Food Protection Trends - March/April 2021 - 185

adulterated under section 402 (a)(1) of the Federal Food,
Drug, and Cosmetic Act.
Listeria monocytogenes can grow with or without oxygen, at
a maximum water phase salt of 10%, a minimum pH of 4.4,
and minimum water activity of 0.92 (21). L. monocytogenes
can grow at a minimum temperature of −0.4°C (31.2°F)
(21). In a survey of 130 samples from 13 lots of refrigerated,
vacuum-packaged, cold-smoked salmon packed in six Danish
smokehouses, the pH and water phase salt ranged from 6.1
to 6.3 and 3.5 to 8.9%, respectively (7). These levels provide
a suitable environment for the growth of L. monocytogenes.
A review of six studies showed an exponential growth rate
of 0.050 to 0.556 log CFU/day at 5°C (41°F) for L. monocytogenes inoculated in cold-smoked salmon (26). These
results indicate that L. monocytogenes can grow throughout
the shelf life of the product without temperature abuse.
Cold-smoked fish processing is a complex multistep
process that relies on effective sanitation controls to prevent
L. monocytogenes contamination (3). The heat applied during
smoking is not sufficient to eliminate L. monocytogenes (e.g.,
FDA recommends smoking not exceed 32°C (90°F)), and
cold-smoked fish is considered a raw RTE food by FDA (20).
Environmental sampling and molecular typing methods,
such as ribotyping, pulsed-field gel electrophoresis (PFGE),
and, more recently, whole genome sequencing, have been
used to compare isolates and subsequently identify routes
of contamination, which can then lead to the design of
control measures (3, 16). A 1994 review article of 11 studies
reported that the overall prevalence of L. monocytogenes
on cold-smoked fish was approximately 10%, with the
exception of two studies that found that 24 and 31% of the
samples contained L. monocytogenes (1). Concern over the
high prevalence of L. monocytogenes in cold-smoked fish
led researchers to track the presence of L. monocytogenes in
processing facilities using environmental sampling (8, 11,
19). A 1995 environmental sampling study of six coldsmoked salmon processing plants concluded that the surface
of frozen and fresh raw salmon was the primary source of
L. monocytogenes contamination and that during processing
this contamination was transferred to equipment, personnel,
and other surfaces, which subsequently became secondary
sources of contamination (8).
Other studies using environmental sampling with
ribotyping have found that insanitation is the most likely
source of finished product contamination (11, 19). In 2000,
512 environmental and 315 raw fish (whitefish, sablefish,
and salmon) samples were collected from two cold-smoked
fish processing plants (A and B) in the United States over
two 8-week periods (11). The results indicated that there
was no significant statistical difference in the positive rate
for L. monocytogenes in raw fish between plant A and plant
B, and the overall prevalence of L. monocytogenes for all raw
fish was 14.6%. However, the prevalence of L. monocytogenes
in environmental samples from plant A was 43.8% and from

plant B was 1.2%. Ribotyping of isolates showed that some
strains from the environmental samples were not detected
in the raw fish samples and that persistent L. monocytogenes
strains in the plant environment were the primary source of
contamination of cold-smoked fish. The study concluded that
(i) environmental contamination is largely separate from the
incoming raw fish, (ii) persistent strains within the plant can
be a continual source of contamination, and (iii) insanitation
in the plant significantly contributes to L. monocytogenes
contamination (11).
The importance of sanitation and L. monocytogenes control
measures was further supported by a 2004 study of four
cold-smoked salmon processing plants in the United States
(19). A total of 234 raw fish, 233 finished products, and 533
environmental samples were collected monthly throughout
1 year. L. monocytogenes was isolated from 3.8% of the raw
salmon and 1.3% of the cold-smoked salmon. This study
used ribotyping of environmental samples to identify specific
subtypes of L. monocytogenes and routes of contamination. The
prevalence of L. monocytogenes in environmental samples from
the four plants ranged from 0 to 30%. Drains and nonfood
contact surfaces were identified as the most frequently
contaminated areas. This study found that the four plants
received similar raw ingredients and produced similar finished
products but varied in sanitation practices and procedures to
prevent cross-contamination. Of the four plants, plant 1 had
the highest prevalence of L. monocytogenes in environmental
and finished product samples. The ribotyping data for plant
1 showed that transient subtypes were constantly being
introduced into the plant by equipment, employees, and raw
materials and also showed two persistent subtypes in the plant.
One of the persistent subtypes of L. monocytogenes was found
in floor drains, on the gloves of an employee, and, ultimately,
in the finished product. In plant 2, although L. monocytogenes
was not found in finished product, a persistent subtype was
identified in the raw materials processing area that was also
found on a door handle adjacent to the finished product area,
indicating that cross-contamination from the raw materials
area may have occurred. In plant 3, ribotyping data suggested
that a niche in the floor mat harbored a persistent subtype of
L. monocytogenes, which subsequently contaminated finished
product. These results from plants 1, 2, and 3 showed the
importance of effective cleaning and sanitization procedures
to eliminate niches where L. monocytogenes persists and the
importance of procedures to prevent cross-contamination.
Plant 4 was substantially different from the other three plants
in that L. monocytogenes was not isolated from environmental
or finished product samples; it was observed that the floors
and equipment had sufficient time to dry between processing
times, indicating the importance of a dry processing
environment. The study concluded that L. monocytogenes
contamination in the processing environment was the most
likely source of finished product contamination and that
sanitation and L. monocytogenes control measures are critical.

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