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Korean school children was linked to enterotoxigenic E. coli
O169-contaminated kimchi that was only lightly fermented
(9). Investigation into the illnesses did not identify contamination on the raw vegetables (radish and cabbage) but
did identify contamination on the prepared kimchi that the
school children consumed, suggesting that contamination
had occurred during preparation.
In the production of a shelf-stable finished product,
a validated pasteurization treatment may be applied to
ensure destruction of surviving vegetative microbiota
that could alter the product during room-temperature
storage, potentially raising product pH and creating a risk
of C. botulinum outgrowth (22). For example, Bacillus
licheniformis has been shown to survive and grow in acidic
tomato products, increasing product pH over time (61).
Generally, however, properly fermented vegetable products are very stable. In fact, large commercial processors of
fermented cucumbers rely on the 5-log pathogen reduction achieved during fermentation to ensure safety and
effectively manage re-contamination risks during desalting
and packing of the final product (Fred Breidt, personal
communication). Processors wishing to avoid pasteurization would need to verify the shelf stability of their
product, generally based on chemical inhibitors.
Intrinsic and extrinsic factors influence microbial
survival
The proliferation or destruction of microbiota present
in the fermentation vessel at the start of the fermentation
period are influenced by intrinsic factors such as composition and physiochemical properties of the growth substrate
as well as by extrinsic factors such as addition of NaCl and
temperature control. Vegetable fermentation systems generally contain 2-4% simple sugar at the outset and near-neutral pH, providing a favorable environment for all types of
microbial growth. Some raw ingredients commonly utilized
in vegetable fermentation contain compounds with varying
degrees of natural antimicrobial capacity. For example, red
pepper, such as the Korean red chili pepper used in kimchi
production, as well as the addition of dried red pepper
flakes to the fermentation brines of some fermented cucumber pickles, introduces capsaicin, a bioactive plant metabolite with known antimicrobial activity (58). Minced, dried,
or whole garlic cloves are sometimes included during the
fermentation of cucumber and cabbage. The thiosulphinate
allicin, found in garlic and other alliums, is antimicrobial,
especially against yeast, although the concentration of allicin can vary throughout the bulk of the fermentation vessel
(59). Capsaicin has also been shown to suppress spoilage
(19). In general, however, natural antimicrobial capacity in
raw materials such as red peppers or garlic should not be
relied upon to contribute to final product safety because of
the considerable variability in these raw materials based on
cultivar and growing and processing conditions.

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Extrinsic factors also play a major role in microbial
survival in traditional vegetable fermentations. The level of
NaCl addition is critical for mediating the relative growth
potential among the various microbial species in the ferment as well as for imparting important sensory characteristics to the final product. While traditional vegetable fermentations rely on levels of added NaCl that are not directly
antimicrobial (<2 to 4% w/w), Dupree and colleagues
demonstrated that these typical NaCl levels do preferentially select for the outgrowth of the LAB that biosynthesize the organic acids responsible for pathogen lethality
(13). Decreasing or eliminating NaCl may still result in a
fermented product with sufficient acid content to achieve
a 5-log reduction in pathogenic E. coli, but these ferments
are more likely to be unstable fermentations, systems that
support secondary fermentation reactions wherein lactate is
metabolized to acetate, then to propionate and eventually to
butyrate, with an accompanying rise in pH (5). In contrast,
including more than 2.5% NaCl in fermentation brines
tends to limit the initial growth of heterofermentative LAB,
thereby limiting production of important organoleptic
compounds that support the complex aroma profile associated with fermented vegetables (41). Because yeasts and
filamentous fungi tend to be more halotolerant than most
foodborne bacterial species, including LAB, NaCl levels
typical in fermentation brines will select for fungal spoilage
if oxygen is present (50). A desire to decrease NaCl content
should therefore be evaluated with both food safety and
quality in mind.
Other added ingredients, e.g., sugars or acetic acid, may
impact the fate of a microbial fermentation. While a small
portion of sugar, e.g., 0.1 g/liter, may be added at the start of
fermentation to enhance LAB proliferation, the addition of
sugar is not typically used in the fermentation of cucumbers
or cabbage, because these vegetable tissues naturally contain
>2% sugar. Calcium acetate may be added to brine to buffer
the fermentation system and allow for greater sugar utilization (17). On occasion, processors add acetic acid or use
diluted recycled fermentation brines to reduce the typical
starting brine pH of ~6 to ~5. Recent research showed that
the addition of acetic acid to a fermentation brine reduced
Enterobacteriaceae at the start of fermentation (34). While
added ingredients influence microbial growth and death,
most are not managed as CCPs, since they do not represent
necessary or sufficient intervention strategies.
Oxygen content in the fermentation vessel is an important
controlling factor. Film yeast are often found growing at the
brine-air interface of vegetable ferments if the fermentation
vessel is not well sealed. While outgrowth of spoilage biota
does not typically constitute a food safety hazard, it may create
undesirable and unmarketable finished products. The best way
to mitigate this problem is to maintain anaerobic conditions.
Another extrinsic factor relevant to the success of vegetable fermentations is the temperature at which the fermen-

Food Protection Trends - July/August 2020

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