-
Evidence for antimicrobial stewardship and reduced antimicrobial resistance in the Mid-West of Ireland, 2012 to 2023: findings from a One Health study
-
James Powell1,2
, Santosh Sharma2
, Alan Johnson3
, Siobhan Barrett4 , Caroline Garvan5 , Nuala H O’Connell1,2
, Colum P Dunne2,6
-
View Affiliations Hide AffiliationsAffiliations: 1 Department of Microbiology, University Hospital Limerick, Limerick, Ireland 2 School of Medicine and Centre for Interventions in Infection, Inflammation, and Immunity (4i), University of Limerick, Limerick, Ireland 3 Regional Veterinary Laboratory, Knockalisheen, Limerick, Ireland 4 Pharmacy Department, University Hospital Limerick, Limerick, Ireland 5 Department of Agriculture, Food and the Marine, Backweston Campus, Celbridge, Kildare, Ireland 6 School of Pharmacy, Queen’s University Belfast, Belfast, Northern IrelandColum P Dunnecolum.dunne ul.ie
-
View Citation Hide Citation
Citation style for this article: Powell James, Sharma Santosh, Johnson Alan, Barrett Siobhan, Garvan Caroline, O’Connell Nuala H, Dunne Colum P. Evidence for antimicrobial stewardship and reduced antimicrobial resistance in the Mid-West of Ireland, 2012 to 2023: findings from a One Health study. Euro Surveill. 2025;30(13):pii=2400512. https://doi.org/10.2807/1560-7917.ES.2025.30.13.2400512 Received: 31 Jul 2024; Accepted: 27 Nov 2024
Abstract
Escherichia coli, a pathogen commonly infecting humans and bovines, is a prime sentinel indicator and predictor for antimicrobial resistance (AMR). Tracking epidemiological trends of AMR is essential to address this global One Health threat.
To perform a comprehensive retrospective epidemiological analysis of AMR trends in E. coli isolated from human urine and blood and bovine specimens, and compare with antimicrobial consumption or sales data for humans.
All E. coli isolates with susceptibility results from human urine (n = 122,419), blood (n = 2,373) and bovine specimens (n = 585) from 2012–23 in the Mid-West of Ireland were analysed. The resistance trends of nine commonly used antimicrobials were compared with their consumption by humans or sales in community and hospital settings.
Over the 12-year period, resistance against common antimicrobials was lowest among the bovine isolates (range: 2–44%). Human urine isolates showed lower resistance (5–59%) than bloodstream isolates (12–69%). There was a downward trend in resistance to all antimicrobials between 2012 and 2023 in the human isolates (p < 0.001), except for piperacillin/tazobactam where resistance increased, in each case correlating with antimicrobial usage. Bovine isolates demonstrated reduced resistance to co-amoxiclav (p = 0.001), with no trend observed for other antimicrobials.
Our data showed reduced resistance to many antimicrobials for E. coli from human and bovine populations in our region. Increased use of ‘preferred’ antimicrobials in humans and reduced use of those ‘to be avoided’ was observed. The findings indicate the emerging effectiveness of AMR strategies and highlight the value of One Health AMR.

Article metrics loading...


Full text loading...
