Intersecting social and environmental determinants of multidrug-resistant urinary tract infections in East Africa beyond antibiotic use.
Humans
Urinary Tract Infections
/ drug therapy
Female
Male
Adult
Anti-Bacterial Agents
/ therapeutic use
Drug Resistance, Multiple, Bacterial
Cross-Sectional Studies
Middle Aged
Young Adult
Bayes Theorem
Adolescent
Tanzania
/ epidemiology
Africa, Eastern
/ epidemiology
Kenya
/ epidemiology
Risk Factors
Uganda
/ epidemiology
Socioeconomic Factors
Aged
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
31 Oct 2024
31 Oct 2024
Historique:
received:
01
03
2024
accepted:
07
10
2024
medline:
1
11
2024
pubmed:
1
11
2024
entrez:
1
11
2024
Statut:
epublish
Résumé
The global health crisis of antibacterial resistance (ABR) poses a particular threat in low-resource settings like East Africa. Interventions for ABR typically target antibiotic use, overlooking the wider set of factors which drive vulnerability and behaviours. In this cross-sectional study, we investigated the joint contribution of behavioural, environmental, socioeconomic, and demographic factors associated with higher risk of multi-drug resistant urinary tract infections (MDR UTIs) in Kenya, Tanzania, and Uganda. We sampled outpatients with UTI symptoms in healthcare facilities and linked their microbiology data with patient, household and community level data. Using bivariate statistics and Bayesian profile regression on a sample of 1610 individuals, we show that individuals with higher risk of MDR UTIs were more likely to have compound and interrelated social and environmental disadvantages: they were on average older, with lower education, had more chronic illness, lived in resource-deprived households, more likely to have contact with animals, and human or animal waste. This suggests that interventions to tackle ABR need to take account of intersectional socio-environmental disadvantage as a priority.
Identifiants
pubmed: 39482320
doi: 10.1038/s41467-024-53253-x
pii: 10.1038/s41467-024-53253-x
doi:
Substances chimiques
Anti-Bacterial Agents
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
9418Subventions
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : RCUK | Medical Research Council (MRC)
ID : MR/S004785/1
Organisme : Scottish Funding Council (SFC)
ID : GCRF Consolidator Award
Organisme : Scottish Funding Council (SFC)
ID : GCRF Consolidator Award
Organisme : RCUK | MRC | Medical Research Foundation
ID : MR/S004785/1
Organisme : RCUK | MRC | Medical Research Foundation
ID : MR/S004785/1
Organisme : RCUK | MRC | Medical Research Foundation
ID : MR/S004785/1
Organisme : Foundation for the National Institutes of Health (Foundation for the National Institutes of Health, Inc.)
ID : U01CA207167
Investigateurs
Annette Aduda
(A)
Alison Elliott
(A)
Catherine Kansiime
(C)
John Maina
(J)
John Stelling
(J)
Informations de copyright
© 2024. The Author(s).
Références
O’Neill, J. Antimicrobial Resistance: Tackling a Crisis for the Health and Wealth of Nations. (Rev. Antimicrob. Resist., 2014).
Murray, C. J. et al. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. Lancet 399, 629–655 (2022).
doi: 10.1016/S0140-6736(21)02724-0
van Duin, D. & Paterson, D. L. Multidrug-resistant bacteria in the community: trends and lessons learned. Infect. Dis. Clin. 30, 377–390 (2016).
