Journal of Applied Microbiology, 2022, 134, 1–12 https://doi.org/10.1093/jambio/lxac059 Advance access publication date: 21 December 2022 Research Article The antibiotic resistome in Escherichia coli isolated from human, food, and animal sources Isadora de Alcântara Rodrigues 1 , Rafaela Gomes Ferrari 2,4,* , Pedro Panzenhagen 2 , Anamaria Mota Pereira dos Santos 2 , Grazielle Lima Rodrigues 2 , Carlos Adam Conte Junior 1,2,3 , Sergio Borges Mano 1 1 Molecular and Analytical Laboratory Center, Department of Food Technology, Faculty of Veterinary, Universidade Federal Fluminense, Rua Miguel de Frias 9, Niterói, RJ 24220-900, Brazil 2 Chemistry Institute, Food Science Program, Universidade Federal do Rio de Janeiro, Av. Pasteur 250, Rio de Janeiro, RJ 21941-901, Brazil 3 National Institute of Health Quality Control, Fundação Oswaldo Cruz, Rio de Janeiro, RJ 21040-900, Brazil 4 Laboratory for the Evaluation of Products of Animal Origin (LAPOA), Center for Agricultural Sciences, Department of Animal Science, Federal University of Paraíba, Cidade Universitária, João Pessoa, Areia, PB 58397-000, Brazil ∗ Corresponding author. Chemistry Institute, Food Science Program, Universidade Federal do Rio de Janeiro, Av. Pasteur 250, Rio de Janeiro, RJ 21941-901, Brazi. E-mail: rafaela.ferrari@academico.ufpb.br Abstract Aims: The aim of this study was to analyze and compare the prevalence and distribution of resistance genes in Escherichia coli genomes isolated from human clinical samples and animal-based foods worldwide. Methods and results: We download from NCBI Pathogen Detection Database the corresponding metadata of the 7,123 E. coli genome to access the information about the antimicrobial resistance gene content. The geographic location and the source of isolation were also obtained and compiled with the antimicrobial resistance gene for statistical analysis, results and discussion. Our criteria considered four groups for analyzing the antimicrobial resistance gene distribution. The first group of genomes from invasive clinical human (ICH) samples from countries with Human Development Index (HDI) ≥ 0.850; the second group of ICH from countries with an HDI ≤ 0.849; the third group of animal-based foods (ABF) from countries with HDI ≥ 0.850 and the fourth group of ABFs from countries with HDI ≤ 0.849. The most prevalent genes in the first group were blaCTX-M-134 (96.53%) and blaCTX-M-27 (86.35%). In the second group, ere(A) (95.96%), soxS (94.49%), qepA8 (90.81%), blaCTX-M-15 (85.66%), and fosA3 (80.88%). In the third group, the most frequently detected were aadA12 (98.5%), ant(3”) (89.92%), and blaCARB-2 (87.2%). In the fourth group, aadA12 and aac(3)-IV were identified in 100% of the analyzed genomes. Conclusions: It was clear that the use of aminoglycosides in animal production is increasing the selective pressure on micro-organisms in both groups of countries since genes linked to aminoglycoside resistance are related to E. coli from ABF samples. The genomic profile of E. coli from HDI ≥ 0.850 countries indicates a selective pressure aimed at cephalosporins given the high prevalence in both sources. Significance and impact of study: Through our study, we observed how one of the most lethal micro-organisms, E. coli, is armed against antimicrobials. This study revealed the need for new policies to combat antimicrobial resistance, especially concerning aminoglycosides and cephalosporins in animal production and human clinical practice, respectively. Keywords: antibiotic resistance genes, animal-based foods, invasive bacteria, food-borne bacteria Introduction Escherichia coli is a micro-organism that is part of the gram- negative Enterobacteriaceae family. This bacterium is found in the environment and food and composes the normal mi- crobiota of humans and animals. When it is in its commensal form, it does not cause problems; however, it can cause illness when an imbalance occurs in the organism (Kaper et al. 2004). In addition, some pathogenic E. coli pathovars can cause in- testinal infections, acquired mainly through the consumption of contaminated water and animal foods (Glantz and Jacks 1969, FDA 2019). Farm animals, such as cattle, swine, and poultry, spread infections caused by E. coli. These animals can harbor pathogenic E. coli in their feces and are able to trans- mit them to humans through their products, such as meat and milk (Kaper et al. 2004). The E. coli pathovars responsible for causing enteric dis- eases are enterotoxigenic E. coli (traveler’s diarrhea syn- drome), enterohemorrhagic E. coli (hemolytic uremic syn- drome), enteroaggregative E. coli (persistent diarrhea), en- teropathogenic E. coli (in newborn diarrhea), diffusely ad- herent E. coli, and enteroinvasive E. coli (Nataro and Kaper 1998). Pathogenic E. coli is one of the main bacteria caus- ing death from diarrhea worldwide (Khalil et al. 2018). Ad- ditionally, one of the most common extra-intestinal infections caused by pathogenic E. coli thrives in the urinary tract (Kaper et al. 2004). Regarding drug resistance, E. coli has a great ability to ac- quire and disseminate antimicrobial resistance genes (ARGs) through horizontal gene transfer. This mechanism is stimu- lated by the inadequate use of these substances in medicine and animal production, which leads to the selection and dis- Received: April 12, 2022. Revised: September 23, 2022. Accepted: November 24, 2022 C  The Author(s) 2022. Published by Oxford University Press on behalf of Applied Microbiology International. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com Downloaded from https://academic.oup.com/jambio/article/134/2/lxac059/6955818 by guest on 18 March 2023