pak, and Marguerite Romatelli in the Office of the Chief Communications Officer; Stephanie Miceli in the Office of News and Public Information; Julie Eubank in the Office of Congressional and Government Affairs; and Mandy Enriquez, Dempsey Price, and Alejandro Velazquez in the Office of Conference Management. We extend particular thanks to Roberta Wedge for joining the project and providing invaluable analysis and Rebekah Hutton for her work on the cover design.
The committee’s work was enhanced by the systematic analysis of Kristine Moore and Anje Mehr whose commissioned paper informed this report. We also thank Yunxin Joy Jiao for graciously sharing her graphic designs for reprint in Chapter 1.
The committee thanks all the speakers and moderators who participated in committee meetings, as well as others who provided information, input, and assistance. They include the following: Frank Møller Aarestrup, Mark Albrecht, Neena Anadaraman, Anand Balachandran, Manica Balasegaram, Helen Boucher, Susan Bright, Felipe C. Cabello, Angela Caliendo, Amanda Cash, Clare Chandler, Ryan Cirz, Michael Craig, Chris Crnich,
Peter Panduro Damborg, Gautam Dantas, Mary Denigan-Macauley, Lynn Filpi, William Flynn, Heather Fowler, Jay Garland, Cyril Gay, Claire Gordon, Luca Guardabassi, Tim Jinks, Bill Keleher, Wes Kim, Jane Knisely, Kevin Krause, Ramanan Laxminarayan, Brian Lubbers, John Lynch, Marc Mendelson, Mark Miller, Chris Murray, Kevin Outterson, Mark Papich, Timothy Persons, Carmem L. Pessoa-Silva, Jessica Petrillo, Tom Pilcher, John Rex, Jennifer Schneider, Anand Shah, Gunnar Skov Simonsen, Brad Spellberg, Padmini Srikantiah, Bruce Stewart-Brown, Fred C. Tenover, Paige Waterman, Craig Wilson, and Barbara Zimmer. To Dr. Christopher Murray, Institute for Health Metrics and Evaluation, University of Washington, and the Global Research on Antimicrobial Resistance team, we extend particular thanks for sharing key findings from their Lancet paper in review.
Finally, we extend special thanks to the National Institute of Allergy and Infectious Diseases of the National Institutes of Health for generously funding this project.
Contents
Human Action Exacerbates Resistance
Antimicrobial Resistance Is a Global Problem
Antimicrobial Resistance Is a Complex Adaptive Problem
One Health Is a Complex Adaptive Response
3 THE HEALTH AND ECONOMIC BURDEN OF RESISTANCE
Challenges of Quantifying the Burden of Resistance
Developing More Precise Estimates of the Burden of Antimicrobial Resistance
Monitoring Antimicrobial Resistance in Water
5 STEWARDSHIP AND INFECTION PREVENTION
Stewardship in Human Medicine in the United States
Stewardship in Animal Medicine in the United States
Diagnostic Stewardship in the United States
Strategies to Prevent the Emergence of Resistance, Especially in Low- and Middle-Income Countries
6 BRINGING NEW PRODUCTS TO MARKET AND ENSURING THEIR REACH
Investing in One Health Solutions
7 THE NATIONAL ACTION PLAN FOR COMBATING ANTIBIOTIC-RESISTANT BACTERIA
Government Accountability Office Reports
Federal Government Implementation of the 2015 National Action Plan
National Action Plan for Combating Antibiotic-Resistant Bacteria, 2020–2025
8 A ROLE FOR THE UNITED STATES IN COORDINATED GLOBAL ACTION
A Committee Member Biographies
Boxes, Figures, and Tables
BOXES
1-1 The Goals of the National Action Plan for Combating Antibiotic-Resistant Bacteria 2015 to 2020
2-1 Antimicrobials and the Microbiome
2-3 The Challenge of Treating Gram-Negative Bacteria
2-4 The Ecosystem Value of the Oyster Microbiome
3-1 Naylor and Colleagues’ Guidelines for Research Measuring the Burden of Resistant Infections
4-1 Foundational Steps for Surveillance of Antimicrobial Resistance
4-2 The World Health Organization’s (WHO’s) Global Antimicrobial Surveillance and Use System
4-3 Wastewater Surveillance and COVID-19
5-1 Multidrug-Resistant Candida auris and COVID-19
5-2 University of Washington Tele-ASP
5-3 Antimicrobial Use in Companion Animals
5-4 Study Design Considerations for Assessing the Value of Diagnostics
6-2 The Global Antibiotic Research and Development Partnership
6-3 The Onshoring Essential Antibiotics Act
6-4 Legal and Regulatory Pull Incentives in the United States
7-1 Five Goals and Objectives of the National Strategy for Combating Antibiotic-Resistant Bacteria
7-2 National Targets to Combat Antimicrobial-Resistant Bacteria
7-3 GAO Recommendations for Improving Progress on the National Action Plan
7-4 GAO Recommendations on the Use of Medically Important Drugs in Food Animals
7-5 Building Off the Previous 5-Year Action Plan
FIGURES
1-1 Selective pressure encourages antimicrobial resistance
1-2 Resistance genes can pass through vertical or horizontal mechanisms
