Risk Factors, Temporal Dependence, and Seasonality of Human Extended-Spectrum β-Lactamases-Producing Escherichia coli and Klebsiella pneumoniae Colonization in Malawi: A Longitudinal Model-Based Approach.


Journal

Clinical infectious diseases : an official publication of the Infectious Diseases Society of America
ISSN: 1537-6591
Titre abrégé: Clin Infect Dis
Pays: United States
ID NLM: 9203213

Informations de publication

Date de publication:
05 07 2023
Historique:
received: 08 11 2022
medline: 6 7 2023
pubmed: 5 3 2023
entrez: 4 3 2023
Statut: ppublish

Résumé

Sub-Saharan Africa has the highest estimated death rate attributable to antimicrobial resistance, especially from extended-spectrum β-lactamase-producing Enterobacterales (ESBL-E). However, the dynamics of human colonization in the community with ESBL-E are not well described. Inadequate water, sanitation, and hygiene infrastructure and associated behaviors are believed to play an important role in transmission of ESBL-E, and an improved understanding of the temporal dynamics of within-household transmission could help inform the design of future policies. In this 18-month study, using microbiological data and household surveys, we built a multivariable hierarchical harmonic logistic regression model to identify risk factors for colonization with ESBL-producing Escherichia coli and Klebsiella pneumoniae, reflecting household structure and temporal correlation of colonization status. Being male was associated with a lower risk of colonization with ESBL-producing E. coli (odds ratio [OR], 0.786; credible interval [CrI], .678-.910), whereas the use of a tube well or a borehole was associated with an increased risk (OR, 1.550; CrI, 1.003-2.394). For ESBL-producing K. pneumoniae, recent antibiotic exposure increased risk of colonization (OR, 1.281; CrI, 1.049-1.565), whereas sharing plates decreased that risk (OR, 0.672; CrI, .460-.980). Finally, the temporal correlation range of 8 to 11 weeks provided evidence that within-household transmission occurs within this time frame. We describe different risks for colonization with different enteric bacterial species. Our findings suggest interventions to reduce transmission targeted at the household level need to focus on improving water, sanitation, and hygiene infrastructure and associated behaviors, whereas at the community level, they should focus on both environmental hygiene and antibiotic stewardship.

Sections du résumé

BACKGROUND
Sub-Saharan Africa has the highest estimated death rate attributable to antimicrobial resistance, especially from extended-spectrum β-lactamase-producing Enterobacterales (ESBL-E). However, the dynamics of human colonization in the community with ESBL-E are not well described. Inadequate water, sanitation, and hygiene infrastructure and associated behaviors are believed to play an important role in transmission of ESBL-E, and an improved understanding of the temporal dynamics of within-household transmission could help inform the design of future policies.
METHODS
In this 18-month study, using microbiological data and household surveys, we built a multivariable hierarchical harmonic logistic regression model to identify risk factors for colonization with ESBL-producing Escherichia coli and Klebsiella pneumoniae, reflecting household structure and temporal correlation of colonization status.
RESULTS
Being male was associated with a lower risk of colonization with ESBL-producing E. coli (odds ratio [OR], 0.786; credible interval [CrI], .678-.910), whereas the use of a tube well or a borehole was associated with an increased risk (OR, 1.550; CrI, 1.003-2.394). For ESBL-producing K. pneumoniae, recent antibiotic exposure increased risk of colonization (OR, 1.281; CrI, 1.049-1.565), whereas sharing plates decreased that risk (OR, 0.672; CrI, .460-.980). Finally, the temporal correlation range of 8 to 11 weeks provided evidence that within-household transmission occurs within this time frame.
CONCLUSIONS
We describe different risks for colonization with different enteric bacterial species. Our findings suggest interventions to reduce transmission targeted at the household level need to focus on improving water, sanitation, and hygiene infrastructure and associated behaviors, whereas at the community level, they should focus on both environmental hygiene and antibiotic stewardship.

Identifiants

pubmed: 36869813
pii: 7069457
doi: 10.1093/cid/ciad117
pmc: PMC10320086
doi:

Substances chimiques

beta-Lactamases EC 3.5.2.6
Anti-Bacterial Agents 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1-8

Subventions

Organisme : Medical Research Council
ID : MR/S004793/1
Pays : United Kingdom
Organisme : Department of Health
Pays : United Kingdom

Informations de copyright

© The Author(s) 2023. Published by Oxford University Press on behalf of Infectious Diseases Society of America.

Déclaration de conflit d'intérêts

Potential conflicts of interest. N. F. reports grants or contracts for Environmental Surveillance for Vaccine Impact Assessment (BMGF 2022-2025), for Global Health Professorship from NIHR (NIHR 2022-2027), for NeoTrack from BMGF (BMGF 2021-2023), from UKRI as the co-investigator for Strength in Places (UKRI 202-2025), and for Chatinkha Seq from BMGF (BMGF 2020-2022); participation in a Data Safety Monitoring or Advisory Board for a Phase 2 trial to assess the safety and immunogenicity of Trivalent Salmonella Conjugate Vaccine with the Centre for Vaccine Development, University of Maryland; roles as Chair of Wellcome's Surveillance and Epidemiology of Drug Resistant Infections and Chair of UK Department of Health and Social Care's Fleming Fund Technical Advisory Group. All other authors report no potential conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.

