Carriage of Extended Spectrum Beta-Lactamase and Carbapenemase Genes in Food Animals and Their Human Handlers: A One Health Perspective in a Low-Resource Setting in Africa

Abstract

We investigated fecal colonization with third-generation cephalosporin-resistant (3GC-r) Enterobacterales and carbapenem-resistant Enterobacterales among food animals and their handlers in Ghana. A total of 252 fecal samples were collected from 211 animals and 41 human handlers across 20 farms between May and August 2023. Enterobacterales were isolated using standard methods and identified using Matrix-Assisted Laser Desorption/Ionization Time-of-Flight Mass Spectrometry fingerprints and 16SrRNA sequencing. Antibiotic susceptibility testing was done using standard methods. Extended spectrum beta-lactamase (ESBL) and carbapenemase genes were identified by PCR and sequencing. A total of 264 Enterobacterales were isolated, comprising 44 from human handlers and 220 from food animals. Among human isolates, 31 (70.5%) were 3GC-r, with 9 (20.5%) expressing the ESBL phenotype and 2 (4.5%) producing carbapenemases. The most common ESBL genes detected were bla_CTX-M-15 (n = 5/9) and bla_CTX-M-14 (n = 2/9), while carbapenemase-producing isolates harbored bla_NDM-1 (n = 1/2) or bla_IMP-1 (n = 1/2). In food animals, 94 (42.7%) of Enterobacterales isolates were 3GC-r, with 11 (5.0%) carrying ESBL genes, predominantly bla_CTX-M-15 (n = 5/11). One E. coli isolate exhibited carbapenemase production (bla_NDM-1) with an ESBL gene (bla_CTX-M-1). Meropenem was the most effective antibiotic agent against the study isolates (≤5% resistance). Concordance of isolate/resistance gene combinations was observed at three farms where at least one human handler and at least one farm animal carried the same 3GC-r Escherichia coli with the same resistance genes, including bla_CTX-M-15, bla_TEM-10, and bla_NDM-1. The findings indicate a potential for zoonotic transmission of resistance genes between food animals and their human handlers.