FOODBORNE PATHOGENS AND DISEASE

Volume 12, Number 1, 2015

ª Mary Ann Liebert, Inc.
DOI: 10.1089/fpd.2014.1821

Reported Foodborne Outbreaks Due to Fresh

Produce in the United States and European Union:
Trends and Causes

Raquel M. Callejón,1 M. Isabel Rodrı́guez-Naranjo,1 Cristina Ubeda,1,2 Ruth Hornedo-Ortega,1

M. Carmen Garcia-Parrilla,1 and Ana M. Troncoso1

Abstract
The consumption of fruit and vegetables continues to rise in the United States and European Union due to healthy
lifestyle recommendations. Meanwhile, the rate of foodborne illness caused by the consumption of these products
remains high in both regions, representing a significant public health and financial issue. This study addresses the
occurrence of reported foodborne outbreaks associated with fresh fruits and vegetables consumption in the United
States and European Union during the period 2004–2012, where data are available. Special attention is paid to
those pathogens responsible for these outbreaks, the mechanisms of contamination, and the fresh produce vehicles
involved. Norovirus is shown to be responsible for most of the produce-related outbreaks, followed by Salmonella.
Norovirus is mainly linked with the consumption of salad in the United States and of berries in the European
Union, as demonstrated by the Multiple Correspondence Analysis (MCA). Salmonella was the leading cause of
multistate produce outbreaks in the United States and was the pathogen involved in the majority of sprouts-
associated outbreaks. As is reflected in the MCA, the pattern of fresh produce outbreaks differed in the United
States and European Union by the type of microorganism and the food vehicle involved.

Introduction lieve that the benefits of eating fresh fruits and vegetables
outweigh the risk of contracting a foodborne illness by con-

C onsumption of fruit and vegetables is associated with

a healthy lifestyle. Various international organizations,
such as the World Health Organization, encourage the daily
intake of at least 400 g of fruit and vegetables per day (ex-
cluding potatoes and other starchy tubers) for the prevention
of chronic diseases, such as heart disease, cancer, diabetes,
and obesity.
A large portion of this produce is consumed raw, and the
number of foodborne outbreaks associated with these prod-
ucts has increased correspondingly (Buck et al., 2003; Lynch
et al., 2009; Olaimat and Holley, 2012). In this context, un-
pasteurized fruit juices and raw sprouts are also considered
high-risk foods. The 2011 Escherichia coli O104:H4 out-
break from sprouted seeds in Germany gives a clear indica-
tion of the emerging relevance of the consumption of these
products within food safety issues (Soon et al., 2013).
Globalization and growing international trade can also
increase the risk, especially if produce comes from countries
with lower safety standards (Newell et al., 2010). Never-
theless, nutrition educators and healthcare professionals be-
suming fresh produce (Nyachuba, 2010).
The number of reported outbreaks (defined as the occur-
rence of two or more cases of similar illness resulting from
the ingestion of a common food) reported both in the United
States and European Union represents only a fraction of the
actual number of outbreaks that occur (Arendt et al., 2013).
Large outbreaks, outbreaks associated with food service and
institutions, and outbreaks that have a longer duration or
cause serious disease are more likely to be investigated and
reported. Conversely, the data may not reflect what occurs in
sporadic cases (O’Brien et al., 2002; EFSA, 2008). More-
over, there are differences in the sensitivity of the national or
state systems in identifying and investigating foodborne
outbreaks.
A wide spectrum of pathogens and food vehicles has been
documented in produce-associated outbreaks (Berger et al.,
2010). The occurrence of food-related infections due to fresh
produce calls for better control interventions and the need for
improved prevention strategies worldwide, since food can be
contaminated at any point in the food chain, and interventions

1
Área de Nutrición y Bromatologı́a, Facultad de Farmacia, Universidad de Sevilla, Sevilla, Spain.
2
Universidad Autónoma de Chile, Santiago, Chile.