Gandra, S. et al. The mortality burden of multidrug-resistant pathogens in India: a retrospective, observational study. Clin. Infect. Dis. 69, 563–570 (2019).
doi: 10.1093/cid/ciy955
pubmed: 30407501
Belete, M. A. & Saravanan, M. A systematic review on drug resistant urinary tract infection among pregnant women in developing Countries in Africa and Asia; 2005–2016. Infect. Drug Resist. 13, 1465–1477 (2020).
doi: 10.2147/IDR.S250654
pubmed: 32547115
pmcid: 7245001
Léger, A. et al. Characterizing social-ecological context and success factors of antimicrobial resistance interventions across the One Health spectrum: analysis of 42 interventions targeting E. coli. BMC Infect. Dis. 21, 873 (2021).
doi: 10.1186/s12879-021-06483-z
pubmed: 34445962
pmcid: 8390193
Davis, A. & Sharp, J. Rethinking one health: emergent human, animal and environmental assemblages. Soc. Sci. Med. 113093 https://doi.org/10.1016/j.socscimed.2020.113093 (2020).
Chatterjee, A. et al. Quantifying drivers of antibiotic resistance in humans: a systematic review. Lancet Infect. Dis. 18, e368–e378 (2018).
doi: 10.1016/S1473-3099(18)30296-2
pubmed: 30172580
Collignon, P., Beggs, J. J., Walsh, T. R., Gandra, S. & Laxminarayan, R. Anthropological and socioeconomic factors contributing to global antimicrobial resistance: a univariate and multivariable analysis. Lancet Planet. Health 2, e398–e405 (2018).
doi: 10.1016/S2542-5196(18)30186-4
pubmed: 30177008
Tompson, A. C., Manderson, L. & Chandler, C. I. R. Understanding antibiotic use: practices, structures and networks. JAC-Antimicrob. Resist. 3, dlab150 (2021).
doi: 10.1093/jacamr/dlab150
pubmed: 34617017
Charani, E. et al. Navigating sociocultural disparities in relation to infection and antibiotic resistance—the need for an intersectional approach. JAC-Antimicrob. Resist. 3, dlab123 (2021).
doi: 10.1093/jacamr/dlab123
pubmed: 34604747
Asiimwe, B. B. et al. Protocol for an interdisciplinary cross-sectional study investigating the social, biological and community-level drivers of antimicrobial resistance (AMR): Holistic Approach to Unravel Antibacterial Resistance in East Africa (HATUA). BMJ Open 11, e041418 (2021).
doi: 10.1136/bmjopen-2020-041418
pubmed: 34006022
pmcid: 7942251
Maldonado-Barragán, A. et al. Predominance of multidrug-resistant (MDR) bacteria causing urinary tract infections (UTIs) among symptomatic patients in East Africa: a call for action. JAC-Antimicrob. Resist. 6, dlae019 (2024).
Silago, V. et al. Multidrug-Resistant uropathogens causing community acquired urinary tract infections among patients attending health facilities in Mwanza and Dar es Salaam, Tanzania. Antibiotics 11, 1718 (2022).
doi: 10.3390/antibiotics11121718
pubmed: 36551375
pmcid: 9774515
Craig, J. et al. Behavior-change interventions to improve antimicrobial stewardship in human health, animal health, and livestock agriculture: a systematic review. PLOS Glob. Public Health 3, e0001526 (2023).
doi: 10.1371/journal.pgph.0001526
pubmed: 37155592
pmcid: 10166487
Graells, T. et al. Studying factors affecting success of antimicrobial resistance interventions through the lens of experience: a thematic analysis. Antibiotics 11, 639 (2022).
doi: 10.3390/antibiotics11050639
pubmed: 35625282
pmcid: 9137464
Costelloe, C., Metcalfe, C., Lovering, A., Mant, D. & Hay, A. D. Effect of antibiotic prescribing in primary care on antimicrobial resistance in individual patients: systematic review and meta-analysis. BMJ 340, c2096 (2010).
doi: 10.1136/bmj.c2096
pubmed: 20483949
Chokshi, A., Sifri, Z., Cennimo, D. & Horng, H. Global contributors to antibiotic resistance. J. Glob. Infect. Dis. 11, 36–42 (2019).
doi: 10.4103/jgid.jgid_110_18
pubmed: 30814834
Ndaki, P. M. et al. Dispensing antibiotics without prescription at community pharmacies and accredited drug dispensing outlets in Tanzania: a cross-sectional study. Antibiotics 10, 1025 (2021).
