Foodborne Microbial Communities as Potential Reservoirs of Antimicrobial Resistance Genes for Pathogens: A Critical Review of the Recent Literature

Abstract

Antimicrobial resistance (AMR) is a global and increasing threat to human health. Several genetic determinants of AMR are found in environmental reservoirs, including bacteria naturally associated with widely consumed fermented foods. Through the food chain, these bacteria can reach the gut, where horizontal gene transfer (HGT) can occur within the complex and populated microbial environment. Numerous studies on this topic have been published over the past decades, but a conclusive picture of the potential impact of the non-pathogenic foodborne microbial reservoir on the spread of AMR to human pathogens has not yet emerged. This review critically evaluates a comprehensive list of recent experimental studies reporting the isolation of AMR bacteria associated with fermented foods, focusing on those reporting HGT events, which represent the main driver of AMR spread within and between different bacterial communities. Overall, our analysis points to the methodological heterogeneity as a major weakness impairing determination or a causal relation between the presence of AMR determinants within the foodborne microbial reservoir and their transmission to human pathogens. The aim is therefore to highlight the main gaps and needs to better standardize future studies addressing the potential role of non-pathogenic bacteria in the spread of AMR.

Keywords: antibiotic resistance; conjugation; lactic acid bacteria; mobile elements; one health.

Figure 1

Frequency of occurrence of fermented food matrices and their geographical origin in the analyzed studies. (a) Distribution of the analyzed fermented foods within the three categories of food matrices (dairy, plant, meat/fish); (b) Geographical origin of the fermented foods, analyzed in the studies, expressed as their percentage originating from each continent. The food products originating from Turkey, a trans-continental country belonging to both Europe and Asia, were assigned to the Asian continent, which includes the vast majority of the Turkish territory; (c) World map showing the distribution of fermented foods analyzed in each country. The number of food products/country spans between 1 and 10 and is represented by a color gradient (the world map was created with Microsoft Excel using Bing technology).

Figure 2

Taxonomical identity of AMR bacteria and their distribution in the different food matrices. (a) Number of studies identifying each of the indicated genera among AMR bacteria. Two of the analyzed studies are not represented ([26,56]), as they analyzed the food metagenome and did not report the isolation of specific AMR species/strains; (b) Percent occurrence of the AMR genera shown in panel (a) within the three fermented food categories. Dairy matrices are represented by the black portion of the bars, plant-derived matrices are shown in dark gray; meat or fish matrices are shown in light gray. The graph shows only the genera that were reported in at least 4 studies in panel (a).