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Journal of Food Protection, Vol. 69, No. 7, 2006, Pages 1611-16/S

Antimicrobial Activity of Potassium Hydroxide and Lauric Acid

against Microorganisms Associated with Poultry Processingt
ARTHUR HINTON, JR.' ANI) KIMBERLY D. INGRAM

6 Cente,,
poultry Processing Unit, Agricultural Research Service, U.S. Department of Agriculture, 950 College Station Road, Russell Research
Athens, Georgia 30605, USA

MS 05-623: Received 15 December 2005/Accepted 21 February 2006

ABSTRACT

The antimicrobial activity of solutions of potassium hydroxide (KOFI) and mixtures of KOH and laurie acid against
microorganisms associated with poultry processing was determined. In vitro tests were performed by enumerating viable
microorganisms recovered from bacterial cultures suspended in peptone water (control) and in solutions of 0.1% KOH or
mixtures of 0.1% KOH and 0.25 or 0.501/c laurie acid. Additional studies were conducted to identify changes in the native
microbial flora of poultry skin washed in distilled water. KOH. or KOH—lauric acid. Although results of in vitro studies
indicated that significantly fewer bacteria (P -^ 0.05) were recovered from cultures suspended in KOl-! than from cultures
suspended in peptone water, there were also significantly fewer bacteria recovered from cultures suspended in KOH—lauric
acid than from cultures suspended in KOH. Results of experiments with broiler skin indicated that although rinsates of skin
washed in 1.0% KO1-I solutions contained significantly fewer total aerobic bacteria and enterococci than did skin washed in
water, significantly fewer of these microorganisms were generally recovered from rinsates of skin washed in mixtures of 1.0%
KOH and 0.5. 1.0. 1.5, or 2.0% laurie acid than from skin washed in KOH alone. Washing of broiler skin in solutions of 0.25
to 1.00% KOH or mixtures containing these concentrations of KOH and two parts lauric acid (wtivol) also significantly
reduced the populations of bacteria and yeasts in the native flora of broiler skin. Enterococci, lactic acid bacteria, and staph-
ylococci in the native flora of the skin had the highest level of resistance to the bactericidal activity of KOH—lauric acid. These
findings indicate that the antimicrobial activity of KOH—lauric acid is significantly greater than that of KOH alone in vitro
and on poultry skin. Thus. KOH—lauric acid may he useful for reducing the level of microbial contamination associated with
poultry processing.