doi: 10.3390/antibiotics10081025
pubmed: 34439074
Olamijuwon, E. et al. Antibiotic dispensing practices during COVID-19 and implications for antimicrobial resistance (AMR): parallel mystery client studies in Uganda and Tanzania. Antimicrob. Resist. Infect. Control 12, 10 (2023).
doi: 10.1186/s13756-022-01199-4
pubmed: 36774512
pmcid: 9919751
Keenan, K. et al. Unravelling patient pathways in the context of antibacterial resistance in East Africa. BMC Infect. Dis. 23, 414 (2023).
doi: 10.1186/s12879-023-08392-9
pubmed: 37337134
pmcid: 10278291
Green, D. L. et al. The role of multidimensional poverty in antibiotic misuse: a mixed-methods study of self-medication and non-adherence in Kenya, Tanzania, and Uganda. Lancet Glob. Health 11, e59–e68 (2023).
doi: 10.1016/S2214-109X(22)00423-5
pubmed: 36521953
Alividza, V. et al. Investigating the impact of poverty on colonization and infection with drug-resistant organisms in humans: A systematic review. Infect. Dis. Poverty 7, 76 (2018).
doi: 10.1186/s40249-018-0459-7
pubmed: 30115132
pmcid: 6097281
Charani, E. et al. Optimising antimicrobial use in humans – review of current evidence and an interdisciplinary consensus on key priorities for research. Lancet Reg. Health Eur. 7, 100161 (2021).
doi: 10.1016/j.lanepe.2021.100161
pubmed: 34557847
pmcid: 8454847
Tenney, J., Hudson, N., Alnifaidy, H., Li, J. T. C. & Fung, K. H. Risk factors for aquiring multidrug-resistant organisms in urinary tract infections: a systematic literature review. Saudi Pharm. J. 26, 678–684 (2018).
doi: 10.1016/j.jsps.2018.02.023
pubmed: 29991911
pmcid: 6035314
Tilahun, M. et al. Uro-pathogens: multidrug resistance and associated factors of community-acquired UTI among HIV patients attending antiretroviral therapy in Dessie Comprehensive Specialized Hospital, Northeast Ethiopia. PLOS ONE 19, e0296480 (2024).
doi: 10.1371/journal.pone.0296480
pubmed: 38820330
pmcid: 11142584
Larramendy, S. et al. Risk Factors of extended-spectrum Beta-Lactamases-Producing Escherichia coli Community acquired urinary tract infections: a systematic review. Infect. Drug Resist. 13, 3945–3955 (2020).
doi: 10.2147/IDR.S269033
pubmed: 33177845
pmcid: 7650195
Yelin, I. et al. Personal clinical history predicts antibiotic resistance of urinary tract infections. Nat. Med. 25, 1143–1152 (2019).
doi: 10.1038/s41591-019-0503-6
pubmed: 31273328
pmcid: 6962525
Rousham, E. K., Unicomb, L. & Islam, M. A. Human, animal and environmental contributors to antibiotic resistance in low-resource settings: integrating behavioural, epidemiological and One Health approaches. Proc. R. Soc. B Biol. Sci. 285, 20180332 (2018).
doi: 10.1098/rspb.2018.0332
Vikesland, P. et al. Differential drivers of antimicrobial resistance across the World. Acc. Chem. Res. 52, 916–924 (2019).
doi: 10.1021/acs.accounts.8b00643
pubmed: 30848890
Iskandar, K. et al. Drivers of antibiotic resistance transmission in low-and middle-income countries from a “one health” perspective—a review. Antibiotics 9, 1–23 (2020).
doi: 10.3390/antibiotics9070372
Jimenez, C. E. P. et al. Biosecurity and water, sanitation, and hygiene (WASH) interventions in animal agricultural settings for reducing infection burden, antibiotic use, and antibiotic resistance: a One Health systematic review. Lancet Planet. Health 7, e418–e434 (2023).
