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Susceptibility of Antibiotic-Resistant and Antibiotic-Sensitive Foodborne Pathogens to Acid Anionic Sanitizers

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Acid anionic sanitizers for treatment of fruits and vegetables were prepared using ingredients generally recognized as safe by the U.S. Food and Drug Administration or anionic surfactants and organic acid food additives. They met the regulatory definition as sanitizers by showing bactericidal efficacy of 99.999% in 30 s against Staphylococcus aureus ATCC 6538 and Escherichia coli ATCC 11229. These sanitizers showed a broad spectrum of microbicidal activity against both gram-positive and gram-negative bacteria. Antibiotic-sensitive and resistant strains of Listeria monocytogenes and Salmonella typhimurium were equally susceptible to these sanitizers. The acid anionic sanitizers showed microbicidal efficacy equal to that of hypochlorite against Aeromonas hydrophila, E. coli O157:H7, L. monocytogenes, Pseudomonas aeruginosa, S. typhimurium, and S. aureus. Unlike most other sanitizers, these agents do not covalently react with organic components of food; unlike cationic agents, they do not leave residues. The acid anionic sanitizers are prepared using stable, biodegradable, and nontoxic ingredients. Rapid microbicidal activity and the ease of storage, transportation, and use make these sanitizers an attractive alternative to hypochlorite for sanitizing fruits and vegetables.
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Journal of Food Protection, Vol. 61, No. 10, 1998, Pages 1390--1395
Copyright
©,
International Association ot Milk, Food and Environmental Sanitarians
Research Note
Susceptibility of Antibiotic-Resistant and Antibiotic-Sensitive
Foodborne Pathogens to Acid Anionic Sanitizers
JOHN A. LOPES*
Microcide, Inc., 2727 Second Avenue, Detroit, Michigan 48201
MS 98-40: Received 9 February 1998/Accepted 22 April 1998
ABSTRACT
Acid anionic sanitizers for treatment of fruits and vegetables were prepared using ingredients generally recognized as safe by
the U.S. Food and Drug Administration or anionic surfactants and organic acid food additives. They met the regulatory definition
as sanitizers by showing bactericidal efficacy of 99.999% in 30 s against Staphylococcus aureus ATCC 6538 and Escherichia coli
ATCC 11229. These sanitizers showed a broad spectrum of microbicidal activity against both gram-positive and gram-negative
bacteria. Antibiotic-sensitive and resistant strains of Listeria monocytogenes and Salmonella typhimurium were equally
susceptible to these sanitizers. The acid anionic sanitizers showed microbicidal efficacy equal to that of hypochlorite against
Aeromonas hydrophila, E. coli OI57:H7, L. monocytogenes, Pseudomonas aeruginosa, S. typhimurium, and S. aureus. Unlike
most other sanitizers, these agents do not covalently react with organic components of food; unlike cationic agents, they do not
leave residues. The acid anionic sanitizers are prepared using stable, biodegradable, and nontoxic ingredients. Rapid microbicidal
activity and the ease of storage, transportation, and use make these sanitizers an attractive alternative to hypochlorite for sanitizing
fruits and vegetables.
The magnitude of economic loss, human suffering, and
public health impact of foodborne illnesses has been under-
estimated by the general public and health-care profession-
als until the last few years. Foodborne illnesses result in
about 9,000 fatalities and economic loss of 5 billion dollars
annually in the United States alone (1, 11). Fresh fruits and
vegetables probably account for about 6% of the foodborne
infections (7). Salmonella outbreaks have been due to
consumption of contaminated alfalfa sprouts, cantaloupes,
watermelons, unpasteurized orange juice, and raw tomatoes
(6, 10,
19, 29, 32, 34). Shigellosis was traced to the
consumption of green onions (19). Imported raspberries
were implicated in Cyclospora infections (20). Contami-
nated apple cider caused Escherichia coli 0157:H7 infec-
tions (3). Thus, there is a need for safe and effective
sanitizing agents for treating produce.
The gravity of foodborne illnesses is further accentu-
ated by frequently encountered drug-resistant pathogens.
The indiscriminate use of antibiotics in human therapy and
the introduction of these antibiotics in poultry and animal
husbandry have been incriminated in the rapid development
of drug-resistant foodborne pathogens. These pathogens are
easily introduced in the food chain through contaminated
poultry, milk, meat, and fruits and vegetables grown on
manure contaminated with them (25).
