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      Drivers of antimicrobial resistance in layer poultry farming: Evidence from high prevalence of multidrug-resistant Escherichia coli and enterococci in Zambia

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          Abstract

          Background and Aim:

          Inappropriate use of antimicrobials exacerbates antimicrobial resistance (AMR) in the poultry sector. Information on factors driving AMR in the layer poultry sector is scarce in Zambia. This study examined the drivers of AMR in the layer poultry sector in the Lusaka and Copperbelt Provinces of Zambia.

          Materials and Methods:

          This cross-sectional study employed a structured questionnaire in 77 layer poultry farms in the provinces of Lusaka and Copperbelt, Zambia, from September 2020 to April 2021. Data analysis was conducted using Stata version 16.1. Antimicrobial resistance was defined as the presence of multidrug resistance (MDR) isolates. Multivariable regression analysis was used to identify drivers of AMR.

          Results:

          In total, 365 samples were collected, from which 339 (92.9%) Escherichia coli and 308 (84.4%) Enterococcus spp. were isolated. Multidrug resistance was identified in 39% of the E. coli and 86% of the Enterococcus spp. The overall prevalence of AMR in layer poultry farms was 51.7% (95% confidence interval [CI]: 40.3%–63.5%). Large-scale farmers (Adjusted odds ratio [AOR] = 0.20, 95% CI: 0.04%–0.99%) than small-scale and farmers who were aware of AMR than those who were unaware (AOR = 0.26, 95% CI: 0.08%–0.86%) were less likely to experience AMR problems.

          Conclusion:

          This study found a high prevalence of AMR in layer poultry farming linked to the type of farm management practices and lack of AMR awareness. Evidence of high MDR in our study is of public health concern and requires urgent attention. Educational interventions must increase AMR awareness, especially among small- and medium-scale poultry farmers.

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          Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance.

          A-P Magiorakos, A. Srinivasan, R.B. Carey … (2012)
          Many different definitions for multidrug-resistant (MDR), extensively drug-resistant (XDR) and pandrug-resistant (PDR) bacteria are being used in the medical literature to characterize the different patterns of resistance found in healthcare-associated, antimicrobial-resistant bacteria. A group of international experts came together through a joint initiative by the European Centre for Disease Prevention and Control (ECDC) and the Centers for Disease Control and Prevention (CDC), to create a standardized international terminology with which to describe acquired resistance profiles in Staphylococcus aureus, Enterococcus spp., Enterobacteriaceae (other than Salmonella and Shigella), Pseudomonas aeruginosa and Acinetobacter spp., all bacteria often responsible for healthcare-associated infections and prone to multidrug resistance. Epidemiologically significant antimicrobial categories were constructed for each bacterium. Lists of antimicrobial categories proposed for antimicrobial susceptibility testing were created using documents and breakpoints from the Clinical Laboratory Standards Institute (CLSI), the European Committee on Antimicrobial Susceptibility Testing (EUCAST) and the United States Food and Drug Administration (FDA). MDR was defined as acquired non-susceptibility to at least one agent in three or more antimicrobial categories, XDR was defined as non-susceptibility to at least one agent in all but two or fewer antimicrobial categories (i.e. bacterial isolates remain susceptible to only one or two categories) and PDR was defined as non-susceptibility to all agents in all antimicrobial categories. To ensure correct application of these definitions, bacterial isolates should be tested against all or nearly all of the antimicrobial agents within the antimicrobial categories and selective reporting and suppression of results should be avoided. © 2011 European Society of Clinical Microbiology and Infectious Diseases. No claim to original US government works.
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            Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis

