INVITED ARTICLE FOOD SAFETY

Frederick J. Angulo, Section Editor

The Growing Threat of Foodborne Bacterial

Enteropathogens of Animal Origin
Herbert L. DuPont
University of Texas–Houston School of Public Health, St. Luke’s Episcopal Hospital, and Baylor College of Medicine, Houston, Texas

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Campylobacter and Salmonella species and Shiga toxin–producing Escherichia coli (STEC; the majority of which are type
O157:H7) efficiently enter the human food chain from infected or colonized animals. Poultry contamination with Campy-
lobacter and/or Salmonella species and produce contamination with STEC have become major public health challenges. The
global food supply, which allows us to purchase desired items throughout the year, a growing interest in consuming fresh
vegetables and fruits, and an increasing number of persons who consume foods at restaurants all assure that the health
threats associated with these pathogens will continue. Antibiotic use by humans and food animals selects for the development
of resistance among Campylobacter and Salmonella strains, promoting invasive forms of infection and complicating therapy
of illness. A comprehensive public health approach is needed that focuses on disease surveillance and infection control in
the food industry continuum, from harvesting and processing, to distribution, to later preparation in public eating estab-
lishments and in homes. Good Agricultural Practices, including the Hazard Analysis and Critical Control Point Program
and validation of critical infection-control points at all stages of the food industry cycle, coupled with other food safety
interventions, including irradiation for certain higher-risk foods, should help us improve the quality of food with regard to
microbials and reduce human disease.

Each year, an estimated 76 million cases of foodborne illness
occur, resulting in 325,000 hospitalizations and 5000 deaths
[1]. The annual cost associated with infection due to the 4 most
common bacterial enteropathogens acquired from contami-
nated food is ∼$7 billion [2]. The collateral damage adds im-
portantly to the cost, with lost productivity and litigation sec-
ondary to resultant illnesses. Three of the 4 common
enteropathogens (Campylobacter and nontyphoid Salmonella
species and Shiga toxin–producing Escherichia coli [STEC])
have an animal reservoir, can be associated with fatal compli-
cations, and are presently threatening our food supply.
The following topics are covered in this review: (1) the chang-
ing pattern of food consumption; (2) surveillance of foodborne
infectious diseases and disease-control methods; (3) emerging
public health threats associated with Campylobacter and Sal-
Received 29 May 2007; accepted 17 July 2007; electronically published 4 October 2007.
Presented in part: 15th Annual James H. Steele DVM Lecture at the University of Texas–
Houston School of Public Health, Houston, Texas, 4 April 2007.
Reprints or correspondence: Dr. H. L. DuPont, 6720 Bertner Ave., MC 1-164, Houston, TX
77030 (Herbert.L.Dupont@uth.tmc.edu).
Clinical Infectious Diseases 2007; 45:1353–61
 2007 by the Infectious Diseases Society of America. All rights reserved.
1058-4838/2007/4510-0018$15.00
DOI: 10.1086/522662
monella species and STEC, including the emergence of anti-
biotic-resistant strains of Campylobacter and Salmonella species;
and (4) the future and improved safety of the food supply.
CHANGING PATTERN OF FOOD CONSUMPTION
The general public became increasingly interested in consuming
fresh fruits and vegetables after the release of health claims
regarding the practice. Healthy People 2010 is a US government
program aimed at increasing the amount of fruits and vege-
tables in the diet, with the objective of increasing the percentage
of persons aged ⭓2 years who eat at least 2 daily servings of
fruit and at least 3 daily servings of vegetables to 75% and 50%,
respectively [3]. The last survey obtained (in 2005) by the Be-
havioral Risk Factor Surveillance System found rates of 33%
and 27%, respectively [3]. During the 1950s, grocery stores in
the United States stocked an average of 300 food items, whereas
this number grew 180-fold in the 1990s, to 25,000–50,000 dif-
ferent food items [4]. Increased availability of fresh foods in-
creases the risk of human illness associated with foodborne
pathogens [5]. More and more people are eating at commercial
food service establishments [6]. The risk of foodborne illness
is greater when food is eaten in public restaurants rather than
in homes [7, 8].