Complete sterilization of fruits and vegetables without
extensive destruction of tissues is hard to achieve by
*
Author for correspondence. Tel: 248-526-9663; Fax: 248-526-9663;
E-mail: lopes@microcidenic.com.
chemical samtIzmg agents (14). Additionally, fruits and
vegetables harbor insects that in tum have their own
intestinal microbiota. The number of aphids, thrips, and/or
mites allowed within the defect action level established by
the U.S. Food and Drug Administration (FDA) is 30, 50, and
60 per 100 g of frozen Brussel sprouts, spinach, and
broccoli, respectively; 5% wormy or moldy canned peaches
are also allowed (16). Chemical disinfecting agents, al-
though effective, fail to reach hidden sites to kill microorgan-
isms. However, chemical sanitizers offer convenience of use
and economic benefits over other sanitizing agents.
Acid anionic sanitizing agents offer distinct advantages
over most chemical sanitizing agents, including aldehydes,
hypochlorites, peroxygen, and quaternary compounds: the
absence of covalent reactions, chemical stability, conve-
nience of use, freedom from organoleptic properties, environ-
mental safety, and biodegradability. However, presently
available acid anionic sanitizers contain ingredients not
allowed by regulatory agencies for direct use on food
products. Acid anionic sanitizers formulated with ingredi-
ents either classified as generally regarded as safe or food
additives suitable for direct use on fruits and vegetables
were evaluated for their microbicidal properties in the
following investigation.
MATERIALS AND METHODS
Chemicals and media. The antibiotics and chemicals were
purchased from Sigma Chemical Co, St. Louis, Mo.; the media
from Difco Laboratories, Detroit, Mich.; the Stomacher 400 from
Seward Medical Co., London, England; and API E and Listeria
identification kits from Biomerieux Vitek, Hazelwood, Mo.
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1. Food Prot., Vol. 61, No. 10 SUSCEPTffiILITY OF PATHOGENS TO ACID ANIONIC SANITIZERS 1391
Preparation of sanitizers. The acid anionic sanitizers AP,
DO, and DL are concentrated products made up of organic acids
and anionic surfactants patented by Microcide, Inc. (26, 27).
Concentrations of sodium lauryl sulfate, dioctyl sodium sulfosucci-
nate, and sodium capryl lactylate in the final dilution of the
sanitizers for use were 1.00, 0.67, and 1.25 mM, respectively.
Sanitizer AP consists of sodium lauryl sulfate and citric acid,
sanitizer DO contains dioctyl sodium sulfosuccinate and glacial
acetic acid, and sanitizer DL contains sodium capryllactylate and
lactic acid. The concentrations of citric acid, acetic acid, and lactic
acid in the final dilution for use of the sanitizers were 19.3, 161.5,
and 94.76mM, respectively.
Bacterial cultures. E. coli ATCC 11229, Staphylococcus
aureus ATCC 6538, Listeria monocytogenes ATCC 7644, Salmo-
nella typhimurium ATCC 7823, Aeromonas hydrophila ATCC
7965, and Pseudomonas aeruginosa ATCC 10145 were purchased
from the American Type Culture Collection (Bethesda, Md.).
Nalidixic acid-resistant strains of S. typhimurium were obtained
from Dr. Stan Bailey of the U.S. Department of Agriculture
Research Station (Athens, Ga.). These bacterial cultures were
resistant to 200 Ilg/ml of nalidixic acid; they were labeled as
S. typhimurium BAl7, BAl8, BAI9, BA20, and BA21 in the
present investigation. E. coli 0157:H7 and L. monocytogenes Scott
A were obtained from Dr. Robert Brackett at the University of
Georgia (Griffin, Ga.). Antibiotic-resistant L. monocytogenes strains
(F5069, Scott A, ATCC 19115, NCF-U2K3, and NCF-FKK4)
carrying the chloramphenicol, erythromycin, and rifampin resis-
tance plasmid pGKl2 were obtained from Dr. Peggy Foegeding of
North Carolina State University, Raleigh, N.C. (15). Permission to
use plasmid-carrying strains was obtained by Dr. Jan Kok of the
Genetisch Instituut, Haren, The Netherlands.
Maintenance of cultures. E. coli ATCC 11229 and S. aureus
ATCC 6538 were maintained on nutrient agar as outlined by the
Association of Official Analytical Chemists (AOAC) (14). All
other cultures were maintained on brain heart infusion (BHI) agar
except the antibiotic-resistant strains, which were maintained on
BHI agar containing either 100 Ilg of nalidixic acid per ml in the
case of Sa. typhimurium or 3 Ilg each of chloramphenicol and
erythromycin per ml in the case of L. monocytogenes.
