The growing burden of foodborne outbreaks due to
contaminated fresh produce: risks and opportunities
M. F. LYNCH1*, R. V. TAUXE1AND C. W. HEDBERG2
1Division of Foodborne, Bacterial and Mycotic Diseases, National Center for Zoonotic, Vectorborne, and Enteric
Diseases, United States Centers for Disease Control and Prevention, Atlanta, GA, USA
2Division of Environmental Health Sciences, School of Public Health, University of Minnesota, Minneapolis,
(Accepted 17 December 2008)
Foodborne outbreaks from contaminated fresh produce have been increasingly recognized in
many parts of the world. This reflects a convergence of increasing consumption of fresh produce,
changes in production and distribution, and a growing awareness of the problem on the part of
public health officials. The complex biology of pathogen contamination and survival on plant
materials is beginning to be explained. Adhesion of pathogens to surfaces and internalization of
pathogens limits the usefulness of conventional processing and chemical sanitizing methods in
preventing transmission from contaminated produce. Better methods of preventing
contamination on the farm, or during packing or processing, or use of a terminal control such as
irradiation could reduce the burden of disease transmission from fresh produce. Outbreak
investigations represent important opportunities to evaluate contamination at the farm level and
along the farm-to-fork continuum. More complete and timely environmental assessments of these
events and more research into the biology and ecology of pathogen-produce interactions are
needed to identify better prevention strategies.
Key words: Foodborne, outbreaks, produce.
as a source of foodborne outbreaks in many parts of
the world. In the USA, the proportion of outbreaks
linked to fresh produce increased from <1% of all
reported outbreaks with known food vehicle in the
1970s to 6% in the 1990s . The median size of
produce-related outbreaks also doubled and the pro-
portion of outbreak-associated cases accounted for
by fresh produce increased from <1% to 12% of
illnesses in that same time period. In Australia, fresh
produce accounted for 4% of all foodborne outbreaks
reported from 2001 to 2005 . In Europe, recent
outbreaks have revealed new and unexplained links
between Shigella and imported baby corn , Yersinia
pseudotuberculosis and lettuces , and noroviruses
and raspberries , to cite but a few. In the USA,
recent outbreaks of Escherichia coli O157:H7 infec-
tions linked to bagged baby spinach , Salmonella
underline the challenges related to fresh produce.
Several produce-related outbreaks have been multi-
national in scope (Table 1). In the wake of these out-
breaks, research has begun to define the biological
* Author for correspondence: M. F. Lynch, MD, MPH, Centers
for Disease Control and Prevention, 4770 Buford Highway,
Mailstop F-22, Atlanta, GA 30341, USA.
Epidemiol. Infect. (2009), 137, 307–315.
f 2009 Cambridge University Press
Printed in the United Kingdom
interactions between microbes and produce, which
can be surprisingly complex.
The increase in reported outbreaks related to
produce may be the result of several trends. The per
capita consumption of fresh produce has increased in
the USA, and perhaps in other industrialized nations
. The desire for fresh produce year round means
that in the cold season it is likely to be transported
from farther away, either the subtropics or from the
other hemisphere. Due to changes in processing, more
cutting and coring may be performed in the field at the
time of harvest. As agriculture becomes more inten-
sive, produce fields may be next to animal production
zones, and the ecological connections between wild
animals, farm animals, and produce may be closer.
Reports in this issue of Epidemiology and Infection
further highlight the challenges, and the need for im-
proved prevention strategies worldwide. The range of
vehicles associated with these outbreaks – fresh basil,
carrots, and mung bean sprouts – represent three dis-
tinct production, storage, and use characteristics.
Salmonella and other enteric bacterial pathogens in
these outbreaks were able to survive extensive trans-
portation or storage for prolonged periods of time.
Subsequent handling of the contaminated produce
items allowed amplification of the organisms and re-
sulted in the reported outbreaks. Although measures
taken at the point of service can reduce the likelihood
that contamination will cause outbreaks in commer-
cial food service and institutional settings, primary
prevention of contamination is needed to stop widely
PUBLIC HEALTH RECOGNITION
Identifying the source of contamination in any out-
break requires a careful assessment of potential ex-
posures. In outbreaks in defined groups, such as
Y. pseudotuberculosis infections  and entero-
toxigenic E. coli infections  associated with school
meals, or shigellosis in airline passengers , menus
may provide a set of hypotheses that can be directly
tested. Outbreaks with cases widespread in the com-
munity present a special challenge, as the list of poss-
ible exposures includes all foods consumed over a
period of several days, as well exposure to other
persons, water and other environmental sources.
