1 figure omitted
On November 21, 2003, this report was posted on the MMWR website (http://www.cdc.gov/mmwr). However, two errors* were found. The text of the
report printed here has been corrected.
The Pennsylvania Department of Health and CDC are investigating an outbreak
of hepatitis A outbreak among patrons of a restaurant (Restaurant A) in Monaca,
Pennsylvania. As of November 20, approximately 555 persons with hepatitis
A have been identified, including at least 13 Restaurant A food service workers
and 75 residents of six other states who dined at Restaurant A. Three persons
have died. Preliminary sequence analysis of a 340 nucleotide region of viral
RNA obtained from three patrons who had hepatitis A indicated that all three
virus sequences were identical. Preliminary analysis of a case-control study
implicated green onions as the source of the outbreak.
Among 207 persons with hepatitis A who were interviewed and who ate
at Restaurant A only once during the 2-6 weeks (i.e., the typical incubation
period for hepatitis A) before illness, dates of illness onset were between
October 14 and November 12. These 207 patrons reported eating food prepared
in Restaurant A during September 14–October 17; a total of 181 (87%)
persons reported eating at Restaurant A during October 3-6 (Figure). All infected
Restaurant A food service workers became ill after October 26, suggesting
that a food service worker could not have been the source of the outbreak.
However, during late October-early November, these ill food service workers
were working in Restaurant A when they could have been infectious. For this
reason, immune globulin has been provided to approximately 9,000 persons who
ate food from Restaurant A during this time or had exposures to ill persons
involved in the outbreak. The restaurant has been closed.
A case-control study was conducted to identify menu item(s) or ingredient(s)
associated with illness. A case-patient was defined as a person who had illness
onset during October 14–November 12, had laboratory confirmation of
acute hepatitis A virus (HAV) infection (i.e., positive IgM anti-HAV), reported
eating food prepared at Restaurant A during October 3-6, and had eaten only
once at Restaurant A during the 2-6 weeks before illness onset. Controls included
persons without hepatitis A who either had dined with case-patients at Restaurant
A or were identified through credit card receipts as having dined at Restaurant
A during October 3-6. Controls with a previous history of hepatitis A, hepatitis
A vaccination, or receipt of immune globulin within 2 weeks after eating Restaurant
A food were excluded. Enrolled case-patients and controls were asked about
Restaurant A food that they had eaten.
The median age of the 181 case-patients in the study was 34 years (range:
4-73 years), and that of the 83 controls was 28 years (range: 2-81, p>0.05).
Of 133 menu items, only chili con queso and mild salsa were associated significantly
with illness. Mild salsa was eaten by 94% of case-patients, compared with
39% of controls (odds ratio [OR] = 24.2; 95% confidence interval [CI] = 11.4-51.4).
Chili con queso was eaten by 15% of case-patients, compared with 3% of controls
(OR = 5.2, 95% CI = 1.5-17.8). Both menu items associated with illness contained
uncooked or minimally heated fresh green onions. Among 11 case-patients who
reported not eating mild salsa, seven ate at least one of the other 52 menu
items that contained green onions. Of 103 ingredients used at the restaurant,
12 were associated with illness in a univariate analysis. Of these, 10 had
been consumed by <50% of case-patients. Eating a menu item containing green
onions was reported by 98% of case-patients, compared with 69% of controls
(OR = 20.2, 95%CI = 6.8-59.9). Eating a menu item containing white onions
also was associated with illness. However, among the 176 case-patients who
reported eating white onions, 174 (99%) also ate green onions. Among the four
case-patients and 28 controls who reported not eating green onions, white
onions were not associated with illness (OR = 2.5, 95% 0.3-20.9).
During interviews conducted at Restaurant A, food service workers described
green onion storage, washing, and preparation practices. Green onions were
shipped in 8.5-lb. boxes containing multiple small bundles (6-8 green onions
per bundle). Each box was unpacked, and bundles were stored upright (root
side down) and refrigerated in a bucket with ice included in the shipment.
Green onions were stored ≤5 days before processing, which consisted of
rinsing intact onion bundles, cutting the roots off, and removing the rubber
bands. Green onions from each box were chopped by machine to yield approximately
8 qts. Chopped green onions were refrigerated for approximately 2 days.
Periodically (i.e., every 1-3 days), salsas were prepared in batches
of 40-80 qts. Mild salsa included chopped fresh green onions; hot salsa did
not. Salsas were refrigerated in 8-quart containers with a shelf life of 3
days. Mild and hot salsa were ladled into bowls and provided free with tortilla
chips upon seating at Restaurant A.
The Food and Drug Administration (FDA), CDC, and the state health departments
are investigating the source of the green onions associated with this outbreak
and how they became contaminated with HAV. Preliminary traceback information
indicates that green onions supplied to Restaurant A were grown in Mexico.
V Dato, MD, A Weltman, MD, K Waller, MD, Bur of Epidemiology, Pennsylvania
Dept of Health. MA Ruta, Ohio Dept of Health. U.S. Food and Drug Administration.
