578

Journal of Food Protection, Vol. 66, No. 4, 2003, Pages 578–583

Copyright q, International Association for Food Protection

Determination of Thermal Lethality of Listeria monocytogenes in

Fully Cooked Chicken Breast Fillets and Strips during Postcook
In-Package Pasteurization
R. Y. MURPHY, 1* L. K. DUNCAN, 2 K. H. DRISCOLL, 1 B. L. BEARD, 1 M. B. BERRANG, 3 AND J. A. MARCY 4

1Department of Biological and Agricultural Engineering and 2 Department of Mathematical Sciences, University of Arkansas, Fayetteville,

Arkansas 72701; 3 U.S. Department of Agriculture, Agricultural Research Service, 934 College Station Road, Athens, Georgia 30605; and
4Center of Excellence in Poultry Science, University of Arkansas, Fayetteville, Arkansas 72701, USA

MS 02-263: Received 2 August 2002/Accepted 30 October 2002

ABSTRACT
Fully cooked chicken breast Ž llets and strips were surface inoculated with a cocktail of Listeria monocytogenes culture.
The inoculation level was 107 to 108 CFU/g meat. The inoculated products were vacuum packaged and pasteurized at 908C
with a pilot-scale steam or hot water cooker. After heat treatment, the survivors of L. monocytogenes were enumerated. No
signiŽ cant difference was found on survivors of L. monocytogenes between steam- and hot water–treated products. To achieve
a 7-log10 (CFU/g) reduction, approximately 5, 25, and 35 min were needed for single-packaged Ž llets, 227-g package strips,
and 454-g strips, respectively. The results from this study were subsequently veriŽ ed by a computer model that could predict
the thermal lethality of pathogens in fully cooked meat and poultry products during postcook in-package pasteurization.

