Context.— Acidic foods such as orange juice have been thought to be unlikely vehicles
of foodborne illness.
Objective.— To investigate an outbreak of Salmonella enterica serotype Hartford (Salmonella Hartford) infections
among persons visiting a theme park in Orlando, Fla, in 1995.
Design.— Review of surveillance data, matched case-control study, laboratory
investigation, and environmental studies.
Setting.— General community.
Participants.— The surveillance case definition was Salmonella
Hartford or Salmonella serogroup C1 infection
in a resident of or a visitor to Orlando in May or June 1995. In the case-control
study, case patients were limited to theme park hotel visitors and controls
were matched to case patients by age group and hotel check-in date.
Main Outcome Measures.— Risk factors for infection and source of implicated food.
Results.— Sixty-two case patients from 21 states were identified. Both Salmonella Hartford and Salmonella enterica
serotype Gaminara (Salmonella Gaminara) were isolated
from stool samples of 1 ill person. Thirty-two case patients and 83 controls
were enrolled in the case-control study. Ninety-seven percent of case patients
had drunk orange juice in the theme park vs 54% of controls (matched odds
ratio, undefined; 95% confidence interval, 5.2 to undefined). The orange juice
was unpasteurized and locally produced. Salmonella
Gaminara was isolated from 10 of 12 containers of orange juice produced during
May and July, indicating ongoing contamination of juice probably because of
inadequately sanitized processing equipment.
Conclusions.— Unpasteurized orange juice caused an outbreak of salmonellosis in a
large Florida theme park. All orange juice was recalled and the processing
plant closed. Pasteurization or other equally effective risk-management strategies
should be used in the production of all juices.
AN ESTIMATED 2 to 4 million cases of salmonellosis occur annually in
the United States.1 Although foods of animal
origin (eg, eggs, poultry, beef, dairy products) are the vehicles of transmission
in most Salmonella outbreaks, contaminated fresh
fruits and vegetables are now recognized as a source of salmonellosis and
other foodborne diseases.2-5
Unpasteurized acidic fruit juices were previously thought to be safe; however,
recent highly publicized outbreaks of Escherichia coli
O157:H7 infections and cryptosporidiosis occurring in 1996 in the northeast
and western United States associated with unpasteurized apple cider and apple
juice illustrate the potential for acidic juices to carry human pathogens.6,7 We report an outbreak of Salmonella enterica serotype Hartford (Salmonella Hartford) infections associated with another popular unpasteurized
fruit drink, orange juice.
Salmonellosis caused by Salmonella Hartford,
a serogroup C1Salmonella (Salmonella C1), is uncommon. From 1984 to 1994, an annual
mean of only 68 isolates were reported to the Centers for Disease Control
and Prevention's (CDC) national Salmonella surveillance
system, representing less than 0.2% of reported isolates.8
In June 1995, a review of Salmonella serotype-based
surveillance by the New Jersey Department of Health identified a cluster of Salmonella Hartford infections among 7 New Jersey residents
returning from vacation in Orlando, Fla. None of them were acquainted with
one another or had traveled together. One person was coinfected with Salmonella Hartford and Salmonella enterica serotype Gaminara (Salmonella Gaminara),
a serogroup I Salmonella (Salmonella I), which is also exceedingly rare, with an annual mean of only 40
isolates reported to the CDC from 1984 to 1994. A preliminary investigation
failed to identify a common hotel, restaurant, or food exposure among ill
persons; however, all had visited a large tourist theme park in Orlando during
May 1995. An investigation was conducted to determine the source and extent
of the outbreak.
To find cases, we reviewed the CDC's national Salmonella surveillance system for reports of Salmonella
Hartford infections since May 1995 and asked state health departments to interview
patients with this infection. We also reviewed Salmonella surveillance system data to determine if there were significant increases
in reports of Salmonella Gaminara or Salmonella I. All Florida local health departments and area health
care facilities were notified of the outbreak and asked to immediately report
any cases of Salmonella Hartford, Salmonella Gaminara, or Salmonella C1 or I infections. A review of the theme park's employee and visitor
medical clinic logs was also conducted.
A confirmed case was defined as Salmonella
Hartford infection in a resident of or visitor to Orlando in May or June 1995.
Because some laboratories serogroup Salmonella isolates
but do not send all Salmonella isolates to their
respective state's public health laboratory for serotyping, a probable case
was defined as Salmonella C1 infection
in a resident of or visitor to Orlando in May or June 1995.
