1299

Journal of Food Protection, Vol. 64, No. 9, 2001, Pages 1299–1304

Copyright , International Association for Food Protection

Survival of Salmonellae in Pasteurized, Refrigerated

Calcium-FortiŽ ed Orange Juice
MANAN SHARMA, LARRY R. BEUCHAT, MICHAEL P. DOYLE, AND JINRU CHEN*

Center for Food Safety and Quality Enhancement, Department of Food Science and Technology, The University of Georgia, 1109 Experiment Street,
GrifŽ n, Georgia 30223-1797, USA

MS 00-473: Received 29 December 2000/Accepted 30 March 2001

ABSTRACT
Studies were done to determine the survival of salmonellae in orange juice as affected by fortiŽ cation with calcium. Four
brands of commercially pasteurized orange juice fortiŽ ed with calcium (350 mg/240-ml serving) and nonfortiŽ ed juice were
inoculated separately with three types of inocula: strains of Salmonella Muenchen (inoculum 1), serotypes of human and
animal origin (inoculum 2), and isolates from raw produce- and juice-associated outbreaks (inoculum 3). Juice inoculated with
populations of 6.6 to 7.0 log10 CFU of Salmonella per ml was held at 48C for up to 32 days. The number of cells of inoculum
1 that survived in juice fortiŽ ed with calcium lactate/tricalcium phosphate (CaL/TCP) was signiŽ cantly lower (P 0.05) (2.80
log10 CFU/ml) than in nonfortiŽ ed juice (3.50 log10 CFU/ml) after 32 days’ storage. Death of salmonellae in inocula 1 and 2
was less in juice fortiŽ ed with TCP (3.21 and 3.33 log10 CFU/ml, respectively) than in the nonfortiŽ ed juice (3.75 and 4.15
log10 CFU/ml, respectively). During the 32-day storage period, populations in inocula 1 and 3 showed signiŽ cantly less
inactivation (2.62 and 3.12 log10 CFU/ml, respectively) in juice fortiŽ ed with calcium citrate (CC) than in nonfortiŽ ed juice
(3.14 and 3.60 log10 CFU/ml, respectively). There were no signiŽ cant differences in the survival of Salmonella in juice fortiŽ ed
with calcium citrate malate (CCM) and nonfortiŽ ed juice. Polymerase chain reaction (PCR) typing of randomly selected
Salmonella colonies revealed that Salmonella Heidelberg in inoculum 2 and Salmonella Baildon and Salmonella Poona in
inoculum 3 were the most prevalent at the end of the 32-day storage period at 48C, suggesting that serotypes selected for use
in inocula differed in tolerance to acidic environments. This study reveals that the form of calcium used to fortify orange juice
may affect the survival of Salmonella.