Listeria monocytogenes is a well-documented food-
borne pathogen and has been associated with many product
recalls (12). Exposure of fully cooked meat or poultry after
cooking, but before packaging, could be a point of contam-
ination with L. monocytogenes (14). Isolation of L. mono-
cytogenes from  oors, drains, or stepping ladders in a poul-
try further processing plant has been reported (1). The pres-
ence of L. monocytogenes in processing environments ren-
ders meat or poultry products at risk for contamination after
cooking and before packaging. Therefore, contamination by
L. monocytogenes of fully cooked meat or poultry products
as a result of exposure to processing environments is a con-
cern.
Several studies have evaluated postcook pasteurization
to reduce or eradicate Listeria on fully cooked meat (2, 11)
or poultry products (6). Cygnarowicz-Provost et al. (2)
studied surface pasteurization of beef frankfurters and ob-
tained 4-log10 (CFU/ml) reductions of Listeria innocua on
the surface of the frankfurters after they had been treated
with 115 to 1368C steam for 30 to 40 s. Roering et al. (11)
found that L. monocytogenes was reduced about 3 log10
(CFU/g) in vacuum-packaged summer sausage after being
treated for 30, 60, or 90 s in a water bath at 99, 88, or
778C, respectively.
Continuous or batch pasteurization processes were
evaluated in a previous study by Murphy et al. (6) for their
effectiveness in reducing Salmonella Senftenberg and L. in-
nocua in commercially packaged chicken breast strips. The
reduction of Salmonella Senftenberg or L. innocua in the
product that was processed in a batch cooker was slower
* Author for correspondence. Tel: 479-575-2542; Fax: 479-575-2846;
E-mail: rymurph@uark.edu.
(18%) than that in a continuous cooker (6). Studies have
also compared steam with hot water pasteurization on mi-
crobial lethality and found that there was no signiŽ cant (at
a 5 0.05) difference on microbial lethality between steam
and hot water treatment (4).
The objective of this study was to determine the effec-
tiveness of in-package pasteurization on eliminating L.
monocytogenes from three types of vacuum-packaged fully
cooked chicken breast meat products (Ž llets or strips) that
were treated with a continuous pilot-scale steam or hot wa-
ter cooker. The results from this study were conŽ rmed by
a computer model (ThermoPro; contact: Dr. Rong Murphy,
Thermal Processing and Food Safety Program, 203 Engi-
neering Hall, University of Arkansas, Fayetteville, AR
72701) that could predict the thermal lethality of pathogens
in different locations of products. The model (ThermoPro)
was developed on the basis of previous studies by Murphy
and Berrang (4) and Murphy et al. (5–8).
MATERIALS AND METHODS
Product. Fully cooked chicken breast meat products were
used in this study. The products were obtained from a commercial
processor and kept at 2208C until use. The products were used
within 4 months.
Culture preparation. Five strains of L. monocytogenes were
obtained on slants from Dr. M. E. Berrang (1). From each slant,
a loopful of culture was transferred to 10 ml of tryptic soy broth
plus yeast extract (TSB1YE) in a test tube and then incubated
overnight at 358C as a stock culture. The test tubes were vortexed,
and 1 ml of each stock culture was transferred to a 250-ml Erlen-
meyer  ask containing 100 ml of sterile TSB1YE. Each culture
was individually incubated overnight at 358C on an orbit shaker
at 600 rpm. An equal volume of each culture (109 CFU/ml) was
J. Food Prot., Vol. 66, No. 4
FIGURE 1. Thermal proŽ les during heating for fully cooked and
vacuum-packaged chicken breast meat products. (a) Fillets and
(b) strips.
pipetted into a sterile  ask and mixed just before the inoculation
of the meat products.
Inoculation. Three types of packaged chicken breast meat
products were evaluated in this study. They included chicken
breast strips in 454- or 227-g packages or single-packagedchicken
breast Ž llets (120 g each, approximately 127 mm in diameter by
13 mm thick). The strips were obtained by slicing the chicken
breast Ž llets into 13-mm-wide strips. Each product (Ž llets or
strips) was surface inoculated with a cocktail of Ž ve L. monocy-
togenes cultures by dripping the culture at a ratio of 5 ml of
culture per 500 g of meat samples to cover the entire sample