To determine risk factors for infection, we conducted a matched case-control
study. For this study, a case was defined as diarrhea (3 or more loose stools
in 24 hours) in a theme park hotel visitor who visited the park in May or
June 1995, with documented Salmonella Hartford or Salmonella C1 infection. Cases were limited
to visitors to the theme park's hotels because most patients had stayed at
1 of these 13 hotels. If a family had more than 1 ill member, only the first
ill person in the household was eligible. Cases were excluded if no matched
controls could be identified.
We attempted to enroll 3 controls per case patient individually matched
by age group, hotel, check-in date, and number of days spent visiting the
theme park. Potential controls were identified using hotel records provided
by the theme park and contacted by telephone. Potential controls were excluded
if they gave a history of vomiting or diarrhea during their visit to the theme
park or within 7 days of returning home.
A standard questionnaire was administered by telephone with trained
interviewers. Information was collected on tourist attractions visited, foods
eaten, beverages consumed, exposures to animals, and clinical illness.
Based on the results of our case-control study, we traced the implicated
product, orange juice, back through its production process and conducted site
inspections of the involved processing facilities and farms. Site inspections
consisted of a review of processing procedures, production plant sanitary
conditions and water quality, and an overview of growing and harvesting practices.
Clinical isolates of the outbreak strains of Salmonella were obtained from the New Jersey and Florida departments of health
laboratories and serotyping results were confirmed by the CDC.9
Implicated orange juice samples were refrigerated and transported to CDC for
examination. The pH of orange juice and the presence of fecal indicator bacteria
(total coliforms, fecal coliforms, and E coli) were
determined by standard methods.10 Samples were
examined for Salmonella in duplicate using tetrathionate
broth with brilliant green dye (TET).11 The
TET was incubated at 35°C for 24 hours. It was then subcultured into fresh
TET and incubated at 42°C for 24 hours before streaking onto Hektoen enteric
and brilliant green agar.
An independent microbiologic evaluation of the implicated processing
plant was conducted by the University of Florida Citrus Research and Education
Center in August and September 1995. Specimen collection and culture methods
are described elsewhere.12
The US Food and Drug Administration (FDA), using a modified drag-swab
environmental sampling method, collected whole fruit and environmental samples
from 2 Florida farms supplying fruit to the implicated processor during the
outbreak period.13 To isolate Salmonella from swabs, the FDA used a modified culture method procedure
with novobiocin supplemental plating media and delayed secondary selective
enrichment.13
Antimicrobial susceptibility testing for chloramphenicol, trimethoprim-sulfamethoxazole,
tetracycline, ciprofloxacin, nalidixic acid, ampicillin, sulfisoxazole, streptomycin,
kanamycin, gentamicin, ceftriaxone, and amoxicillin–clavulanic acid
was performed on representative human and environmental Salmonella isolates by standard disk-diffusion techniques.14
Pulsed-field gel electrophoresis (PFGE) was performed on isolates to
subtype and characterize the outbreak strains using previously described methods
for E coli O157:H715
and Salmonella enterica serotype Typhimurium (Salmonella Typhimurium).16
Numerical data were entered and analyzed with Epi Info, Version 6.02
(CDC).17 Mantel-Haenszel matched odds ratios
(MORs) and 95% confidence intervals (CIs) were calculated to evaluate associations
between categorical variables.18 Fisher exact
test lower 95% CIs were calculated for undefined MORs.19
Fifty-two confirmed and 10 probable cases of Salmonella Hartford infection were identified among visitors to Orlando from
21 states. All onset dates were in May and June and the peak of illness onsets
occurred during the week of May 22 through 28 (Figure 1). No Orlando residents or theme park employees met the
case definition and review of the theme park's clinical records showed no
notable increase in the number of employees or visitors presenting there
with gastrointestinal symptoms.
Forty-nine (83%) of 59 patients for whom hotel information was available
stayed in 1 of the theme park's 13 hotels in the 7 days before illness onset;
2 persons reported eating all meals exclusively within the theme park. Patients'
ages ranged from 1 to 63 years (median, 10 years) and 53% were male. Salmonella Hartford or Salmonella
C1 was cultured from stool (n = 58), urine (n = 1), blood (n =
2), or abscess (n = 1).
Both Salmonella Hartford and Salmonella Gaminara were isolated from the stool of 1 patient; however,
no additional isolates of Salmonella Gaminara or Salmonella I were identified among persons with a recent
travel history to Orlando and no significant increases were observed in reports
of Salmonella. Gaminara or Salmonella I infection during the outbreak period from Florida or other states.