FOOD SAFETY • CID 2007:45 (15 November) • 1353

SURVEILLANCE OF FOODBORNE INFECTIOUS
DISEASES AND CURRENT DISEASE-CONTROL
METHODS
In 1996, the Food Safety and Inspection Service of the US
Department of Agriculture adapted the Pathogen Reduction,
Hazard Analysis and Critical Control Point Program (HACCP)
to the food industry. HACCP is a 7-point, science-based in-
fection-control strategy aimed at disease prevention involving
identification of controllable hazards, monitoring, verification,
and record keeping [9]. That year, the Emerging Infections
Program of the Centers for Disease Control and Prevention
(CDC), the US Department of Agriculture (via the Food Safety
tified risk factors for sporadic infection in infants include not
having been breast fed, increased exposure to reptiles, riding a
shopping cart next to meat or poultry, and consumption of
concentrated liquid infant formula during the 5 days before
exposure [28]. Breast-feeding appears to be protective in spo-
radic infantile salmonellosis [29].
Although the various Salmonella serotypes are found in many
foods, making it difficult to pinpoint the source and vehicles
of infection, identified risk factors for the more common se-
rotypes are identified and referenced in table 3.
Salmonella enterica serotype Typhimurium, which charac-
teristically demonstrates multidrug resistance, is responsible for
10%–30% of human Salmonella infections in the United States

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and Inspection Service), and the US Food and Drug Admin-
istration (FDA), together with selected state health depart-
ments, established the FoodNet program of active national sur-
veillance for 7 bacterial and 2 parasitic agents that are known
to be causes of foodborne illness. Also in 1996, the CDC, in
collaboration with cooperating state health departments, es-
tablished PulseNet, the national molecular subtyping network
for foodborne disease surveillance; PFGE was adopted as the
standard approach to subtyping. Now active in 50 states, the
PulseNet network has been replicated in Canada, Europe, Latin
America, and the Asia Pacific region to provide an international
approach to identify and respond to multinational outbreaks
of foodborne disease [10].
EMERGING PUBLIC HEALTH THREATS
ASSOCIATED WITH CAMPYLOBACTER AND
SALMONELLA SPECIES AND STEC
The estimated burden and clinical outcome of disease due to
the 3 zoonoses are provided in table 1. Identified risk factors
for pathogen-specific infection are discussed.
Campylobacter infection. Risk factors for human Cam-
pylobacter infection, including infection due to ciprofloxacin-
resistant strains, include recent foreign travel and consumption
of chicken or turkey at a commercial establishment [13]
(table 2).
Salmonella infection. The highest age-specific incidence of
salmonellosis is seen for infants aged !12 months [27]. Iden-
[30]. The major vehicles of transmission of this serotype are
beef and dairy products, including eggs [30, 37]. A case-control
study using 5 FoodNet surveillance sites found that prior receipt
of an antimicrobial agent was an important risk factor for
sporadically occurring multidrug-resistant S. Typhimurium in-
fection [31]. In case-control studies, independent risk factors
for sporadic S. Typhimurium DT 104 gastroenteritis include
prior antibiotic use, residence on a livestock farm, previous
international travel [32], consumption of raw eggs or under-
cooked meat, previous use of antibiotics, use of proton pump
inhibitors or H2 antagonists, and playing in a sandbox [33].
For S. enterica Enteritidis, the first or second most common
cause of Salmonella infection in the United States, important
host risk factors for sporadic infection include egg consumption
[38], chicken consumption outside the home [39], and inter-
national travel [40].
Between 1998 and 2002, the prevalence of multidrug-resis-
tant S. enterica Newport increased 5-fold, becoming the third
or fourth most common Salmonella serotype in the United
States [58]. This serotype and S. Typhimurium DT 104 are
typically resistant to the same drugs, including ampicillin, chlo-
ramphenicol, sulfamethoxazole, streptomycin, and tetracycline,
as well as the extended-spectrum cephalosporins (e.g., ceftriax-
one) [59], the treatment of choice for systemic pediatric sal-
monellosis. Risk factors for acquisition of multidrug-resistant
S. Newport infection include receipt of an antibiotic to which

Table 1. Estimates of annual disease burden for selected foodborne bacterial enteropathogens of animal origin.

