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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

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  • Derek Cocker
  • Kondwani Chidziwisano
  • Madalitso Mphasa
  • Taonga Mwapasa
  • Joseph M Lewis
  • Winnie Bakali
  • Chifundo Salifu
  • Allan Zuza
  • Mary Charles
  • Tamandani Mandula
  • Victor Maiden
  • Stevie Amos
  • Shevin T Jacob
  • Henry Kajumbula
  • Lawrence Mugisha
  • David Musoke
  • Rachel Byrne
  • Thomas Edwards
  • Rebecca Lester
  • Nicola Elviss
  • Adam P Roberts
  • Andrew C Singer
  • Tracy Morse
  • Nicholas A Feasey
<mark>Journal publication date</mark>31/07/2023
<mark>Journal</mark>The Lancet. Microbe
Issue number7
Number of pages10
Pages (from-to)e534-e543
Publication StatusPublished
Early online date16/05/23
<mark>Original language</mark>English


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.