Among the 62 persons identified through case-finding efforts with probable
or confirmed Salmonella Hartford infection, 32 were
enrolled in the case-control study along with 83 matched controls. Thirty
ill persons were excluded because they did not stay in a theme park hotel
(n = 7), were not the household's primary patient (n = 3), did not have diarrhea
(n = 2), were identified after the study ended (n = 2), could not be reached
by telephone (n = 15), or refused to participate (n = 1).
The symptoms and signs reported for the 32 persons enrolled in the case-control
study included diarrhea (100%), abdominal cramps (97%), fever (97%), headache
(73%), bloody stool (71%), and vomiting (66%). The median duration of illness
was 7 days (range, 3-23 days), and 7 persons (22%) were hospitalized for a
median of 3 days (range, 1-5 days); there were no deaths.
Consumption of orange juice in the theme park was strongly associated
with illness (Table 1). Thirty-one
(97%) of 32 ill persons drank orange juice compared with 43 (54%) of 80
matched controls (MOR, undefined; 95% CI, 5.2 to undefined, P <.001). The 1 case patient who reported no orange juice consumption
was matched to controls who also reported no orange juice consumption; therefore,
the MOR and the upper 95% CI are undefined. On univariate analysis, waffles
were also statistically associated with illness but were consumed by only
16 (53%) of 30 ill persons. A significant positive association between orange
juice and illness remained significant after those persons who reported eating
waffles were excluded from the analysis.
"Character breakfasts" served in the theme park were the only specific
event or meal associated with illness. Twenty-nine (91%) of 32 ill persons
attended a character breakfast compared with 48 (58%) of 83 controls (MOR,
6.5; 95% CI, 1.8-23.3). All ill persons who attended a character breakfast
reported drinking orange juice during their meal. Character breakfasts are
special breakfasts unique to the theme park in which costumed cartoon characters
visit with the guests. They are conducted in various locations throughout
the park but most are held in the theme park's hotels; however, no single
hotel accounted for the majority of illnesses. No other tourist attractions
in the Orlando area or other pertinent exposures, such as swimming in water
parks and hotel pools or direct contact with animals, were associated with
illness.
The theme park received shipments of orange juice every other day and
reportedly used all juice within 2 or 3 days of delivery. Orange juice was
distributed and sold throughout the theme park and was not opened before being
received by the park's hotels, restaurants, and attractions. Orange juice
was served in sealed, single-serving containers, poured from larger containers
into pitchers or glasses, or poured into self-serve juice dispensers. Eighty-eight
percent of all orange juice served at the theme park and all orange juice
served at character breakfasts was purchased from a local juice processor
and was unpasteurized.
The company that provided all of the unpasteurized orange juice to the
theme park is a small citrus juice processing plant (production capacity is
approximately 40000 L/d) located in a community adjacent to Orlando; the plant
produced only unpasteurized juices. Approximately 75% of the juice company's
orange juice was sold to the theme park and most of the remaining product
was sold by local Florida distributors. At the juice company's processing
plant, whole oranges were conveyed on moving pallets through a phosphoric
acid wash and rinsed with water before being sliced in half and juiced. The
juice was then chilled and bottled. The final product contained no added water,
sugar, preservatives, or disinfectants and had a 12- to 17-day shelf life.
A site inspection of the juice company identified several deficiencies
in its processing plant. The processing room was poorly sealed from the outside
environment: cracks and holes were visible in the walls and ceiling, rodent
and bird droppings were present, and there were reports of frogs being observed
around processing equipment. In addition, despite reported twice-daily sanitization
of equipment, a buildup of precipitate created from the mechanical reaming
of the orange was observed on the inside of the fruit-squeezing machine. No
problems were reported with the chlorinated municipal water used at the plant
and no fecal coliforms were detected in a bacteriological analysis of the
water conducted on August 1, 1995, by the Florida Department of Health's Public
Health Laboratory.
Four citrus growers provided the juice company with oranges during the
peak outbreak period in May; 1 grove (grove A) provided the majority (76%)
of oranges. Four other Florida citrus groves provided oranges used to produce
contaminated juice in July; 1 grove (grove B) provided most (63%) of these
oranges. These 2 orange groves (groves A and B) used similar methods for growing,
harvesting, and picking fruit. Oranges were typically hand-picked, dropped
to the ground, collected in large bins, and shipped to the juice company within
24 hours without being cleaned or refrigerated. However, the groves were not
associated with each other and did not use common water sources, fruit-picking
crews, equipment, or transport. They are separated by approximately 96 km
(60 miles) and sold different varieties of oranges to the juice company.