Estimated no. Estimated no.

No. of cases of hospitalizations of deaths
Pathogen per year Complications of illness per year per year Reference(s)
Campylobacter species 1.4–2.5 million Reactive arthritis, Guillain-Barré syndrome 13,000 100 [1]
Nontyphoid Salmonella 1.4 million Sepsis, meningitis, reactive arthritis, 115,000 400–600 [1, 11]
species urinary tract infection
STEC 100,000 Hemorrhagic colitis, “ischemic colitis” 2000 91 [1, 12]
in elderly persons, HUS

NOTE. HUS, hemolytic uremic syndrome; STEC, Shiga toxin–producing Escherichia coli.

1354 • CID 2007:45 (15 November) • FOOD SAFETY

 Table 2. Risk factors for acquisition of diarrhea due to Campylobacter species and
fluoroquinolone-resistant Campylobacter species.

Infection, identified risk factors Reference(s)

Infection due to any Campylobacter strain
Consumption of undercooked poultry [14]
Consumption of chicken prepared by a commercial food establishment [15, 16]
Consumption of nonpoultry meat at a restaurant [16]
Consumption of unpasteurized milk [17]
Consumption of improperly treated surface water [18]
Receipt of antibiotics before exposure [15]
Contact with home pets [19, 20]
Exposure to farm animals [21]
Recent international travel [16, 19]

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Infection due to fluoroquinolone-resistant Campylobacter strains
Antibiotic use in animals [22, 23]
Recent foreign travel [13, 22, 24, 25]
Receipt of a fluoroquinolone or other antibiotic before exposure [22, 26]
Consumption of chicken or turkey at a commercial establishment [13]

the strain is resistant during the month before illness and con-
sumption of uncooked ground beef, runny scrambled eggs, or
omelets prepared in the home during the 5 days before the
onset of illness [41]. Bovine sources appear to be particularly
important for acquisition of multidrug-resistant S. Newport
infection [42].
Outbreaks of gastroenteritis due to S. enterica Heidelberg,
the third or fourth most commonly identified Salmonella se-
rotype in the United States, are characteristically related to
consumption of poultry or eggs [43, 44]. In one study of spo-
radic illness, egg consumption outside the home was found to
be particularly important [45].
ANTIBACTERIAL RESISTANCE OF
CAMPYLOBACTER AND SALMONELLA
SPECIES
Antibiotic use in agriculture exceeds that in human populations
[60–62] and is credited for producing resistance among enteric
bacterial pathogens, causing illnesses in humans that are dif-
ficult to treat [22, 62–64], including campylobacteriosis [23]
and salmonellosis [65]. The growth-promoting effects of an-
tibiotics in food animals should be better quantified, with em-
phasis on nonantimicrobial drugs that have equivalent benefits
for the food production industry [66]. Abolishment of the use
of antibiotics for growth promotion will lead to reductions in
the rate of drug resistance among bacterial enteropathogens
[67] while increasing meat costs by only fractions of a cent per
pound [60], making it cost-effective, considering both animal
production and human health goals [68].
The fluoroquinolones sarafloxacin and enrofloxacin were
first licensed for use in animals in 1995 and 1996, respectively;
the presence of fluoroquinolone-resistant Campylobacter strains
in chickens dramatically increased thereafter [69]. The removal
of fluoroquinolones from use in animal populations in the
European Union [70] and the United States [71] was a major
public health accomplishment. Additional efforts are needed
to reduce fluoroquinolone use by humans in our fight to slow
the emergence of antibacterial resistance among Salmonella spe-
cies [31] and Campylobacter species [22, 26].
A national registry study in Denmark demonstrated that pa-
tients with fluoroquinolone-resistant Campylobacter infection
had a 6-fold (95% CI, 1.62–23.47-fold) increased risk of in-
vasive disease or death ⭐30 days after obtainment of a stool
sample for culture, compared with patients whose illness was
due to fluoroquinolone-susceptible strains [72]. Compared
with drug-susceptible strains, multidrug-resistant Salmonella
strains were shown to have greater virulence [73], resulting in
more-severe infection and higher rates of hospitalization [74]
and mortality [75]. In a FoodNet study, bloodstream Salmonella
infection occurred more frequently among patients who were
infected with an isolate that was resistant to at least 1 anti-
bacterial drug (adjusted OR, 1.6; 95% CI, 1.2–2.1), compared
with patients who were infected with drug-susceptible strains
[76].
STEC, INCLUDING E. COLI O157:H7
In a study of 5 FoodNet sites, the following risk factors of
sporadic STEC infection were identified: eating at a table-ser-
vice restaurant (matched OR, 1.7; 95% CI, 1.0–2.9), eating a
pink (i.e., undercooked) hamburger at home (matched OR,
5.0; 95% CI, 1.7–15) and away from home (matched OR, 5.0;
95% CI, 1.3–20), using immunosuppressive medications
(matched OR, 11; 95% CI, 1.6–72), and living on or visiting
a farm for persons aged ⭓6 years (matched OR, 10; 95% CI,