References
-
Paitan Y. Current trends in antimicrobial resistance of Escherichia coli. Curr Top Microbiol Immunol. 2018;416:181-211. https://doi.org/10.1007/82_2018_110 PMID: 30088148
-
Allocati N, Masulli M, Alexeyev MF, Di Ilio C. Escherichia coli in Europe: an overview. Int J Environ Res Public Health. 2013;10(12):6235-54. https://doi.org/10.3390/ijerph10126235 PMID: 24287850
-
Botrel MA, Haenni M, Morignat E, Sulpice P, Madec JY, Calavas D. Distribution and antimicrobial resistance of clinical and subclinical mastitis pathogens in dairy cows in Rhône-Alpes, France. Foodborne Pathog Dis. 2010;7(5):479-87. https://doi.org/10.1089/fpd.2009.0425 PMID: 19919286
-
Yamamura F, Sugiura T, Munby M, Shiokura Y, Murata R, Nakamura T, et al. Relationship between Escherichia coli virulence factors, notably kpsMTII, and symptoms of clinical metritis and endometritis in dairy cows. J Vet Med Sci. 2022;84(3):420-8. https://doi.org/10.1292/jvms.21-0586 PMID: 35082195
-
Bourély C, Coeffic T, Caillon J, Thibaut S, Cazeau G, Jouy E, et al. Trends in antimicrobial resistance among Escherichia coli from defined infections in humans and animals. J Antimicrob Chemother. 2020;75(6):1525-9. https://doi.org/10.1093/jac/dkaa022 PMID: 32049276
-
Perestrelo S, Amaro A, Brouwer MSM, Clemente L, Ribeiro Duarte AS, Kaesbohrer A, et al. Building an international One Health strain level database to characterise the epidemiology of AMR threats: ESBL-AmpC producing E. coli as an example-challenges and perspectives. Antibiotics (Basel). 2023;12(3):12. https://doi.org/10.3390/antibiotics12030552 PMID: 36978419
-
O’Doherty J, Leader LFW, O’Regan A, Dunne C, Puthoopparambil SJ, O’Connor R. Over prescribing of antibiotics for acute respiratory tract infections; a qualitative study to explore Irish general practitioners’ perspectives. BMC Fam Pract. 2019;20(1):27. https://doi.org/10.1186/s12875-019-0917-8 PMID: 30764777
-
Meena PR, Priyanka P, Singh AP. Extraintestinal pathogenic Escherichia coli (ExPEC) reservoirs, and antibiotics resistance trends: a one-health surveillance for risk analysis from "farm-to-fork". Lett Appl Microbiol. 2023;76(1):ovac016. https://doi.org/10.1093/lambio/ovac016 PMID: 36688760
-
Hesp A, Veldman K, van der Goot J, Mevius D, van Schaik G. Monitoring antimicrobial resistance trends in commensal Escherichia coli from livestock, the Netherlands, 1998 to 2016. Euro Surveill. 2019;24(25):1800438. https://doi.org/10.2807/1560-7917.ES.2019.24.25.1800438 PMID: 31241037
-
Klein EY, Van Boeckel TP, Martínez EM, Pant S, Gandra S, Levin SA, et al. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A. 2018;115(15):E3463-70. https://doi.org/10.1073/pnas.1717295115 PMID: 29581252
-
Austin DJ, Kristinsson KG, Anderson RM. The relationship between the volume of antimicrobial consumption in human communities and the frequency of resistance. Proc Natl Acad Sci U S A. 1999;96(3):1152-6. https://doi.org/10.1073/pnas.96.3.1152 PMID: 9927709
-
Peñalva G, Högberg LD, Weist K, Vlahović-Palčevski V, Heuer O, Monnet DL, ESAC-Net study group, EARS-Net study group. Decreasing and stabilising trends of antimicrobial consumption and resistance in Escherichia coli and Klebsiella pneumoniae in segmented regression analysis, European Union/European Economic Area, 2001 to 2018. Euro Surveill. 2019;24(46):1900656. https://doi.org/10.2807/1560-7917.ES.2019.24.46.1900656 PMID: 31771708
-
Noyes NR, Slizovskiy IB, Singer RS. Beyond antimicrobial use: a framework for prioritizing antimicrobial resistance interventions. Annu Rev Anim Biosci. 2021;9(1):313-32. https://doi.org/10.1146/annurev-animal-072020-080638 PMID: 33592160
-
World Organisation for Animal Health (WHOA). 8th annual report on antimicrobial agents intended for use in animals. Paris: WHOA; 2024. Available from: https://www.woah.org/app/uploads/2024/05/woah-amu-report-2024-final.pdf
-