Unopened and opened containers of fresh and frozen orange juice were
collected from the theme park, the juice company, and a local supermarket
(where the juice company's orange juice was also distributed) by public health
officials. The pH of orange juice samples ranged from 4.1 to 4.5 (mean pH,
4.3). All juice samples tested contained coliforms (range, 5000 to >16000
colony-forming units [CFUs] per 100 mL), fecal coliforms (range, 220-3500
CFUs per 100 mL), and E coli (range, 170-1700 CFUs
per 100 mL). Salmonella Gaminara (range, 2-4 CFUs
per 100 mL) was cultured from 10 (83%) of 12 juice containers representing
4 lots produced in May and July 1995 (Table
2).
Seventy samples were collected from the juice company's processing plant
consisting of equipment swabs, fruit surface swabs, and juice and other environmental
samples.12Salmonella
Hartford and Salmonella enterica serotype Newport
(Salmonella Newport) were isolated from a toad found
just outside the juice-processing building. In addition, salmonellae were
isolated from unopened bottled juice produced in July (Salmonella enterica serotype Rubislaw), the surface of unwashed oranges
held in cold storage for several weeks (Salmonella enterica serotype Saintpaul), and 4 tree frogs (Salmonella Newport) also found outside of the processing building.
All 95 oranges sampled from 19 different orange grove tracts (comprising
approximately 250 acres) from groves A and B had negative test results for Salmonella. Salmonella enterica
serotypes Braenderup and Muenchen, however, were isolated from 2 (11%) of
18 environmental swabs obtained from the soil surrounding 18 orange trees
located in 2 of 6 tracts sampled from grove A. Neither of these serotypes
was isolated from ill persons.
Antimicrobial susceptibility testing of human isolates of Salmonella Hartford (n = 17) and Salmonella
Gaminara (n = 1), orange juice isolates of Salmonella
Gaminara (n = 14), and the single toad isolate of Salmonella Hartford determined that all isolates were susceptible to all antimicrobials
tested. Seven representative human isolates of Salmonella Hartford were indistinguishable by PFGE; however, the PFGE pattern
of the toad isolate and 9 reference isolates were distinctly different from
the outbreak strain. Two PFGE patterns (subtypes A and B) were identified
from 10 Salmonella Gaminara isolates cultured by
the CDC from juice samples. Isolates of Salmonella
Gaminara with PFGE pattern A were identified in juice samples produced in
both May and July. However, both juice subtypes were dissimilar from the subtype
identified in the single human isolate of Salmonella
Gaminara and from 5 reference isolates.
This outbreak of diarrheal illness affected at least 62 visitors to
a large tourist theme park in Orlando. The case-control study and laboratory
findings support the hypothesis that unpasteurized orange juice contaminated
with Salmonella was the vehicle of transmission.
The case-control study determined that orange juice was consumed by
97% of ill persons and was a strong risk factor for illness. The association
between illness and attendance at any character breakfast, regardless of location,
is explained by the fact that all such breakfasts served only the juice supplied
by the park's principal juice supplier; other park venues served a variety
of orange juice brands. Waffles were statistically associated with illness;
however, only 53% of persons ate waffles and these persons also drank orange
juice.
In the laboratory investigation, every lot of orange juice had positive
findings for fecal indicator organisms and multiple lots contained Salmonella. Although Salmonella Hartford was
not isolated from orange juice, only 2 samples of juice from the peak of the
outbreak in May were available for analysis; nevertheless, these samples and
multiple other samples from July did yield Salmonella
Gaminara, a very rare serotype isolated from 1 ill person who had a dual infection
with Salmonella Hartford. Salmonella Gaminara isolated from orange juice obtained in an Orlando supermarket
not affiliated with the theme park suggests that the outbreak may have extended
beyond the theme park. However, no patients infected with Salmonella Hartford or Salmonella Gaminara
reported consumption of orange juice purchased outside the theme park.