Processed poultry products may be contaminated with
pathogenic microorganisms that cause human foodborne
diseases and with spoilage microorganisms that reduce the
shelf life of poultry products (3). Canip.vlohacter and Sal-
monella are currently recognized as the major bacterial
pathogens associated with poultry (4, 25), but poultry prod-
ucts contaminated with Lisleria m000cvrogene s (7). Staph-
vlococcu.c aureus, and Clostridium perfringens (25) also
cause a significant number of cases of human foodhorne
diseases. Spoilage microorganisms such as Pseudomona,s
spp., BrochotrLv therrnosphacta, and yeasts (3, ii) and fe-
cal indicator bacteria such as Escherichia co/i (6) also may
represent a significant portion of the microbial flora of pro-
cessed poultry.
Several chemicals are currently used as sanitizers to
reduce microbial contamination in poultry processing op-
erations (4). Chlorine is the most widely used sanitizer in
commercial poultry-processing facilities because it is in-
expensive and relatively effective against microorganisms
found in poultry-processing environments (19. 26). The use
of the alkaline sanitizer trisodium phosphate also has been
* Author for correspondence. Tel: 706-546-3621; Fax: 706-546-3633:
E-mail: ahinton@saa.ars.usda.gov.
t Mention of a trade name, proprietary product, or specific equipment
does not constitute a guarantee or warranty by the U.S. Department of
Agriculture and does not imply its approval to the exclusion of other
products that may he suitable.
approved by the U.S. Department of Agriculture for the
reduction of Salmonella contamination of poultry carcasses
during commercial processing operations (9). Despite the
use of these and other available sanitizers, microbial con-
tamination of processed poultry continues to he a signifi-
cant food safety issue. and research on technology to extend
the shelf life of fresh poultry continues.
Previous research has indicated that the antimicrobial
activity of mixtures of potassium triphosphate and fatty ac-
ids can reduce populations of microorganisms in vitro and
on skin of processed broiler carcasses (12-14). Fatty acids
are naturally occurring microbicides that have little or no
human toxicity (15). The potassium and sodium salts of
fatty acids (soaps). which are formed by adding potassium
hydroxide (KOH) or sodium hydroxide to fats, also possess
antimicrobial activity (1). These compounds have a long
history of safe use as cleansers and food preservatives (15.
16). The purpose of the present study was to examine the
antimicrobial activity of KOH and mixtures of KOH and
laurie acid in vitro and on poultry skin.
MATERIALS AND METHODS
Antimicrobial solutions. Solutions containing various con-
centrations of KOH (Sigma Chemical Co.. St. Louis, Mo.) or mix-
tures of KOl-I and laurie acid (Sigma) were prepared. KOH so-
lutions were made by dissolving KOH pellets in distilled water
(wtivol), and mixtures of KOH and laurie acid were prepared by
 612 HINTON AND INGRAM
TABLE l. Microorganisms recovered q
,fter culture in peptone water, KOH solution, or KOH—laurjc acid So/ulionsa
Microorganisms recovered (log CFU/ml) -
Acinetohacier Aero,nonas Brochotrix Camp
Solution calcoacc',(cus sohpja the rniocpha eta
Peptone water 5.63 ± 0.19c 5.73 ± 0.09c
5.73 ± 0.19c 6.35 ± 0.04B 5.93 ± 0.14B
0.10% KOH 2.93 ± 0.06 B 3,44 ± 0-10B 5.22 ± 0.05 u
3.09 ± 0.04 B 1.63 ± 0.35 A NRA 1.56 ± 0.24
0.10% KOH +
0.025% lauric acid NR A NR A NR A
0.10% KOH +
0.05% laurie acid NR A NR A NR
A NR A NR A
a Values are means ± standard deviations.
n = 3. NR,
(P 0.05). none recovered. Within columns, different letters indicate significant differences
dissolving lauric acid in KOH solutions. All solutions were filter
sterilized by passage through 0.2-p.m-pore-site filters (Nalge
Nunc International, Rochester, N.Y.). The final pH of the solutions
was measured with an electronic pH meter (Corning Inc., Corning,
N. Y.).
Microbial isolates. The antimicrobial activity of KOH and
KOH—lauric acid solutions in vitro was determined by enumer-
ating viable microorganisms recovered from microbial suspen-
sions mixed in the solutions. Previously identified microbial iso-
lates that had been recovered from rinsates of commercially pro-
cessed broiler carcass skin (13) were used in the present study. A
B. thermosphacta isolate was recovered from rinsale.s of broiler
carcass skin plated on streptomycin sulfate thallous acetate acti-
dionc agar (2) and incubated at 20°C for 3 days.. A C. perfringens
isolate was recovered from skin rinsates plated on Perfringens
agar base with egg emulsion and tryptose sulfite cycloserine se-
lective supplement (Oxoid Ltd.. Basingstoke, Hampshire, UK) and
incubated anaerobically in an anaerobic chamber (Coy Laboratory
