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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

Cocker, Derek, Chidziwisano, Kondwani, Mphasa, Madalitso, Mwapasa, Taonga, Lewis, Joseph ORCID: https://orcid.org/0000-0002-3837-5188, Rowlingson, Barry, Sammarro, Melodie, Bakali, Winnie, Salifu, Chifundo, Zuza, Allan, Charles, Mary, Mandula, Tamandani, Maiden, Victor, Amos, Stevie, Jacob, Shevin T, Kajumbula, Henry, Mugisha, Lawrence, Musoke, David, Byrne, Rachel, Edwards, Thomas, Lester, Rebecca ORCID: https://orcid.org/0000-0002-0259-9630, Elviss, Nicola, Roberts, Adam ORCID: https://orcid.org/0000-0002-0760-3088, Singer, Andrew C, Jewell, Christopher, Morse, Tracy and Feasey, Nicholas A (2023) '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, Vol 4, Issue 7, e534-e543.

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Abstract

Background
Low-income countries have high morbidity and mortality from drug-resistant infections, especially from enteric bacteria such as Escherichia coli. In these settings, sanitation infrastructure is of variable and often inadequate quality, creating risks of extended-spectrum β-lactamase (ESBL)-producing Enterobacterales transmission. We aimed to describe the prevalence, distribution, and risks of ESBL-producing Enterobacterales colonisation in sub-Saharan Africa using a One Health approach.

Methods
Between April 29, 2019, and Dec 3, 2020, we recruited 300 households in Malawi for this longitudinal cohort study: 100 each in urban, peri-urban, and rural settings. All households underwent a baseline visit and 195 were selected for longitudinal follow-up, comprising up to three additional visits over a 6 month period. Data on human health, antibiotic usage, health-seeking behaviours, structural and behavioural environmental health practices, and animal husbandry were captured alongside human, animal, and environmental samples. Microbiological processing determined the presence of ESBL-producing E coli and Klebsiella pneumoniae, and hierarchical logistic regression was performed to evaluate the risks of human ESBL-producing Enterobacterales colonisation.

Findings
A paucity of environmental health infrastructure and materials for safe sanitation was identified across all sites. A total of 11 975 samples were cultured, and ESBL-producing Enterobacterales were isolated from 1190 (41·8%) of 2845 samples of human stool, 290 (29·8%) of 973 samples of animal stool, 339 (66·2%) of 512 samples of river water, and 138 (46·0%) of 300 samples of drain water. Multivariable models illustrated that human ESBL-producing E coli colonisation was associated with the wet season (adjusted odds ratio 1·66, 95% credible interval 1·38–2·00), living in urban areas (2·01, 1·26–3·24), advanced age (1·14, 1·05–1·25), and living in households where animals were observed interacting with food (1·62, 1·17–2·28) or kept inside (1·58, 1·00–2·43). Human ESBL-producing K pneumoniae colonisation was associated with the wet season (2·12, 1·63–2·76).

Interpretation
There are extremely high levels of ESBL-producing Enterobacterales colonisation in humans and animals and extensive contamination of the wider environment in southern Malawi. Urbanisation and seasonality are key risks for ESBL-producing Enterobacterales colonisation, probably reflecting environmental drivers. Without adequate efforts to improve environmental health, ESBL-producing Enterobacterales transmission is likely to persist in this setting.

Item Type: Article
Subjects: WA Public Health > WA 30 Socioeconomic factors in public health (General)
WA Public Health > Sanitation. Environmental Control > General Sanitation and Environmental Control > WA 670 General works
WC Communicable Diseases > Infection. Bacterial Infections > Enteric Infections > WC 290 Escherichia coli infections
Faculty: Department: Biological Sciences > Department of Tropical Disease Biology
Clinical Sciences & International Health > Clinical Sciences Department
Education
Digital Object Identifer (DOI): https://doi.org/10.1016/S2666-5247(23)00062-9
SWORD Depositor: JISC Pubrouter
Depositing User: JISC Pubrouter
Date Deposited: 19 May 2023 10:57
Last Modified: 11 Jul 2023 09:00
URI: https://archive.lstmed.ac.uk/id/eprint/22524

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