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 and Chidziwisano, Kondwani and Mphasa, Madalitso and Mwapasa, Taonga and Lewis, Joseph M and Rowlingson, Barry and Sammarro, Melodie and Bakali, Winnie and Salifu, Chifundo and Zuza, Allan and Charles, Mary and Mandula, Tamandani and Maiden, Victor and Amos, Stevie and Jacob, Shevin T and Kajumbula, Henry and Mugisha, Lawrence and Musoke, David and Byrne, Rachel and Edwards, Thomas and Lester, Rebecca and Elviss, Nicola and Roberts, Adam P and Singer, Andrew C and Jewell, Christopher and 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. The Lancet Microbe, 4 (7). e534-e543. ISSN 2666-5247 (https://doi.org/10.1016/S2666-5247(23)00062-9)

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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. Funding Medical Research Council, National Institute for Health and Care Research, and Wellcome Trust. Translation For the Chichewa translation of the abstract see Supplementary Materials section.

ORCID iDs

Cocker, Derek, Chidziwisano, Kondwani, Mphasa, Madalitso, Mwapasa, Taonga, Lewis, Joseph M, 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, Elviss, Nicola, Roberts, Adam P, Singer, Andrew C, Jewell, Christopher, Morse, Tracy ORCID logoORCID: https://orcid.org/0000-0003-4185-9471 and Feasey, Nicholas A;
CORE (COnnecting REpositories)