surface and then mixed with sterile tongs for 4 min in a sterile
pan. The surface-inoculated Ž llets or strips were placed on a ster-
ile wire rack. The inoculated meat samples were kept at 48C for
30 min to allow bacterial attachment. In a preliminary study, it
was found that 20 min at 48C was sufŽ cient for the pathogen to
attach to fully cooked chicken breast meat tissues (unpublished
data). The inoculation level in each batch of meat samples was
enumerated to be 107 to 108 CFU/g meat. The inoculated products
were placed in 0.08-mm-thick plastic pouches (152 by 254 mm
for 454-g strips or 140 by 140 mm for 227-g strips or Ž llets) and
sealed under 1.0 bar vacuum (105 Pa).
Heat treatment. Each package was individually heat treated
at a temperature of 908C with a steam cooker (Model 102, Stein-
DSI FMC, Sandusky, Ohio) or a hot water cooker (Magni Whirl,
Blue M Electric Company, Blue Island, Ill.) for 0.5 to 40 min.
Six packages were processed at each trial as one experimental
unit. After thermal treatment, the products were immediately sub-
merged in an ice-water bath. During heating and cooling, the meat
temperatures were monitored every 1 s by a data acquisition sys-
tem (CR23X Micrologger, Campbell ScientiŽ c, Inc., Logan, Utah)
with Ž ve thermocouple probes (gauge 40, type K) that were sealed
LETHALITY OF LISTERIA IN CHICKEN PRODUCTS 579
FIGURE 2. Heating rate at the center and product-package in-
terface for fully cooked and vacuum-packaged chicken breast Ž l-
lets.
at different locations in a pouch. The thermal proŽ les were veri-
Ž ed by the computer model (ThermoPro).
Microbial enumeration. After the product was cooled to
,208C in an ice-water bath, the pouch was blotted with paper
towels and wiped with 75% ethanol, and a 25-mm slot was asep-
tically made. Fifty milliliters of sterile 0.1% peptone solution was
pipetted into the pouch and massaged by hand for 4 min. From
this point, serial dilutions were made in sterile 0.1% peptone so-
lution and spread plated in duplicate on thin-agar-layer overlay
plates that consisted of modiŽ ed Oxford medium overlaid with 5
ml of TSA1YE to resuscitate heat-injured cells (3). Preliminary
testing compared cell counts from heat-treated samples when
plates were incubated at 25 and 358C, respectively. Incubation
temperature made no substantial difference to the plate counts
from heat-treated samples (unpublished data). In this study, the
plates were incubated at 358C and counted every day for 4 days.
Data analysis. Three different packages of chicken breast
meat products (227-g strips, 454-g strips, and 120-g Ž llets) were
cooked by one of two treatment methods (steam or hot water) for
varying amounts of time. The products were inoculated with L.
monocytogenes before cooking. The amount of L. monocytogenes
remaining on the product was enumerated after cooking. The goal
of the analysis was to determine whether the survival of L. mon-
ocytogenes was different between steam- and hot water–treated
samples and to obtain a statistical model that would describe the
survivors of L. monocytogenes in each product.
Because the initial cell counts were large and the data sets
were overdispersed between initial counts and Ž nal counts, a neg-
ative binomial model was used to Ž t the data. Considering the
variations among the product shapes and sizes, each type of prod-
uct (Ž llets or strips) was analyzed separately. SigniŽ cant differ-
ences between the treatments (steam or hot water) were conducted
by type III statistical analysis. The analysis was also conducted
to determine whether the thermal lethality of L. monocytogenes
was signiŽ cantly different between 227- and 454-g package strips.
Statistical analysis was performed using SAS version 8.1 (copy-
right 1999–2000, SAS Institute, Inc., Cary, N.C.).
RESULTS AND DISCUSSION
Thermal proŽ le and heating rate. Figure 1 shows the
thermal proŽ les for fully cooked and vacuum-packaged
chicken breast Ž llets and strips during heat treatment. The
temperature at the interface between product and packaging
Ž lm increased much faster than the temperature inside the
product. The center temperature of the chicken breast Ž llets
reached 708C in about 5 min. For the strips, the temperature
580 MURPHY ET AL. J. Food Prot., Vol. 66, No. 4