32
US–EU REPORTED OUTBREAKS IN FRESH PRODUCE
must be applied where appropriate at every step. Hence, the
future success of global efforts to prevent produce-related
outbreaks depends on the understanding of the key contrib-
uting factors and the maintenance of best practices to reduce
and eliminate contamination (Kozak et al., 2013).
The purpose of this article is to review and analyze the
factors that contribute to the occurrence of foodborne out-
breaks due to the consumption of fruit and raw vegetables: the
produce vehicles, the mechanisms of contamination, and
the microorganisms responsible for these outbreaks across the
United States and European Union over the last decade.
Materials and Methods
Literature search, data sources, and selection criteria
This study is focused on reported outbreaks associated
with fresh fruits and vegetables, also described as ‘‘produce-
associated outbreaks,’’ being defined as two or more cases of
the same illness in which the epidemiologic investigation
implicated the same uncooked produce item, such as fruit,
vegetable, salad, or juice (Sivapalasingam et al., 2004). Raw
sprouts have also been considered in this context.
Literature searches were performed using PubMed and
Google Scholar as well as subject-specific (CAB Direct,
AGRICOLA, Food Science, and Technology Abstracts) da-
tabases to identify potentially relevant publications, priori-
tizing peer-reviewed journals. The keywords included in the
literature search were as follows: fruit, fresh vegetables, leafy
greens, sprouts, berries, foodborne outbreaks, food-borne
outbreaks, biological hazards, prevention and control, good
hygiene practices, decontamination, food handlers, and the
specific pathogens (Norovirus [NoV] and other viruses such
as Hepatitis A virus, Adenovirus and Rotavirus, Salmonella,
E. coli, Campylobacter, Shigella, Staphylococcus, Clos-
tridium, Listeria, Cryptosporidium, Cyclospora, Giardia).
In the United States, the Centers for Disease Control and
Prevention (CDC) collects data on outbreaks of foodborne
disease (CDC’s OutbreakNet Foodborne Outbreak Online
Database, http://wwwn.cdc.gov/foodborneoutbreaks) (CDC,
2013a). This database provides information from 1998 to
2012 on the following: year of the outbreak, region, type of
location in which the infected food was reported to have been
served, specific strain or type of virus, and the food vehicle of
the outbreak.
In the European Union, the system for the monitoring and
collection of information on zoonoses is based on Directive
2003/99/EC (2003), which obliges Member States to collect
data on the occurrence of foodborne outbreaks and other
zoonosis-related information. The European Food Safety
Authority (EFSA) is assigned the tasks of examining these
data and publishing annual European Union Summary Re-
ports in cooperation with the European Centre for Disease
Prevention and Control (ECDC). Annual data of each
Member State are used as a basis for the EFSA and ECDC
European Union Summary Reports on Trends and Sources of
Zoonoses, zoonotic agents, antimicrobial resistance, and
foodborne outbreaks in European Union. The National
Zoonosis Country Reports include information regarding
foodborne outbreaks for each country. These data are avail-
able through the EFSA webpage: www.efsa.europa.eu/en/
zoonosesscdocs/zoonosescomsumrep.htm. It is important to
note that the foodborne outbreak investigation systems at
33
national level are not harmonized among Member States
(MS). Therefore, the differences in the number and type of
reported outbreaks, as well as in the causative agents may not
necessarily reflect the level of food safety among MS; rather,
they may indicate differences in the sensitivity of the national
systems in identifying and investigating foodborne outbreaks
(EFSA, 2013). Moreover, there is a significant difference
between the number of inhabitants (United States around 320
million; European Union around 500 million).
To have comparable data on foodborne outbreaks that
occur in both regions (United States and European Union),
the earliest year included in the present study was 2004, the
first year for which European reports are available.
Only those outbreaks with laboratory detection of the
suspected causative agent in a fresh vegetable or fruit were
included.
Statistical data analysis
To further explore and visualize the relationships between
regions (United States or European Union), microorganism,
and food vehicle, a MCA of the outbreak data was carried out
(with Statgraphics Centurion XVI 16.1.18 software). MCA is
a technique for analyzing the relationships of several cate-
gorical variables (Greenacre, 1984), in our case, region, mi-
croorganism and food vehicle. Specifically, MCA is obtained
by using a standard correspondence analysis on an indicator
matrix. Thus, MCA computes the inertia (equivalent to the
variance) for quantitative variables and breaks down the total
inertia along axes that gradually explain less of the inertia
(Greig and Ravel, 2009). In this way, MCA is able to rep-
resent a multidimensional dataset on a two-dimensional map
that minimizes the deformation and underscores the rela-
tionship between categories. The interpretation of MCA is
based upon proximities between the points, the two axes, and
the distances between points (Greig and Ravel, 2009).
To facilitate and simplify the MCA, the food vehicles were
grouped into categories (Table 1): Salad, leafy vegetables,
tomato, other vegetables, sprouts, berries, melon-like, fruit
juices, and other fruits.
Results and Discussion
Produce-associated outbreaks in the United States
and European Union
Tables 2 and 3 summarize the reported outbreaks associ-
ated with fresh vegetables, sprouts, and fruits from 2004 to
2012 in the two regions (United States and European Union,
respectively). In addition, specific information regarding
year, country/state, pathogen, food vehicle involved, and
location of exposure of each outbreak are available on CDC’s
database and EFSA Summary Reports. Based on the avail-
ability of these data, the location of exposure or consumption
was known for 95% (318 of 337) and 76% (141 of 185) of
those outbreaks occurring in the United States and European
Union, respectively.
The United States and European Union have reported a
total of 377 and 198 produce-associated outbreaks, respec-
tively, for the period under study. This high number of out-
breaks linked to fresh produce may be due to improved
surveillance, but it might also be related to changes in con-
sumer food preferences, food production and distribution
34 CALLEJÓN ET AL.