The European Commission (EC). Farm to Fork Strategy. Brussels: EC. [Accessed: 12 Jul 2024] Available from: https://food.ec.europa.eu/horizontal-topics/farm-fork-strategy_en
-
European Medicines Agency (EMA). European Surveillance of Veterinary Antimicrobial Consumption (ESVAC): Interactive ESVAC database. Amsterdam: EMA. [Accessed: 6 Apr 2024] Available from: https://www.ema.europa.eu/en/veterinary-regulatory-overview/antimicrobial-resistance-veterinary-medicine/european-surveillance-veterinary-antimicrobial-consumption-esvac-2009-2023
-
Health Products Regulatory Authority (HPRA). Sales of veterinary antibiotics in Ireland during 2022. Dublin: www.hpra.ie. [Accessed: 20 Feb 2025]. Available from: https://assets.hpra.ie/data/docs/default-source/regulatory-report/veterinary-medicines/sales-of-veterinary-antibiotics-in-ireland/report-on-sales-of-veterinary-antibiotics-in-ireland-during-2022.pdf?sfvrsn=e776258f_1
-
Department of Health. Ireland’s National Action Plan on Antimicrobial Resistance. Dublin: gov.ie. [Accessed: 28 Apr 2024] Available from: https://www.gov.ie/en/publication/ec1fdf-irelands-national-action-plan-on-antimicrobial-resistance-2017-2020
-
Dept. of Health and Dept. of Agriculture Food and Marine. Ireland’s second One Health Action Plan on Antimicrobial Resistance 2021-2025 (iNAP2). Dublin: gov.ie; 2021. Available from: https://assets.gov.ie/215951/3a18768d-69dc-40fd-bfe5-ec4b31767d30.pdf
-
O’Neill J. Tackling drug-resistant infections globally: final report and recommendations. 2016. Available from: https://amr-review.org/Publications.html
-
European Food Safety Authority, European Centre for Disease Prevention and Control (ECDC). The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2014. EFSA J. 2015;13(12):4329. https://doi.org/10.2903/j.efsa.2015.4329
-
European Centre for Disease Prevention and Control (ECDC), European Food Safety Authority (EFSA) and European Medicines Agency (EMA). JIACRA IV: Fourth joint inter-agency report on integrated analysis of consumption of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from humans and food-producing animals in the EU/EEA. Stockholm, Parma, Amsterdam: ECDC, EFSA, EMA; 2024. Available from: https://www.ema.europa.eu/en/veterinary-regulatory-overview/antimicrobial-resistance-veterinary-medicine/analysis-antimicrobial-consumption-resistance-jiacra-reports#report-on-2019-21-jiacra-iv-65438
-
Daly M, Powell J, O’Connell NH, Murphy L, Dunne CP. Antimicrobial resistance is prevalent in E.coli and other enterobacterales isolated from public and private drinking water supplies in the republic of ireland. Microorganisms. 2023;11(5):1224. https://doi.org/10.3390/microorganisms11051224 PMID: 37317198
-
Andrade L, Chique C, Hynds P, Weatherill J, O’Dwyer J. The antimicrobial resistance profiles of Escherichia coli and Pseudomonas aeruginosa isolated from private groundwater wells in the Republic of Ireland. Environ Pollut. 2023;317:120817. https://doi.org/10.1016/j.envpol.2022.120817 PMID: 36481470
-
Farrell ML, Joyce A, Duane S, Fitzhenry K, Hooban B, Burke LP, et al. Evaluating the potential for exposure to organisms of public health concern in naturally occurring bathing waters in Europe: A scoping review. Water Res. 2021;206:117711. https://doi.org/10.1016/j.watres.2021.117711 PMID: 34637971
-
Farrell ML, Chueiri A, O’Connor L, Duane S, Maguire M, Miliotis G, et al. Assessing the impact of recreational water use on carriage of antimicrobial resistant organisms. Sci Total Environ. 2023;888:164201. https://doi.org/10.1016/j.scitotenv.2023.164201 PMID: 37196970
-
Byrne AW, Garvan C, Bolton J, Naranjo-Lucena A, Madigan G, McElroy M, et al. Antimicrobial resistance in Escherichia coli isolated from pigs and associations with aggregated antimicrobial usage in Ireland: A herd-level exploration. Zoonoses Public Health. 2024;71(1):71-83. https://doi.org/10.1111/zph.13086 PMID: 37899534
-