The dissimilarity of PFGE patterns between human and toad isolates of Salmonella Hartford and between human and juice isolates
of Salmonella Gaminara is likely explained by 1 of
several factors. First, the PFGE pattern reported for each isolate was based
on the testing of only a single colony; therefore, we did not determine if
multiple subtypes of Salmonella Hartford or Salmonella Gaminara existed within a single specimen. Second,
although Salmonella Hartford and Salmonella Gaminara are rarely isolated from humans, they may be common
in this environment, with a significant amount of heterogeneity present among
serotypes. Nevertheless, our PFGE analyses do not alter our main conclusion
that unpasteurized orange juice contaminated with salmonellae was the cause
of this outbreak.
Although the true magnitude of the outbreak is undetermined, a review
of human salmonellosis by Chalker and Blaser20
estimated that only 1% to 5% of actual cases are reported. Given a 1% to 5%
case-ascertainment rate and 62 culture-confirmed cases, we estimate that between
1240 and 6200 cases of salmonellosis could have resulted from this outbreak.
The unusually high percentage of persons with salmonellosis enrolled in our
case-control study with bloody stool (71%) also suggests many milder illnesses
were not detected. It is likely that only those persons who were the most
severely ill with bloody diarrhea would have sought medical treatment and
been evaluated with a stool culture.
The original source of the Salmonella is unknown;
however, salmonellae are found in a broad variety of hosts, including insects,
reptiles, amphibians, birds, and mammals, and may survive long periods in
soil or water contaminated with animal feces. Amphibians such as the toad
from which Salmonella Hartford was isolated could
easily have entered the poorly sealed processing facility and contaminated
oranges and processing equipment. In addition, because oranges are frequently
harvested after being dropped to the ground, the exterior of oranges may have
become contaminated with Salmonella directly from
animals or indirectly from soil, surface water used for irrigation, or improperly
prepared manure used as fertilizer. Although the implicated Salmonella serotypes (Hartford and Gaminara) were not isolated from
the exterior of oranges tested in this investigation, several limiting factors
must be considered. The oranges collected in our environmental investigations
were unripe, obtained more than 2 months after the peak outbreak period, and
picked primarily from the trees and not the ground. Other Salmonella serotypes were isolated from unwashed orange surfaces and
environmental swabs collected from soil surrounding orange trees in 1 grove
providing oranges to the juice company.
Regardless of the environmental source and means of contamination, once Salmonella was introduced into the processing plant, inadequate
cleaning and sanitization of processing equipment probably contributed to
production of contaminated juice. The presence of a specific fecal indicator
organism in all samples of orange juice tested indicates improper sanitation
in the processing plant. The identification of the same subtype of a rare Salmonella serotype (Gaminara) in juice produced during
a 3-month span (May-July) suggests that there was an ongoing source of Salmonella within the plant.
Orange juice and other acidic fruit juices are generally believed to
be unusual vehicles of transmission for human pathogens. Although varying
by season, the average pH level of Florida orange juice is 3.7 (range, 3.4-4.0).21 While the pH of orange juice implicated in this outbreak
was less acidic than expected (mean pH, 4.3), the FDA does not consider foods
with a pH level of 4.6 or less to be "potentially hazardous."22
The FDA Food Code also states that a food that does
not support the rapid and progressive growth of infectious or toxigenic microorganisms
is not considered potentially hazardous even though the food may contain infectious
or toxigenic organisms at a level sufficient to cause illness. However, recent
outbreak investigations challenge these suppositions.