TABLE 1. Type III statistical analysis for the effect of heating
time (minutes) on different packages of fully cooked chicken
breast meat products during postcook in-package pasteurization
Product Source x2 P . x2
Fillets Time 17.16 ,0.0001
Time2 76.23 ,0.0001
227-g packaged strips Time 4.86 0.0275
Time2 86.53 ,0.0001
454-g packaged strips Time 65.02 ,0.0001
Time2 122.60 ,0.0001
at the package center reached 708C in about 25 and 35 min
for 227- and 454-g packaged strips, respectively. Strips be-
came heated much slower than Ž llets because of the greater
thickness of the packaged products. The thickness of the
Ž llet packages was about 13 mm. The thickness of the strip
packages was 35 and 44 mm for 227- and 454-g packages,
respectively.
Figure 2 illustrates the heating rate (temperature
change with a unit time change, dT/dt) for fully cooked
chicken breast Ž llets at the product-Ž lm interface and the
package center. The heating rate varied with location and
time. At the interface between packaging Ž lm and product,
the heating rate was highest at the beginning of the heat
treatment; then, it gradually decreased until reaching zero
(steady-state). At the center of the Ž llet, the heating rate
gradually increased to the maximum (23.48C/min) and then
decreased. Similar proŽ les of heating rates were also ob-
tained for vacuum-packaged chicken breast strips, except
the maximum heating rate at the package center was 4.2
and 38C/min, respectively, for 227- and 454-g packages,
which was 82 or 87% slower than that of Ž llets (data not
shown). This result was apparently because single-pack-
aged Ž llets (13 mm thick) were thinner than multipackaged
strips (35 or 44 mm thick).
Treatments. In this study, there were no signiŽ cant (at
a 5 0.05) differences in the thermal lethality of L. mono-
cytogenes between steam- and hot water–treated products.
This result was consistent with a previous Ž nding by Mur-
phy and Berrang (4) for Salmonella and L. innocua in fully
cooked and vacuum-packaged chicken breast strips. Since
steam and hot water treatments were not signiŽ cantly dif-
ferent in this study, the results from steam and hot water
treatments were pooled together. Because of the geometrical
differences between Ž llets and strips, further data analysis
was performed separately for Ž llets and strips. The Ž nal
statistical model for the survival of L. monocytogenes in
fully cooked and vacuum-packaged chicken breast strips
was expressed, by a quadratic model, as ln(N/N0) 5 a 1 b
(time) 1 c (time)2, where a, b, and c were the parameters
for constant, linear, and quadratic terms, respectively, and
time was in minutes.
The results in Table 1 indicate that the heating time
signiŽ cantly (at a 5 0.05) affected survivors of L. mono-
cytogenes for all three types (Ž llets and strips) of chicken
breast meat products during postcook in-package pasteuri-
zation. The deviance/df values were 1.2745, 1.2149, and
1.2089 for the Ž llets, 227-g packaged strips, and 454-g
packaged strips, respectively. These values indicate that the
models Ž tted the data well. The perfect Ž t would have a
deviance/df value equal to 1.
Fillets. The parameter estimates for the model are giv-
en in Table 2. The log10 (CFU/g) reduction of L. monocy-
togenes is plotted in Figure 3 along with the 95% conŽ -
dence limits (broken lines) and experimental values (sym-
bols). In Figure 3, a stochastic model underestimated the
log10 reduction of L. monocytogenes in chicken breast Ž l-
lets, which meant that the model would give a more con-
servative prediction. After pasteurizing for about 5 min, L.
monocytogenes was reduced by 7 log10 (CFU/g). Because
the product was surface inoculated and the culture may mi-
grate from the surface inward to some degree, the survivors
of L. monocytogenes in the Ž llets could vary with the depth
from the product surface to center. However, since the enu-
meration of L. monocytogenes in different depths of the
Ž llet was experimentally impossible, a computer model (8)
was used to predict the thermal lethality of L. monocyto-
genes at different depths of the Ž llet.
In the model, the thermophysical and heat transfer pa-
rameters from Murphy et al. (8), Murphy and Marks (9),
and Murphy et al. (10) were used. With these parameters,