Unpasteurized orange juice has been the vehicle of sev-
eral outbreaks of salmonellosis. Salmonella Typhi was
identiŽ ed as the causative agent in an outbreak of infections
in Ohio in 1944, which resulted in 18 cases of illness and
one death (6, 11). Consumption of unpasteurized orange
juice at a New York hotel in 1989 led to 67 cases of sal-
monellosis, again linked to Salmonella Typhi (2). The
source of Salmonella in both of these incidents was most
likely infected food handlers.
In 1995, 63 conŽ rmed cases of Salmonella Hartford
infection were associated with the consumption of Salmo-
nella Hartford-contaminated unpasteurized orange juice at
a Florida theme park, with estimates of up to 6,300 persons
being infected (5). The source of Salmonella Hartford may
have been amphibians that introduced the pathogen into the
orange juice-processing facility (12). In 1999, 298 cases of
salmonellosis in the United States and Canada were asso-
ciated with drinking unpasteurized orange juice containing
Salmonella Muenchen (4). Oranges, the processing envi-
ronment, and storage and transport equipment were poten-
tial sources of the pathogen.
These outbreaks indicate that Salmonella can survive
refrigeration temperatures in an acidic environment for suf-
Ž cient times and at populations high enough to cause ill-
* Author for correspondence. Tel: 770-412-4738; Fax: 770-229-3216;
E-mail: jchen@cfs.grifŽ n.peachnet.edu.
ness. Unpasteurized orange juice presents a greater public
health risk than pasteurized juice because of the lack of a
physical or chemical intervention to destroy pathogenic mi-
croorganisms. Salmonella can grow on the surface of fresh-
ly peeled oranges at 248C (10). Warm oranges, when placed
in a cold suspension of Escherichia coli O157:H7, inter-
nalized the pathogen (16), thus potentially resulting in pro-
tection against cleaning processes to which oranges are sub-
jected before juicing. Vigilant plant sanitation and close
monitoring of transport and storage temperatures are cur-
rently utilized in an attempt to prevent contamination and
potential growth of pathogens in unpasteurized juice.
Fruit juices fortiŽ ed with calcium have become in-
creasingly popular in recent years. Orange juice is fortiŽ ed
to provide 35% (350 mg) of the Dietary Reference Intake
value of calcium per 240-ml (8 oz) serving. Various cal-
cium salts, including a calcium lactate/tricalcium phosphate
(CaL/TCP) combination, TCP, calcium citrate malate
(CCM), and calcium citrate (CC), are used to fortify orange
juice. CaL is also used to fortify orange juice at a concen-
tration of 300 mg/240-ml serving. However, calcium for-
tiŽ cation of orange juice has not been assessed to determine
if it affects on survival or growth of Salmonella.
The objectives of this study were to evaluate the effect
of various calcium salt supplements on survival of sal-
monellae in orange juice stored at 48C for up to 32 days
1300 SHARMA ET AL.
and to determine if Salmonella Muenchen has unique sur-
vival characteristics in orange juice when compared with
isolates of Salmonella originating from sources other than
orange juice.
MATERIALS AND METHODS
Orange juice. Four brands of pasteurized orange juice were
purchased from a local supermarket. Calcium-fortiŽ ed and non-
fortiŽ ed juices of each brand were evaluated. Brand A was forti-
Ž ed with a combination of CaL and TCP, and brand B contained
orange juice fortiŽ ed with CCM. TCP was used as the fortiŽ cant
in brand C, whereas brand D was fortiŽ ed with CC. All calcium-
fortiŽ ed juices provided 350 mg of calcium per 240 ml (8 oz) of
orange juice. Juices were selected so that the only known differ-
ence between calcium-fortiŽ ed and nonfortiŽ ed juices in each
brand was the presence of the calcium supplement listed on the
ingredient label. Brand A and C orange juices were made from
concentrate. Juices were stored at 48C in our laboratory for 2 days
until used. The pH of each type of orange juice was measured at
days 0 and 32 of the storage study using a pH probe (model 8000;
VWR ScientiŽ c, West Chester, Pa.).
Strains used. Three Ž ve-strain Salmonella inocula were
used. Inoculum 1 contained Ž ve Salmonella Muenchen isolates
provided by Dr. Ramesh Gauton at the State of Washington De-
partment of Health, Seattle, Wash. Inoculum 2 contained Salmo-
nella Typhimurium, Salmonella Heidelberg, Salmonella Thomp-
son, Salmonella Infantis, and Salmonella Enteritidis from human
or animal sources. Serotypes implicated in produce-associated out-
breaks were used to prepare inoculum 3: Salmonella Gaminara
(orange juice), Salmonella Hartford (orange juice), Salmonella
Michigan (cantaloupe), Salmonella Baildon (tomato), and Sal-
monella Poona (cantaloupe).
Stock cultures of Salmonella spp. were inoculated onto brain
heart infusion agar (Difco Laboratories, Detroit, Mich.) plates and
incubated at 378C for 24 h. Cultures were then transferred onto
fresh brain heart infusion agar plates and incubated under the same
conditions. A single colony of each strain was inoculated into 10
