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Resistance diagnostics as a public health tool to combat antibiotic resistance: A model-based evaluation

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      Abstract

      Rapid point-of-care resistance diagnostics (POC-RD) are a key tool in the fight against antibiotic resistance. By tailoring drug choice to infection genotype, doctors can improve treatment efficacy while limiting costs of inappropriate antibiotic prescription. Here, we combine epidemiological theory and data to assess the potential of resistance diagnostics (RD) innovations in a public health context, as a means to limit or even reverse selection for antibiotic resistance. POC-RD can be used to impose a nonbiological fitness cost on resistant strains by enabling diagnostic-informed treatment and targeted interventions that reduce resistant strains’ opportunities for transmission. We assess this diagnostic-imposed fitness cost in the context of a spectrum of bacterial population biologies and find that POC-RD have a greater potential against obligate pathogens than opportunistic pathogens already subject to selection under “bystander” antibiotic exposure during asymptomatic carriage (e.g., the pneumococcus). We close by generalizing the notion of RD-informed strategies to incorporate carriage surveillance information and illustrate that coupling transmission-control interventions to the discovery of resistant strains in carriage can potentially select against resistance in a broad range of opportunistic pathogens.

      Abstract

      Point-of-care resistance diagnostics represent an opportunity to tailor antibiotic treatment protocols to specific bacterial strains. This study shows that conditioning on both point-of-care and carriage diagnostics can produce effective patient care that also selects against resistance.

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      Most cited references 57

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      Antibiotic resistance-the need for global solutions.

      The causes of antibiotic resistance are complex and include human behaviour at many levels of society; the consequences affect everybody in the world. Similarities with climate change are evident. Many efforts have been made to describe the many different facets of antibiotic resistance and the interventions needed to meet the challenge. However, coordinated action is largely absent, especially at the political level, both nationally and internationally. Antibiotics paved the way for unprecedented medical and societal developments, and are today indispensible in all health systems. Achievements in modern medicine, such as major surgery, organ transplantation, treatment of preterm babies, and cancer chemotherapy, which we today take for granted, would not be possible without access to effective treatment for bacterial infections. Within just a few years, we might be faced with dire setbacks, medically, socially, and economically, unless real and unprecedented global coordinated actions are immediately taken. Here, we describe the global situation of antibiotic resistance, its major causes and consequences, and identify key areas in which action is urgently needed. Copyright © 2013 Elsevier Ltd. All rights reserved.
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        The global burden of group A streptococcal diseases.

        The global burden of disease caused by group A streptococcus (GAS) is not known. We review recent population-based data to estimate the burden of GAS diseases and highlight deficiencies in the available data. We estimate that there are at least 517,000 deaths each year due to severe GAS diseases (eg, acute rheumatic fever, rheumatic heart disease, post-streptococcal glomerulonephritis, and invasive infections). The prevalence of severe GAS disease is at least 18.1 million cases, with 1.78 million new cases each year. The greatest burden is due to rheumatic heart disease, with a prevalence of at least 15.6 million cases, with 282,000 new cases and 233,000 deaths each year. The burden of invasive GAS diseases is unexpectedly high, with at least 663,000 new cases and 163,000 deaths each year. In addition, there are more than 111 million prevalent cases of GAS pyoderma, and over 616 million incident cases per year of GAS pharyngitis. Epidemiological data from developing countries for most diseases is poor. On a global scale, GAS is an important cause of morbidity and mortality. These data emphasise the need to reinforce current control strategies, develop new primary prevention strategies, and collect better data from developing countries.
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          Burden of Clostridium difficile infection in the United States.

          The magnitude and scope of Clostridium difficile infection in the United States continue to evolve.
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            Author and article information

            Affiliations
            [1 ] Fuqua School of Business and Department of Economics, Duke University, Durham, North Carolina, United States of America
            [2 ] School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, United States of America
            [3 ] Center for Communicable Disease Dynamics, Department of Epidemiology and Department of Immunology and Infectious Diseases, Harvard T. H. Chan School of Public Health, Boston, Massachusetts, United States of America
            [4 ] Center for Microbial Dynamics and Infection, Georgia Institute of Technology, Atlanta, Georgia, United States of America
            The Pennsylvania State University, UNITED STATES
            Author notes

            The authors have declared that no competing interests exist.

