A review of the impact of food processing on antimicrobial-resistant bacteria in secondary processed meats and meat products

Abstract

For meat and meat products, secondary processes are those that relate to the downstream of the primary chilling of carcasses. Secondary processes include maturation chilling, deboning, portioning, mincing and other operations such as thermal processing (cooking) that create fresh meat, meat preparations and ready-to-eat meat products. This review systematically identified and summarised information relating to antimicrobial resistance (AMR) during the manufacture of secondary processed meatand meat products (SPMMP). Systematic searching of eight literature databases was undertaken and the resultantpapers were appraised for relevance to AMR and SPMMP. Consideration was made that the appraisal scores, undertaken by different reviewers, were consistent. Appraisal reduced the 11,000 initially identified documents to 74, which indicated that literature relating to AMR and SPMMP was not plentiful. A wide range of laboratory methods and breakpoint values (i.e. the concentration of antimicrobial used to assess sensitivity, tolerance or resistance) were used for the isolation of AMR bacteria.The identified papers provided evidence that AMR bacteria could be routinely isolated from SPMMP. There was no evidence that either confirmed or refuted that genetic materials capable of increasing AMR in non-AMR bacteria were present unprotected (i.e. outside of a cell or a capsid) in SPMMP. Statistical analyses were not straightforward because different authors used different laboratory methodologies.However, analyses using antibiotic organised into broadly-related groups indicated that Enterobacteriaceaeresistant to third generation cephalosporins might be an area of upcoming concern in SPMMP. The effective treatment of patients infected with Enterobacteriaceaeresistant to cephalosporins are a known clinical issue. No AMR associations with geography were observed and most of the publications identified tended to be from Europe and the far east.AMR Listeria monocytogenes and lactic acid bacteria could be tolerant to cleaning and disinfection in secondary processing environments. The basis of the tolerance could be genetic (e.g. efflux pumps) or environmental (e.g. biofilm growth). Persistent, plant resident, AMR L. monocytogenes were shown by one study to be the source of final product contamination. 4 AMR genes can be present in bacterial cultures used for the manufacture of fermented SPMMP. Furthermore, there was broad evidence that AMR loci could be transferred during meat fermentation, with refrigeration temperatures curtailing transfer rates. Given the potential for AMR transfer, it may be prudent to advise food business operators (FBOs) to use fermentation starter cultures that are AMR-free or not contained within easily mobilisable genetic elements. Thermal processing was seen to be the only secondary processing stage that served as a critical control point for numbers of AMR bacteria. There were significant linkages between some AMR genes in Salmonella. Quaternary ammonium compound (QAC) resistance genes were associated with copper, tetracycline and sulphonamide resistance by virtue of co-location on the same plasmid. No evidence was found that either supported or refuted that there was any association between AMR genes and genes that encoded an altered stress response or enhanced the survival of AMR bacteria exposed to harmful environmental conditions.