Orange juice has been identified as the vehicle of transmission in at
least 5 previous foodborne outbreaks. Orange juice was first reported as a
vehicle of transmission in an outbreak of typhoid fever at a hotel in Cleveland,
Ohio, in 1944.23 Subsequently, it has been
implicated in outbreaks of hepatitis A virus in a hospital in St Louis, Mo,
in 1962,24 probable viral gastroenteritis among
spectators at a football game in California in 1966,25,26
typhoid fever at a resort hotel in New York in 1989,27
and enterotoxigenic E coli in India in 1992.28
Other acidic fruit juices have also been implicated in outbreaks of
gastroenteritis. Unpasteurized apple cider and apple juice were associated
with outbreaks of Salmonella Typhimurium infection,29E coli O157:H7 infection,6,7,30 postdiarrheal hemolytic
uremic syndrome (likely caused by E coli O157:H7
infection),31 and cryptosporidiosis.7,32
Laboratory studies of the survival of Salmonella
and other bacterial pathogens in orange juice also support the hypothesis
that acidic juices can be vehicles of pathogen transmission. Survival studies
of salmonellae in orange juice using, in part, strains isolated from case
patients and orange juice described in this outbreak investigation showed
that salmonellae survived in detectable numbers up to 27 days at pH 3.5, 46
days at pH 3.8, 60 days at pH 4.1, and 73 days at pH 4.4.33
In a review by Mitscherlich and Marth,34 investigators
inoculated samples of orange juice (pH of 3.0-3.1 held at 5°C) each with
106/mL viable cells of Salmonella species, Shigella sonnei, and E coli. Four
decimal reductions in the number of viable organisms required 27 days for Salmonella species and E coli
and 35 days for S sonnei. Investigators in 1 of the
aforementioned orange juice–associated typhoid fever outbreaks inoculated
orange juice with the outbreak strains and recovered viable bacilli up to
6 days later.27Salmonella
enterica serotype Typhi has survived on the surface of cut and whole
oranges for 6 and 14 days, respectively.34
Orange juice is the most popular fruit drink in the United States. In
1995, Americans consumed an estimated 20.7 L (5.45 gal) of orange juice per
person, which accounted for 60% of all fruit juice consumed.35
Although consumption data on unpasteurized orange juice are limited, the FDA
recently estimated that 44.5 million L (11.7 million gal) or 187 million 240-mL
(8-oz) servings per year of unpasteurized orange juice are consumed in the
United States.36 Thus, less than 1% of all
orange juice is consumed unpasteurized.
After our investigation, the theme park decided to sell only pasteurized
orange juice. In addition, Florida public health officials ordered a temporary
closing of the orange juice processor and, with the assistance of the FDA,
a recall of the plant's unpasteurized orange juice. The Florida Department
of Citrus enacted new rules regulating the production of fresh-squeezed unpasteurized
orange juice, including banning the use of oranges picked from the ground
for the production of juice, washing fruit with an acid wash or other equivalent
cleaning method, rinsing fruit with hypochlorite or other equivalent bactericide,
completely enclosing the juice-processing area, conducting routine microbiologic
surveillance of unpasteurized juice, and establishing documented quality control,
good manufacturing practices, or a Hazard Analysis Critical Control Point
(HACCP) program.37 Hazard Analysis Critical
Control Point is a preventive system of hazard control whereby food producers
are responsible for identifying and evaluating food safety hazards that can
affect the safety of their products and instituting controls. Small Florida
producers, such as gift-fruit shippers, retail processors, and roadside stand
operators, are exempt from these new regulations. Additional research is needed
to determine to what extent these measures improve the safety of unpasteurized
juice, how widely and consistently they are practiced, and what other possible
interventions need to be considered.
The potential role of fruit and vegetable juices in foodborne disease
has recently begun to receive national attention. United States federal governmental
agencies primarily responsible for preventing foodborne disease (ie, CDC,
FDA, US Department of Agriculture, Environmental Protection Agency), are now
collaborating on a national food safety initiative. In a report to President
Clinton in May 1997, development of new preventive measures for fresh fruit
and vegetable juices was proposed.38
As a consequence of recent outbreaks associated with juices, the FDA
recently proposed new rules to improve the safety of fresh and processed fruit
and vegetable juices and juice products.39
The FDA's proposal would mandate the application of HACCP principles to the
processing of these foods to prevent bacterial, chemical, and physical contamination.
Similar HACCP regulations have already been enacted by the FDA for seafood,
meat, and poultry processors. Under the proposed regulations, juice processors
would be required by the FDA to demonstrate that their HACCP program reduces
the numbers of pathogenic bacteria to the same degree as that achieved by
pasteurization. Until the final rule is implemented, the FDA has also proposed
regulations (effective November 5, 1998) that require packaged juice not pasteurized
or otherwise processed to control pathogenic microorganisms to bear a warning
statement informing consumers of the potential risk of foodborne illness associated
with the product. However, in the current version of the proposal very small
processors who manufacture fewer than 152000 L (40000 gal) of juice per year
would be exempt from HACCP requirements, and retailers that sell juice by
the glass would be exempt from both HACCP and labeling regulations.
We describe the largest reported outbreak of salmonellosis associated
with unpasteurized orange juice. Although the vast majority of orange juice
and other fruit and vegetable juices produced within the United States are
pasteurized and safe to consume, this outbreak illustrates the importance
of the current national debate and regulatory activity regarding the safety
of unpasteurized juices. Pasteurization or other risk-management strategies
proven to be at least as effective as pasteurization should be used in the
production of juices, including those previously thought to be too acidic
to transmit infection. Consumers need to be aware that all unpasteurized juices
may potentially transmit enteric infections. Until production methods at least
as effective as pasteurization are developed, evaluated, and implemented,
consumers can reduce their risk for illness by drinking only pasteurized fruit
and vegetable juices.