Byrne N, O’Neill L, Dίaz JAC, Manzanilla EG, Vale AP, Leonard FC. Antimicrobial resistance in Escherichia coli isolated from on-farm and conventional hatching broiler farms in Ireland. Ir Vet J. 2022;75(1):7. https://doi.org/10.1186/s13620-022-00214-9 PMID: 35459196
-
Prendergast DM, Slowey R, Burgess CM, Murphy D, Johnston D, Morris D, et al. Characterization of cephalosporin and fluoroquinolone resistant Enterobacterales from Irish farm waste by whole genome sequencing. Front Microbiol. 2023;14:1118264. https://doi.org/10.3389/fmicb.2023.1118264 PMID: 37032887
-
Ali S, Ryan L. Antimicrobial susceptibility patterns of community-acquired uropathogenic Escherichia coli, Dublin 2010-2022. Access Microbiol. 2023;5(8):acmi000633.v3. https://doi.org/10.1099/acmi.0.000633.v3 PMID: 37691841
-
Whelan SO, Kyne S, Dore A, Glynn M, Higgins F, Hanahoe B, et al. Paediatric Escherichia coli urinary tract infection: susceptibility trends and clinical management-a retrospective analysis of a 10-year period. Ir J Med Sci. 2024;193(4):1891-900. https://doi.org/10.1007/s11845-024-03670-0 PMID: 38565823
-
Stapleton PJ, Lundon DJ, McWade R, Scanlon N, Hannan MM, O’Kelly F, et al. Antibiotic resistance patterns of Escherichia coli urinary isolates and comparison with antibiotic consumption data over 10 years, 2005-2014. Ir J Med Sci. 2017;186(3):733-41. https://doi.org/10.1007/s11845-016-1538-z PMID: 28054236
-
Central Statistics Office (CSO). Census 2016 Small Area Population Statistics. Cork: CSO. [Accessed: 16 Jan 2022]. Available from: https://www.cso.ie/en/census/census2016reports/census2016smallareapopulationstatistics
-
European Committee on Antimicrobial Susceptibility Testing (EUCAST). Clinical breakpoints and dosing of antibiotics. Växjö: EUCAST; 2024. Available from: https://www.eucast.org/clinical_breakpoints
-
Health Protection Surveillance Centre (HPSC). Surveillance of antimicrobial consumption. Dublin: HPSC. [Accessed: 23 Feb 2025] Available from: https://www.hpsc.ie/a-z/microbiologyantimicrobialresistance/europeansurveillanceofantimicrobialconsumptionesac
-
Norwegian Institute of Public Health (FHI). ATC/DDD Index 2024. Oslo: FHI. [Accessed: 15 Jun 2024]. Available from: https://atcddd.fhi.no/atc_ddd_index
-
European Centre for Disease Prevention and Control (ECDC). Antimicrobial consumption in the EU/EEA (ESAC-Net) - Annual Epidemiological Report for 2022. Stockholm: ECDC; 2023. Available from: https://www.ecdc.europa.eu/en/publications-data/surveillance-antimicrobial-consumption-europe-2022
-
European Medicines Agency (EMA). Annual report on sales of veterinary antimicrobial medicinal products. Amsterdam: EMA. [Accessed: 24 Feb 2025]. Available from: https://www.ema.europa.eu/en/veterinary-regulatory-overview/antimicrobial-resistance-veterinary-medicine/european-surveillance-veterinary-antimicrobial-consumption-esvac-2009-2023#annual-report-on-sales-of-veterinary-antimicrobial-medicinal-products-12821
-
European Centre for Disease Prevention and Control (ECDC). Surveillance Atlas of Infectious Diseases. Stockholm: ECDC. [Accessed: 10 May 2024]. Available from: https://www.ecdc.europa.eu/en/surveillance-atlas-infectious-diseases
-
Keighley C, van Oijen AM, Brentnall SJ, Sanderson-Smith M, Newton P, Miyakis S. Multi-year antimicrobial-resistance trends in urine Escherichia coli isolates from both community-based and hospital-based laboratories of an Australian local health district. J Glob Antimicrob Resist. 2022;31:386-90. https://doi.org/10.1016/j.jgar.2022.11.008 PMID: 36436824
-
Ong A, Mahobia N, Browning D, Schembri M, Somani BK. Trends in antibiotic resistance for over 700,000 Escherichia coli positive urinary tract infections over six years (2014-2019) from a university teaching hospital. Cent European J Urol. 2021;74(2):249-54. https://doi.org/10.5173/ceju.2021.0053 PMID: 34336246
-
Criscuolo NG, Pires J, Zhao C, Van Boeckel TP. resistancebank.org, an open-access repository for surveys of antimicrobial resistance in animals. Sci Data. 2021;8(1):189. https://doi.org/10.1038/s41597-021-00978-9 PMID: 34294731