FOOD SAFETY • CID 2007:45 (15 November) • 1355

 Table 3. Risk factors for acquiring nontyphoid Salmonella infection.

Salmonella enterica serotype Risk factors References

S. Typhimurium Consumption of undercooked meat or ground beef and diary prod- [30–36]
ucts, particularly eggs (raw eggs are associated with the highest
risk); receipt of antibiotics, H2 antagonists, or proton pump in-
hibitors before exposure; residence on a farm with livestock; in-
ternational travel; playing in a sand box
S. Enteritidis Consumption of eggs, particularly outside of the home; interna- [37–40]
tional travel
S. Newport Receipt of antibiotics before exposure; consumption of uncooked [41, 42]
ground beef, runny scrambled eggs, or omelets prepared in the
home; consumption of ground beef
S. Heidelberg Consumption of poultry or eggs, especially consumption of eggs [43–46]
outside of the home

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All Salmonella serotypes In addition to the risk factors above, consumption of raw vegeta- [47–55]
bles, including sprouts; nosocomial acquisition; exposure to rep-
tiles (lizards, snakes, and turtles), amphibians (frogs and newts),
baby poultry, and household pets fed natural pet treats, raw
food diets, and other animal food; and cleaning aquaria in sinks
Antibiotic-resistant Salmonella strainsa Antibiotic use in animals, receipt of antibiotics before exposure [31, 56, 57]
a
Most strains found in foods are antibiotic resistant.

