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Published Date: 2008-09-03 21:00:30
Subject: PRO/AH> Salmonellosis, serotype Saintpaul, tomatoes - USA (17): peppers
Archive Number: 20080903.2759

SALMONELLOSIS, SEROTYPE SAINTPAUL, TOMATOES - USA (17): PEPPERS
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Date: Thu 29 Aug 2008
Source: MMWR 57; 929-934 [edited]
<http://www.cdc.gov/mmwr/preview/mmwrhtml/mm5734a1.htm?s_cid=mm5734a1_e>

On 22 May 2008, the New Mexico Department of Health (NMDOH) notified
CDC about 4 persons infected with _Salmonella [enterica_ serotype]
Saintpaul strains that were indistinguishable from each other by
pulsed-field gel electrophoresis (PFGE) and 15 other persons with
Salmonella infections whose isolates had not yet been characterized.
In the following weeks, cases continued to be reported, and the
outbreak expanded to include 43 states, the District of Columbia
(Figure 1 [for figures, see original URL - Mod.LL]), and Canada. This
report is an interim summary of results from 7 epidemiologic studies,
traceback investigations, and environmental investigations related to
the outbreak. Further data collection and analyses are ongoing.

As of 25 Aug 2008, a total of 1442 persons had been reported infected
with the outbreak strain. At least 286 persons have been
hospitalized, and the infection might have contributed to 2 deaths.
The outbreak began late in April 2008, and most persons became ill in
May or June 2008. The outbreak appears to be over; however, CDC and
state health departments are continuing to conduct surveillance for
cases of infection with the outbreak strain. Preliminary
epidemiologic and microbiologic results to date support the
conclusion that jalapeno peppers were a major vehicle by which the
pathogen was transmitted, and serrano peppers also were a vehicle;
tomatoes possibly were a vehicle, particularly early in the outbreak.
Contamination of produce items might have occurred on the farm or
during processing or distribution; the mechanism of contamination has
not been determined. These findings indicate that additional measures
are needed to enhance food safety and reduce illnesses from produce
that is consumed raw.

Epidemiologic Studies
---------------------
A case was defined as laboratory-confirmed infection with _S._
Saintpaul with XbaI pattern JN6X01.0048, the outbreak strain. Of the
1442 cases reported, public health agencies have reported illness
onset information for 1414 patients. Illnesses began during 16 Apr
2008-11 Aug 2008; most persons became ill in May or June 2008 (Figure
2). Complete demographic information is available for 565 ill
persons. Of these, 52 percent were male; 79 percent were white, 8
percent were American Indian/Alaska Native, 3 percent were black, 2
percent were Asian/Pacific Islander, and 7 percent reported other or
multiple races. Hispanic ethnicity was reported for 22 percent.
Patient ages ranged from less than one to 99 years (median age: 33
years), and the highest incidence was among persons aged 20-29 years.
Cases were distributed among 43 states, the District of Columbia, and
Canada, with particularly high incidence rates in New Mexico and
Texas (Figure 1).

Soon after the 1st cases were detected in mid-May 2008, additional
cases were identified in Texas and the Navajo Nation through PulseNet
(the national molecular subtyping network for foodborne disease
surveillance). 19 ill persons were initially interviewed in detail to
generate hypotheses about the source of their illnesses. To identify
the source, NMDOH, the Texas Department of State Health Services
(TXDSHS), Navajo Nation, the Indian Health Service (IHS), and CDC
conducted a multistate case-control study of laboratory-confirmed
infections. For this case-control study, a case was defined as
diarrheal illness (3 or more loose stools in a 24 hour period) that
began on or after 1 May 2008 in a person infected with the outbreak
strain. Controls were well persons in the community matched by age
and location using reverse telephone directories and by face-to-face
interviews. The matched analysis included 51 case-patients and 106
controls. Using a questionnaire based on hypotheses generated by the
preliminary interviews, study participants were asked about foods
consumed during the week preceding their illness. On univariate
analysis, illness was significantly associated with eating raw
tomatoes (matched odds ratio [mOR] = 6.7) and had a borderline
association with eating tortillas (mOR = 2.8) in the week preceding
illness onset (Table [for table, see original URL - Mod.LL]). Illness
remained significantly associated with eating raw tomatoes (mOR =
5.6) after adjusting for consumption of tortillas. Illness was not
significantly associated with eating salsa (mOR = 1.7), guacamole
(mOR = 1.6), or any other food item.

In June 2008, increasing numbers of cases were reported from a
growing number of states. State and local health departments
identified clusters of illness in restaurants by interviewing ill
persons whose isolates had the outbreak PFGE pattern and asking about
exposures to suspect foods and about any recent meals at restaurants.