Table 1. Description of the Categories Used for Classifying Food Vehicles

Category Food vehicle
Salad All produce items related to salad:
Bar salad, vegetable salad, broccoli salad, coleslaw, mixed salad, Caesar salad, French salad,
aubergine salad, green salad, cucumber salad, speciality salads, house salad, asparagus citrus
salad, chef salad, broccoli salad, garden salad, Greek salad
Leafy vegetables All produce items related to leaves:Iceberg lettuce, lettuce, lollo bionda lettuce, mixed lettuce
leaves, romaine lettuce, ruccula, fresh spinach, baby spinach, shredded lettuce
Tomato Tomato
Other vegetables The remaining vegetables not included in the previous categories:
Vegetables, carrots, pepper, beetroot, onion, baby corn, peas, avocado, cucumber
Sprouts All produce items related to sprouts:
Alfalfa sprouts, bean sprouts, mung bean sprouts, sprouts of fenugreek seed, clover sprouts
Berries All produce items related to berries:
Strawberries, raspberries, berries, frozen raspberries, blueberries, blackberries
Melon-like Melon, watermelon, cantaloupe
Fruit juices All produce items related to unpasteurized juices:
Apple juice unpasteurized, apple cider unpasteurized, orange juice unpasteurized, fresh fruit juice
Other fruits The remaining of fruits not included in the previous categories:
Banana, fruits, fruit salad, grapes, mixed fruit, pineapple, papaya

practices, as well as the emergence of new foodborne path-
ogens (Harris et al., 2003; Sivapalasingam et al., 2004).
For the United States, the absolute number of outbreaks
due to fresh produce ranged from 23 to 60 per year, not
showing a clear trend along this period. In fact, there were
substantial increases in 2006 (57 outbreaks), 2008 (51 out-
breaks), and 2011 (60 outbreaks) (CDC’s database). Ac-
cording to Purayidathil and Ibrahim (2012), the incidence of
total foodborne outbreaks in the United States has decreased
since 1990, although major outbreaks continue to occur, as in
2006. Nevertheless, the number of produce-associated out-
breaks remains high and represents a significant health and
financial issue (Lynch et al., 2009; Berger et al., 2010). In
addition, 49 of all produce-associated outbreaks (13%) oc-
curring during the period under study were multistate out-
breaks. Multistate outbreaks are outbreaks that either spread
to other states or originate from the same vector in multiple
states at the same time (Purayidathil and Ibrahim, 2012).
For the European Union, the number of outbreaks oscil-
lated between 10 and 42, highlighting increases in 2006 (29
outbreaks), 2009 (34 outbreaks), and 2010 (44 outbreaks).
Hence, they also lack a clear tendency (EFSA Summary
Reports).
Microorganisms, food vehicles, and locations
of exposure
A wide spectrum of microorganisms and food vehicles are
involved in produce-associated outbreaks (Tables 2 and 3).
Among all microorganisms, NoV was the main pathogen