Experimental procedure. The sanitizing efficacy of sanitiz-
ers AP, DO, and DL against E. coli ATCC 11229 and S. aureus
ATCC 6538 were first evaluated by the sanitizer and germicidal
detergent test specified by the AOAC (2). Fifty micrograms per
milliliter of hypochlorite was used as a positive control. The
bacterial cultures were transferred for three consecutive days on
nutrient agar. For use in the test, the cultures were grown on
nutrient agar in french square bottles at 37°C for 18 to 22 h.
Growth was suspended in a phosphate buffer dilution solution
and adjusted to a cell density of 10 X1010 CFU/rnl by the
previously established relationship of optical density at 560 nm to
cell numbers. Dilutions for use of the test sanitizers and control
solutions were prepared in 99 ml of water with 500 Ilg/ml of
synthetic water hardness. Sterile solutions containing 19.3, 161.5,
and 94.76 mM concentrations of citric acid, glacial acetic acid, and
lactic acid, respectively, served as acid controls. Sterile solutions
containing 1.00, 0.67, and 1.25 mM concentrations of sodium
lauryl sulfate, dioctyl sodium sulfosuccinate and sodium capryl
lactylate, respectively, served as anionic surfactant controls. Ninety-
nine milliliters of sterile water was used in place of sanitizer
solution as a negative control. Hypochlorite was included at 50
Ilg/ml (1 mM) as a positive control.
The tests were carried out in 250-ml wide-mouth Erlenmeyer
flasks at room temperature (24°C). One milliliter of the bacterial
suspension was added to 99 rnl of the sanitizer solution while
rapidly mixing by a swirling motion. After 30 and 60 s, respec-
tively, I rnl of the test mixture was withdrawn, added to 9 rnl of the
neutralizer solution, and mixed with a vortex mixer. Other controls
described above were also used. The neutralizer solution consisted
of 1\veen 80 and lecithin in phosphate buffer (pH 7.2) (2). To
neutralize the hypochlorite, 0.1 ml of 10% filter-sterilized sodium
thiosulfate solution was added to 9 rnl of the autoclaved neutralizer
solution (25). One and
O.
I milliliters of the neutralized test mixture
was then plated in duplicates on plate count agar by the pour plate
method. After 48 h at 37°C, the bacterial colonies were counted.
The efficacy of the sanitizers AP, DO, and DL against
S. typhimurium, L. monocytogenes, A. hydrophila, and P. aerugi-
nosa was evaluated essentially by the modified AOAC detergent
and germicidal sanitizer test (24). Hypochlorite at 50 Ilg/ml (I mM)
and 100 Ilg/ml (2 mM) was used as a control. The sanitizers were
tested against both natural isolates and the antibiotic-resistant
strains of L. monocytogenes and S. typhimurium.
The bacteria were grown in 50 ml of BHI broth in 150 ml
Erlenmeyer flasks for 18 to 22 h on a Lab-Line Environ rotary
shaker (Lab-Line Instruments Inc., Melrose Park, 111.)at 150 rpm
and 35°C. By using the previously obtained relationship of optical
density at 560 nm of the cell suspension to cell numbers, the cell
suspension was adjusted to 7.5 X109to 1.25 X1010CFU/rnl. One
milliliter of the cell suspension was used in the test.
The test was carried out essentially by the AOAC germicidal
and detergent sanitizer procedure as described above. After neutral-
ization, the test mixture was plated on BHI agar by the pour plate
method. The surviving bacterial colonies were counted after 48 h of
incubation at 37°C.
RESULTS
Controls with the anionic surfactants or the organic
acids alone did not exhibit microbicidal activity under the
test conditions within 30 and 60 s. The microbicidal activity
was only observed when anionic surfactants were combined
with acids in the sanitizer formulations. Table 1 shows the
results for the AOAC sanitizer test. The test sanitizers AP,
DO, and DL, as well as the hypochlorite control (50 I1g/ml),
showed a 99.999% (5-log) reduction in the bacterial popula-
tion in 30 s from the initial count of between 75 to 125 X 106
cells per ml (approximately 8.0 log CFU/ml) and thus meets
the U.S. Environmental Protection Agency regulatory require-
ment for sanitizing agents. The ability of the sanitizers to be
effective in water with 500 I1g/ml hardness shows that these
sanitizers can maintain their microbicidal efficacy with hard
water under field conditions.