Beginning on 20 Jun 2008, TXDSHS and CDC investigated a cluster of 47
ill persons associated with a Mexican-style restaurant in Texas. For
this case-control study, a case was defined as diarrheal illness in a
person who ate at the restaurant in the week before illness began;
culture confirmation was not required. Controls were well meal
companions. The analysis included 47 case-patients and 36 controls.
On multiple logistic regression, illness was significantly associated
only with eating salsa (adjusted odds ratio [aOR] = 62.3) (Table).
The salsa ingredients included raw tomatoes and raw jalapeno peppers.

Beginning on 24 Jun 2008, TXDSHS and CDC investigated another cluster
of 33 ill persons, this one associated with a local Mexican-style
restaurant chain in Texas. For this case-control study, a case was
defined as diarrheal illness in a person who ate at either of 2
restaurants in the chain during the week before illness began;
culture confirmation was not required. Controls were well meal
companions and restaurant patrons identified by credit card receipts.
The analysis included 33 case-patients and 62 controls. Illness was
significantly associated only with eating salsa (aOR = 7.5) (Table).
The salsa ingredients included commercially canned tomatoes and raw
jalapeno peppers, but not raw tomatoes. These results indicated that
jalapeno peppers were a likely source of illness.

Beginning on 26 Jun 2008, to further investigate possible food
vehicles, CDC and state and local health departments in 29 states
conducted a 2nd multistate case-control study of laboratory-confirmed
infections identified through PulseNet. A case was defined as
diarrheal illness that began on or after 1 Jun 2008 in a person
infected with the outbreak strain. Controls were well persons in the
community matched by age and location using reverse telephone
directories. The matched analysis included 141 cases and 281
controls. After adjusting for sex, Hispanic ethnicity, and additional
age variation, illness was significantly associated with eating at a
Mexican-style restaurant in the week preceding illness onset (mOR =
4.6) (Table). Illness also was significantly associated with eating
pico de gallo (mOR = 4.0), corn tortillas (mOR = 2.3), and freshly
prepared salsa (mOR = 2.1) (Table). Illness was not significantly
associated with any other individual food items or ingredients.

Beginning on 30 Jun 2008, the Minnesota Department of Health
investigated a cluster of 19 persons with _S._ Saintpaul infection
associated with a natural food restaurant. For this case-control
study, a case was defined as diarrheal illness in a person infected
with the outbreak strain who ate at the restaurant in the week before
illness began. Controls were well meal companions and restaurant
patrons identified by credit card receipts. The analysis included 19
case-patients and 73 controls. On univariate analysis, illness was
significantly associated with eating any of several items including
salsa, guacamole, red bell peppers, cilantro, and jalapeno peppers.
Both types of peppers had been diced before they arrived at the
restaurant. On multivariate analysis, illness was only significantly
associated with eating raw, jalapeno peppers (OR = 62.0) (Table).
This study provided more evidence that consumption of raw jalapeno
peppers was a major risk factor for illness.

Beginning on 7 Jul 2008, the North Carolina Division of Public
Health, the Mecklenburg County Health Department, and CDC
investigated a cluster of 13 ill persons associated with a local
Mexican-style restaurant. For the case-control study, a case was
defined as diarrheal illness in a person infected with the outbreak
strain who ate at the restaurant in the week before illness began.
Controls were well restaurant patrons identified by credit card
receipts. The analysis included four case-patients and 113 controls.
On multivariate analysis, illness was significantly associated only
with eating guacamole (aOR = 8.7) (Table). The guacamole ingredients
included avocado, raw Roma tomatoes, raw red onions, raw serrano
peppers, cilantro, salt, and lime juice, but not jalapeno peppers.
This study demonstrated that not all of the outbreak illnesses could
be linked to eating jalapeno peppers.

During 22 May 2008-7 Aug 2008 state and local health departments in
14 states and the District of Columbia reported a total of 33
restaurant-associated clusters of illness. The median number of
laboratory confirmed cases for all clusters was 4; 26 (79 percent) of
the 33 clusters had 8 or fewer laboratory-confirmed cases. Raw
jalapeno peppers were not served in 4 of the restaurants, serrano
peppers were not served in 19 restaurants, and raw tomatoes of
various types were served in all restaurants. Of the 4 restaurants
without raw jalapeno peppers, 2 had serrano peppers.

