Risk of Listeria:
Fresh Produce
A Guide for Food Manufacturers
A document produced jointly by iNet and University of Nottingham
Catherine Rees
Christine Dodd
Ogueri Nwaiwu
Associate Professor of Food Microbiology
Professor of Food Microbiology
UoN Research Fellow
Risk of Listeria: Fresh Produce
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Risk of Listeria: Fresh
Produce
A Guide for Food Manufacturers
ERDF-iNet
Partnership with
Universities

The Food Standards
Agency (FSA) aims to
Introduction
reduce the number of cases
of listeriosis in the UK by
Consumption of fresh produce continues to increase, and
associated with this has been an increase in producelinked food poisoning outbreaks. It has been reported
that larger scale production and more efficient
distribution of fresh produce over the past two decades
have contributed to an increase in the number of
illnesses associated with these products.
Pathogen
contamination of fresh produce may originate before or
after harvest and once contaminated, produce is difficult
to sanitize. This problem is compounded if the bacteria
invade the vascular system of the plants as they are then
protected from any conventional surface sanitation
treatments applied. Such treatments reduce the overall
microbial load and reduce the levels of surface
contamination, but do not penetrate the plant tissue.
The organism Listeria monocytogenes is best known as a
serious human pathogen that is transmitted to humans
via the consumption of contaminated food products.
However it is also a bacterium that occurs commonly in
soils, associated with decaying plant matter. Hence it
can be naturally associated with any plant product grown
in contact with soil. Unusually for human pathogens, it
can use plant sugars for growth and hence the organism
is often a problem associated with minimally processed
fruit or vegetables. Specifically, when vegetables or fruit
are cut, sugars are released which the organism can
the year 2015 through the
Listeria Risk Management
Programme. The program
has three areas of focus:
firstly Listeria awareness
with reference to consumer
behaviour, secondly
procurement of food to the
vulnerable and thirdly
industrial compliance. To
this end, the ERDF-iNet
has entered a partnership
with the University of
Nottingham to help local
food producers by
establishing a Knowledge
Network. Producers will
be encouraged to report
any information they have
about products affected by
Listeria contamination and
the University will collate
and analyse the
information collected, and
then share the information
anonymously with the
wider industry.
THE FSA LRMP 2010-2015.
http://food.gov.uk/multime
dia/pdfs/lrmp.pdf
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Risk of Listeria: Fresh Produce
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utilize for growth. However it is still unclear whether
Listeria can become internalised in plant tissue.
Internalization of bacteria in plant tissue
It has been very well established that some bacterial
pathogens can internalise into plant tissue. There is still a
lack of knowledge about exactly how far bacteria are
transmitted into the plant vascular system, and also little
knowledge of whether these bacteria are simply surviving
– protected from sanitizers by the plant tissue – or are
actively growing within the plant.
Because of their
association with very large outbreaks of food borne
infection transmitted via fresh vegetables, most studies
have been carried out on Gram-negative bacterial
pathogens, such as E. coli and Salmonella. Hence there
is very limited research describing the interaction of
Listeria with plants.
Celery
Outbreak
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In 2010, the Texas
Department of State Health
Services ordered a San
Antonio produce
processing plant to halt
operations and launched a
widespread recall after
laboratory tests found
Listeria monocytogenes in
packages of chopped celery
sold to hospitals,
restaurants and schools.
The investigation into the
company was prompted by
a spate of 10 cases of
listeriosis (including five
deaths) reported to the
health department over a
period of eight months.
Although the celery was
not sold directly to the
public, investigators linked
contaminated celery to at
least six of these cases of
listeriosis.
(Reproduced with permission: license number: 3250221223803)
Internalisation of E. coli in leaf stomata (from Berger et al., 2010
Environmental Microbiology (2010) 12(9), 2385–2397)
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Source: Los Angeles Times,
October, 2010
Risk of Listeria: Fresh Produce
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Routes of entry for bacteria into plant tissue
This is a topic that is still being debated, but clearly there
are two obvious explanations of why bacteria are found
within plant tissue. Firstly they enter through natural
openings in the plant surface (stomata, lenticels, sites of
lateral root emergence, etc.) and/or through sites of
biological or physical damage. Secondly they are pulled
into the internal tissues along with water.