1-3 Microbes and resistomes travel across habitats
1-5 The timeline of key U.S. government publications on antimicrobial resistance
2-1 A conceptual framework for the role of modifiable drivers of antimicrobial resistance
2-2 Historic use of antibiotics in Norwegian aquaculture
3-1 Trends in antimicrobial resistance across OECD countries, 2005 to 2014
3-10 Interactions between COVID-19 and the emergence of antimicrobial resistance
3-12 Seven key challenges in collecting data to inform estimates of the burden of resistance
3-13 The global antimicrobial resistance platform for ONE-burden estimates
4-2 Requirements for the flow of surveillance data and proposed solutions to key challenges
4-5 Whole genome sequencing compares DNA sequence data to AMR determinants in reference databases
4-6 Examples of metagenomic analysis of antimicrobial resistance in microbial communities
5-2 The CDC’s core elements of hospital antibiotic stewardship programs
5-3 New antibiotics introduced into country markets, 1999–2014
5-4 Mechanisms through which vaccines can contribute to reducing antimicrobial resistance
6-1 Push and pull incentives operate at different stages of antimicrobial development
6-2 Research and development cost, both direct and cost of capital, by clinical trial phases
6-3 Failure is increasingly less likely as drug candidates move to later stages of development
6-5 Overview of the preclinical pipeline for antimicrobials and related products
6-6 Distribution of CARB-X applications based on stage of technology in development
6-7 BARDA’s antimicrobial portfolio, fall 2021
6-9 Antimicrobial drug pipeline, by stage of development over time
6-10 Simulation of an adaptive randomized controlled trial for gram-negative bloodstream infections
8-1 Environmental conditions in health facilities in 78 low- and middle-income countries
8-2 The iterative steps of antimicrobial stewardship design
TABLES
3-1 Change in Infections Caused by Some CDC Priority Pathogens Between 2013 and 2019
3-4 The Social Costs of Hospital-Acquired Infections
3-5 Adjusted Attributable Cost by Pathogen for Community and Hospital Onset Infections
3-6 Estimates of the Effect of Antimicrobial Resistance on Mortality from Recent Prominent Reports
5-1 Vaccines Can Work Through Many Pathways to Reduce Bacterial Infections
6-1 Comparison of CDC and BSA Priority Bacterial Threats
6-3 Clinical Needs for Rapid Point-of-Care Diagnostics for Respiratory Tract Infections
6-4 Regulation of Directly Fed Micro-Organisms (Probiotics) by FDA
Acronyms and Abbreviations
3GC | third-generation cephalosporin |
AACTING | Network on quantification of veterinary Antimicrobial usage at herd level and Analysis Communication and benchmarking to improve responsible usage |
ABSSSI | acute bacterial skin and skin structure infections |
ACTIV | Accelerating COVID-19 Therapeutic Interventions and Vaccines |
AIDS | acquired immunodeficiency syndrome |
AMR | antimicrobial resistance |
AMU | antimicrobial use |
AR | antibiotic resistance |
ARG | Argentina |
ARLG | Antibacterial Resistance Leadership Group |
ARLN | Antibiotic Resistance Laboratory Network |
ASPR | HHS Office of the Assistant Secretary for Preparedness and Response |
AUS | Australia |
AUT | Austria |
AVMA | American Veterinary Medical Association |
AWaRe | WHO’s Access, Watch, Reserve classification of antibiotics |
BARDA | Biomedical Advanced Research and Development Authority |
BGR | Republic of Bulgaria |
BL | beta-lactam |
BLI | beta-lactamase inhibitor |
BSI | bloodstream infection |
C. auris | Candida auris |
C. difficile | Clostridioides difficile |
CABP | community-acquired bacterial pneumonia |
CARB | National Action Plan for Combating Antibiotic-Resistant Bacteria |
CARB-X | Combating Antibiotic-Resistant Bacteria Biopharmaceutical Accelerator |
CDC | Centers for Disease Control and Prevention |
CDI | Clostridioides difficile infection |
CHE | Switzerland |
CHL | Chile |
CI | confidence interval |
cIAI | complicated intra-abdominal infection |
CLIA | Clinical Laboratory Improvement Amendments of 1988 |
CLSI | Clinical and Laboratory Standards Institute |
CLSI-VAST | veterinary antimicrobial susceptibility testing |
CMS | Centers for Medicare & Medicaid Services |
CO-ADD | Community for Open Antimicrobial Drug Discovery |
COVID-19 | coronavirus disease 2019 |
CR | carbapenem-resistant |
CRAB | carbapenem-resistant Acinetobacter baumannii |
CRE | carbapenem-resistant Enterobacterales |
cUTI | complicated urinary tract infection |
CYP | Cyprus |
CZE | Czech Republic |
DALY | disability-adjusted life year |
DARPA | Defense Advanced Research Projects Agency |