ml of brain heart infusion broth (Difco) and incubated with agi-
tation (165 rpm) until cultures reached an optical density at 600
nm of 0.90 to 0.95. Cultures were held at 48C until used. Inocula
consisted of a mixture of Ž ve strains of Salmonella Muenchen
(inoculum 1) or mixtures of Ž ve serotypes (inocula 2 and 3). Cul-
tures of each set of strains or serotypes were combined, and each
Ž ve-strain or Ž ve-serotype mixture (5 ml) was sedimented by cen-
trifugation (2,700 3 g for 20 min at 208C). The supernatant  uid
was decanted, and the cell pellet was resuspended in 5 ml of the
same brand of orange juice into which it would be inoculated.
Each inoculum (1 ml) was added to 99 ml of orange juice. In-
oculated juice was mixed thoroughly and held at 48C for up to 32
days.
Enumeration of Salmonella. Juice was analyzed for popu-
lations of Salmonella 15 times during the 32-day storage period.
The juice was mixed for 10 s immediately before it was analyzed.
One milliliter of juice was withdrawn, serially diluted (1/10) in
sterile 0.1% peptone water, and plated (0.1 ml, in duplicate) on
bismuth sulŽ te agar (Difco). Plates were incubated at 378C for 24
h before colonies were counted. Each experiment was replicated
twice.
Statistical analysis. Data were analyzed using multiple re-
gression analysis with SAS software (SAS Institute, Cary, N.C.).
Populations (log10 CFU/ml) were plotted versus time (days) of
storage at 48C. The slopes of the survival curves of Salmonella
J. Food Prot., Vol. 64, No. 9
in calcium-fortiŽ ed orange juice were compared to slopes in non-
fortiŽ ed juice for signiŽ cant differences (P 0.05).
Polymerase chain reaction (PCR) Ž ngerprinting of Sal-
monella serotypes. Salmonella isolated from orange juice inoc-
ulated with inoculum 2 or 3 and stored 32 days at 48C was sub-
jected to PCR Ž ngerprinting to determine if one or more serotypes
predominated. Five colonies randomly selected from bismuth sul-
Ž te agar plates on which samples of control or calcium-fortiŽ ed
juice were spread were streaked onto tryptic soy agar (Difco)
plates and incubated at 378C for 24 h. Cells from colonies were
transferred to 200 l of tryptic soy broth (Difco) in a 1.5-ml
microcentrifuge tube (Eppendorf; Brinkman Instruments, West-
bury, N.Y.) and incubated at 378C for 16 to 18 h. Cultures were
sedimented by centrifugation at 16,000 3 g for 3 min. The su-
pernatant  uid was decanted, and cell pellets were washed twice
in 200 l of sterile deionized water. After the Ž nal wash, the pellet
was resuspended in 200 l of deionized water and heated in a
boiling water bath for 10 min, followed by centrifugation at
16,000 3 g for 10 min. The DNA in the supernatant  uid was
used as a template in PCR ampliŽ cation. The reaction mixture
consisted of 13 l of sterile water, 5 l of 103 PCR buffer, 3 l
of MgCl2 (25 mM), 6 l of dNTP (10 mM), 20 l of template
DNA, 2 l of ERIC2 primer (8), and 1 l of Taq DNA poly-
merase (1 U/ l). All molecular reagents were obtained from
Roche Molecular Biochemicals (Indianapolis, Ind.). Reactions
were carried out in a DNA thermal cycler 480 (Perkin Elmer,
Norwalk, Conn.) under the following conditions: 948C for 5 min
(one cycle), 928C for 45 s, 258C for 1 min, 688C for 10 min (30
cycles), and 728C for 20 min (one cycle), then held at 48C. PCR
products were then separated on 1% agarose gel. Following elec-
trophoresis, gels were stained in ethidium bromide solution (1 g/
ml) and viewed and photographed using the Gel Doc 2000 system
(BioRad, Hercules, Calif.).
Cluster analysis of PCR Ž ngerprints of Salmonella strains
was performed using 1D Advantage software (Advanced Ameri-
can Biotechnology, Fullerton, Calif.).
RESULTS
Survival of salmonellae in orange juice. Initial Sal-
monella populations (day 0) in orange juice inoculated with
inocula 1, 2, and 3 ranged from 6.69 to 6.93 log10 CFU/
ml, 6.61 to 6.77 log10 CFU/ml, and 6.83 to 6.98 log10 CFU/
ml, respectively. Changes in populations of Salmonella
Muenchen in orange juice containing inoculum 1 are shown
in Figure 1. Populations in brand A juice fortiŽ ed with CaL/
TCP declined at a signiŽ cantly faster rate (P 0.05) com-
pared to the nonfortiŽ ed control over the 32-day storage
period. The presence of CCM in brand B juice did not
in uence the rate of death of Salmonella Muenchen. How-
ever, populations in brand C juice containing TCP and
brand D juice containing CC declined at signiŽ cantly
slower rates than those in respective nonfortiŽ ed controls.
Survival curves of salmonellae of inoculum 2 are
shown in Figure 2. The rate of inactivation of Salmonella
was not signiŽ cantly in uenced by fortiŽ cation of brand A
juice with CaL/TCP, fortiŽ cation of brand B with CCM, or
fortiŽ cation of brand D juice with CC. Survival of Sal-
monella serotypes in inoculum 2 was enhanced in brand C
juice fortiŽ ed with TCP.
Calcium fortiŽ cation of brand A (CaL/TCP), brand B
(CCM), and brand C (TCP) did not have a signiŽ cant effect
J. Food Prot., Vol. 64, No. 9 SURVIVAL OF SALMONELLAE IN ORANGE JUICE 1301