Major Product
Recall 2013

An America sprout grower
recalled all sprouted seeds
sold by the firm and
Normally, water movement is driven by capillary action
from the stem scar/calyx into the core of fruit. Other
sources could be through wounds or bruises in the
surface of a fruit or leaf, entry via the roots following
exposure to pathogen-contaminated water and from
stamen via the pollen tube into new fruit. There is
evidence that some bacteria may be able to persist in the
complete plant life cycle, from seed to sprout. Evidence
for bacterial contamination via hydroponic systems has
been demonstrated and this can lead to entry into plants
via both roots or leaves.
distributed throughout
Hence, during production, water is used to soak seeds,
irrigate plants and wash produce crops following harvest,
and all of these processes can be seen as potential
sources of contamination.
by the Department of
Washington, Oregon,
Alaska and British
Columbia in Canada due
to discovery of Listeria
contamination.
The initial recall included
broccoli, clover and spicy
sprouts and alfalfa sprouts
where the contamination
was discovered following
testing of finished product
Agriculture. However this
was voluntarily expanded
to include all of the
company’s products,
including bean sprouts,
sandwich sprouts, deli
Sprouts, Wheatgrass and
Pea Shoots after further
tests were carried out at
the firm’s production
facility.
http://www.foodsafetynew
s.com/2013/02/pacificnorthwest-sprout-growerexpands-listeria-recall/
recall/#.UjIjgMZJPZM
Reproduced from Deering et al., 2012 Food Research International, 45 (2) 567–575
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Risk of Listeria: Fresh Produce
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Listeria in plant tissue
The information currently available on the internalization
of Listeria is from very limited studies and some of the
results are contradictory. It has been shown that, like E.
coli, Listeria can enter the stomata of leaves but whether
this is an active process or a passive entrapment of
bacteria within the structure (which is far larger than the
bacterial cell) has not been determined.
However
bacteria able to enter natural openings in the plant can
be protected from various sanitizers following closure of
the guard cells.
Since the organism is commonly found in soil, the entry
of Listeria into leaf tissue is more likely to occur postharvest rather than during growth. Studies have shown
that fruit and vegetable crops can be contaminated postharvest when there is a big enough temperature
differential between the crop and wash water to allow
movement of water into the plant tissue. Following entry
it is likely that the bacteria are transported via the mass
flow of water entering the plant and moving within it. This
process has been demonstrated by using bacteria-sized
polystyrene beads which could be found within the body
of a plant after being taken up from the soil.
Onions
Contamination
•••
A US company voluntarily
recalled 13,600 pounds of
its products including
pasta, chicken and ham
salads because these
products may be
contaminated with Listeria
monocytogenes. The recall
was caused by a supplier
who was producing diced
and slivered onions, and a
mix of diced onion and
celery who were notified
that a random sample of
diced yellow onions
collected at a retail location
had tested positive for
Listeria.
The exception to this is when Listeria-contaminated
manure has been used as a fertilizer, as occurred in the
Maritime coleslaw outbreak in 1981. This was the first
outbreak of L. monocytogenes that could be definitely
linked to food and was caused by commercially prepared
coleslaw in Canada and resulted in at least 41 cases and
7 confirmed deaths. In this case it was found that manure
from Listeria-infected sheep had been used as an organic
fertilizer when growing the cabbages used to prepare the
salad, leading to heavy leaf contamination.
After investigation by the
U.S. Food and Drug
Administration (FDA)
Listeria was found in both
product and the
production facilities of the
onion supplier based in
California and the recall
was extended to include all
products containing onion
produced over a 10 day
period in July 2012.
Bacteria can also reach the interior of the plants by the
roots. However, again, there are very few studies that
have been described investigating whether Listeria can
Source: Food Safety News
July 19, 2012
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Risk of Listeria: Fresh Produce
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enter plants by this system and the published reports
suggest that they do not readily enter plant tissue via the
roots. This would be consistent with the biology of the
bacterium in that it is attracted towards the sugar
cellobiose which is produced from the breakdown of
cellulose. This breakdown is most frequently carried out
by fungi and bacteria that live in the rhizosphere – the
community of organisms associated with the plant roots.
So the highest concentration of these Listeria-attractive
plant sugars are likely to be found outside the root
structures rather than within the plant tissue.
This ability to use these plant sugars may explain why
produce outbreaks seemed to be frequently associated
with processed produce and often involved storage under
suboptimal conditions (for instance the Canteloupe melon
outbreak in 2011) or environmental cross-contamination
after processing.
Cantaloupe
melon
outbreak

In 2011 the US Jensen
Farms cantaloupe outbreak
resulted in 146 cases of
listeriosis, 30 deaths and
one miscarriage.