Identifying the source starts with the generation
and evaluation of reasonable hypotheses regarding
suspected food vehicles . Hypothesis formation
is guided by previous experience and biological
plausibility, perceptions of which are also guided by
previous experience. One caveat to this common ap-
proach is that over-reliance on experience and known
biology may inhibit recognition of novel or unusual
food vehicles, such as certain items of fresh produce.
However, produce-related outbreaks are no longer
novel. With increasing awareness of raw produce as a
vehicle for foodborne infections, investigators are less
likely to dismiss the idea once it has arisen. Thus,
direct food consumption history-taking to identify
foods suspected as the source of S. Branderup in-
fections in multiple USA states, they were building on
the knowledge that tomatoes had been well docu-
mented as a vehicle for Salmonella [17, 18].
The growing recognition of raw produce as an im-
portant source of foodborne outbreaks may be better
understood when compared with other foods that are
now well-recognized sources of infection with par-
ticular pathogens. Several outbreaks of Salmonella
Enteritidis (SE) infections caused by duck eggs in the
first half of the last century showed that eggs were
a possible source of this infection , and fore-
shadowedthe SEpandemic due to contaminated hen’s
eggs in the last decades of the century . Numerous
SE outbreaks due to eggs during the 1980s confirmed
that eggs were an accepted source, indeed the expected
source, of SE outbreaks . This relationship
between food and pathogen was recognized by
Table 1. Selected recent multinational foodborne outbreaks due to contaminated produce items [3, 6, 7, 9–11]
countriesAffected regions Implicated food
Escherichia coli O157:H7
Europe, North America
Fresh peppers, ?tomatoes
Raw baby corn
308 M. F. Lynch, R. V. Tauxe and C. W. Hedberg
outbreak investigators even before the complex cycle
of vertical transmission in the egg-laying hens and in-
ternal contamination of eggs was understood .
Even more dramatically, the first recognized outbreak
of E. coli O157 infections heralded both the newly
recognized foodborne pathogen and what turned out
to be its predominant food vehicle, ground beef
. Although subsequent outbreaks added many
other foods to the list, particularly fresh produce
items, ground beef continued to be a leading source
of foodborne E. coli O157 outbreaks . As seen
through these examples, the progression of public
health system awareness follows a consistent pattern:
following initial outbreak investigations that demon-
strate that a particular transmission pathway is poss-
ible, repeated investigations lead to an acceptance
that it occurs, and then to an expectation that it oc-
The public health system has now reached this
same expectation stage with respect to foodborne
outbreaks from fresh produce. Fresh produce is rou-
tinely considered to be a possible source of foodborne
outbreaks caused by a variety of pathogens. In fact,
several specific pathogen–food combinations have
emerged in recurrent outbreaks – salmonellosis from
melons , tomatoes [18, 26], and several varieties of
sprouts ; E. coli O157 infections from leafy green
vegetables ; Cyclospora spread by raspberries ;
hepatitis A infections by green onions . The
food vehicle in the first outbreak for each of these
produce–pathogen pairs was novel at the time and
subsequent similar outbreaks confirmed the food–
pathogen pairing. These food–pathogen pairs may
yet shed more light on the mechanisms and routes
of contamination. Outbreaks due to the same produce
item from different growing areas, such as salmonel-
losis due to melons grown in Mexico  and Australia
 suggest that the problem is probably related to
common conditions in the growing environment or
undefined peculiarities of plant–pathogen biology.
Recurrent outbreaks from produce grown in the same
area, such as infections with the same strain of
growing region in the USA , suggests these eco-
logical conditions may persist over time.
Although fresh produce is now a well-recognized
outbreak food vehicle, many challenges remain in
the investigation of such outbreaks. Produce in the
local market is often globally sourced and can be
widely distributed from a central production area.
Contamination of these items may lead to widely
dispersed cases and outbreaks that are difficult to
detect. Pathogen subtyping in routine enteric disease
surveillance improves recognition of these outbreaks,
as in the recent outbreaks due to contaminated
tomatoes in the USA [17, 31]. However, this practice
requires an expansion of chronically scarce public
health resources and national and international
subtyping networks that are still developing .