Table 2. Summary of Outbreaks Associated with Fresh Vegetables and Fruits in United States,
2004–2012 (Center for Disease Control and Prevention’s Outbreaknet Foodborne Outbreak
Online Database. http://wwwn.cdc.gov/foodborneoutbreaks/)
Food vehicle
Vegetables Fruits
Total
Type of pathogen Salad Leafy Tomato Other Sprouts Berries Melon Juices Other outbreaks
Norovirus 97 62 5 9 0 5 9 3 33 223
Salmonella spp. 8 8 17 3 14 2 14 0 5 71
Escherichia coli 10 22 0 0 4 2 0 6 2 46
Campylobacter spp. 4 2 1 0 0 0 1 0 1 9
Shigella spp. 1 2 0 0 0 0 0 0 0 3
Clostridium spp. 0 0 0 0 0 0 0 0 0 0
Staphylococcus spp. 2 0 0 0 0 0 0 0 0 2
Yersinia spp. 0 0 0 0 0 0 0 0 0 0
Bacillus spp. 1 0 0 0 0 0 0 0 1 2
Giardia spp. 0 1 0 1 0 0 0 0 0 2
Cyclospora spp. 1 1 0 1 0 3 0 0 2 8
Cryptosporidium spp. 0 0 0 0 0 0 0 3 0 3
Other foodborne viruses 0 1 1 1 0 0 0 0 2 5
(hepatitis A virus)
Other microorganism 0 0 0 0 2 0 1 0 0 3
(Listeria monocytogenes)
US–EU REPORTED OUTBREAKS IN FRESH PRODUCE 35

Table 3. Summary of Outbreaks Associated with Fresh Vegetables and Fruits in Europe
in Accordance with Directive 2003/99/EC, 2004–2012 (EFSA Summary Reports.
www.efsa.europa.eu/en/zoonosesscdocs/zoonosescomsumrep.htm)
Food vehicle
Vegetables Fruits
Total
Type of pathogen Salad Leafy Tomato Other Sprouts Berries Melon Juices Other outbreaks
Norovirus 15 26 1 9 0 55 0 0 2 108
Salmonella spp. 8 12 1 3 11 0 1 1 3 40
Escherichia coli 3 0 0 1 3 0 0 0 0 7
Campylobacter spp. 2 1 0 0 0 0 0 0 0 3
Shigella spp. 1 0 0 3 0 0 0 0 1 5
Clostridium spp. 0 1 0 6 0 0 0 0 0 7
Staphylococcus spp. 0 0 0 3 1 0 0 0 0 4
Yersinia spp. 0 0 0 3 0 0 0 0 0 3
Bacillus spp. 2 0 0 3 0 1 0 0 0 5
Giardia spp. 0 0 0 0 0 0 0 0 0 0
Cyclospora spp. 0 0 0 0 0 0 0 0 0 0
Cryptosporidium spp. 1 0 0 0 0 0 0 0 0 1
Other foodborne viruses 2 0 0 0 2 0 0 0 1 5
Other microorganisms 0 0 0 9 0 0 0 0 0 9

responsible (59% in the United States and 53% in the Euro-
pean Union) followed by Salmonella (18% in the United
States and 20% in European Union).
NoV is now widely viewed as the leading cause of food-
borne illness and is likely to be a much larger contributor to
produce-associated outbreaks than previously reported due to
improvements in diagnostics (Butot et al., 2008; Tuan Zai-
nazor et al., 2010; Radin et al., 2011). Specifically in the
United States, NoV outbreaks were strongly correlated with
the consumption of salads; in the European Union, this
pathogen was mainly linked to berries (raspberries) (Tables 2
and 3).
These results can be visualized by applying the MCA
(Fig. 1). Thus, dimension 1 clearly separates the United
States from the European Union. NoV is located slightly to
the left of the graph due to the higher number of produce
outbreaks reported in the United States, and it appears close
to berries and salad. In addition, according to dimension 1,
berries are placed in the same quadrant as the European
Union, and salad appears close to the United States.
Table 3 shows the increase of foodborne outbreaks associ-
ated with NoV in the European Union. A significant example is
the number of outbreaks linked to raspberries in the European
Union, which may be due to an increased distribution and