FIGURE 1. Survival of Salmonella

Muenchen (inoculum 1) in orange juice
stored at 48C for 32 days.

FIGURE 2. Survival of Salmonella from

human and animal origin (inoculum 2) in
orange juice stored at 48C for 32 days.
1302 SHARMA ET AL. J. Food Prot., Vol. 64, No. 9

FIGURE 3. Survival of Salmonella from

produce-associated outbreaks (inoculum
3) in orange juice stored at 48C for 32
days.

on the survival of serotypes in inoculum 3 (Fig. 3). Forti-
Ž cation of brand D with CC resulted in protection of in-
oculum 3 against inactivation.
Comparison of different Salmonella inocula. With
the exception of brand A orange juice, the three test inocula
responded similarly when inoculated into each brand of cal-
cium-fortiŽ ed and nonfortiŽ ed juice. Compared to salmo-
nellae in inocula 2 and 3, Salmonella Muenchen in inocu-
lum 1 declined signiŽ cantly more slowly in the nonfortiŽ ed
control of brand A control juice.
PCR Ž ngerprint results. Thirty-eight isolates from or-
ange juices inoculated with inoculum 2 and 40 isolates from
juice inoculated with inoculum 3 were Ž ngerprinted using
PCR. PCR Ž ngerprints indicate that Salmonella Heidelberg
made up 24 of 38 (63%) isolates from juice inoculated with
inoculum 2 (Table 1). Nine of the 38 colonies (24%) were
Salmonella Enteritidis. Salmonella Thompson and Salmo-
nella Infantis matched the PCR Ž ngerprint for 8% (3 of 38)
and 5% (2 of 38) of the colonies tested, respectively. No
Salmonella Typhimurium colonies were identiŽ ed. For in-

TABLE 1. Serotype distribution of Salmonella in orange juices stored at 48C for 32 daysa
Brand A Brand B Brand C Brand D
Salmonella
serotypes NF CaL/TCP NF CCM NF TCP NF CC Totalb