Subtyping methods may similarly illuminate the epi-
demiology of norovirus, the most common cause of
foodborne outbreaks in the USA . Foodborne
norovirus outbreaks are often attributed to contami-
nation in the final kitchen, altthough subtyping
systematically applied, may in the future connect
outbreaks and isolated cases to more remote sources
of contamination. The short shelf life, rapid distri-
bution, and consumption of most produce along
with the intrinsic time delays in outbreak recognition,
investigation, and traceback limit opportunities to
prevent further outbreak-related illness. While field
investigations of the outbreak source can be daunt-
ing, these outbreaks represent major opportunities to
learn what went wrong and how to prevent the next
outbreak. Harvest is often finished by the time the
outbreak is even recognized, much less by the time the
harvest site is identified. The multi-disciplinary nature
of the problem, limited jurisdiction by food safety
regulators, and the lack of established procedures
for a non-regulatory, multi-disciplinary investigation
further hinders field work that could result in prac-
tical control measures. Nevertheless, any insights
gained in the field that contribute to control efforts
are of high potential yield. Since we eat much pro-
duce fresh, without cooking, and the effect of washing
contaminated produce appears to be weak , pre-
vention of contamination is paramount to control
BIOLOGY AND ECOLOGY OF
While fresh produce can become contaminated at any
point in the chain of food production, there are often
few intervening steps between farm and table. The
likelihood of contamination is highest during three
periods: in the field, during initial processing, and
during the final preparation in the kitchen. Early
contamination may come from wild animals that may
contaminate fields or processing sheds, from farm
workers without access to latrines or handwashing
Growing burden produce outbreaks 309
stations, and from the water used to irrigate or spray
fungicides on the plants. During processing, it may
come from contaminated water used for washing,
chill tanks or sprays and shipping ice. Late contami-
nation in the restaurant or home kitchen may occur
if produce is prepared with unclean implements, if
surfaces and hands are also used to prepare raw
meat or poultry, through cross contamination during
storage, or if an infected foodhandler with poor hy-
giene is shedding the pathogen as food is prepared.
Recent work by plant pathologists and food micro-
biologists indicates that the connections between
foodborne bacterial pathogens and produce may be
more complicated than simple passive transfer .
Although these organisms are well adapted to life in
the vertebrate gut, they can also survive and flourish
on and in plants. Salmonella applied to leaves of
young coriander (cilantro) plants grow rapidly to take
up 80% of the carrying capacity of the leaf surface
and then persist indefinitely in greenhouse conditions
. Similarly, Salmonella can grow to high densities
on the surface of tomatoes, and then persist there for
weeks . Although Campylobacter will not survive
on leaves, where exposure to the atmosphere in-
activates them, they will persist for at least 4 weeks in
the root zone . Salmonella and E. coli may persist
on or in alfalfa and mung seeds indefinitely, and then
rapidly grow to high counts in the warm and moist
conditions used to convert them to alfalfa or bean
sprouts [39, 40].
The bacterial pathogens can also reach the interior
of the plants by a variety of routes. Once the pathogen
is inside, it is not affected by surface washing or dis-
infection. The pathways of internalization can be
simple. Bacteria can move with water by capillary
action from the stem scar or the calyx of an apple into
the core . They can enter through wounds or
bruises in the surface of a fruit or leaf . They can
enter plants through the roots following experimental
flooding with contaminated water. For example, in
experimental greenhouse settings, E. coli O157 pres-
ent at high levels in irrigation water is taken up by
mature lettuce, and Salmonella of certain serotypes is
taken up by young tomato plants; in both cases the
concentrations of the pathogen in above-ground plant
tissues can reach 103c.f.u./g. When alfalfa seeds con-
taminated with E. coli O157 or with Salmonella are
sprouted, the bacteria enter the growing sprout, and
appear throughout the deep tissues of the young
plant, without causing it harm [43, 44]. Enteric bac-
teria can also ride along on another important part
of the plant life cycle. After they are applied to the
stamen of the tomato flower, some strains of
Salmonella can be recovered from the internal tissues
of the mature tomato a month later, suggesting that
they can pass via the pollen tube and colonize the new
fruit . Although it has not been demonstrated, it is
possible that enteric bacteria may in fact be able to
persist in the complete plant life cycle, from seed to
sprout to mature plant to fruit and seed again. It
could also be that the capacity to contaminate the
fruit or other edible tissues represents an ecological
strategy for gaining access to the gut of another her-
Although virtually all work has been done with
bacterial pathogens, it may also be occurring with
viruses. In one recent experiment, vaccine viral RNA
was detected in the tissues of green onions, after they
had been irrigated with killed hepatitis A vaccine virus
The infected human is ultimately presumed to be
the source of contamination for infections with noro-
virus, hepatitis A, Shigella and other pathogens with
exclusively human reservoirs, and occasionally for
other pathogens. Contamination may be direct, via
unwashed faecally contaminated hands, or somewhat
less direct. In norovirus infections, vomitus can be
highly infectious. The persons who vomit may not
scrupulously wash their hands, or the surrounding
area; they also may not perceive themselves as ill, and
thus not exclude themselves from working in the
kitchen . Pathogens from human reservoirs may
be introduced before produce reaches the kitchen.