During 11-25 Jul 2008, NMDOH, the Arizona Department of Health
Services, Navajo Nation, IHS, and CDC conducted a household-based
case-control study among non-restaurant-associated cases in New
Mexico, Arizona, and the Navajo Nation. A case-household was defined
as a household with a case (defined as diarrheal illness beginning on
or after 1 Jun 2008 in a person infected with the outbreak strain).
Control-households were enrolled systematically from the same
community and had no members who reported diarrheal illness on or
after 1 Jun 2008. The matched analysis included 41 case-households
and 107 control-households and compared the presence of specific
foods in the household regardless of whether the respondent
remembered eating them. On univariate analysis, illness in the
household was significantly associated with having a raw jalapeno
pepper in the household (mOR = 2.9), and illness had a borderline
association with having a raw serrano pepper in the household (mOR =
3.0) during the week preceding illness onset (Table). Illness was not
significantly associated with the presence of any other food item in
the household. A concurrent case-control study that evaluated
individual-level exposures asked the case-patient in each
case-household and respondents in control-households about recent
food exposures. This study did not identify an association between
illness in the case-patients and eating raw jalapeno or serrano
peppers. These results suggested that at the time these illnesses
were occurring, jalapeno peppers and perhaps serrano peppers were
likely vehicles for illness among persons not associated with a
restaurant cluster, although persons might not have specifically
recalled consuming the peppers.

Environmental and Traceback Investigations
--------------------------------------
The Food and Drug Administration (FDA) traced back the processing and
distribution pathway for tomatoes associated with several ill
persons. These tracebacks did not converge onto a single packer,
distributor, or growing area of tomatoes. Tomatoes linked to ill
persons and tomatoes randomly collected from the distribution chain
in several states were cultured; none of these cultures yielded
_Salmonella_. FDA traced the source of the jalapeno peppers
associated with illness in the 2 previously described Texas
restaurant-associated clusters to distributors in Texas that received
jalapeno peppers from Mexico. On 21 Jul 2008, FDA reported isolation
of the outbreak strain from a jalapeno pepper sample obtained from
one of these distributors. The pepper likely was grown on a farm in
Tamaulipas, Mexico (farm A); this farm also grew serrano peppers and
Roma tomatoes. FDA did not isolate the outbreak strain from
environmental samples from farm A but did isolate the outbreak strain
from a sample of serrano peppers and a sample of water from a holding
pond used for irrigation from another farm (farm B) in Tamaulipas.
Farm B also grew jalapeno peppers, but not tomatoes. Farms A and B
provided produce to a common packing facility in Mexico that exports
to the USA. In addition, on 29 Jul 2008, the Colorado Department of
Public Health and Environment (CDPHE) reported isolation of the
outbreak strain from a jalapeno pepper collected from the household
of a person in Colorado who had developed illness with the outbreak
strain. CDPHE traced this pepper from the grocery store where it had
been purchased to another distributor in Texas, which reportedly
received jalapeno peppers from farms in Mexico; however, the specific
farms have not been identified.

Control Measures
----------------
Since 3 Jun 2008, CDC, FDA, and public health partners have issued
multiple public advisories recommending that consumers avoid eating
certain produce items. A limited advisory recommending that consumers
in New Mexico and Texas avoid eating certain types of tomatoes was
issued on 3 Jun 2008, and the advisory was expanded nationwide on 7
Jun 2008 (Figure 2 [for figures see original URL - Mod.LL]). After
associations were identified between illness and eating jalapeno and
serrano peppers, CDC and FDA issued successive advisories
recommending that consumers avoid eating jalapeno and serrano peppers
grown in Mexico; the 1st nationwide jalapeno pepper advisory was
issued on 9 Jul 2008 (Figure 2). The tomato advisory was lifted on 17
Jul 2008; the jalapeno and serrano pepper advisories remain in effect.

[Byline: Jungk J, Baumbach J, Landen M, et al]

Editorial Note:
--------------
Contaminated produce eaten raw is an increasingly recognized vehicle
for transmission of _Salmonella_ and other pathogens (1). Each year,
approximately 36 000 laboratory-confirmed cases of salmonellosis are
reported in the USA through national serotype-based surveillance (2).
_S._ Saintpaul is an uncommon serotype, causing, on average, 1.6
percent of all reported laboratory-confirmed salmonellosis each year.
In 2007, only 40 human isolates of the outbreak strain were submitted
to PulseNet. This report describes the largest foodborne disease
outbreak identified in the USA in the past decade, based on the
number of culture-confirmed cases. Because many persons with
salmonellosis do not seek care or have a stool specimen tested, many
more illnesses likely have occurred than those reported (3).

In this outbreak, epidemiologic studies revealed associations between
illness and more than a single raw produce item. Although most
multistate enteric disease outbreaks have been linked to a single
food vehicle, an outbreak attributed to both parsley and cilantro
grown on one farm has been reported (4). The initial case-control
study identified an association between illness and eating raw
tomatoes. Subsequent studies identified an association between
illness and eating raw jalapeno peppers, an item commonly eaten with
tomatoes in Mexican-style cuisine. Epidemiologic data also suggested
an association with raw serrano peppers. These associations triggered
product alerts and led to product tracing and microbiologic studies,
which indicated that jalapeno and serrano peppers grown, harvested,
or packed in Mexico were contaminated with the outbreak strain. The
epidemiologic and microbiologic results support the conclusion that
jalapeno peppers were a major vehicle by which the pathogen was
transmitted, and that serrano peppers also were a vehicle.
Consumption of peppers was not implicated in either of the 2
multistate case-control studies. However, produce items such as
peppers that are typically consumed in small quantities as
ingredients of other dishes might not be remembered and can be
difficult to implicate (5).