1.Pavia AT, Tauxe RV. Salmonellosis: nontyphoidal. In: Evans AS, Brachman PS, eds. Bacterial Infections of Humans:
Epidemiology and Control . 2nd ed. New York, NY: Plenum Medical Book
Co; 1991:573-591.
2.Hedberg CW, MacDonald KL, Osterholm MT. Changing epidemiology of food-borne disease: a Minnesota perspective.
Clin Infect Dis.1994;18:671-682.Google Scholar 3.Altekruse SF, Swerdlow DL. The changing epidemiology of foodborne diseases.
Am J Med Sci.1996;311:23-29.Google Scholar 4.Stephenson J. Public health experts take aim at a moving target: foodborne infections.
JAMA.1997;277:97-98.Google Scholar 5.Altekruse SF, Cohen ML, Swerdlow DL. Emerging foodborne diseases.
Emerg Infect Dis.1997;3:285-293.Google Scholar 6.Centers for Disease Control and Prevention. Outbreak of
Escherichia coli O157:H7 infections
associated with drinking unpasteurized commercial apple juice—British
Columbia, California, Colorado, and Washington, October 1996.
MMWR Morb Mortal Wkly Rep.1996;45:975.Google Scholar 7.Centers for Disease Control and Prevention. Outbreaks of
Escherichia coli O157:H7 infection
and cryptosporidiosis associated with drinking unpasteurized apple cider—Connecticut
and New York, 1996.
MMWR Morb Mortal Wkly Rep.1997;46:4-8.Google Scholar 8.Centers for Disease Control and Prevention. Salmonella Surveillance Report: 1993-1994 . Washington, DC: US Public Health Service; 1995.
9.Ewing WH. Edward's and Ewing's Identification of Enterobacteriaceae. 4th ed. New York, NY: Elsevier Science Publishing Co Inc; 1986.
10.American Public Health Association, American Water Works Association,
Water Environment Federation. Standard Methods for the Examination of Water and Wastewater . 18th ed. Washington, DC: American Public Health Association, American
Water Works Association, Water Environment Federation; 1992.
11.Wells JG, Puhr ND. Comparison of methods for isolation of Salmonella from orange juice. In: Abstracts of the 97th General Meeting of the American Society
for Microbiology; May 4-8, 1997; Miami Beach, Fla. Abstract 453.
12.Parish ME. Coliforms,
Escherichia coli, and
Salmonella serovars associated with a citrus-processing facility implicated
in a salmonellosis outbreak.
J Food Prot.1998;61:280-284.Google Scholar 13.Mallinson ET, Tate CR, Miller RG, Bennett B, Russek-Cohen E. Monitoring poultry farms for
Salmonella by
drag-swabbing sampling and antigen-capture immunoassay.
Avian Dis.1989;33:684-690.Google Scholar 14.National Committee for Clinical Laboratory Standards. Performance Standards for Antimicrobial Disk Susceptibility Tests,
6th Edition: Approved Standard . Wayne, Pa: National Committee for Clinical Laboratory Standards;
1995. NCCLS document M100-S6.
15.Barrett TJ, Lior H, Green JH.
et al. Laboratory investigation of a multistate food-borne outbreak of
Escherichia coli O157:H7 by using pulsed-field gel electrophoresis
and phage typing.
J Clin Microbiol.1994;32:3013-3017.Google Scholar 16.Angulo FJ, Tippen S, Sharp DJ.
et al. A community waterborne outbreak of salmonellosis and effectiveness
of a boil water order.
Am J Public Health.1997;87:580-584.Google Scholar 17.Dean AG, Dean JA, Coulombier D.
et al. Epi Info Version 6: A Word Processing, Database, and Statistics
Program for Epidemiology on Microcomputers . Atlanta, Ga: Centers for Disease Control and Prevention; 1994.
18.Robins J, Greenland S, Breslow NE. A general estimator for variance of the Mantel-Haenszel odds ratio.
Am J Epidemiol.1986;124:719-723.Google Scholar 19.Martin D, Austin H. An efficient program for computing conditional maximum likelihood estimates
and exact confidence intervals for a common odds ratio.