Sanitizers AP, DO, and DL exhibited a broad spectrum
of bactericidal activity against both gram-positive and
gram-negative bacteria (Tables 1 and 2). All three sanitizers
were effective as microbicidal agents against A. hydrophila,
E. coli 0157:H7, L. monocytogenes, P. aeruginosa, and S.
typhimurium. These sanitizers reduced cell populations by
99.999% within 30 s.
Tables 3 and 4 show that, irrespective of the type of
antibiotic resistance, the test sanitizers showed lethal activi-
ties against antibiotic-resistant strains of Sa. typhimurium
and L. monocytogenes respectively. The level of 1 mM
hypochlorite, commonly used as control, in the AOAC
sanitizer test was ineffective, however. Two millimolar
hypochlorite was required to reduce the population of
S. typhimurium and L. monocytogenes by 99.999% in 30 s.
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1392
LOPES
J. Food Prot., Vol. 61, No. 10
TABLE 1. Efficacy of sanitizers against S. aureus ATCC 6538 and E. coli ATCC 11229 by the AOAC gennicidal and detergent sanitizer test
Test organism
S. aureus ATCC 6538
E. coli ATCC 11229
Challenge
logCFU/ml
8.0
8.5
Number of surviving bacteria
b
(log CFU/ml) after contact time
30 s 60 s
Test
sample
a
log CFU/ml %kill logCFU/ml %kill
AP 2.1::':: 0.0 >99.999 <1.0 >99.999
DL <1.0 >99.999 <1.0 >99.999
DO 2.2::':: 0.1 >99.999 1.3 ::'::0.5 >99.999
HOCL1 mM <1.0 >99.999 <1.0 >99.999
AI' <1.0 >99.999 <1.0 >99.999
DL <1.0 >99.999 <1.0 >99.999
DO 1.3 ::'::0.1 >99.999 0.5::':: 0.7 >99.999
HOCLlmM 1.0::':: 0.0 >99.999 <1.0 >99.999
aAP, DO, and DL are test sanitizers; HOC!, hypochlorite control.
bValues given are the mean of two tests.
Similar results with hypochlorite have been previously
reported for these two species (4, 24).
DISCUSSION
The use of E. coli ATCC 11229 and S. au reus ATCC
6538 served in evaluating the activity of anionic sanitizing
agents to meet the regulatory requirement for microbicidal
agents as sanitizers. Without meeting this requirement, the
test formulations cannot be labeled and used as sanitizers.
The activity of these sanitizing agents against antibiotic-
resistant bacteria demonstrated their potential use to reduce
the danger of foodbome illnesses from both antibiotic-
susceptible and resistant bacteria.
The active components of the acid anionic sanitizers are
safe and nontoxic for washing fruits and vegetables. All
three organic acids, namely, acetic, citric, and lactic acids are
widely used in food preparations. The organic acids were
selected on the basis of their solubility in water, absence of
color or other organoleptic properties, chemical stability,
minimum corrosivity at the use concentration, availability in
concentrated form, and availability at low cost. The anionic
sanitizers are nontoxic surfactants used either in food or
TABLE 2. Efficacy of sanitizers against selected microorganisms by the AOAC gennicidal and detergent sanitizer test
Number of surviving bacteria
b
(log CFU/ml) after contact time
30 s 60 s
Challenge Test
Test organism logCFU/ml sample
a
log CFU/ml %kill log CFU/ml %kill
A. hydrophila ATCC 7965 8.0 AP <1.0 >99.999 <1.0 >99.999
E. coli 0157:H7 8.0 AP <1.0 >99.999 <1.0 >99.999
L. monocytogenes ATCC 7644 8.1 AP 1.3 ::'::0.1 >99.999 <1.0 >99.999
P. aeruginosa ATCC 10145 8.3 AP <1.0 >99.999 <1.0 >99.999
Sa. typhimurium ATCC 7823 8.1 AP <1.0 >99.999 <1.0 >99.999
A. hydrophila ATCC 7965 8.0 DL 1.4 ::'::0.2 >99.999 <1.0 >99.999
E. coli ATCC 0157:H7 8.0 DL <1.0 >99.999 <1.0 >99.999
L. monocytogenes ATCC 7644 8.1 DL <1.0 >99.999 <1.0 >99.999
P. aeruginosa ATCC 10145 8.3 DL <1.0 >99.999 <1.0 >99.999
Sa. typhimurium ATCC 7823 8.1 DL 0.5::':: 0.7 >99.999 <1.0 >99.999
A. hydrophila ATCC 7965 8.0 DO <1.0 >99.999 <1.0 >99.999
E. coli ATCC 0157:H7 8.0 DO <1.0 >99.999 <1.0 >99.999
L. monocytogenes ATCC 7644 8.2 DO <1.0 >99.999 <1.0 >99.999
P. aeruginosa ATCC 10145 8.3 DO 1.4 ::'::0.5 >99.999 1.2::':: 0.0 >99.999
Sa. typhimurium ATCC 7823 8.1 DO <1.0 >99.999 <1.0 >99.999
A. hydrophila ATCC 7965 8.0 HOCL4mM 0.5::':: 0.7 >99.999 <1.0 >99.999
E. coli ATCC 0157:H7 8.0 HOCL2mM <1.0 >99.999 <1.0 >99.999
L. monocytogenes ATCC 7644 8.2 HOCL1mM 2.8::':: 0.0 >99.999 2.2::':: 0.0 >99.999
P. aeruginosa ATCC 10145 8.3 HOCL4mM 1.2 ::'::0.3 >99.999 0.5::':: 0.7 >99.999
Sa. typhimurium ATCC 7823 8.1 HOCL1mM
TC
<99.999 2.9::':: 0.0 >99.999
aAP, DO, and DL represent test sanitizers; HOC!, hypochlorite.