Products inc., Grass Lake, Mich.) at 35°C for 18 to 24 h. B.
the rmosphacta and C. peifringens isolates were identified with the
MIDI Sherlock Microbial Identification System, as previously de-
scribed (11, 24). Fresh cultures of Acinetobacter ca/coaceticus,
Aeromonas .cobr,a, B. thenno.cphacta Entero/,acier cloacae, En-
terococcus faeca/is, E. co/i P01 , L. ?nonocvtoçenes Salmonella
Enteritidj s, Salmonella Typh im un urn, S. aureus, Staph viococcus
chromogenes KP06. and Pseudomonas aeruginosa were grown
aerobically in tryptic soy broth (Difco, Becton Dickinson, Sparks.
Md.) for 18 to 24 h at 35°C. Cultures of C. perfringens were
grown anaerobically in reinforced clostridia medium broth (Difco,
Becton Dickinson) for 18 to 24 h at 35°C. Campv/obacterjejuni
cultures were grown on Remel blood agar (Remel Inc., Lenexa,
Kans.) for 48 h at 42°C under microaerophilic conditions in a
GasPak jar (BBL, Becton Dickinson) with an activated CampyPak
Plus Hydrogen + CO2 with Integral Palladium Catal y st (Becton
Dickinson). All microbial cultures were harvested and suspended
in a solution of 0.1% Bacto Peptone water (Difco, Becton Dick-
inson) as previously described (13).
In vitro antimicrobial tests. In vitro trials were conducted
by adding 0.1 ml of each microbial isolate culture to separate
tubes containing 10 ml of peptone water (control), 0.1% KOH
solution, or mixtures of 0.1% KOH and 0.025 or 0.050% laurie
acid to produce a final microbial concentration of approximately
106 CFU/ml. Test tubes containing the suspensions were placed
on a laboratory rotator (Glas-Col, Terre Haute, hid.) and mixed
for S mm. Aliquots of the microbial suspensions were then re-
moved and mixed with an equal volume of Butterfield's phos-
J. 100(1 Piot.. Vol. 69, NO 7
yfobacter Clostridjwn Enterobacrer
jejuni pefringens cloacae
A
NR A NR A NR A
NR A
phate-buffered dilution water (28) to neutralize the alkalinity of
the KOH or KOH—lauric acid solutions. Microorganisms in the
suspensions were then enumerated by plating on the appropriate
agar medium with an Autoplate 4000 automated spiral plater (Spi-
ral Biotech, Bethesda. Md.). Cultures of E. cloacae, E. fliecalis,
E. coil, L. monocvlogenes, Salmonella Enteritidis, Salmonella Ty-
phirnurium, S. aureus, S. chromogenes, and P. aerugino.s'a
were
plated onto plate count agar (PCA: Difco, Becton Dickinson) and
incubated aerobically at 35°C for 24 to 48 h. Cultures of C. jejuni
were plated on Remel blood agar and incubated rnieroaerobically
at 42°C for 48 h. Cultures of C. pefringens were plated on re-
inforced clostridia agar (Difeo, Becton Dickinson) and incubated
anaerobically at 35°C for 18 to 24 h. After incubation, the con-
centration of each isolate recovered from the peptone water, KOH,
or KOH—lauric acid suspensions was determined. Each experiment
was repeated three times.
Determinatioji of the effect of KOH and KOH—laurie acid
on the microbial flora of poultry skin. Broiler carcasses were
taken from the processing line of a local commercial poultry pro-
cessing plant immediately after feathers had been removed by a
mechanical picker. These carcasses were placed on crushed ice
and transported to the laboratory, where the carcass skin was man-
ually removed. The skin was cut into 50-g pieces, placed in sterile
stomacher bags (Seward Ltd., London. UK). and stored at 4°C
until used. All skin samples were used within 5 da y s after being
removed from the carcasses.
Differences in the number of total aerohcs and enterococci
recovered from broiler skin washed in mixtures containing KOH
and various concentrations of laurie acid was determined. Skin
samples were washed in 100 ml of sterile distilled water (control).
1.0% KOH solution, or mixtures of 1.0% KOI-1 and 0.5, 1.0, 1.5.
or 2.0% laurie acid in a Stomacher 400 (Seward) on high speed
for 1 mm. The washed skin was then transferred to a sterile stom-
acher bag containing 100 ml of fresh Butterfield's phosphate-buff-
ered dilution water and stomached for I nun on high speed. Al-
iquots of the buffer rinsates were removed for immediate micro-
bial analyses. An automated spiral plater was used to plate the
rinsates on the skin samples on agar media. Rinsates were plated
on PCA and incubated at 35°C for 24 It to enumerate total aerobic
bacterial flora and on enterococci agar (Difco. Becton Dickinson)
incubated at 35°C for 48 h to enumerate enterococci
Differences in the microflora of broiler skin washed in so-
lutions containing various concentrations of KOI-I or mixtures of
KOH with two parts laurie acid (wtivol) were also determined.
Skin samples were washed in distilled water (control), in solutions
of 0.25. 0.50. 0.75, or 1 fific/ K011. or in nH\tUrcs oil) :; KOH