The FDA report concluded
that both crosscontamination between
livestock and farm
equipment and the use of a
potato-washing machine
that had not been
Growth of Listeria on fresh produce
disinfected contributed to
Recent reports show that commodities can differ in their
ability to support growth.
Some studies have been
carried out to compare growth on intact and damaged or
cut produce. Growth has been reported on intact
tomatoes, but studies on carrots, cabbage, peppers and
cantaloupe melon reported growth only on cut, shredded
or damaged produce. In general Listeria grew well on
shredded lettuce, with populations increasing during
storage.
the outbreak. Also the
canteloupes were stored
under conditions that
allowed Listeria to grow (a
moist environment created
by water pools on the floor
next to packing equipment)
and a lack of pre-cooling
prior to cold storage
resulting in condensation
on the melon surface.
Survival and growth patterns on vegetables have been
found to vary with strain, product type and packaging
atmosphere. It has been suggested that packaging under
modified atmosphere increases the ability of L.
monocytogenes to grow by inhibiting competing micro
flora, but this remains to be proven, and the effect may
differ by commodity, atmosphere composition, and
storage conditions. However, packaging under modified
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They concluded that this
outbreak highlighted the
importance of employing
good agricultural and
management practices in
packing facilities as well as
in growing fields.
Risk of Listeria: Fresh Produce
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atmosphere evidently does not inhibit growth of L. monocytogenes, and the
prolonged shelf life may in itself increase the listeriosis risk.
Significant differences have been observed in terms of the ability of Listeria to
survive in heat and acidic conditions and on packaged vegetables. Cooked or
pasteurized produce usually supports rapid growth and may represent a risk after
post-processing contamination, especially if not refrigerated and consumed
without heating. It is now accepted that most produce commodities support
growth of L. monocytogenes.
Practical steps to control Listeria in fresh produce
Assuming the bacteria are not internalised in the plant tissue, surface sanitisation
is normally an effective way to remove Listeria from product. Many reports show
that contaminated surfaces are most likely the source of product contamination,
and that the risk of contamination is highest between the primary trimming and
chopping and packaging stages.
Sources of
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contamination that should be considered are:
Hands and gloves and personal protective equipment
Slicers
Conveyors
Washing tanks and wash water
Holding containers
Racks for packaging and packaging equipment
In addition general plant or factory sanitation and employee hygiene must be
taken into consideration for effective control of Listeria. More advice can be found
in a previous technical publication (“Dealing with Listeria” by UoN/Diversey).
Concluding remarks
Listeria is unlike many other bacteria that cause food borne disease. As well as
being able to infect the human body, it can readily adapt to survive and grow in
the environment, and forms a natural part of the soil micro flora. Hence its
association with fresh produce does not always indicate that there has been a
major contamination event – rather the organism may have entered the
production facility and its versatility has allowed it to take advantage of this
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Risk of Listeria: Fresh Produce
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situation. For this reason, the more we understand the biology of this bacterium,
the more likely we are to be able to develop methods to combat it.
Acknowledgements
This work was funded by the ERDF and iNet. Figure reproduced by permission of
publisher John Wiley & Sons.
Disclaimer
Every effort has been made to ensure the information in this document is
accurate. However University of Nottingham does not accept any responsibility or
liability whatsoever for any error of fact, omission, interpretation or opinion that
may be present, however it may have occurred.
References
Beirne, D.O. (2007) Microbial safety of fresh-cut vegetables. Acta Horticulturae,
746,159-172.
Francis, G.A. and O'Beirne, D. (2005) Variation among strains of Listeria
monocytogenes: Differences in survival on packaged vegetables and in response to
heat and acid conditions. Food Control 16, 687-694.
Gorski et al. (2004) Strain-Specific differences in the attachment of Listeria
monocytogenes to Alfalfa sprouts. J. Food Prot 67, 2488-2495.
Hoelzer et al. (2012) Listeria monocytogenes growth dynamics on produce: A review of
the available data for predictive modelling. Foodborne Path Dis 9, 661-673.
Olaimat, A.N. and Holley, R.A (2012) Factors influencing the microbial safety of fresh
produce: A review. Food Microbiology 32, 1-19.
Rees, C.E.D and Dodd, C.E.R (2013) Dealing with Listeria: A guide for food
manufacturers. A document produced jointly by Diversey, now a part of Sealed Air,
and University of Nottingham (available on request).
Suslow, T. and Harris, L. (2000) Guidelines for controlling Listeria monocytogenes in
small- to medium-scale packing and fresh cut operations. Publication 8015
University of California.
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