Hidden Places for Foodborne Bacterial Pathogens and Novel Approaches to Control Biofilms in the Meat Industry

Abstract

Biofilms are of great concern for the meat industry because, despite the implementation of control plans, they remain important hotspots of contamination by foodborne pathogens, highlighting the need to better understand the ecology of these microecosystems. The objective of this paper was to critically survey the recent scientific literature on microbial biofilms of importance for meat safety and quality, also pointing out the most promising methods to combat them. For this, the databases PubMed, Scopus, Science Direct, Web of Science, and Google Scholar were surveyed in a 10-year time frame (but preferably papers less than 5 years old) using selected keywords relevant for the microbiology of meats, especially considering bacteria that are tolerant to cleaning and sanitization processes. The literature findings showed that massive DNA sequencing has deeply impacted the knowledge on the species that co-habit biofilms with important foodborne pathogens (Listeria monocytogenes, Salmonella, pathogenic Escherichia coli, and Staphylococcus aureus). It is likely that recalcitrant commensal and/or spoilage microbiota somehow protect the more fastidious organisms from harsh conditions, in addition to harboring antimicrobial resistance genes. Among the members of background microbiota, Pseudomonas, Acinetobacter, and Enterobacteriales have been commonly found on food contact and non-food contact surfaces in meat processing plants, in addition to less common genera, such as Psychrobacter, Enhydrobacter, Brevundimonas, and Rothia, among others. It has been hypothesized that these rare taxa may represent a primary layer in microbial biofilms, offering better conditions for the adhesion of otherwise poor biofilm formers, especially considering their tolerance to cold conditions and sanitizers. Taking into consideration these findings, it is not only important to target the foodborne pathogens per se in cleaning and disinfection plans but the use of multiple hurdles is also recommended to dismantle the recalcitrant structures of biofilms. In this sense, the last part of this manuscript presents an updated overview of the antibiofilm methods available, with an emphasis on eco-friendly approaches.

Keywords: biofilm control; biofilm microbiota; foodborne pathogens; meat processing; meats; multispecies biofilms.

Figure 1

Stages of biofilm formation on industrial surfaces used for food handling. Planktonic cells approach food contact and or non-food contact surfaces and, depending on physico-chemical factors, can reversibly adhere and multiply. These initial steps may be guided by cell-to-cell communication mediated by Quorum-Sensing (QS) signaling molecules. Next, the sessile microorganisms form a matrix composed of Extracellular Polymeric Substances (EPSs), which characterize a mature biofilm, and the cells adhere irreversibly. Finally, mature biofilms can shed cells with the ability to colonize other sites in a process called dispersion, which can be mediated by several mechanisms. Source: the authors, based on [1].

Figure 2

Intercommunication between two microbial populations (symbolized by black and red elongated circles): (A) Mutualism both organisms benefit from the association. E.g.: cross-feeding, with reciprocal benefits for both organisms by exchanging metabolites or by removing one another’s inhibitory substances (symbolized by blue and green bubbles). (B) Commensalism one organism is favoured, with no harm to the other. E.g.: one organism scavenges products released by the other (symbolized by blue bubbles), with no prejudice for the latter. (C) Amensalism one organism thrives at the expense of its partner (symbolized by black X). E.g.: production of antimicrobial compounds and competition by nutrients. (D) Neutralism two organisms live in the same microenvironment but there is no interaction between them. Source: the authors, based on Islam et al. [10].

Figure 3

Main hotspots for biofilm formation in meat processing industries. (A,D) Grooves and cracks in plastic surfaces caused by excessive handling time or friction with bony parts of meat cuts. (B) Table edges, prominent welds, and hidden corners. (C) Accumulation of organic matter on discs and knives used for cutting meat. (E,F) Excessive condensation and accumulation of organic material in areas that are difficult to access for cleaning, such as areas near walls (back of equipment) and fan blades. (G) Accumulation of waste (meat particles, fat, blood, and other organic material) in drains. Source: the authors.

Figure 4

Basic mechanisms of promising technologies for controlling microbial biofilms in industrial environments. Source: the authors.