Div of Viral Hepatitis, National Center for Infectious Diseases; A Highbaugh-Battle,
C Hembree, S Evenson, Epidemiology Program Office; C Wheeler, MD, T Vogt,
PhD, EIS officers, CDC.
This report describes a large hepatitis A outbreak associated with eating
a food item containing green onions at a single restaurant. The majority of
ill patrons interviewed as of November 21 were exposed during a 3-day period
in early October. No ill food service worker identified could have been the
source of the outbreak. The green onions likely were contaminated with HAV
in the distribution system or during growing, harvest, packing, or cooling.
Traceback investigations completed to date have determined that the green
onion source is one or more farms in Mexico.
Both green onions and white onions were associated with illness in the
univariate analysis. However, white onions were not associated with illness
among those who did not eat green onions. This association with white onions
observed in the univariate analysis might not remain when multivariate modeling
is completed. Restaurant A purchases previously chopped white onions and adds
them to several menu items, including hot and mild salsa. Mild salsa, which
contains both green onions and white onions, was associated with illness;
however, hot salsa, which contains only white onions, was not associated with
The genetic sequence of the outbreak strain is very similar to viral
sequences obtained from persons involved in hepatitis A outbreaks in Tennessee,
Georgia, and North Carolina during September 2003 that were linked epidemiologically
to green onions. These sequences also were identical or very similar to sequences
observed among persons with hepatitis A living along the United States-Mexico
border and travelers returning from Mexico, consistent with a source in Mexico
(CDC, unpublished data, 2003). Raw green onions from three firms in Mexico
have been implicated in the Tennessee and Georgia outbreaks. FDA is still
reviewing records to determine if additional firms are involved. The Mexican
government is assisting with the traceback investigation in Mexico and the
investigation to determine the source of the contamination.
Previous hepatitis A outbreaks linked to green onions have been reported
and have involved patrons of a single restaurant.1 However,
the outbreak at Restaurant A was unusually large. Several characteristics
of the way food was prepared and served in Restaurant A could have contributed
to the outbreak's size, including (1) multiple opportunities for intermingling
of uncontaminated and contaminated green onions in a common bucket for 5 days
with the ice in which they were shipped and (2) serving contaminated items
with a relatively long shelf life (e.g., mild salsa) to a large proportion
of patrons over several days.
HAV is transmitted by the fecal-oral route. Green onions require extensive
handling during harvesting and preparation for packing. Contamination of green
onions could occur (1) by contact with HAV-infected workers, especially children,
working in the field during harvesting and preparation and (2) by contact
with HAV-contaminated water during irrigation, rinsing, processing, cooling,
and icing of the product. Green onions and other selected produce items (e.g.,
strawberries2) might be more vulnerable
to contamination because plant surfaces are particularly complex or adherent
to viral or fecal particles. Outbreaks of other enteric pathogens linked to
green onions have been reported.3
On November 15, FDA issued an alert to consumers about the recent hepatitis
A outbreaks associated with green onions (available at http://www.fda.gov/bbs/topics/ANSWERS/2003/ANS01262.html). FDA advised consumers concerned about the possibility of getting
hepatitis A from green onions to cook green onions thoroughly before eating
and to ask about use of green onions in prepared foods. Unless directed otherwise
by public health officials, persons who have recently eaten green onions do
not need postexposure prophylaxis (i.e., immune globulin).
CDC is working with state health departments to identify other hepatitis
A outbreaks associated with green onions. As of November 21, no other hepatitis
A outbreaks have been identified. To identify other cases related to these
outbreaks, state and local health officials should interview persons with
hepatitis A with onset after October 1. Persons without typical risk factors
for hepatitis A4 should be asked about food
and restaurant exposures during their incubation period. Because molecular
epidemiologic techniques have been useful for identifying related cases of
foodborne hepatitis A in previous outbreaks,2 health
departments might consider obtaining serum specimens for cases of interest.
An increasing proportion of reported foodborne outbreaks have been linked
to fresh produce.3 This increase might be
attributed to increased consumption of fresh produce or better surveillance
techniques. HAV contamination of fresh produce can be reduced by using approaches
such as the application of Good Agricultural Practices/Good Manufacturing
Practices recommended by FDA5 Recommended
control measures include providing sanitary facilities for field workers,
ensuring appropriate water quality, use of properly treated manure or biosolids,
and ensuring worker health. Reducing HAV transmission in areas where produce
is grown and discouraging the presence of children in areas where food is
harvested also will reduce opportunities for HAV contamination. Further investigation
of this and other hepatitis A outbreaks linked to green onions, including
observation of cultivation and harvesting practices, can guide additional
specific critical control measures.
*In the fourth sentence of the fifth paragraph, green onions were stated
to have been stored for ≥5 days before processing rather than ≤5 days.
In the third sentence of the fifth paragraph of the Editorial Note, the word
"of" appeared before "plant surfaces are particularly complex or adherent
to viral or fecal particles."
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