Food Protection Trends - September/October 2017 - 357

the same or multi-species communities are enclosed in a
self-produced polymeric matrix (25). Biofilms are found in
animals and humans, on horticulture crops, in primary production environments and in water sources, and potentially
on every non-sterile surface along the food chain (17).
While biofilms can offer a safe haven for its resident bacteria
and protect them from antimicrobials, they may also be a
niche for facilitation of AMR emergence and transmission
(25). In biofilms, bacteria are present in high density and
in close contact; the matrix concentrates nutrients and
compounds that facilitate cell interaction and protects the
bacteria from biotic and abiotic exposures. Periodically
bacteria-laden fragments slough off, disseminating contamination. Biofilms provide ideal protective structures that
can enhance transfer of genetic elements, bacterial fitness
and persistence and, in reverse, these elements may even
promote biofilm formation.
Alexander Fleming was already aware of the potential
risk of antimicrobial resistance, noting during his Nobel
Prize speech that "there is the danger, that the ignorant man
may easily under dose himself and by exposing his microbes
to non-lethal quantities of the drug make them resistant"
(15). He may not have realized the extent to which his
observation would become a reality or the extent to which
resistant organisms could emerge in non-clinical settings
and become part of our food ecosystem. Exposure of
bacteria to levels of antimicrobials exceeding the minimal
inhibitory concentration (MIC) that inhibits susceptible
strains results in the selection of resistant strains that
can grow and outcompete susceptible strains; however,
understanding the emergence of AMR bacteria is still
evolving (33). Increasing attention is being given to the
potential for antimicrobial concentrations below the
MIC, even several fold below, to result in the emergence
of AMR bacteria that can subsequently be enriched in
human, animal and environmental niches (33). Low
concentrations of antimicrobials can be present in various
body tissues during and following human and veterinary
therapy (33). Likewise, the antimicrobial concentration
within tissues can vary over the treatment period. Low
levels of antimicrobials are found in the tissues of food
animals treated therapeutically (33), in environments (e.g.,
sewage, waste water, soils) (1) and in biofilms, as already
described (25). Antimicrobial residue levels in foods are
generally considered to be reduced through the food chain,
during food processing, and in the human gut to levels not
considered hazardous to consumers. However, the effect of
low residues levels on AMR among food microflora requires
further investigation and understanding.
The transfer of AMR genes and the selection and
enrichment of AMR bacteria in food systems is complex
and can be influenced by the food matrix, environmental
conditions, and the physiological state and growth fitness
of a bacterium (1, 37). Verraes et al. (2013) reviewed

the mechanisms of AMR transmission and noted that a
variety of food matrices have been shown experimentally
to support the transfer of AMR encoding genetic material
by conjugation and transformation among Enterobacteriaceae and lactic acid bacteria and in Campylobacter
jejuni and Bacillus spp. (37). Hurdles used for the control
of growth of pathogens in food, e.g., low temperature
and modified atmosphere packaging (MAP), may not
necessarily prevent plasmid transfer among bacteria in
food (36). For example, plasmid transfer of AMR genes has
been demonstrated experimentally between Lactobacillus
sakei and L. monocytogenes in cooked ham at 7°C, given
sufficient time and under MAP conditions (36). Bacteria
along the food chain can exist in varying physiological
states and are subject to various stressors. Sub-lethal food
preservation stresses (e.g., high or low temperature, osmotic
and pH stress) have been shown to significantly alter the
levels of phenotypic AMR, both positively and negatively,
in pathogens such as E. coli, Salmonella Typhimurium,
Staphylococcus aureus and Cronobacter sakazakii in food, and
these changes may or may not be sustained after removal
of the stress (26, 37). This could have consequences in
minimally processed foods.
Food reservoirs of bacteria and AMR elements
Except for commercially sterile foods, foods can be contaminated with a various bacterial species, and our knowledge is limited to those culturable in laboratories, which
represents only a small portion of those present. Raw foods
have the highest culturable bacterial concentrations, followed
by minimally and fully processed foods, while bacteria can
also be purposefully cultured in foods or included as pro-,
pre- and synbiotics. Additional food contamination can
occur when food is handled and as a consequence of environmental exposure, and the degree of contamination varies with
the level of food chain sanitation and hygiene conditions. In
FAO/WHO-supported studies of food chains in regions with
poor hygiene management, more than half of raw chickens
at markets were contaminated with ≥ 2 log10 colony forming
units (CFU) E. coli/ml rinsate; 75% of isolates were resistant
to at least one antimicrobial tested, and some were multidrug resistant (29). Even with good hygiene conditions,
ready-to-eat foods can be considered to be of satisfactory microbiological quality when contaminated with up to 104 CFU
aerobic bacteria/g and this can include pathogens, e.g., a few
E. coli/g or up to 100 coagulase-positive staphylococci/g, as
well as others. Resistance to antimicrobials critical in human
medicine and multi-resistance have been reported among
opportunistic human pathogens isolated from foods and
food processing environments, e.g., mesophilic and psychrotrophic Pseudomonas spp. isolated from goat and lamb slaughterhouse processing areas (21) and Acinetobacter baumannii
on fresh vegetables collected from farmers' markets (19) and
on commercial raw meat (24).

September/October Food Protection Trends

357

Table of Contents for the Digital Edition of Food Protection Trends - September/October 2017