"u. 7
J FOU'- 'i-oi.. \'ol. 69.
TABLE 1. Extended
- Microorganisms recovered (log CFU/ml)
I'seudonionas So/inane/la Solnione//o
EnterOCOcclL Escherichia Listeria aureus KPOÔ
,nonocviogenes aeruginoso Enterilidis Typhimurium
faeca/is - co/i P0!
± 0.19 c 5.70 ± 0.09 c 6.38 ± 0.06 c 6.59 ± 0.04 B
5.66 ± 0.17 c 5.97 ± 0.04 c 6.82
5.01 ± 0.11 it 2.12 ± 0.20 B 2.48 ± 0.11 B 1.56 ± 0.24
.33 ± 0.61 B 3.60 ± 0.09 B
A NR NRA
1.39 ± 0.18 A 1.45 ± 0.28
NR NR NR NRA
and 0.50% lauric acid. 0.50% KOH and 1.00% laurie acid, 0.75%
KOH and 1.50% lauric acid, or 1.00% KOH and 2.00% laurie
acid. Except for the E. co/i, selected populations of the microbial
flora of the skin rinsates were enumerated by plating the rinsates
on the appropriate microbial media with an automated spiral plat-
er. Total plate counts were determined on PCA incubated at 35°C
for 24 h. Campy/oboe/er counts were determined on Oxoid blood
agar base supplemented with 7.0% lysed horse blood (Lampire
Biological Laboratories, Pipersvillc, Pa.) and Oxoid campvlobac-
icr selective supplement (Blaser-Wang) incubated at 42°C for 48
h. Enterococci counts were determined on enterococci agar incu-
bated at 35°C for 48 li. Lactic acid bacteria counts were deter-
mined on lactic acid bacteria agar (2) incubated anaerobically at
35°C for 48 h. Psychrolrophic bacteria counts were determined on
PCA incubated at 4°C for It) days. Staphylococci counts were
determined on Bacto Baird-Parker agar base (Difco. Becton Dick-
inson) supplemented with egg yolk tellurite enrichment agar
(BBL. Becton Dickinson) incubated at 35°C for 48 h. Yeast counts
were determined on acidified Sabouraud dextrose agar (Difco,
Becton Dickinson) incubated at 28°C for 3 days. E. co/i coLints
were determined on coljform/E. co/i Petrifllm (3M Co., St. Paul.
Minn.) incubated at 35°C for 24 to 48 h. Morphologically distinct
colonies were removed from Baird-Parker agai enterococci agar
PCA, and lactic acid bacteria agar.
Additional studies were conducted to confirm the identity of
staphylococci, enterococci. and lactic acid bacteria that exhibited
the highest resistance to the antimicrobial activity of KOH- laurie
acid mixtures on broiler skin. Skin samples were washed in a
mixture of 1.0% KOH and 0.5% laurie acid, and skin rinsates
were plated on PCA. Baird-Parker agar, enterococci agar. and lac-
TABLE 2. Mean ph of solutions of KOhl and KOH-Iauric a ul
Solution composition (4. wi/volt
KOH 1,auric acid pH
0.10 0.0 12.22 ± 0.15 AB
0.25 0.0 12.48 ± 0.23 ABC
0.50 0.0 12.83 ± 0.21 BC
0.75 0.0 13.05 ± 0.24 c
1.00 0.0 13.19 ± 0.17 c
0.10 0.025 12.15 ± 0.07 A
0.10 0.05 12.04 ± 0.15 A
12.12 ± 0.39 A
0.25 0.5
0.50 1.00 12.27 ± 0.30 An
0.75 1.50 12.48 ± 0.24 ABC
Values are means ± standard deviations. n = 3. Different letters
indicate significant differences (P ::-^ 0.05).
1613
ANTIMICROBIAL ACTIVITY OF K011 ,.\r\1) I AIJRIC ACID
Staphylococcus
stelplivlococcus cli roinogenes
5.22 ± 0.05 n 5.22 ± 0.05 c
1.56 ± 0.24 A 3.97 ± 0.08 B
A
NRA NR NRA
NRA NR NRA NR
tic acid bacteria agar and incubated as described. Isolates from
each medium were identified with the MIDI Sherlock Microbial
Identification System.
Statistical analysis. All statistical analyses were performed
with the GraphPad StatMate and GraphPad InStat version 4.00 for
Windows 95 (GraphPad Software, San Diego. Calif.). One-way
analysis of variance (ANOVA) with Tukey-Kramer multiple com-
parison tests was performed to determine among group means.
Differences were considered significant at P 5 0.05.
RESULTS AND DISCUSSION
Results of in vitro studies indicated that solutions of
KOH and solutions of KOH-lauric acid possess antimicro-
bial activity against several microor g anisms associated with
processed poultry (Table I). Significantly fewer gram-neg-
ative and gram-positive bacteria were recovered from cul-
tures suspended in KOH than from cultures suspended in
peptone water. However, mixtures of KOH and laurie acid
were more bactericidal than were solutions of KOH alone.
The only viable cells recovered from mixtures of 0.10%
KOH and 0.025% laurie acid were from cultures of the
gram-positive coccus E. faeca/is and the gram-negative rod
E. co/i. However, no viable cells were recovered from any
cultures suspended in mixtures of 0.10% KOH and 0.050%
laurie acid. Although alkaline sanitizers such as tripotas-
sium phosphate (13) and trisodium phosphate (5, 20) may
significantly reduce populations of gram-negative bacteria,
these sanitizers are generally more effective for killing
gram-positive bacteria and yeasts (13). The mechanism of
the antimicrobial activity of alkaline sanitlzcrs is not
known, but this activity may he related to the high pH of
these compounds (5). The pH values of solutions of KOH
and KOH-lauric acid are greater than 12.0 (Table 2), and
bactericidal solutions of 4.0% potassium triphosphate have
a pH of 12.4 (14). However, fatty acids are known to kill
microorganisms because of their surfactant activity and
their ability to cause cellular lysis by disrupting cell mem-
branes (10, 17, 27). The antimicrobial activity of fatty acids
is generally more effective against gram-positive bacteria
and yeasts (18, 29) than against gram-negative bacteria (21,
23) because the protective lipopolysaccharide layer of
gram-negative bacteria serves as a barrier to penetration by
fatty acids (22. 23). The ability of KOH-lauric acid solu-
tions to kill gram-positive and grani-negative bacteria and