Références

Nutrients. 2019 Apr 05;11(4):
pubmed: 30959779
Environ Sci Technol. 2017 Oct 17;51(20):11537-11552
pubmed: 28926696
PLOS Glob Public Health. 2022 Jun 8;2(6):e0000314
pubmed: 36962375
Glob Health Action. 2019;12(1):1639388
pubmed: 31339473
Environ Sci Technol. 2017 Aug 1;51(15):8725-8734
pubmed: 28686435
Antimicrob Agents Chemother. 2015;59(6):3652-5
pubmed: 25845871
PLoS One. 2016 Dec 9;11(12):e0168024
pubmed: 27936054
PLoS One. 2018 Aug 13;13(8):e0200894
pubmed: 30102698
J Antimicrob Chemother. 2020 Mar 1;75(3):492-507
pubmed: 31742611
JAMA. 2004 Jun 2;291(21):2607-15
pubmed: 15173152
Lancet Infect Dis. 2017 Oct;17(10):1042-1052
pubmed: 28818544
Am J Trop Med Hyg. 2018 Jul;99(1):233-238
pubmed: 29692302
Trans R Soc Trop Med Hyg. 2014 Jun;108(6):313-25
pubmed: 24812065
Am J Trop Med Hyg. 2018 Mar;98(3):803-813
pubmed: 29363444
Int J Environ Res Public Health. 2020 Sep 15;17(18):
pubmed: 32942533
Trop Med Int Health. 2018 Jan;23(1):2-9
pubmed: 29121443
Lancet. 2022 Feb 12;399(10325):629-655
pubmed: 35065702
Trop Med Int Health. 2020 Aug;25(8):1016-1023
pubmed: 32406987
Clin Infect Dis. 2016 Aug 1;63(3):310-8
pubmed: 27143671
Wellcome Open Res. 2019 Oct 23;4:160
pubmed: 31976380
Integr Environ Assess Manag. 2020 Nov;16(6):871-884
pubmed: 32048797
Int J Environ Res Public Health. 2019 Jun 17;16(12):
pubmed: 31213008
BMC Infect Dis. 2016 Apr 29;16:187
pubmed: 27129719
Antimicrob Resist Infect Control. 2021 Jan 22;10(1):18
pubmed: 33482919
Clin Microbiol Infect. 2016 Oct;22(10):891.e1-891.e4
pubmed: 27404368
Nat Microbiol. 2022 Oct;7(10):1593-1604
pubmed: 36065064

Auteurs

Melodie Sammarro (M)

Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Centre for Health Informatics, Computing, and Statistics, Lancaster University, Lancaster, United Kingdom.

Barry Rowlingson (B)

Centre for Health Informatics, Computing, and Statistics, Lancaster University, Lancaster, United Kingdom.

Derek Cocker (D)

Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Malawi-Liverpool-Wellcome Research Programme, Kamuzu University of Health Sciences, Blantyre, Malawi.

Kondwani Chidziwisano (K)

Centre for Water, Sanitation, Health and Appropriate Technology Development (WASHTED), Malawi University of Business and Applied Sciences (MUBAS), Blantyre, Malawi.
Department of Civil and Environmental Engineering, University of Strathclyde, Glasgow, United Kingdom.

Shevin T Jacob (ST)

Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Global Health Security Department, Infectious Disease Institute, Makerere University, Kampala, Uganda.

Henry Kajumbula (H)

Department of Medical Microbiology, College of Health Sciences, Makerere University, Kampala, Uganda.

Lawrence Mugisha (L)

College of Veterinary Medicine, Animal Resources and Biosecurity (COVAB), Makerere University, Kampala, Uganda.
Conservation & Ecosystem Health Alliance, Kampala, Uganda.

David Musoke (D)

Department of Disease Control and Environmental Health, College of Health Sciences, Makerere University, Kampala, Uganda.

Rebecca Lester (R)

Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Malawi-Liverpool-Wellcome Research Programme, Kamuzu University of Health Sciences, Blantyre, Malawi.

Tracy Morse (T)

Centre for Water, Sanitation, Health and Appropriate Technology Development (WASHTED), Malawi University of Business and Applied Sciences (MUBAS), Blantyre, Malawi.
Department of Civil and Environmental Engineering, University of Strathclyde, Glasgow, United Kingdom.

Nicholas Feasey (N)

Department of Clinical Sciences, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.
Malawi-Liverpool-Wellcome Research Programme, Kamuzu University of Health Sciences, Blantyre, Malawi.

Chris Jewell (C)

Centre for Health Informatics, Computing, and Statistics, Lancaster University, Lancaster, United Kingdom.

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