2 figures omitted
Three outbreaks of Salmonella infections associated
with eating Roma tomatoes were detected in the United States and Canada in
the summer of 2004. In one multistate U.S. outbreak during June 25–July
18, multiple Salmonella serotypes were isolated,
and cases were associated with exposure to Roma tomatoes from multiple locations
of a chain delicatessen. Each of the other two outbreaks was characterized
by a single Salmonella serotype: Braenderup in one
multistate outbreak and Javiana in an outbreak in Canada. In the three outbreaks,
561 outbreak-related illnesses from 18 states and one province in Canada were
identified. This report describes the subsequent investigations by public
health and food safety agencies. Although a single tomato-packing house in
Florida was common to all three outbreaks, other growers or packers also might
have supplied contaminated Roma tomatoes that resulted in some of the illnesses.
Environmental investigations are continuing. Because current knowledge of
mechanisms of tomato contamination and methods of eradication of Salmonella in fruit is inadequate to ensure produce safety, further
research should be a priority for the agricultural industry, food safety agencies,
and the public health community.
In July 2004, a total of 429 culture-confirmed, outbreak-associated
salmonellosis cases were identified in nine states (Maryland, Michigan, Missouri,
North Carolina, New Hampshire, Ohio, Pennsylvania, Virginia, and West Virginia);
these cases occurred among persons eating at delicatessen chain A sites, with
symptom onset during July 2-27. The median age of patients was 35 years (range:
1-81 years); 52% were male. No deaths occurred, but 30% of patients were hospitalized.
These cases yielded Salmonella serotypes Javiana
(383), Typhimurium (27), Anatum (five), Thompson (four), Muenchen (four),
and Group D untypable (six).
State and local health departments, in collaboration with CDC, conducted
a case-control study, which included 53 case-patients and 53 well meal-companion
controls. Of the 53 case-patients, 47 (90%) ate Roma tomatoes, compared with
24 (48%) of the controls. Multivariate analysis data demonstrated a strong
association with consumption of Roma tomatoes (adjusted odds ratio = 7.1;
95% confidence interval [CI] = 1.5-34). Delicatessen chain A had
purchased presliced Roma tomatoes from a single processor for all of its 302
stores in five states. S. Anatum, with a pulsed-field
gel electrophoresis (PFGE) pattern indistinguishable from that of five cases
in four states, was isolated from presliced Roma tomatoes sampled at a delicatessen
chain A site on July 13.
Roma tomatoes were removed from all delicatessen chain A sites on July
14. A total of 22 (5%) patients reported illness onset after July 19, outside
the incubation period for Salmonella. These illnesses
might be explained by factors such as continued Roma tomato use, poor recall,
low infectious dose, food saved and eaten later, or secondary transmission.
In the summer of 2004, a total of 125 confirmed cases of S. Braenderup infection with an indistinguishable PFGE pattern were
identified from 16 states (Delaware, Connecticut, Georgia, Iowa, Kansas, Maryland,
Massachusetts, Missouri, New Hampshire, New Jersey, New York, Ohio, Pennsylvania,
Virginia, West Virginia, and Wisconsin); patients had illness onset during
June 18–July 21. The median age of patients was 30 years (range: 0-84
years); 66% were female. No deaths occurred, but 20% of patients were hospitalized.
State and local health departments, in collaboration with CDC, conducted
a case-control study among persons aged 15-60 years. A case was defined as
infection with S. Braenderup yielding the outbreak
PFGE pattern, with illness onset after June 15. Controls were enrolled through
sequential-digit telephone dialing by using patients’ area codes. A
total of 38 case-patients and 79 controls were included. Patients were more
likely than controls to have eaten out multiple times during the 5 days preceding
illness onset (53% versus 34%) (odds ratio [OR] = 2.1; CI = 1.0-4.7). A higher
proportion of patients than controls ate cheese, lettuce, and tomatoes outside
the home, but these differences were not statistically significant. Using
meal information from 27 case-patients and 29 controls, restaurant managers
were asked about specific types of cheese, lettuce, and tomatoes used in dishes
eaten by customers. Roma tomatoes, which were eaten by 41% of case-patients
but only 14% of controls (OR = 4.1; CI = 1.1-15.3), were the only exposure
significantly associated with illness. These restaurants purchased whole Roma
tomatoes from tomato distributors.
Seven confirmed cases of S. Javiana infections
with indistinguishable PFGE patterns, but with patterns distinct from the
multiserotype Salmonella outbreak, were identified
from one Canadian province, Ontario; illness onset occurred during July 4-8,
2004. The median age of ill persons was 28 years (range: 23-36 years). No
deaths were reported, but 14% of persons were hospitalized. All patients ate
at the same restaurant. Although a case-control study was not conducted, Roma
tomatoes were the suspected outbreak vehicle because Roma tomatoes were the
only common food exposure among all patients.