            (2022)
            Summary Background Antimicrobial resistance (AMR) poses a major threat to human health around the world. Previous publications have estimated the effect of AMR on incidence, deaths, hospital length of stay, and health-care costs for specific pathogen–drug combinations in select locations. To our knowledge, this study presents the most comprehensive estimates of AMR burden to date. Methods We estimated deaths and disability-adjusted life-years (DALYs) attributable to and associated with bacterial AMR for 23 pathogens and 88 pathogen–drug combinations in 204 countries and territories in 2019. We obtained data from systematic literature reviews, hospital systems, surveillance systems, and other sources, covering 471 million individual records or isolates and 7585 study-location-years. We used predictive statistical modelling to produce estimates of AMR burden for all locations, including for locations with no data. Our approach can be divided into five broad components: number of deaths where infection played a role, proportion of infectious deaths attributable to a given infectious syndrome, proportion of infectious syndrome deaths attributable to a given pathogen, the percentage of a given pathogen resistant to an antibiotic of interest, and the excess risk of death or duration of an infection associated with this resistance. Using these components, we estimated disease burden based on two counterfactuals: deaths attributable to AMR (based on an alternative scenario in which all drug-resistant infections were replaced by drug-susceptible infections), and deaths associated with AMR (based on an alternative scenario in which all drug-resistant infections were replaced by no infection). We generated 95% uncertainty intervals (UIs) for final estimates as the 25th and 975th ordered values across 1000 posterior draws, and models were cross-validated for out-of-sample predictive validity. We present final estimates aggregated to the global and regional level. Findings On the basis of our predictive statistical models, there were an estimated 4·95 million (3·62–6·57) deaths associated with bacterial AMR in 2019, including 1·27 million (95% UI 0·911–1·71) deaths attributable to bacterial AMR. At the regional level, we estimated the all-age death rate attributable to resistance to be highest in western sub-Saharan Africa, at 27·3 deaths per 100 000 (20·9–35·3), and lowest in Australasia, at 6·5 deaths (4·3–9·4) per 100 000. Lower respiratory infections accounted for more than 1·5 million deaths associated with resistance in 2019, making it the most burdensome infectious syndrome. The six leading pathogens for deaths associated with resistance (Escherichia coli, followed by Staphylococcus aureus, Klebsiella pneumoniae, Streptococcus pneumoniae, Acinetobacter baumannii, and Pseudomonas aeruginosa) were responsible for 929 000 (660 000–1 270 000) deaths attributable to AMR and 3·57 million (2·62–4·78) deaths associated with AMR in 2019. One pathogen–drug combination, meticillin-resistant S aureus, caused more than 100 000 deaths attributable to AMR in 2019, while six more each caused 50 000–100 000 deaths: multidrug-resistant excluding extensively drug-resistant tuberculosis, third-generation cephalosporin-resistant E coli, carbapenem-resistant A baumannii, fluoroquinolone-resistant E coli, carbapenem-resistant K pneumoniae, and third-generation cephalosporin-resistant K pneumoniae. Interpretation To our knowledge, this study provides the first comprehensive assessment of the global burden of AMR, as well as an evaluation of the availability of data. AMR is a leading cause of death around the world, with the highest burdens in low-resource settings. Understanding the burden of AMR and the leading pathogen–drug combinations contributing to it is crucial to making informed and location-specific policy decisions, particularly about infection prevention and control programmes, access to essential antibiotics, and research and development of new vaccines and antibiotics. There are serious data gaps in many low-income settings, emphasising the need to expand microbiology laboratory capacity and data collection systems to improve our understanding of this important human health threat. Funding Bill & Melinda Gates Foundation, Wellcome Trust, and Department of Health and Social Care using UK aid funding managed by the Fleming Fund.
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              Antibiotic resistance-the need for global solutions.

              Ramanan Laxminarayan, Adriano Duse, Chand Wattal … (2013)
              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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                Author and article information

                Journal
                Journal ID (nlm-ta): Vet World
                Journal ID (iso-abbrev): Vet World
                Title: Veterinary World
                Publisher: Veterinary World (India )
                ISSN (Print): 0972-8988
                ISSN (Electronic): 2231-0916
                Publication date (Print): September 2023
                Publication date (Electronic): 14 September 2023
                Volume: 16
                Issue: 9
                Pages: 1803-1814
                Affiliations
                [1 ]Department of Pharmacy, School of Health Sciences, University of Zambia, Lusaka, Zambia
                [2 ]Department of Disease Control, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia
                [3 ]Department of Medicine and Clinical Sciences, School of Medicine, Eden University, Lusaka, Zambia
                [4 ]Department of Biological Sciences, School of Natural Sciences, University of Zambia, Lusaka, Zambia
                [5 ]Department of Pathology and Microbiology Laboratory, University Teaching Hospitals, Lusaka, Zambia
                [6 ]Centre for Infectious Disease Research in Zambia, Lusaka, Zambia
                [7 ]Department of Public Health, Michael Chilufya Sata School of Medicine, Copperbelt University, Ndola, Zambia
                [8 ]Department of Clinical Research, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine, London, United Kingdom
                [9 ]Department of Anatomy and Physiological Sciences, Institute of Basic and Biomedical Sciences, Levy Mwanawasa Medical University, Lusaka, Zambia
                [10 ]Food and Agriculture Organization (FAO) of the United Nations, House No. 5 Chaholi, off Addis Ababa drive, Lusaka, Zambia
                [11 ]Department of Food Science and Nutrition, School of Agricultural Sciences, University of Zambia, Lusaka, Zambia
                [12 ]Department of Paraclinical Studies, School of Veterinary Medicine, University of Zambia, Lusaka, Zambia
                Author notes
                Article
                Publisher ID: Vetworld-16-1803
                DOI: 10.14202/vetworld.2023.1803-1814
                PMC ID: 10583887
                PubMed ID: 37859964
                SO-VID: e1f60098-e575-4aef-ab67-e837057455ea
                Copyright © Copyright: © Mudenda, et al.
                License:

                Open Access. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 01 June 2023
                Date accepted : 10 August 2023
                Categories
                Subject: Research Article

                Keywords: antimicrobial resistance,drivers,escherichia coli,poultry,risk factors,zambia
                Data availability:
                Keywords: antimicrobial resistance, drivers, escherichia coli, poultry, risk factors, zambia

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