bValues given are the mean of two tests.
C
Too numerous to count in both tests.
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J. Food Prot., Vol. 61, No. 10 SUSCEPTIBILITY OF PATHOGENS TO ACID ANIONIC SANITIZERS 1393
TABLE 3. Efficacy of sanitizers against S. typhimurium by the AOAC germicidal and detergent sanitizer test
Number of surviving bacteria
b
(log CFU/ml) after contact time
30 s60 s
S. typhimurium Challenge Test
culture no. logCFU/ml sample
a
log CFU/ml
%
kill logCFU/ml
%
kill
BA17 8.1 AP <1.0 >99.999 <1.0 >99.999
BA18 8.0 AP <1.0 >99.999 <1.0 >99.999
BA19 8.0 AP <1.0 >99.999 <1.0 >99.999
BA20 8.2 AP 0.5:': 0.7 >99.999 <1.0 >99.999
BA21 8.3 AP <1.0 >99.999 <1.0 >99.999
BA17 8.1 DL 0.5:': 0.7 >99.999 <1.0 >99.999
BA18 7.7 DL <1.0 >99.999 <1.0 >99.999
BA19 8.0 DL <1.0 >99.999 <1.0 >99.999
BA20 8.0 DL <1.0 >99.999 <1.0 >99.999
BA21 8.0 DL <1.0 >99.999 <1.0 >99.999
BA17 8.1 DO <1.0 >99.999 <1.0 >99.999
BA18 7.7 DO <1.0 >99.999 <1.0 >99.999
BA19 8.0 DO <1.0 >99.999 <1.0 >99.999
BA20 8.0 DO <1.0 >99.999 <1.0 >99.999
BA21 8.0 DO <1.0 >99.999 <1.0 >99.999
BA17 8.1 HOCL TC <99.999 2.9:': 0.0 >99.999
BA18 7.7 HOCL T <99.999 2.4:': 0.0 >99.999
BA19 8.0 HOCL T <99.999 T <99.999
BA20 8.0 HOCL T<99.999 T <99.999
BA21 8.0 HOCL T<99.999 3.0:': 0.0 2:99.999
a
AP, DO, and DL represent test sanitizers; HOC!, 1 mM of hypochlorite.
b
Values given are the mean of two tests.
CToo numerous to count in both tests.
pharmaceutical preparations. Sodium lauryl sulfate is used
in gelatin for the preparation of marshmallows, egg white
solids, acidulated fruit drinks, and in much higher levels in
numerous oral hygiene products (17). Dioctyl sodium sulfo-
succinate is allowed as a component of a number of acidified
soft drinks, as an emulsifying agent in gelatin deserts, stool
softeners, and other pharmaceutical preparations (17). So-
dium capryllactylate has been approved as a food additive
(17). It is rapidly hydrolyzed by esterases in the body to the
fatty acid and lactic acid.
Acid anionic sanitizers do not covalently react with the
organic matter of fruits and vegetables (13). Thus their use
lacks the potential to permanently alter and modify food
ingredients by covalent chemical reactions, as is the case
with highly reactive chemicals such as hypochlorites, glutar-
aldehyde, ozone, or peracetic acid. Although cationic sanitiz-
ers may not covalently react with organic matter, the
positively charged quaternary ammonium compounds
strongly bind to the negatively charged cellulosic plant
material to leave substantial amounts of residue (useful for
fabric softening). The negatively charged anionic agents are
less likely to leave large amounts of residue on treated
produce. Preliminary tests carried out in our laboratory
confirmed that treatment with the sanitizer AP left only low
levels of sodium lauryl sulfate on treated vegetables.
