Prevalence and phenotypic profiles of ESBL-producing Escherichia coli across the human-animal-environment interface: a One-Health surveillance during the first year of implementation of the Tricycle project in Burkina Faso

Abstract

Antimicrobial resistance (AMR) is a major global health threat. The WHO Tricycle protocol applies a “One Health” approach to monitor extended-spectrum beta-lactamase-producing Escherichia coli (ESBL-Ec) in humans, animals, and the environment. This study was aimed at presenting the results of the multi-sectoral surveillance conducted during the first year of the WHO Tricycle project’s implementation in Burkina Faso. A descriptive cross-sectional study was conducted in 2024 in Ouagadougou and Bobo-Dioulasso. Samples included 465 rectal swabs from healthy pregnant women, 3,840 blood cultures, 388 chicken ceca, and 49 environmental water samples. Blood culture isolates were recovered through routine diagnostic procedures. Rectal swabs and chicken caeca were cultured on MacConkey agar supplemented with cefotaxime (CTX), while water samples were cultured on TBX agar supplemented with cefotaxime. Isolates were identified using matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF MS). Antibiotic susceptibility testing was performed using the disk diffusion method, and ESBL production was screened via the double-disk synergy test. ESBL-Ec prevalence was varied across sectors: 66% (307/465) in pregnant women (78.3%; 166/212 in Ouagadougou vs. 55.7%; 141/253 in Bobo-Dioulasso), 1.8% (69/3,840) in blood cultures (69.7%; 69/99 of E. coli isolates) and 29.4% (114/388) in chicken ceca (38.2%; 91/238 in Bobo-Dioulasso vs. 15.3%; 23/150 in Ouagadougou; 54.5% (67/123) in the rainy season vs. 17.7% (47/265) during the dry season). Overall, ESBL-Ec was detected in 77.6% (38/49) of environmental samples, with a higher prevalence in wastewater (87.5%, 28/32) than in river water (58.8%, 10/17). This included 55.6% (5/9) of upstream river samples, 62.5% (5/8) of downstream river samples, 83.3% (10/12) of wastewater treatment plant influent samples, 66.7% (4/6) of treated effluent samples, and in all slaughterhouse wastewater samples collected before (8/8) and after treatment (6/6). Median concentrations of total E. coli and ESBL-Ec ranged from 4.6 to 7.3 log CFU/100 mL and 3 to 6 log CFU/100 mL, respectively, across the sampled sites in environment ( p < 0.001). Multivariable analysis identified sampling location as the only independent predictor of ESBL-Ec carriage among pregnant women, whereas in poultry, ESBL-Ec prevalence was significantly associated with both the rainy season and sampling in Bobo-Dioulasso ( p < 0.001). Blood culture isolates showed the highest resistance rates, particularly to fluoroquinolones (80% to ciprofloxacin), aminoglycosides (43% to gentamicin), and cotrimoxazole (91%), compared with isolates from human carriage, food chain, or the environment. These findings highlight the high prevalence and broad distribution of ESBL-Ec across various sectors in Burkina Faso, underscoring the urgent need to enhance hygiene practices, strengthen integrated surveillance, and promote rational antibiotic use. Further genomic investigations are needed to clarify transmission pathways across sectors.