FIG. 1. Map resulting from the Multiple Correspondence Analysis of the microorganisms and the food vehicles of
foodborne outbreaks that occurred in the United States and in the European Union.
36
consumption of this fruit in that geographical area. The EFSA
has reported that a significantly high number of foodborne
outbreaks from 2007 to 2011 were caused by the combination
of NoVs and fresh and frozen raspberries (27 outbreaks), fol-
lowed by NoVs and leafy greens eaten raw as salads (24
outbreaks) in countries of Northern Europe (EFSA, 2013).
Other viruses such as hepatitis A, adenovirus, and rotavirus
appear as causative agents to a lesser extent (CDC’s database
and EFSA Summary Reports), and they did not show a clear
relationship between etiology and food vehicle (Fig. 1).
Salmonella was the most common bacterial pathogen re-
sponsible for produce outbreaks (Sivapalasingam et al.,
2004), accounting for nearly half of the outbreaks due to
bacteria (53% in the United States and 50% in the European
Union). In addition, Salmonella was the main bacterium re-
sponsible for multistate produce-associated outbreaks in the
United States (n = 24). For the European Union, the number
of Salmonella outbreaks has decreased since 2004, whereas it
has increased in the United States (EFSA Summary Reports
and CDC’s database). A total of 26 different Salmonella se-
rotypes have been identified so far (EFSA Summary Reports
and CDC’s database). Salmonella Typhimurium and Sal-
monella Newport were most involved in United States out-
breaks, both linked mainly to the consumption of tomatoes
(CDC’s database). In contrast, Salmonella Enteritidis was the
most common serotype in the European Union, associated
primarily with salad, followed by Salmonella Newport,
which is mostly related to the consumption of lettuce ac-
cording to EFSA Summary Reports. Salmonella outbreaks
stood out as the microorganism involved in the majority of
sprouts-associated outbreaks (n = 14 in the United States and
n = 11 in the European Union) (Tables 2 and 3). The types of
sprouts included alfalfa, bean, and mung bean. These results
are reflected in the MCA (Fig. 1). Much research has been
performed to try to find an explanation for the increase in
Salmonella outbreaks. Currently, the internalization theory is
gaining strength since several studies have indicated that
Salmonella spp. is capable of replicating to relatively high
levels on or within the plant (Schikora et al., 2008; Deering
et al., 2012). It is likely that bacteria can enter the plant and
move through it passively, being transported via the mass
flow of water entering the plant and moving within it
(Deering et al., 2012). Salmonella internalization occurs in
several leafy vegetables and fresh herbs and the level of in-
ternalization largely varies among plants and within the same
crop. Since internalized bacteria may evade disinfection, it is
of great interest to identify plants that are more susceptible to
bacterial internalization, as well as plant and environmental
factors that affect internalization (Golberg et al., 2011).
Regarding other microorganisms, E. coli and Campylo-
bacter outbreaks were more prevalent in the United States
(12.2% and 2.4%, respectively) than in the European Union
(3.8% and 1.6%, respectively). In fact, both microorganisms
appear in the same side of the graph quadrant as the United
States (Fig. 1). As expected, E. coli O157 was the most
prevalent strain (Sivapalasingam et al., 2004; Heaton and
Jones, 2008; Berger et al., 2010). Furthermore, E. coli was
the second most common pathogen identified as the cause of
multistate outbreaks in the United States (n = 15). Regarding
food vehicle, E. coli was associated with the consumption of
various fresh vegetables, fruits, and sprouts (Tables 2 and 3),
but especially with lettuce and unpasteurized apple juices
CALLEJÓN ET AL.
(Friesema et al., 2008; Berger et al., 2010; Buchholz et al.,
2011; Althaus et al., 2012; Kase et al., 2012; Orue et al.,
2013). As seen in Table 2, lettuce was the fresh produce most
linked to E. coli infections in the United States, causing eight
multistate outbreaks out of 22 total outbreaks in the period
under consideration. Furthermore, the most important mul-
tistate outbreak occurring in the United States in 2006 was
due to the consumption of fresh spinach, and it resulted in 238
infected cases and 5 deaths (CDC’s database). In the Euro-
pean Union, sprouted fenugreek seeds were involved in the
major food outbreak in 2011 (EFSA Summary Reports), re-
sulting in 3000 cases with bloody diarrhea, 852 cases of he-