Neither raw jalapeno nor serrano peppers have been identified
previously as a vehicle for a foodborne disease outbreak in the USA.
Little is known about the survival and growth characteristics of
_Salmonella_ on these peppers, although rapid growth in jalapeno
pepper extract has been reported (6). Tomatoes possibly were a
vehicle for infection, particularly early in the outbreak. In the
initial case-control study, illness was significantly associated with
consumption of raw tomatoes and not with foods containing peppers,
such as salsa or guacamole. Consumption of jalapeno or serrano
peppers was not assessed in this initial study because in
hypothesis-generating interviews conducted with 19 case-patients,
only 5 (26 percent) reported eating peppers other than red or green
bell peppers in the week before illness began. In addition, a survey
of 75 case-patients in Texas whose illnesses began before 7 Jun 2008,
using a questionnaire that asked specifically about pepper
consumption, found a relatively low proportion who reported eating
raw jalapeno (39 percent) or raw serrano (8 percent) peppers in the
week before illness began, whereas reported raw tomato consumption
was high (85 percent). Finding the outbreak strain on 2 types of
peppers from 2 farms supports the possibility of contamination of
other produce items, including tomatoes, during growing, processing,
or distribution.

Local, state, tribal, and federal response capacity often is strained
during large and complex outbreaks, and structure and capabilities
vary among jurisdictions. This can cause delays in identifying cases
and in conducting investigations. In this outbreak investigation, the
median time from illness onset to submission of the PFGE pattern of
patients' _Salmonella_ isolates to PulseNet was 17 days; 90 percent
were submitted within 27 days. Faster transfer of bacterial strains
to public health laboratories and faster subtyping in those
laboratories would result in more timely investigation of cases of
infection. Epidemiologic investigations can benefit from faster
methods for interviewing ill and well persons, improved interview
formats, and rapidly adaptable electronic data gathering and
transmission platforms. Improvements in the ability to trace
contaminated produce quickly and accurately also would improve the
speed of investigations, the speed and specificity of recalls, and
the determination of the ultimate causes of contamination. For
several years, CDC has been improving the efficiency of epidemiologic
investigations through OutbreakNet, the network of public health
officials that investigates outbreaks of enteric illnesses
nationwide, and through participation in the Council to Improve
Foodborne Outbreak Response,* a multidisciplinary working group. In
addition, FDA has been enhancing the safety of produce by
collaborating with state officials, academia, and industry on
multiyear initiatives to increase the safety of leafy greens and
tomatoes. FDA and its partners are working to improve guidance and
policies intended to minimize outbreaks and to improve produce-safety
research and education.

References
----------
1. Sivapalasingam S, Friedman CR, Cohen L, Tauxe RV: Fresh produce: a
growing cause of outbreaks of foodborne illness in the United States,
1973-1997. J Food Prot 2004;67: 2342-2353.
2. CDC: PHLIS surveillance data: Salmonella annual summary, 2005.
Atlanta, GA: US Department of Health and Human Services, CDC; 2007.
Available at
<http://www.cdc.gov/ncidod/dbmd/phlisdata/salmonella.htm>.
3. Voetsch A, Van Gilder TJ, Angulo FJ, et al: FoodNet estimate of
the burden of illness caused by nontyphoidal Salmonella infections in
the United States. Clin Infect Dis 2004;38: S127-S134.
4. Naimi TS, Wicklund JH, Olsen SJ, et al: Concurrent outbreaks of
Shigella sonnei and enterotoxigenic Escherichia coli infections
associated with parsley: implications for surveillance and control of
foodborne illness. J Food Prot 2003;66: 535-541.
5. Mahon BE, Ponka A, Hall WN, et al: An international outbreak of
Salmonella infections caused by alfalfa sprouts grown from
contaminated seeds. J Infect Dis 1997;175: 876-882.
6. Nutt JD, Li X, Woodward CL, et al: Growth kinetics response of a
Salmonella typhimurium poultry marker strain to fresh produce
extracts. Bioresour Technol 2003;89: 313-316. Information available at
<http://www.cifor.us>.

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Communicated by:
ProMED-mail <promed@promedmail.org>

[This is the CDC formal report of this quite large outbreak of
salmonellosis. The report demonstrates the difficulties in
documenting a single vehicle for transmission. - Mod.LL]

See Also