doi: 10.1016/S2542-5196(23)00049-9
Allel, K. et al. Global antimicrobial-resistance drivers: an ecological country-level study at the human–animal interface. Lancet Planet. Health 7, e291–e303 (2023).
doi: 10.1016/S2542-5196(23)00026-8
pubmed: 37019570
Caudell, M. A. et al. Identification of risk factors associated with carriage of resistant Escherichia coli in three culturally diverse ethnic groups in Tanzania: a biological and socioeconomic analysis. Lancet Planet. Health 2, e489–e497 (2018).
doi: 10.1016/S2542-5196(18)30225-0
pubmed: 30396440
pmcid: 6215761
Cocker, D. et al. Investigating One Health risks for human colonisation with extended spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae in Malawian households: a longitudinal cohort study. Lancet Microbe 4, e534–e543 (2023).
doi: 10.1016/S2666-5247(23)00062-9
pubmed: 37207684
pmcid: 10319635
Sado, K. et al. Treatment seeking behaviours, antibiotic use and relationships to multi-drug resistance: A study of urinary tract infection patients in Kenya, Tanzania and Uganda. PLOS Glob. Public Health 4, e0002709 (2024).
doi: 10.1371/journal.pgph.0002709
pubmed: 38363770
pmcid: 10871516
Hadley, C., Maxfield, A. & Hruschka, D. Different forms of household wealth are associated with opposing risks for HIV infection in East Africa. World Dev. 113, 344–351 (2019).
doi: 10.1016/j.worlddev.2018.09.015
Clinical and Laboratory Standards Institute (CLSI. Performance Standards of Antimicrobial Susceptability Testing, 31st Ed. (Clinical and Laboratory Standards Institute, USA, 2021).
Magiorakos, A.-P. et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect. 18, 268–281 (2012).
doi: 10.1111/j.1469-0691.2011.03570.x
pubmed: 21793988
Benjamini, Y. & Yekutieli, D. The control of the false discovery rate in multiple testing under dependency. Ann. Stat. 29, 1165–1188 (2001).
doi: 10.1214/aos/1013699998
Molitor, J., Papathomas, M., Jerrett, M. & Richardson, S. Bayesian profile regression with an application to the National survey of children’s health. Biostatistics 11, 484–498 (2010).
doi: 10.1093/biostatistics/kxq013
pubmed: 20350957
Papathomas, M., Molitor, J., Hoggart, C., Hastie, D. & Richardson, S. Exploring data from genetic association studies using Bayesian variable selection and the Dirichlet process: application to searching for Gene × Gene Patterns. Genet. Epidemiol. 36, 663–674 (2012).
doi: 10.1002/gepi.21661
pubmed: 22851500
Deltourbe, L., Mariano, L. L., Hreha, T. N., Hunstad, D. A. & Ingersoll, M. A. The impact of biological sex on diseases of the urinary tract. Mucosal Immunol. 15, 857–866 (2022).
doi: 10.1038/s41385-022-00549-0
pubmed: 35869147
pmcid: 9305688
Gautron, J. M. C., Tu Thanh, G., Barasa, V. & Voltolina, G. Using intersectionality to study gender and antimicrobial resistance in low- and middle-income countries. Health Policy Plan. czad054. https://doi.org/10.1093/heapol/czad054 (2023).
R. Core Team. R: A Language and Environment for Statistical Computing Version. R Foundation for Statistical Computing (2023).
Liverani, S., Hastie, D. I., Azizi, L., Papathomas, M. & Richardson, S. PReMiuM: An R Package for Profile Regression Mixture Models Using Dirichlet Processes. J. Stat. Softw. 64, 1–30 (2015).
doi: 10.18637/jss.v064.i07
pubmed: 27307779
pmcid: 4905523