Epidemiology.1991;2:359-362.Google Scholar 20.Chalker RB, Blaser MJ. A review of human salmonellosis, III: magnitude of
Salmonella infection in the United States.
Rev Infect Dis.1988;10:111-124.Google Scholar 21.Attaway JA, Barron RW, Blair JG.
et al. Some new analytical indicators of processed orange juice quality, 1971-72.
Proc Fla State Horticultural Soc.1972;85:192-203.Google Scholar 22.US Food and Drug Administration. Food Code: 1997 Recommendations of the United States Public Health
Service/Food and Drug Administration . Washington, DC: US Food and Drug Administration, Public Health Service,
US Dept of Health and Human Services; 1997. Document PB97-133656.
23.Duncan TG, Doull JA, Miller ER, Bancroft H. Outbreak of typhoid fever with orange juice as the vehicle, illustrating
the value of immunization.
Am J Public Health.1946;36:34-36.Google Scholar 24.Eisenstein AB, Aach RD, Jacobsohn W, Goldman A. An epidemic of infectious hepatitis in a general hospital: probable
transmission by contaminated orange juice.
JAMA.1963;185:171-174.Google Scholar 25.Tabershaw IR, Schmelzer LL, Bruyn HB. Gastroenteritis from an orange juice preparation, I: clinical and epidemiologic
aspects.
Arch Environ Health.1967;15:72-77.Google Scholar 26.Schmelzer LL, Gates JM, Redfearn MS, Tabershaw IR. Gastroenteritis from an orange juice preparation, II: field and laboratory
investigation.
Arch Environ Health.1967;15:78-82.Google Scholar 27.Birkhead GS, Morse DL, Levine WC.
et al. Typhoid fever at a resort hotel in New York: a large outbreak with
an unusual vehicle.
J Infect Dis.1993;167:1228-1232.Google Scholar 28.Singh BR, Kulshreshtha SB, Kapoor KN. An orange juice–borne outbreak due to enterotoxigenic
Escherichia coli.
J Food Sci Technol (India).1996;32:504-506.Google Scholar 29.Centers for Disease Control and Prevention.
Salmonella typhimurium outbreak traced to
commercial apple cider.
MMWR Morb Mortal Wkly Rep.1975;24:87-88.Google Scholar 30.Besser RE, Lett SM, Weber JT.
et al. An outbreak of diarrhea and hemolytic uremic syndrome from
Escherichia coli O157:H7 in fresh-pressed apple cider.
JAMA.1993;269:2217-2220.Google Scholar 31.Steele BT, Murphy N, Arbus GS, Rance CP. An outbreak of hemolytic uremic syndrome associated with ingestion
of fresh apple juice.
J Pediatr.1982;101:963-965.Google Scholar 32.Millard PS, Gensheimer KF, Addiss DG.
et al. An outbreak of cryptosporidiosis from fresh-pressed apple cider.
JAMA.1994;272:1592-1596.Google Scholar 33.Parish ME, Narciso JA, Friedrich LM. Survival of salmonellae in orange juice.
J Food Safety.1997;17:273-281.Google Scholar 34.Mitscherlich E, Marth EH. Microbial Survival in the Environment: Bacteria and Rickettsiae
Important in Human and Animal Health . New York, NY: Springer-Verlag; 1984.
35.Putnam JJ, Alehouse JE. Food Consumption, Prices, and Expenditures, 1970-1995: Statistical
Bulletin . Washington, DC: Economic Research Service, US Dept of Agriculture;
1997.
36.Williams R, Wilcox T, Timbo B.
et al. Preliminary investigation into the morbidity and mortality effects
associated with the consumption of fruit and vegetable juices.
63 Federal Register.24253-24302 (1998) (codified at 21 CFR §101-120).Google Scholar 37.Florida Department of Citrus. Standards for processed citrus products: sanitary requirements . Florida Administrative Code ch 20, §64.020 (1996).
38.US Environmental Protection Agency, US Department of Health and Human
Services, US Department of Agriculture. Food Safety From Farm to Table: A National Food-Safety Initiative:
A Report to the President, May 1997 . Washington, DC: US Environmental Protection Agency, US Dept of Health
and Human Services, US Dept of Agriculture; 1997.
39.US Food and Drug Administration.. Proposed rules: hazard analysis and critical control point (HACCP)
procedures for the safe and sanitary processing and importing of juice; food
labeling: warning notice statements; labeling of juice products
63 Federal Register.20449-20493 (1988) (codified at 21 CFR §101, 120).Google Scholar