The Food and Drug Administration (FDA), in conjunction with state and
provincial food regulatory agencies and state health departments, conducted
traceback investigations of the Roma tomatoes eaten by patients in all three
outbreaks. For each outbreak, Roma tomatoes were traced from restaurants back
to distributors, packers, or growers in the United States. Traceback investigation
of tomatoes from the multiserotype outbreak identified one field-packing operation
and three packing houses from three states as possible sources. Of these four
sources, Florida packing house A was also identified as a possible source
for the two other concurrent Roma tomato–associated salmonellosis outbreaks
(i.e., the S. Braenderup and S. Javiana outbreaks).
Quality-control procedures at the tomato-slicing facility associated
with the multiserotype Salmonella outbreak were inspected
while the facility was in active operation; no source of contamination was
identified. In addition, S. Javiana is typically
associated with the coastal Southeast, whereas the slicing facility is located
in the Northeast.
Environmental investigation of four packers and five associated farms
in Florida and South Carolina during August-November 2004 did not reveal a
clear source of contamination, and the packing houses appeared to be following
food-safety guidance. However, of these nine facilities, only Florida packing
house A and one associated farm were in active operation at the time of inspection.
Investigations will continue during the corresponding 2005 growing season.
R Corby, V Lanni, Brant County Health Unit, Ontario, Canada. V Kistler,
MEd, Allentown Health Bur; V Dato, MD, A Weltman, MD, C Yozviak, K Waller,
MD, K Nalluswami, MD, M Moll, MD, Pennsylvania Dept of Health. Center for
Food Safety and Applied Nutrition; Office of Crisis Management, Food and Drug
Admin. J Lockett, S Montgomery, DVM, M Lynch, MD, C Braden, MD, Div of Bacterial
and Mycotic Diseases, National Center for Infectious Diseases; SK Gupta, MD,
A DuBois, MD, EIS officers, CDC.
Tomatoes originated in South America, were introduced into Europe in
the 16th century, and are now a popular food worldwide. The Roma tomato was
developed in the mid-1950s as a firmer and more disease-resistant variety.1 Uncooked tomatoes have become an integral and nutritious
component of the daily diet. Approximately 5 billion pounds of fresh market
tomatoes are eaten annually in the United States, and thus the potential for
large outbreaks of Salmonella infections is a concern.
This report describes three outbreaks in the United States and Canada in which
Roma tomatoes were implicated; as a result of these outbreaks, 2004 had the
highest number of recorded annual tomato-associated Salmonella infections.
In the eastern United States, tomatoes are grown in natural habitats
for many known Salmonella reservoirs, including birds,
amphibians, and reptiles. Salmonella infections have
been linked to tomatoes since 1990, when S. Javiana
caused 176 illnesses in four midwestern states.2 Those
tomatoes, and those implicated in a subsequent outbreak in 1993, were traced
to a South Carolina packing house. Cross-contamination might have occurred
at the packing house, where substantial numbers of tomatoes passed through
a common wash tank.2 In 1994 and 1995, a Hazard
Analysis Critical Control Points program was implemented at this packing house
and disseminated to the tomato industry.3 The
key critical-control point implemented was maintenance of water quality, specifically
monitoring chlorine levels, pH, and water temperature in the wash tank. Of
seven subsequent tomato-associated Salmonella outbreaks,
six have been traced to other packing houses in the southeastern United States.4,5 Although produce packing houses are
specifically exempt from the requirements of Good Manufacturing Practices
(GMPs), FDA guidance6 to the produce industry
encourages GMP controls for water used in packing houses. However, the extent
to which FDA guidance has been adopted by the industry is unknown. Tomato-associated Salmonella outbreaks reported to CDC have increased in
frequency and magnitude in recent years and caused 1,616 reported illnesses
in nine outbreaks during 1990-2004, representing approximately 60,000 illnesses
when accounting for the estimated proportion (97.5%) of unreported illness.7
Salmonella can enter tomato plants through
roots or flowers8 and can enter the tomato
fruit through small cracks in the skin, the stem scar, or the plant itself.9 However, whether Salmonella can
travel from roots to the fruit, or if seeds can contaminate subsequent generations
of tomato plants, is unknown. Understanding the mechanism of contamination
and amplification of contamination of large volumes of tomatoes is critical
to prevent large-scale, tomato-associated outbreaks. Contamination might occur
during multiple steps from the tomato seed nursery to the final kitchen. Eradication
of Salmonella from the interior of the tomato is
difficult without cooking, even if treated with highly concentrated chlorine
Public health professionals should be aware of tomatoes as a possible
vehicle when investigating Salmonella outbreaks.
Current knowledge of mechanisms of tomato contamination and methods of eradication
of Salmonella in fruit are inadequate to fully define
interventions that will ensure produce safety. Studies into these concerns
should be a priority for the agricultural industry, food safety agencies,
and the public health community.
The findings in this report are based, in part, on contributions by
state public health departments in Connecticut, Delaware, Georgia, Iowa, Kansas,
Maryland, Massachusetts, Missouri, New Hampshire, New Jersey, New York, Ohio,
Pennsylvania, Virginia, West Virginia, and Wisconsin. M Hoekstra, M Balasegaram,
M Perch, C Snider, Div of Bacterial and Mycotic Diseases, National Center
for Infectious Diseases; D Burmeister, EIS Officer, CDC.
Outbreaks of. JAMA. 2005;293(23):2852–2856. doi:10.1001/jama.293.23.2852