Contamination of produce by human sewage around
the time of harvest has been a suspected cause of
several widespread outbreaks of hepatitis A infections
Although the precise mechanism of contamination
in most produce-related outbreaks remains unex-
plained, field research following outbreaks is starting
to shed light on the complex ecology of the growing
environment. For example, outbreak-related and
other strains of E. coli O157:H7 have been isolated
from watersourcesinthe growingarea found tobe the
likely source of several lettuce-related E. coli O157:H7
outbreaks . An environmental investigation fol-
lowing a large spinach-related E. coli O157:H7 out-
break traced to the same growing region suggested
that feral swine may play a role in contamination in
the field . Studies of the interactions of Salmonella
and tomato plants indicate that some serovars are
more likely to persist pre-harvest and to appear in the
310M. F. Lynch, R. V. Tauxe and C. W. Hedberg
fruit than others, suggesting type-specific adaptation
to this niche may have occurred . Investigation of
the circumstances under which mangos became con-
taminated with Salmonella indicated that water baths
used to rid the fruit of fruit-fly larvae were open to the
environment and indifferently chlorinated, and thus
easily contaminated with Salmonella from a variety of
Contamination can be amplified by processing
steps. Plunging a warm fruit or vegetable into a cold
water bath causes the internal airspaces to contract,
drawing water and associated contaminants into the
fruit. This is the likely mechanism of contamination
for the aforementioned outbreak of Salmonella infec-
tions traced to imported mangos, in which the man-
goes were treated with hot water to kill fruit-fly
larvae, and then rapidly chilled in cold water that
may not have been disinfected; the same potential has
been demonstrated for other produce with internal air
spaces . Indeed, because of the potential for con-
taminating tomatoes that way, monitoring tempera-
ture and chlorination of the water baths (in which
warm tomatoes from the field may be placed) are key
control points for the tomato industry .
Once the vegetable or fruit is cut, the nutrients in
the juices are available to pathogens. This means that
after produce is sliced, diced or shredded, contami-
nation can lead to high pathogen counts. After an
outbreak of shigellosis was traced to shredded lettuce,
rapid growth of Shigella sonnei was documented in
the lettuce held at room temperature . Similarly,
an outbreak of salmonellosis traced to pre-diced
tomatoes led to documentation of rapid growth of
Salmonella on the cut surfaces of tomatoes at room
temperature, and ultimately to the United States
Food and Drug Administration (USFDA) including
cut tomatoes among the foods that require tempera-
ture control for safety in retail and food-service op-
erations, as specified in the USFDA Food Code
[55–57]. Similar growth has been shown for cut
melons, for which the Food Code also specifies tem-
perature control . All of these produce items have
a pH >4.0 that permits the growth of Salmonella. In
fact, any produce with pH favourable to bacterial
multiplication may become inherently more hazard-
ous once cut, and thus need particular care in hand-
ling and storing afterwards.
More needs to be learned about the behaviour of
enteric pathogens in relation to raw produce. Are
some types of tomatoes, lettuce or other produce
more susceptible to internal contamination than
others? What is the range for plant hosts to which our
principal enteric pathogens may be adapted? What
are the genetic determinants that permit some strains
of Salmonella to invade tomatoes, but not others? Are
there commensal bacteria or other microorganisms
that can inhibit the uptake or survival of enteric bac-
teria in or on food plants? Can the risk of produce-
related foodborne illness be reduced through better
understanding of the microbial ecologies in which we
produce our food?
KEYS TO PREVENTION
The lessons from numerous outbreaks are clear,
despite the uncertainties regarding the biology of
pathogens on produce. Contamination cannot be
washed off. Produce items that will not be cooked
should be considered ‘ready to eat’. Prevention of
contamination in the first place is vital. In the lexicon
of Hazard Analysis and Critical Control Point sys-
tems (HACCP), prevention of contamination of fresh
produce is a critical control point because once con-
tamination occurs there are at present no points
during the processing, distribution and service of
fresh produce at which microbiological hazards can
be effectively abated .
Following the occurrence of numerous fresh juice-
associated outbreaks in the USA, the USFDA im-
plemented a juice-HACCP rule. The rule required
juice producers to apply interventions capable of
producing a 5-log reduction of pathogens such as
of methods. Implementation of the juice-HACCP rule
has reduced the occurrence of juice-associated out-
breaks in the USA .