Even at 200 fIg/ml (4 mM), hypochlorite treatment
reduced bacterial populations by :52 orders of magnitude on
Brussel sprouts and beef, chicken, and lamb carcasses (4, 5,
23, 30, 31). In the absence of more effective and/or safer
sanitizing agents, hypochlorite has been the most widely
used sanitizer in the food industry. However, its use on raw
food can result in production of harmful organochlorine
compounds (26). Chlorine incorporation in meat, poultry,
shrimp, and vegetables after hypochlorite treatment has been
demonstrated (12, 21, 22). Chicken held in 50 fIg/ml of
chlorine for 5 min at 15°C had average chloroform concen-
trations of 144, 177, and 477 ng/ml in the skin, muscle, and
depot fat, respectively (33). Soybean sprouts and cabbages
treated with solutions of sodium hypochlorite showed in-
creased formation of chloroform and residual chlorine with
increased concentration of hypochlorite and with increases
in treatment temperature (21).
In view of the foregoing investigations, the upper limit
of hypochlorite (0.2% or 2,000 fIg/ml) established by the
U.S. Code of Federal Regulations (21 CPR
§
173.315 (17))
for washing and lye peeling of fruits and vegetables appears
to be dangerously high (7). At these high levels, hypochlo-
rite can produce harmful organochlorine compounds. Chlo-
roform, N-chloro compounds, chlorinated purine and pyrimi-
dines, chlorophenols, and chlorobenzenes are some of the
carcinogenic and toxic compounds resulting from chlorina-
tion of food products and water (8, 18). Thus use of
hypochlorite offers a choice between reduced risk of food-
borne infections and the risk of exposure to carcinogenic
chemicals.
The anionic sanitizing agents exhibited bactericidal
activity equivalent to that ofhypochlorites. This activity was
observed against a broad spectrum of microorganisms,
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1394 LOPES J. Food Prot., Vol. 61, No. 10
TABLE 4. Efficacy of sanitizers against L. monocytogenes by the AOAC germicidal and detergent sanitizer test
Number of surviving bacteria
b
(log CFU/ml) after contact time
30 s 60 s
L. monocytogenes Challenge Test
culture no. 10gCFU/ml sample" log CFU/ml
%
kill 10gCFU/ml
%
kill
F5069 8.1 AP 1.3 ::'::0.0 >99.999 <1.0 >99.999
Scott A 8.1 AP 1.4 ::'::0.0 >99.999 <1.0 >99.999
19115 8.0 AP <1.0 >99.999 <1.0 >99.999
NCF-U2K3 8.0 AP 1.1 ::'::0.2 >99.999 <1.0 >99.999
NCF-FKK4 7.9 AP 1.2::':: 0.3 >99.999 <1.0 >99.999
F5069 8.2 DL <1.0 >99.999 <1.0 >99.999
Scott A 8.3 DL 0.5::':: 0.7 >99.999 <1.0 >99.999
19115 7.9 DL <1.0 >99.999 <1.0 >99.999
NCF-U2K3 8.0 DL 0.5::':: 0.7 >99.999 <1.0 >99.999
NCF-FKK4 8.0 DL <1.0 >99.999 <1.0 >99.999
F5069 8.1 DO <1.0 >99.999 <1.0 >99.999
Scott A 8.1 DO <1.0 >99.999 <1.0 >99.999
19115 8.0 DO <1.0 >99.999 <1.0 >99.999
NCF-U2K3 8.0 DO <1.0 >99.999 <1.0 >99.999
NCF-FKK4 7.9 DO <1.0 >99.999 <1.0 >99.999
F5069 8.1 HOC1 TC <99.999 2.9::':: 0.0 >99.999
Scott A 8.1 HOCl T <99.999 2.4 ::'::0.0 >99.999
19115 8.0 HOC1 T <99.999 T <99.999
NCF-U2K3 8.0 HOCl T <99.999 T <99.999
NCF-FKK4 7.9 HOCl T <99.999 3.0::':: 0.0 ~99.999
a
AP, DO, and DL represent test sanitizers; HOCl, 1 mM of hypochlorite.
bToo numerous to count in both trials.
CValues given are the mean of two tests.
including gram-positive and gram-negative bacteria as well
as protozoan cysts (26, 27, 28). The acid anionic sanitizing
agents offer a choice of safe, stable, convenient, biodegrad-
able, and effective chemical sanitizers for the treatment of
fruits and vegetables.