614 H1Nl(\ \\l) I.\rR \\
PH)L. (YJ •

TABLE 3. Bacteria recovered on plate count agar and entero-

cocci agarfroin rinsates of poultry skin washed in distilled water, N\ C - C
- t C ri -
KOH, or KOH-/auric acida
+1 +1 +1 +1 + +1 +1
Bacteria recovered (log CFU/mI)
M ' t (N

Rinse solution Plate count agar Enterococci agar

Distilled water 0
4.24 ± 0.190 3.03 ± 0.44c
1.0% KOH 3.55 ± 0.14c 1.98 ± 0.41 B
U
1.0% KOH + 0.5% lauric acid 2.94 ± 0.29 n 1.54 ± 0.48 AB CCCCCCCCC
1.0% KOFI + 1.0% lauric acid 2.29 ± 0.54 A NR A +1 +r +1 + + +1 +i +1 +
1.0% KOH + 1.5% lauric acid 2.51 0.36
± AB NR cn OC Q C L1 (NC - -

1.0% KOH + 2.0% lauric acid 2.19 ± 0.33 A NR A ( c r' (N c' (N

° Values are means ± standard deviations, n = 6. NR, none re-

r--r'
covered. Within columns, different letters indicate significant
differences (P S 0.05).
a +I++ C
r'.'(N z z z z
'a
yeasts in vitro is probably due to the combined microbicidal
activity of both compounds.
§2
Ha. U
so L) a a Li a a 5)
I-
KOM solutions and KOH-laurjc acid solutions also ex- 'a
I N r" c "i C C
hibited antimicrobial activity against the native microflora a (N (N r. 't C i N O

of processed broiler skin. Significantly fewer total bacteria a

a . +1 + +1 +1 + I + I +1 +1 + a
0 U
and enterococci were recovered from rinsates of skin (a
a
washed in KOH solutions than from those of skin washed I.. t a 't r rI_:I ', (N (N

in distilled water, and significantly fewer bacteria were re- 5)