            Contributors
            Role: Conceptualization, Role: Formal analysis, Role: Writing – original draft, Role: Writing – review & editing
            Role: Data curation, Role: Writing – review & editing
            ORCID: http://orcid.org/0000-0003-3403-5765, Role: Data curation, Role: Writing – review & editing
            Role: Data curation, Role: Writing – review & editing
            ORCID: http://orcid.org/0000-0003-1892-9275, Role: Conceptualization, Role: Formal analysis, Role: Writing – original draft, Role: Writing – review & editing
            Role: Academic Editor
            Journal
            PLoS Biol
            PLoS Biol
            plos
            plosbiol
            PLoS Biology
            Public Library of Science (San Francisco, CA USA )
            1544-9173
            1545-7885
            16 May 2019
            May 2019
            16 May 2019
            : 17
            : 5
            31095567 6522007 10.1371/journal.pbio.3000250 PBIOLOGY-D-18-01050
            © 2019 McAdams et al

            This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

            Counts
            Figures: 5, Tables: 2, Pages: 18
            Product
            Funding
            Funded by: funder-id http://dx.doi.org/10.13039/100004412, Human Frontier Science Program;
            Award ID: RGP0011/2014
            Award Recipient : ORCID: http://orcid.org/0000-0003-1892-9275
            Funded by: funder-id http://dx.doi.org/10.13039/100000030, Centers for Disease Control and Prevention;
            Award ID: OADS BAA 2016-N-17812
            Award Recipient : ORCID: http://orcid.org/0000-0003-1892-9275
            Funded by: funder-id http://dx.doi.org/10.13039/100000057, National Institute of General Medical Sciences;
            Award ID: U54GM088558
            Award Recipient :
            Funded by: funder-id http://dx.doi.org/10.13039/100000893, Simons Foundation;
            Award ID: 396001
            Award Recipient : ORCID: http://orcid.org/0000-0003-1892-9275
            Funded by: funder-id http://dx.doi.org/10.13039/100000050, National Heart, Lung, and Blood Institute;
            Award ID: U54GM088558
            Award Recipient : ORCID: http://orcid.org/0000-0003-1892-9275
            The project described was supported by the Centers for Disease Control (OADS BAA 2016-N-17812), the National Institute of General Medical Sciences (U54GM088558), the National Heart Lung Blood Institute (R56HL142857), the Simons Foundation (396001), the Wenner-Gren Foundations, and the Royal Physiographic Society of Lund. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript
            Categories
            Research Article
            Biology and Life Sciences
            Microbiology
            Microbial Control
            Antimicrobial Resistance
            Antibiotic Resistance
            Medicine and Health Sciences
            Pharmacology
            Antimicrobial Resistance
            Antibiotic Resistance
            Medicine and Health Sciences
            Pharmacology
            Drugs
            Antimicrobials
            Antibiotics
            Biology and Life Sciences
            Microbiology
            Microbial Control
            Antimicrobials
            Antibiotics
            Medicine and Health Sciences
            Pathology and Laboratory Medicine
            Pathogens
            Opportunistic Pathogens
            Medicine and Health Sciences
            Pharmacology
            Drug Research and Development
            Drug Discovery
            Medicine and Health Sciences
            Pharmaceutics
            Drug Therapy
            Medicine and Health Sciences
            Pathology and Laboratory Medicine
            Pathogens
            Biology and Life Sciences
            Microbiology
            Medical Microbiology
            Microbial Pathogens
            Bacterial Pathogens
            Medicine and Health Sciences
            Pathology and Laboratory Medicine
            Pathogens
            Microbial Pathogens
            Bacterial Pathogens
            Biology and Life Sciences
            Microbiology
            Microbial Control
            Antimicrobial Resistance
            Medicine and Health Sciences
            Pharmacology
            Antimicrobial Resistance
            Custom metadata
            All relevant data are within the paper and its Supporting Information files.

            Life sciences

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