A series of guidance documents issued by USFDA
deal with the more general problems of production
of fresh produce, to Minimize Microbial Food Safety
Hazards for Fresh Fruits and Vegetables , and
to Enhance Safety of Sprouts , and Minimize
Microbial Food Safety Hazards of Fresh-cut Fruits
and Vegetables . These documents promote good
agricultural practices for production and good manu-
facturing practices for processing, using the infor-
mation that is currently available, but do not include
prescriptive regulations and mandatory pathogen
reduction steps represented by the juice-HACCP
Privately, major restaurant chains are working
with suppliers to implement performance standards to
ensure rigorous compliance with good agricultural
Growing burden produce outbreaks 311
practices. These create strong financial incentives for
compliance that may compensate for lack of regulat-
ory prescription for that segment of the market. The
development of egg quality assurance programmes in
both the USA and UK has helped to prevent egg-
associated SE outbreaks and reduce the incidence of
egg-associated infections . Similarly, when the
United States Department of Agriculture (USDA)
required all ground-beef producers in the USA to
consider E. coli O157:H7 a hazard that was reason-
ably likely to occur and to revise their ground-beef
HACCP plans accordingly, the contamination rate of
E. coli O157:H7 in ground-beef products sampled by
USDA fell by 80% and the incidence of E. coli
O157:H7 infections was cut almost by half [65, 66].
Reducing the burden of produce-associated illnesses
will almost certainly require some combination of
regulatory oversight and industry incentives. How-
ever, a better understanding of the risks and benefits
of specific practices are needed to guide the develop-
ment of these interventions.
To facilitate this,moredetailed andtimely outbreak
investigations are needed to identify production
sources for contaminated fresh produce, and to facili-
tate more thorough environmental and ecological
assessments of the contamination events. Whenever
possible, outbreakinvestigations needto include rapid
and detailed traceback and exposure assessments so
that likely sources of contamination can be identified
as far back as the field of production. Assessment of
production variables such as field locations and sur-
roundings, use of irrigation and harvesting techniques
can improve our understanding of these events,
and thus help to develop more effective prevention
methods, on-farm and later in the food production
Given our current understanding, improving the
prevention of fresh-produce-associated outbreaks will
require attention to the five following areas, wherever
that produce is grown, processed, transported or
prepared for eating:
(1) The quality of water. Water used to apply pesti-
cides to plants, and for post-harvest cooling and
processing can transfer microbes directly to the
produce, unless the water is treated to drinking-
water standards. Even though the expense of
water treatment may represent a challenge to
many agricultural production areas, the depen-
dence of fresh produce on water and the efficiency
with which contaminated water can serve as a
vehicle for contaminating fresh produce makes
this a critical safety issue for the production of
these ‘ready-to-eat’ foods. Water used for irri-
gation may also be a source of contamination,
particularly if it is contaminated surface water
and if during irrigation it comes in contact with
the edible portions of the plant.
(2) Protection from faecal contamination. Fresh
produce can be easily contaminated in the field by
direct and indirect contact with farm animal ma-
nure, wild animal faeces and human faeces. The
cutting of plant tissues at harvest increases the
likelihood of internalization of pathogens from
contamination of the cut surfaces.
(3) Washing and sanitizing fresh produce. Currently
available washing and sanitizing agents can re-
duce the levels of surface contamination of raw
and processed fresh produce items, and therefore,
can help reduce the likelihood that large focal
outbreaks may be associated with specific con-
tamination events. Even so, better sanitizing
methods are needed to penetrate biological bar-
riers that shelter pathogens in plant materials; the
use of irradiation as a pasteurizing method for
fresh produce is a possible solution.
(4) Management of the cold storage and supply
chain. Refrigeration of cut produce items that
are not in the process of being served can reduce
the risk of bacterial amplification on the cut sur-
(5) Protecting fresh produce items from contami-
nation by foodhandlers who themselves are ill or
infected with the pathogen. While infected food
workers are a primary source for contamination
with norovirus, hepatitis A virus and Shigella,
they can also be an important source for con-
tamination with Salmonella in commercial food-
The findings and conclusions in this report have not
been formally disseminated by the Centers for Disease
Control and Prevention and do not necessarily con-
stitute official policy of the agency (for authors M.
Lynch and R. Tauxe).
DECLARATION OF INTEREST
312 M. F. Lynch, R. V. Tauxe and C. W. Hedberg
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