Inoculum 2
Typhimurium 0 0 0 0 0 0 0 0 0
Heidelberg 2 4 2 3 2 3 3 5 24
Thompson 0 0 1 0 1 1 0 0 3
Infantis 0 0 0 1 0 0 1 0 2
Enteritidis 3 0 2 1 2 0 1 0 9
Inoculum 3
Gaminara 0 0 0 0 0 0 0 0 0
Michigan 0 0 0 0 0 0 0 0 0
Baildon 0 4 4 2 3 1 0 3 17
Hartford 1 0 0 1 1 4 1 2 9
Poona 4 1 1 2 2 0 4 0 14
a NF, nonfortiŽ ed.
b Number out of 38 colonies from juices containing inoculum 2 and 40 colonies from juices containing inoculum 3.
J. Food Prot., Vol. 64, No. 9
TABLE 2. The initial and Ž nal pH of orange juices held at 48C
for 32 days
Orange juice pH
Brand Treatmenta Initial Final
A NonfortiŽ ed 3.98 3.93
CaL/TCP 4.28 4.20
B NonfortiŽ ed 4.07 3.94
CCM 4.24 4.15
C NonfortiŽ ed 4.02 3.79
TCP 4.07 4.00
D NonfortiŽ ed 3.91 3.85
CC 4.13 4.05
a Salmonella Heidelberg was the dominant serotype in
Juice was not fortiŽ ed with calcium or was fortiŽ ed with CaL/
TCP, CCM, TCP, or CC.
oculum 3 isolates, 43% (17 of 40) of colonies had the same
banding pattern as Salmonella Baildon, 35% (14 of 38)
matched the same Ž ngerprint as Salmonella Poona, and
23% (9 of 40) of the colonies matched that of Salmonella
Hartford. No Salmonella Gaminara or Salmonella Michigan
colonies were identiŽ ed.
DISCUSSION
CaL may act as an antimicrobial in orange juice to
reduce Salmonella populations in orange juice. No antimi-
crobial activity was observed in brand C juice fortiŽ ed with
TCP, possibly indicating that the principal antimicrobial ac-
tivity was attributable to CaL in brand A juice fortiŽ ed with
CaL/TCP. The low pH of orange juice favors antimicrobial
activity of CaL by allowing the undissociated, nonpolar
form of the lactate ion (CH3 CH2OHCOOH) to cross the
bacterial cell membrane and acidify the interior of the cell.
The presence of the lactate ion is known to disrupt the
hydrogen ion ef ux from the bacterial cell and leads to cell
death (14). Sodium lactate has been reported to reduce pop-
ulations of aerobic microorganisms on a variety of meat
products (1, 7, 9).
Adding lactic acid (0.1%) to unpasteurized apple cider
inoculated with E. coli O157:H7 results in a 5-log10 CFU/
ml reduction after subjecting the cider to freezing (48 h at
2208C), thawing (4 h at 48C), and holding for 6 h at 358C
(15). CaL has potential for use in a similar manner, in com-
bination with physical or chemical treatments, to reduce
pathogen populations in unpasteurized fruit juices.
FortiŽ cation of brand C orange juice with TCP en-
hanced survival of Salmonella Muenchen in inoculum 1
and serotypes from humans and animals (inoculum 2). The
pH of the nonfortiŽ ed brand C juice decreased more than
the pH of juice fortiŽ ed with TCP during the 32-day storage
period (Table 2). Salmonellae encountered less acid stress
in juice fortiŽ ed with TCP compared to nonfortiŽ ed juice
and retained higher viability. These results are in agreement
with a previous study (13), which revealed that acid-adapt-
ed salmonellae survived for 27 days in orange juice at pH
3.5, whereas salmonellae in orange juice at pH 4.4 survived
for 73 days.
It is apparent that in all inoculated orange juice sam-
SURVIVAL OF SALMONELLAE IN ORANGE JUICE 1303
ples, there was a lag period between inoculation and the
decline of Salmonella populations (Figs. 1 through 3). This
suggests that the stress-responding mechanism of salmo-
nellae renders cells the ability to buffer extreme pH and to
persist under acidic conditions for several days.
No single commercial juice manufacturer uses all four
types of calcium supplements evaluated in this experiment.
This makes it difŽ cult to compare the survival of Salmo-
nella as in uenced by different calcium salts used for for-
tiŽ cation. Differences in the composition of juices, pack-
aging, and storage and transport conditions may also affect
the survival of Salmonella in commercially fortiŽ ed orange
juices.
juice containing inoculum 2 after storage for 32 days. This
serotype was detected in all brands of juice with or without
added calcium. Salmonella Baildon and Salmonella Poona
were the dominant serotypes in juice containing inoculum
3. Salmonella Baildon was implicated in an outbreak of
salmonellosis associated with diced tomatoes (17). It was
suggested that the Salmonella Baildon isolate from this out-
break might be intrinsically more resistant to acid stress
than other serotypes of Salmonella. Salmonella Poona was
isolated from an outbreak involving the consumption of
cantaloupe (3). Serotypes in inoculum 3 associated with
unpasteurized orange juice (Salmonella Hartford and Sal-
monella Gaminara) were not as prevalent as Salmonella
Baildon and Salmonella Poona at the end of 32 days of
storage. Further investigation into acid tolerance of Sal-
monella Heidelberg, Salmonella Baildon, and Salmonella
Poona is warranted.
In summary, fortiŽ cation of orange juice with three of
four calcium salts affected the survival of Salmonella. CaL/
TCP increased the rate of inactivation of Salmonella
Muenchen, whereas CC and TCP reduced the rate of in-
activation of Salmonella in some instances. FortiŽ cation
with CCM did not in uence the survival of salmonellae.
Using CaL in unrefrigerated fruit juices could cause a more
rapid reduction in spoilage microorganisms because the ef-
Ž cacy of CaL at temperatures higher than 48C would likely
be increased. Concentrations of CaL in orange juice may
be modiŽ ed to increase antimicrobial activity but may also
alter the nutritional or sensory characteristics of orange
juice. The addition of CaL to orange juice may extend the
shelf life of the product and enhance safety while still pro-
viding a nutritional beneŽ t to the consumer.
ACKNOWLEDGMENTS
We thank Jerry Davis for assisting statistical analysis and Ying Mao,
Mahbub Islam, and Joy Adams for support.
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