In addition, the acid anionic sanitizers have the cleaning
action of a detergent, absent in many other sanitizing agents.
Unlike quaternary ammonium sanitizers, which have a pH
range conducive to bacterial growth, the pH values of acid
anionic sanitizers are very low (2 to 3). Pathogenic bacteria
are not known to multiply at such low pH values. Our
previous investigations have shown that even acid-tolerant
lactobacilli are found to be susceptible to the acid anionic
sanitizing agents. The acid anionic sanitizers prepared with
generally-regarded-as-safe or food-additive ingredients are
safe and nontoxic. Thus, these sanitizers offer a better choice
to consumers and to institutional and industrial users for
decontaminating raw fruits and vegetables.
ACKNOWLEDGMENTS
This investigation was partly supported by a Small Business Innova-
tive Research grant in 1992 from the National Institutes of Health Infectious
Disease Branch. Technical assistance of Rose Lopes and Andy Rillo is
greatly appreciated.
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... Clearly, F i = X ii + X ij and F j = N j + N i − X ii − X ij where F i is the final number of bacteria on object i, following the transfer. Hypochlorite Aarnisalo et al., 2007aAarnisalo et al., 2000Best et al., 1990Deza et al. 2005Erkmen, 2004Lopes, 1998Meylheuc et al. 2006Sagripanti et al., 1997Taormina and Beuchat, 2002Virto et al., 2004Yang et al., 2009 11 321 891 5.5 (4.4-6.6) 3 38 117 2.8 (1.6-4.0) ...
... 4.4 (2.5-6.4) Hypochlorite 9 144 412 Aarnisalo et al., 2007aAarnisalo et al., 2000Best et al., 1990Deza et al. 2005Erkmen, 2004Lopes, 1998Sagripanti et al., 1997Taormina and Beuchat, 2002Yang et al., 2009 6.5 (5.0-8.1) 3.8 (2.1-5.4) a Mean log inactivation and corresponding 95% confidence interval surrounding the mean as predicted by generalized linear mixed model. ...
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Listeria monocytogenes is readily found in the environment of retail deli establishments and can occasionally contaminate food handled in these establishments. Here we synthesize the available scientific evidence to derive probability distributions and mathematical models of bacterial transfers between environmental surfaces and foods, including those during slicing of food, and of bacterial removal during cleaning and sanitizing (models available at www.foodrisk.org). Transfer coefficients varied considerably by surface type, and after log(10) transformation were best described by normal distributions with means ranging from -0.29 to -4.96 and standard deviations that ranged from 0.07 to 1.39. 'Transfer coefficients' during slicing were best described by a truncated logistic distribution with location 0.07 and scale 0.03. In the absence of protein residues, mean log inactivation indicated a greater than 5 log(10) reduction for sanitization with hypochlorite (mean: 6.5 log(10); 95% confidence interval (CI): 5.0-8.1 log(10)) and quaternary ammonium compounds (mean: 5.5 log(10); 95% CI: 3.6-7.3 log(10)), but in the presence of protein residues efficacy reduced dramatically for hypochlorite (mean: 3.8 log(10); 95% CI: 2.1-5.4 log(10)) as well as quaternary ammonium compounds (mean: 4.4log(10); 95% CI: 2.5-6.4 log(10)). Overall, transfer coefficients are therefore low, even though cross-contamination can be extremely efficient under certain conditions. Dozens of food items may consequently be contaminated from a single contaminated slicer blade, albeit at low concentrations. Correctly performed sanitizing efficiently reduces L. monocytogenes contamination in the environment and therefore limits cross-contamination, even though sanitization is only performed a few times per day. However, under unfavorable conditions reductions in bacterial concentration may be far below 5 log(10). The probability distributions and mathematical models derived here can be used to evaluate L. monocytogenes cross-contamination dynamics in environments where foods are handled, and to assess the potential impact of different intervention strategies.
... When the ATR was induced in either type of strain by growth in glucose, some strain variations in acid resistance were observed, but no association between susceptibility to antimicrobial agents and potential to survive a low pH stress was made (Bacon and others 2003b). Lopes (1998) reported observing that antibiotic-resistant strains of Salmonella Typhimurium and L. monocytogenes were equally as susceptible to sanitizer treatments as antibiotic sensitive strains. They found that Salmonella Typhimurium strains resistant to nalidixic acid and L. monocytogenes strains carrying plasmid pGK12 encoding resistance to chloramphenicol, erythromycin, and rifampin did not exhibit resistance to organic acid/anionic surfactant-based sanitizers. ...