-
Health Protection and Surveillance Centre (HPSC). Summary of EARS-Net data by pathogen and year. Dublin: HPSC; 2023. Available from: https://www.hpsc.ie/a-z/microbiologyantimicrobialresistance/europeanantimicrobialresistancesurveillancesystemearss/ears-netdataandreports/annualreports/EARS-Net%20National%20Summary_2018-2022_20230918.pdf
-
Sharma NGupta AWalia GBakhshi R. Pattern of antimicrobial resistance of Escherichia coli isolates from urinary tract infection patients: a three year retrospective study. J App Pharm Sci. 2016;6(1):062-065. https://doi.org/10.7324/JAPS.2016.600110
-
Haindongo EH, Ndakolo D, Hedimbi M, Vainio O, Hakanen A, Vuopio J. Antimicrobial resistance prevalence of Escherichia coli and Staphylococcus aureus amongst bacteremic patients in Africa: a systematic review. J Glob Antimicrob Resist. 2023;32:35-43. https://doi.org/10.1016/j.jgar.2022.11.016 PMID: 36526264
-
Health Services Executive (HSE). Urinary Conditions - Antibiotic Prescribing. Dublin: HSE; 2024. Available from: https://www.hse.ie/eng/services/list/2/gp/antibiotic-prescribing/conditions-and-treatments/urinary
-
Health Services Executive (HSE). Preferred antibiotic use in the Community Green/Red Table. Dublin: HSE; 2023. Available from: https://www.hse.ie/eng/services/list/2/gp/antibiotic-prescribing/safe-prescribing/preferred-antibiotic-use-in-the-community-greenred-table.pdf
-
European Medicines Agency (EMA). Sales of veterinary antimicrobial agents in 31 European countries in 2021. Amsterdam: EMA; 2022. Accessed: 24 Feb 2025. Available from: https://www.ema.europa.eu/en/documents/report/sales-veterinary-antimicrobial-agents-31-european-countries-2021-trends-2010-2021-twelfth-esvac_en.pdf
-
Poku E, Cooper K, Cantrell A, Harnan S, Sin MA, Zanuzdana A, et al. Systematic review of time lag between antibiotic use and rise of resistant pathogens among hospitalized adults in Europe. JAC Antimicrob Resist. 2023;5(1):dlad001. https://doi.org/10.1093/jacamr/dlad001 PMID: 36694849
-
Pulingam T, Parumasivam T, Gazzali AM, Sulaiman AM, Chee JY, Lakshmanan M, et al. Antimicrobial resistance: Prevalence, economic burden, mechanisms of resistance and strategies to overcome. Eur J Pharm Sci. 2022;170:106103. https://doi.org/10.1016/j.ejps.2021.106103 PMID: 34936936
-
Kaye KS, Gupta V, Mulgirigama A, Joshi AV, Scangarella-Oman NE, Yu K, et al. Antimicrobial resistance trends in urine Escherichia coli isolates from adult and adolescent females in the United States From 2011 to 2019: rising ESBL strains and impact on patient management. Clin Infect Dis. 2021;73(11):1992-9. https://doi.org/10.1093/cid/ciab560 PMID: 34143881
-
Zay Ya K, Win PTN, Bielicki J, Lambiris M, Fink G. Association between antimicrobial stewardship programs and antibiotic use globally: a systematic review and meta-analysis. JAMA Netw Open. 2023;6(2):e2253806. https://doi.org/10.1001/jamanetworkopen.2022.53806 PMID: 36757700
-
Kelly SA, O’Connell NH, Thompson TP, Dillon L, Wu J, Creevey C, et al. Large-scale characterization of hospital wastewater system microbiomes and clinical isolates from infected patients: profiling of multi-drug-resistant microbial species. J Hosp Infect. 2023;141:152-66. https://doi.org/10.1016/j.jhin.2023.09.001 PMID: 37696473
-
Dembicka KM, Powell J, O’Connell NH, Hennessy N, Brennan G, Dunne CP. Prevalence of linezolid-resistant organisms among patients admitted to a tertiary hospital for critical care or dialysis. Ir J Med Sci. 2022;191(4):1745-50. https://doi.org/10.1007/s11845-021-02773-2 PMID: 34505273
-
Kelly SA, O’Connell NH, Thompson TP, Dillon L, Wu J, Creevey C, et al. Large-scale characterisation of hospital wastewater system and infected patient microbiomes: profiling of multidrug-resistant microbial species. J Hosp Infect. 2023;141:152. https://doi.org/10.1016/j.jhin.2023.09.001 PMID: 37696473

Data & Media loading...
Supplementary data
-
-
Supplement
-