DFUI | diabetic foot ulcer infections |
DISARM Act | Developing an Innovative Strategy for Antimicrobial-Resistant Microorganisms Act |
DNA | deoxyribonucleic acid |
DNDi | Drugs for Neglected Diseases Initiative |
ECU | Ecuador |
EMA | European Medicines Agency |
EPA | Environmental Protection Agency |
EQS | Environmental Quality Standard |
ESBL | extended-spectrum beta-lactamase |
ESP | Spain |
EST | Estonia |
EUCAST | European Committee on Antimicrobial Susceptibility Testing |
FAO | Food and Agriculture Organization of the United Nations |
FDA | Food and Drug Administration |
GAIN Act | Generating Antibiotic Incentives Now Act |
GARDP | Global Antibiotic Research and Development Partnership |
GBR | United Kingdom |
GCI | gonococcal infection |
GCOA | Global Coalition on Aging |
GDP | gross domestic product |
GHA | Ghana |
GLASS | Global Antimicrobial Resistance and Use Surveillance System |
GLASS-EAR | Emerging Antimicrobial Resistance Reporting |
GN | gram-negative |
GRC | Greece |
HABP/VABP | Hospital-associated bacterial pneumonia/ventilator-associated bacterial pneumonia |
HHS | Department of Health and Human Services |
Hib | Haemophilus influenzae type b |
HIC | high-income country |
HIV | human immunodeficiency virus |
HRV | Croatia |
HUN | Hungary |
hVISA | heterogeneous vancomycin-intermediate Staphylococcus aureus |
ICU | intensive care unit |
IDSA | Infectious Diseases Society of America |
IHME | Institute for Health Metrics and Evaluation |
IMF | International Monetary Fund |
IMI | imipenem-hydrolyzing ß-lactamases |
IMP | imipenemase metallo-ß-lactamase |
IND | India |
IPPS | inpatient prospective payment system |
ISL | Iceland |
ITA | Italy |
KPC | Klebsiella pneumoniae carbapenemases |
LIMS | Laboratory Information Management System |
LMIC | low- and middle-income country |
LTU | Lithuania |
LUX | Luxembourg |
LVA | Latvia |
MDR | multidrug-resistant |
MDR G– | multidrug-resistant gram-negative bacteria |
MIC | minimal inhibitory concentration |
MKD | Republic of North Macedonia |
MLST | multilocus sequence |
MRSA | methicillin-resistant Staphylococcus aureus |
NAHMS | National Animal Health Monitoring System |
NARMS | National Antimicrobial Resistance Monitoring System |
NCATS | National Center for Advancing Translational Sciences |
NCBI | National Center for Biotechnology Information |
NDARO | National Database of Antibiotic Resistant Organisms |
NDM | New Delhi metallo-ß-lactamase |
NGO | nongovernmental organization |
NIAID | National Institute of Allergy and Infectious Diseases |
NIDDK | National Institute of Diabetes and Digestive and Kidney Diseases |
NIH | National Institutes of Health |
NITAG | National Immunization Technical Advisory Group |
NLM | National Library of Medicine |
NOR | Norway |
NZL | New Zealand |
OECD | Organisation for Economic Co-operation and Development |
OIE | World Organisation for Animal Health (formerly Office International des Epizooties) |
OXA-48 | Oxacillinase-48 |
PACCARB | Presidential Advisory Council on Combating Antibiotic-Resistant Bacteria |
PCAST | President’s Council of Advisors on Science and Technology |
PCORI | Patient-Centered Outcomes Research Institute |
PCR | polymerase chain reaction |
PCV | pneumococcal conjugate vaccine |
PEPFAR | U.S. President’s Emergency Plan for AIDS Relief |
POCIS | polar organic chemical integrative sampler |
POL | Poland |
PPE | personal protective equipment |
QIDP | qualified infectious disease product |
qPCR | quantitative polymerase chain reaction |
R&D | research and development |
rCDI | recurrent Clostridioides difficile infection |
REVAMP Act | Re-Valuing Anti-Microbial Products Act |
RNA | ribonucleic acid |
ROM | Romania |
rUTI | recurrent urinary tract infection |
S. pneumonia | Streptococcus pneumonia |
SAB | Staphylococcus aureus bacteremia |
SfAM | Society for Applied Microbiology |
SRB | Serbia |
SVK | Slovakia |
SVN | Slovenia |
SWE | Sweden |
TCV | typhoid conjugate vaccine |
THA | Thailand |
TUR | Turkey |
UN | United Nations |
U.S. | United States |
USAID | U.S. Agency for International Development |
USD | U.S. dollars |
USDA | U.S. Department of Agriculture |
UTI | urinary tract infection |
UW | University of Washington |
UW tele-ASP | University of Washington Tele-Antimicrobial Stewardship Program |
VA | Department of Veterans Affairs |
VEN | Venezuela |
VetCAST | EUCAST subcommittee for Veterinary Antimicrobial Susceptibility Testing |
VIM | Verona integron-encoded metallo-ß-lactamases |
VNM | Vietnam |
VRE | vancomycin-resistant Enterococci |
WASH | water, sanitation, and hygiene |
WFD | Water Framework Directive |
WHO | World Health Organization |
WWTP | wastewater treatment plant |
ZAF | South Africa |