molytic uremic syndrome, and 53 deaths (Mora et al., 2011;
Borgatta et al., 2012). The causative agent was E. coli O104:H4,
a new strain not previously reported in the European Union.
Campylobacter jejuni was involved in produce outbreaks
linked to the consumption of salad, lettuce, tomato, and
melon (Tables 2 and 3). On the other hand, certain bacteria
such as Shigella, Bacillus, and Staphylococcus were associ-
ated with higher numbers of produce-associated outbreaks in
the European Union than in the United States.
Additionally, produce outbreaks linked to Clostridium and
Yersinia occurred exclusively in several European Union
countries (EFSA Summary Reports). None of these micro-
organisms showed a clear relationship between etiology and
food vehicle, as reflected in the MCA (Fig. 1). This relative
lack of specificity in association between foods and patho-
gens suggests that cross-contamination, environmental con-
tamination, and food-handler contamination may be common
along the food chain (Greig and Ravel, 2009). In addition,
these microorganisms did not show a clear trend, with the
number of produce outbreaks associated with them ranging
unpredictably between one and three from 2004 to 2012.
The potential for environmental Listeria, mainly
L. monocytogenes, to contaminate fresh produce and lead to
enteric infection has long been recognized (Blakeman, 1985).
However, Listeria outbreaks linked to fresh produce are in-
frequent and tend to be limited to vulnerable groups (Heaton
and Jones, 2008). In fact, Listeria was responsible for only
three multistate outbreaks in the United States (Table 2).
Finally, parasites have rarely been involved in produce-
related outbreaks ( < 4% in the United States), and most of
those outbreaks have been due to Cyclospora.
According to the available data, produce-associated out-
breaks were more likely to take place in food-service estab-
lishments (54% in the United States and 40% in the European
Union), especially in restaurants during preparation by in-
fected food workers (Hall et al., 2014), followed by private
homes. Other common locations of consumption were
workplaces and schools. Limited numbers of outbreaks were
also described in hospitals, residential establishments, food
retailers, and farm shops, among others (CDC’s database and
EFSA Summary Reports).
Most NoV outbreaks due to fresh produce occurred in food-
service establishments (60% in the United States and 45% in
European Union), especially at workplaces (CDC’s database
and EFSA Summary Reports). In the United States, Salmo-
nella was most commonly implicated in outbreaks linked to
food-service establishments (40%) while in the European
Union, it was more prevalent in private homes (34%).
Recommendations to cope with trends include following
the Good Agricultural Practices Guides (FDA, 2008) for
US–EU REPORTED OUTBREAKS IN FRESH PRODUCE
the produce industry as well as protection from contamina-
tion by food handlers who are ill or infected by pathogens,
especially for NoV. The most effective strategies for control
of NoV in fresh vegetables and fruits focus on prevention
measures for avoiding viral contamination. Specifically for
NoV, CDC has published a list of precautions such as hand-
washing with water and soap after contacting the toilet, and
before eating or preparing or handling food, as well as
washing fruits and vegetables carefully before eating them
(CDC, 2013b).
Conclusions
Foodborne disease outbreaks associated with fresh fruits
and vegetables remain prevalent in the European Union and
United States as demonstrated by the number of outbreaks
reported annually, lacking a clear trend to diminish. There is
substantial evidence that contamination of fresh produce with
pathogens is significant and may contribute to the foodborne
illness burden. Within our study, NoV and Salmonella were
the most common pathogens linked to the fresh produce
outbreaks. NoVs were primarily linked with the consumption
of salad in the United States and of berries in the European
Union. Salmonella was the leading cause of multistate pro-
duce outbreaks in the United States and was the pathogen
involved in the majority of sprouts-associated outbreaks.
Disclosure Statement
No competing financial interests exist.
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Address correspondence to:
Ana M. Troncoso, PhD
Área de Nutrición y Bromatologı́a
Facultad de Farmacia
Universidad de Sevilla
C/ P. Garcı́a González n2
E- 41012 Sevilla, Spain
E-mail: amtroncoso@us.es
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