LULi LIa a
covered from skin washed in KOH-lauric acid than from a
U
-a
'1 r C (N 'l
skin washed in distilled water or KOH (Table 3). As the a c' N N r' N -
r C
a

concentration of lauric acid in the KOH-laurjc acid solu- SZ

U
+i + +1 +1 +i -t-r +1 +1
tions used to wash the skin was increased, the population 5)
(N (N .0
of total bacteria and enterococci recovered from the skin (N (N (N (N (N (N - a
5)
rinsates generally decreased. Washing broiler skin in KOH .5)

or KOH-lauric acid solutions also reduced the population I a

-a

of several other types of microorganisms in the native mi- U

croflora ofpoultry skin (Table 4). Although washing skin LXj ZZZZZZ a
C
in KOH alone generally reduced the population of Cain- U

pvlohacter, E. co/i, enterococci, lactic acid bacteria, pseu- a

'a
domonads, staphylococci, and yeasts recovered from skin
(NC-
rinsates, significantly fewer of these microorganisms were v-:c
. CCC<<C<<<
recovered from skin washed in solutions of KOH-laurjc - +! +1 +i V
>
acid. The gram-positive enterococci, lactic acid bacteria, . (.00ZZ_ZzZ
N'(N 5)
and staphylococci exhibited the highest degree of resistance L) rn-- -

a
to the antibacterial activity of these solutions. The micro- C

bicidal activity of KOH-lauric acid may have been reduced i

by proteins and fats in the skin; therefore, more concen- -
-
'r') - (N
N 'r a z

trated solutions were required to reduce microbial popula-

L
tions on chicken skin than in vitro. The identities of some F-
rq 00 z IC
of the gram-positive rods and cocci that were recovered ( r'i e' (N (N (N a
from skin washed in 1.0% KOH and in 0.05% lauric acid

'I
a
are listed in Table 5. >
a 5)
Fatty acids and their salts (15) are generally recognized 'a
a a 9
'a

as safe (GRAS) substances that have a long history of use a

'a
in food products, and KOH also is a GRAS substance. The a a
a a a •c a

aH
use of chlorine as a disinfectant during poultry processing Z3 .2
+1
CaCc
is currently under scrutiny because toxic chiororganic com- - Cv

pounds may be formed when chlorine comes in contact 5)

. I- (N a
5)
.5 p
with proteins and fats during processing (8). .Additionally,
there is an increasing concern about the environmental im- LT1
CCOOCoO a

5)
pact of the high levels of phosphate contained in waste-
C V C ' C
water from processing facilities that use trisodium phos- (N N (N N C >
 \N'Fl\ll('ROIlI \I \('I l\
I'm: N'), \, 7
Bacterial isolates recovered on plate count agar. Baird-Parker agar, enlerococci agar, and lactic acid bacteria agar from
TABLE 5.
broiler chicken skin rinsed in a mixture of I,O'/r KOH and 0.57r lauric acid'
Enterococci agar Lactic acid bacteria agar
Plate count agar Baird-Parker agar
Bacillus ,narinus Corvnehacteriu,n amvcolatum Enterococcus ai'ium
E. faecium GC subgroup A L. salivarius-,salisariiLs
MicrOcoCCUc lutei1s GC sub- Staph ylococcus sitnulans
S. xlosus E. faecium GC subgroup B Streptococcus
group C
Morare11a os/eon
S. aureus GC subgroup C
S. chrotflogei('
S. cohni-cohti
S. saprophyticus
'Identification performed with the MIDI Sherlock Microbial Identification System.
phate as a sanitizer. The safety and effectiveness of sanitiz-
ers that contain fatty acids and their salts indicate that these
products deserve further study to determine whether they
may be used as practical alternatives to sanitiLers currently
in use in poultry processing operations.
ACKNOWLEDGMENTS
The authors acknowledge the technical assistance of Jerrie Barnett
and Fredda G. Murray.
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