1.8–53) or !6 years (matched OR, 5.2; 95% CI, 1.3–22) [77].
Other studies have revealed a variety of risk factors for or
epidemics of STEC infection, including visiting a diary farm
[78] or a petting zoo [79, 80].
There are 3 general modes of transmission of STEC infection
in human populations: foodborne transmission, environmental
transmission from contaminated animals or water, or trans-
mission through person-to-person contact. In a US study that
examined 18000 cases of STEC illness that occurred during
1982–2002 as part of 350 outbreaks occurring in 49 states,
foodborne transmission occurred in 183 cases (52%), person-
to-person transmission occurred in 50 cases (14%), waterborne
transmission occurred in 31 cases (9%), transmission associated
with animal contact occurred in 11 cases (3%), and transmis-
sion associated with laboratory acquisition occurred in 1 case
(0.3%); the transmission route was uncertain in 74 cases (21%)
[81]. In the reported outbreaks of foodborne infection, 75 out-
breaks (41%) were associated with ground beef, and 38 (21%)
were associated with contaminated produce [81].
Multiple-state outbreaks of STEC infection occurred in the
United States in 2005 and in 2006 in association with spinach
and lettuce purchased at retail outlets or at popular restaurant
chains in the United States [82, 83]. These outbreaks have put
great pressure on the growers, processors, distributors, retailers,
consumers, and the government [84]. Most studies of produce
contamination with STEC have focused on store-bought let-
tuce. Little is know about the attachment of STEC to growing
plants in the field, although this appears to be the central prob-
lem in outbreak illness. One study found that fully virulent
strains of STEC persisted in farm environments for 8 weeks
[85], whereas a second study found that the organisms survived
on the farm for 8–12 months [86, 87]. In a third study, when
bovine or poultry manure compost was exposed to irrigation
water contaminated with a pathogenic strain of E. coli O157:
H7 under natural growing conditions, STEC persisted in the
soil for 154–217 days and was detected on lettuce and parsley
for up to 77–177 days [88]. Recovery of viable STEC from the
inner tissues of lettuce may occur when plants are grown in
contaminated manure, providing evidence that STEC bacteria
is capable of entering the lettuce plant through the root system
with migration to the edible portion of the plant [89]. In a
related study, the association of lettuce seedlings with STEC in
soil was studied using experimentally contaminated irrigation
water in a hydroponic model and a soil model [90]. The path-
ogen was found to adhere preferentially to the plant root in
both model systems and to seed coats in the hydroponic system.
The studies support the idea that preharvest crop contami-
nation with STEC strains can occur via irrigation water through
the plant roots, which makes control measures designed to
prevent STEC contamination of produce particularly
challenging.
Although most diagnostic laboratories in the United States
routinely test for Salmonella and Campylobacter species when
stool samples obtained from patients with diarrhea are sub-
mitted for bacteriologic culture, not all routinely test for E. coli
O157:H7 strains [91]. Studies of non-O157 STEC strains that
allow determination of their incidence and disease-producing
capacity are lacking. Increased clinical suspicion and devel-
opment of improved methods of laboratory detection and iso-
lation are needed for this group of organisms [92].

