Impact of Antibiotic Therapies on Resistance Genes Dynamic and Composition of the Animal Gut Microbiota

Abstract

Antibiotics are major disruptors of the gastrointestinal microbiota, depleting bacterial species beneficial for the host health and favoring the emergence of potential pathogens. Furthermore, the intestine is a reactor of antibiotic resistance emergence, and the presence of antibiotics exacerbates the selection of resistant bacteria that can disseminate in the environment and propagate to further hosts. We reviewed studies analyzing the effect of antibiotics on the intestinal microbiota and antibiotic resistance conducted on animals, focusing on the main food-producing and companion animals. Irrespective of antibiotic classes and animal hosts, therapeutic dosage decreased species diversity and richness favoring the bloom of potential enteropathogens and the selection of antibiotic resistance. These negative effects of antibiotic therapies seem ineluctable but often were mitigated when an antibiotic was administered by parenteral route. Sub-therapeutic dosages caused the augmentation of taxa involved in sugar metabolism, suggesting a link with weight gain. This result should not be interpreted positively, considering that parallel information on antibiotic resistance selection was rarely reported and selection of antibiotic resistance is known to occur also at low antibiotic concentration. However, studies on the effect of antibiotics as growth promoters put the basis for understanding the gut microbiota composition and function in this situation. This knowledge could inspire alternative strategies to antibiotics, such as probiotics, for improving animal performance. This review encompasses the analysis of the main animal hosts and all antibiotic classes, and highlights the future challenges and gaps of knowledge that should be filled. Further studies are necessary for elucidating pharmacodynamics in animals in order to improve therapy duration, antibiotic dosages, and administration routes for mitigating negative effects of antibiotic therapies. Furthermore, this review highlights that studies on aminoglycosides are almost inexistent, and they should be increased, considering that aminoglycosides are the first most commonly used antibiotic family in companion animals. Harmonization of experimental procedures is necessary in this research field. In fact, current studies are based on different experimental set-up varying for antibiotic dosage, regimen, administration, and downstream microbiota analysis. In the future, shotgun metagenomics coupled with long-reads sequencing should become a standard experimental approach enabling to gather comprehensive knowledge on GIM in terms of composition and taxonomic functions, and of ARGs. Decorticating GIM in animals will unveil revolutionary strategies for medication and improvement of animals’ health status, with positive consequences on global health.

Short-Term Impact of Oxytetracycline Administration on the Fecal Microbiome, Resistome and Virulome of Grazing Cattle

“…We observed that the microbiome diversity of treated cattle was significantly disturbed in the short term, increasing ARGs conferring resistance to tetracyclines compared to control animals without exposure to OTC. This finding is consistent with previous studies that reported the perturbation of the gut microbiome following antibiotic treatment within a few days after antibiotic exposure [ 25 , 26 , 27 ].…”

Longitudinal study of the short- and long-term effects of hospitalisation and oral trimethoprim-sulfadiazine administration on the equine faecal microbiome and resistome

“…Generally, in all animals, irrespective of the type of antimicrobial administered, a decrease in species richness and alpha-diversity is observed [ 45 ], as was also the case in our study. The most profound effects of TMS on the intestinal microbiota were observed immediately after treatment, which is in line with previous reports that also demonstrated a rapid, significant decrease in alpha-diversity [ 5 , 35 , 46 ].…”

“…In the current study, we did not observe a significant effect of hospitalisation without treatment on microbiota composition, but this might result from the small number of animals making it difficult to observe subtle changes. To our knowledge, no next-generation sequencing studies have been performed on horses to evaluate Generally, in all animals, irrespective of the type of antimicrobial administered, a decrease in species richness and alpha-diversity is observed [45], as was also the case in our study. The most profound effects of TMS on the intestinal microbiota were observed immediately after treatment, which is in line with previous reports that also demonstrated a rapid, significant decrease in alpha-diversity [5,35,46].…”

Comparing the transmission of carbapenemase-producing and extended-spectrum beta-lactamase-producingEscherichia colibetween broiler chickens

“…Twenty-two per cent of the conventional broiler farms in the Netherlands did not use antibiotics in 2020, but 44% had a persistently high antibiotic usage exceeding the action threshold defined by the Netherlands Veterinary Medicines Institute and 5% had a persistently high antibiotic usage exceeding the sector-negotiated action threshold (Bonten et al, 2021). Treatment with antibiotics generally temporarily decreases the number of bacterial species in the gut microbiome and lowers the abundance of some common taxa, allowing the abundance of some low-abundant taxa or opportunistic pathogens to increase (Kim et al, 2017; Rochegüe et al, 2021). This might affect the transmission of bacteria, because a more diverse gut microbiome hinders colonization by exogenous bacteria (Kim et al, 2017; Sorbara and Pamer, 2019), thereby reducing the excretion of these bacteria (Dame-Korevaar et al, 2020b).…”