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... Acidity plays an important role in the control of Salmonella and other pathogens in cheese. As in the present study, previous researchers have found that the behavior of MDR Salmonella strains was similar to that of naturally occurring non-MDR strains when exposed to acidic interventions (4, 32) and sanitizers (39). The ability of Salmonella to survive under low pH conditions also appears to be independent of antimicrobial resistance in acidified minimal and complex media (7). ...
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... A survey of active ingredients approved for use in EPAregistered products revealed several options for organic acid actives and botanical actives based on essential plant oils. The broad spectrum anti-microbial activity of naturally derived citric and lactic acid is well known and these active ingredients are widely used in both consumer and commercial household and personal care products (Hellstrom et al., 2006;Lopes, 1998;Turner et al., 2004). However, the efficacy of these organic acids is optimal under acidic conditions which can result in products that are irritating to eyes and skin (Berner et al., 1988;Swanson et al., 1995;Mangia et al., 1996). ...
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We studied the disappearance of residual chlorine and the formation and behavior of chloroform (CHC13) in vegetables treated with sodium hypochlorite (NaCIO). Soybean sprouts and cabbages were treated with NaCIO solutions of various concentrations, and residual chlorine and formation of CHC13 in the samples were determined. It was found that both residual chlorine and CHC13 increased with an increase in NaCIO concentration. However, CHC13 formation was less in the cabbages than in the soybean sprouts. The soybean sprouts and cabbages treated with NaCIO solution were then kept in glass containers and changes which took place with the passage of time in the residual chlorine and CHC13 were studied. When stored at lower temperatures, the loss of residual chlorine was less and CHC13 increased, while chlorine remained. When the soybean sprouts were immersed in NaCIO solutions and maintained at different temperatures, CHC13 formation was less when the treatment temperature was lower. For treatment of vegetables with NaCIO solution, low temperature treatment is therefore preferable. © 1992, Japanese Society for Food Hygiene and Safety. All rights reserved.
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Pieces of beef, pork and poultry were immersed for 2, 6 and 24 hr in 100 times their weight of water containing 200 ppm chlorine labelled with 36C1. Within 2 hr over 50% of the chlorine had reacted with the meat. Most of the products of chlorination were water-soluble and had leached into the water but small amounts of chlorinated lipids and water-soluble chlorinated compounds were found in the meat. These ranged from 2–3% of the total 36C1 present at 2 hr to 6–8% at 24 hr. Meat treated with chlorinated water was found to increase much more in weight than meat treated with unchlorinated water. Chicken skin was found to absorb more water than lean or fat and increased in weight by 130% after 2 hr in chlorinated water.
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Chlorine incorporation into shrimp was determined following immersion in a 150 mg/L solution of HO36Cl. Approximately 2% of the 36Cl in the original immersion solution was incorporated into the shrimp during the 30-min immersion period; 75% of which was detected in the edible portion. Approximately 3% of the chlorine associated with the edible portion was detected in the CHCl3:CH3OH soluble fraction. Data indicated that chlorine incorporation in lipids is directly related to the degree of unsaturation. The trichloroacetic acid (TCA) precipitable protein fraction contained 22% of the 36Cl associated with the edible portion. Seventy-three percent of the chlorine associated with the edible shrimp tissue existed as 36Cl−. Negligible amounts of chlorine were detected in the control fractions.
Article
To determine whether pediocin is produced and has effective antilisterial activity during food fermentation, six sausage fermentation trials were conducted with antibiotic-resistant, pediocin-producing (Bac+) Pediococcus acidilactici PAC 1.0 (Strr Rifr) and an isogenic pediocin-negative (Bac-) derivative used as a control. Meat was inoculated (ca. 10(5) CFU/g) with a composite of five Listeria monocytogenes strains, each electrotransformed with pGK12 (Cmr Emr). P. acidilactici and L. monocytogenes populations were selectively enumerated by plating on media with antibiotics. This study indicated that the dry sausage fermentation process can reduce L. monocytogenes populations. Effective inactivation of L. monocytogenes was observed when the pH at the end of the fermentation portion of the process was less than 4.9. Pediocin was responsible for part of the antilisterial activity during the fermentation in each of the six trials. Furthermore, inhibition of L. monocytogenes during drying was enhanced in the presence of pediocin in the three trials in which L. monocytogenes could be detected throughout the drying process. Thus, pediocin production contributed to an increase in safety during both the fermentation and drying portions of sausage manufacturing.