1356 • CID 2007:45 (15 November) • FOOD SAFETY

THE FUTURE AND IMPROVED SAFETY
OF THE FOOD SUPPLY
General approaches needed. Validation of the effectiveness of
the HACCP system should be undertaken, with identification
of the most relevant critical control points through hypothesis-
driven research [93, 94]. Methods for controlling contamina-
tion of produce are of greatest importance, requiring research
to define routes of transmission and critical control points at
all phases of the food production-consumption cycle.
Improving food safety in restaurants. Although all eating
establishments are instructed by city and health departments
to have an HACCP plan, the impact of these programs in
preventing foodborne illness remains largely untested. In 1998,
in Los Angeles County, a restaurant hygiene-grading program
was implemented that used publicly posted grade cards [95].
The grading program was associated with a 13.1% decrease
(P ! .01) in the number of foodborne-disease hospitalizations
in the county during the 2 subsequent years of the study.
Improving food safety in homes. With the reduction of
cross-contamination and improvement in personal hygiene, an
estimated 80,000 enteric infections could be prevented each year
in US households, resulting in savings of $138 million [96]. In
ranking behaviors in the home that would lead to reduced food-
borne illness, use of a thermometer for cooking and hand wash-
ing in the kitchen were ranked as the 2 most important behavior
modifications [97]. In a study of home food-handling practices,
a significant association was found between inconsistent hand
washing and food preparation and an increased risk of sporadic
salmonellosis in adults (adjusted OR, 8.3; 95% CI, 1.1–61.8) [98].
An economic model found benefit of a disinfection program for
high-risk food preparation, particularly when the household con-
tained elderly or immunocompromised persons [96]. In-home
foodborne transmission of enteric pathogens is most important
when persons at the extremes of age or others with underlying
medical conditions and compromised immune systems live in
the household [99]. Such persons should not eat certain foods,
including raw seed sprouts [100]. Persons who are receiving long-
term treatment with H2 antagonists and proton pump inhibitors
are at increased risk for foodborne illness [33]. The CDC has
recommended that all consumers avoid consumption of unpas-
teurized milk and milk products and certain raw or undercooked
products, including oysters, eggs, ground beef, and poultry; more
can be found at the Fight Back Web site (http://www.fightbac.org)
[101]. A mathematical model has been proposed to address in-
dividual hygiene practices during food preparation and con-
sumption patterns in private homes that could be tested for an
association with sporadic enteric illness [102].
Food irradiation: an underused method of improving food
quality. Food irradiation is a nonthermal method to reduce
or eliminate pathogenic microbes in food. Cobalt 60 or Cesium
137 emit high-energy photons called gamma rays, which yield
neutrons that penetrate food up to a few feet in depth. E-beam
irradiation directs a stream of high-energy electrons by op-
posing guns resembling the technology seen in televisions. X-
ray irradiation releases electrons, which can pass through thick
foods. In food irradiation, the energy from the rays is trans-
ferred to water and other microbial molecules, creating tran-
sient, reactive chemicals that cause defective microbial DNA,
making organisms unable to propagate. Microbes differ in their
susceptibility to irradiation and the rate at which they can repair
damaged DNA. The larger the pathogen (and the more DNA),
the more susceptible they are to the lethal effects of irradiation.
The methodologies are safe, and the World Health Organization
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has endorsed food irradiation, as have the CDC, the US De-
partment of Agriculture, and the FDA.
There are ∼60 commercial irradiation facilities available in
the United States. In 1997, the FDA approved the use of ion-
izing radiation to inactivate pathogenic bacteria in red meat.
The principal arguments against pursuing food irradiation are
2-fold. First, the technology has not been adequately studied
for harmful effects caused when altered chemical bonds and
potentially toxic ions or free radicals react with constituents in
food to form “radiolytic products” [103]. Second, the specific
foods for which the approach should be used and the specific
methodology for decontamination have not been fully devel-
oped. A major issue in moving this concept forward is con-
sumer acceptance of irradiated foods in the absence of public
health laws and requirements [104]. With efforts to educate
the public about irradiation of food at the grocery store level,
consumer acceptability is likely to improve [105]. This year,
the FDA proposed letting companies use the term “pasteurized”
to describe irradiated foods [106], which could help with public
acceptance. Irradiation will be useful for certain foods, such as
poultry.
CONCLUSIONS
Although the pathogen load of food animals has improved in
response to good hygiene and sanitation practices on farms and
during transportation, there remain obstacles to disease pre-
vention. Expanded surveillance of pathogen-specific foodborne
disease will allow more rapid implementation of control mea-
sures. Methods of reduction of pathogen load present in ani-
mals when slaughtered and in produce at time of harvest are
needed.
There remains a disconnect between government monitoring
and disease-control measures and the complex chain of food
production and preparation, from farms where butchering or
harvesting take place to retail stores, restaurants, and com-
mercial caterers to homes. Focusing on major local and inter-
state outbreaks has helped to implement important control
FOOD SAFETY • CID 2007:45 (15 November) • 1357
measures, yet we are missing many crucial outbreaks [107],
underscoring the need for enhanced capacity for surveillance
of foodborne disease. The capacity of state health departments
to respond to foodborne disease outbreaks will require ad-
dressing shortages in epidemiology and laboratory support for
outbreak investigation [108]. Although efforts are underway to
deal with this issue, there remains a limited worldwide public
health infrastructure to adequately detect outbreaks of food-
borne disease [109], limiting the speed and completeness of
disease-control measures [110].
Food is being increasingly imported from developing coun-
tries [111] where production and surveillance standards are
lower than are those for growers in the United States. Although
good agricultural practices are essential for control of food-
borne disease, we need sensitive, field-tested molecular methods
to detect specific pathogens in foods during production and
distribution [112]. This is difficult, considering sampling prob-
lems and the many pathogens that can potentially cause food-
borne disease. Newer molecular methods, which more actively
fingerprint bacterial enteropathogens, may provide a more ac-
curate approach for molecular typing in outbreak investigations
[113].
We need to move faster with regard to methods of pathogen
reduction in slaughtered animals and harvested produce. Ir-
radiation methods should be use for certain higher-risk foods,
such as poultry. Decontamination of produce remains a chal-
lenge and studies are needed to determine the optimal method
to reduce pathogen loads at harvest, including use of chemicals,
such as peracetic acid [114], ozone [115], and irradiation [116].
Acknowledgments
Potential conflicts of interest. H.L.D.: no conflicts.
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