TABLE 2. Parameter estimates for the model ln(N/N0) 5 a 1 b (time) 1 c (time)2 of Listeria monocytogenes in fully cooked chicken
breast meat products during postcook in-package pasteurization (time is in minutes)
95% conŽ dence limits

Product Parameter Estimate Standard error Lower Upper x2 P . x2

Fillets a 20.4484 0.2559 20.9500 0.0533 3.07 0.0798

b 1.3550 0.2948 0.7772 1.9329 21.12 ,0.0001
c 21.0988 0.0775 21.2507 20.9469 201.03 ,0.0001
227-g packaged strips a 0.0331 0.2235 20.4049 0.4710 0.02 0.8823
b 20.1134 0.0488 20.2090 20.0179 5.41 0.0200
c 20.0208 0.0019 20.0246 20.0169 113.52 ,0.0001
454-g packaged strips a 20.1919 0.2123 20.6079 0.2242 0.82 0.3660
b 0.2514 0.0313 0.1900 0.3127 64.38 ,0.0001
c 20.0210 0.0010 20.0229 20.0190 446.82 ,0.0001
J. Food Prot., Vol. 66, No. 4
the continuity equations that led to the following governing
equations for coupled heat and mass transfer was used (13):
rC p ]T/]t 5 ¹(k¹T) 1 rL]M/]t (1)
]M/]t 5 ¹(D¹M) (2)
in which r was the density in kilograms per cubic meter,
Cp was the speciŽ c heat in joules per kilogram per kelvin,
T was the temperature of product in kelvin, t was the time
in seconds, k was the thermal conductivity in watts per
meter per kelvin, L was the latent heat in joules per kilo-
gram, M was the moisture content in kilograms of moisture
per kilograms of product mass, and D was the mass dif-
fusivity in kilograms per second.
The boundary of the evaluated system might be subject
to heat loss due to evaporation. Therefore, the following
boundary equations were used in describing the process:
k¹T · n 5 h(T a 2 Ts ) 1 DrL¹M· n (3)
rD¹M· n 5 k m (M s 2 M a ) (4)
in which n was a unit vector that is normal to the product
surface in an outward direction, h was the convection heat
transfer coefŽ cient in watts per square meter per kelvin, Ta
was the environmental (steam or hot water) temperature in
kelvin, Ts was the surface temperature in kelvin, km was
the mass transfer coefŽ cient in kilograms per square meter
per second, Ms was the surface moisture content in kilo-
grams of moisture per kilograms of product mass, and Ma
FIGURE 4. Relationship between heating time and product depth
for a 7-log10 (CFU/g) reduction.
LETHALITY OF LISTERIA IN CHICKEN PRODUCTS 581
FIGURE 3. Log10(N0 /N) for L. monocy-
togenes in fully cooked and vacuum-pack-
aged chicken breast Ž llets. The lines are
the Ž tted model with 95% conŽ dence in-
tervals. The symbols are the experimental
values.
was the moisture content of air in kilograms of moisture
per kilograms of air.
Using equations 1 to 4, the time-temperature relation-
ship was obtained and compared with those obtained ex-
perimentally. The veriŽ ed time-temperature relationship
was used to predict the log10 (CFU/g) reduction at different
depths of the product, by ($10(T 2 70)/z dt)/D70, where T was
the temperature at time t, D70 (0.13 min) was the decimal
reduction time at a reference temperature of 708C, and z
(5.728C) was the temperature difference required for the
thermal inactivation curve to drop a logarithmic cycle (5).
The relationship between the product depth and the pas-
teurization time for achieving a 7-log10 (CFU/g) reduction
is shown in Figure 4. Combining the analysis from the sta-
tistical model with that of the computer model prediction,
after 5 min of the pasteurization, about 3.5 mm of the depth
from the product surface toward the center should have
achieved 107 CFU/g of the reduction.
Strips. The parameter estimates for the statistical mod-
els are given in Table 2. Figure 5 shows the log10 (CFU/g)
reduction of L. monocytogenes from the Ž tted models
(lines) and experimental data (symbols) for 227- and 454-g
packaged strips. Stochastic models underestimated the log10
reduction of L. monocytogenes in the packaged chicken
breast strips, indicating that the predictions by the models
from this study would be conservative (Figure 5). In a pre-
vious study, Murphy and Berrang (4) found that product
size interacted with heating time and subsequently affected
the thermal lethality of Salmonella and L. innocua in fully
cooked and vacuum-packaged chicken breast strips. Similar
results were found in this study. The type III statistical anal-
ysis showed that the product size interacted with the heating
time. The P value was 0.0006 for the interaction term (time
3 product), indicating that the effect of product size on
survivors of L. monocytogenes was signiŽ cant at the 95%
level. The speciŽ c time when the number of surviving L.
monocytogenes in the two packaged (227 and 454 g) strips
was signiŽ cantly different was determined by contrast anal-
ysis (Table 3). At a 5 0.05, the survivors of L. monocy-
togenes in the two packaged (227 and 454 g) strips started
to be signiŽ cantly different at a heat treatment time of 6
min (P 5 0.0339).
582 MURPHY ET AL. J. Food Prot., Vol. 66, No. 4

FIGURE 5. Log10(N0 /N) for L. monocy-

togenes in fully cooked and vacuum-pack-
aged chicken breast strips. The lines are
the Ž tted models with 95% conŽ dence lev-
els, and the symbols are experimental val-
ues. (a) 227-g packages and (b) 454-g
packages.

A process lethality model as detailed by Murphy et al. perimentally obtained data from this study. Therefore, if the
(5) was also used to predict the log10 (CFU/g) reduction in correct parameters are used, the process lethality model can
fully cooked and vacuum-packaged chicken breast strips. be used to predict the thermal lethality of the pathogen up
The process lethality, $10(T 2 T(ref))/z dt, was deŽ ned as the to 7 log10 in fully cooked and vacuum-packaged chicken
time required to produce the same degree of the pathogen breast strips during postcook pasteurization.
reduction at a reference temperature T(ref) at the given pro-
CONCLUSIONS
cess under the time (t) and temperature (T) history. As
shown in Figure 6, the prediction by the process lethality This study indicated that both steam and hot water pas-
model indicated that approximately 25 min (for 227-g pack- teurization were effective for the thermal inactivation of L.
ages) or 35 min (for 454-g packages) were needed to
achieve a 7-log10 (CFU/g) reduction of L. monocytogenes
in fully cooked chicken breast strips with steam or hot wa-
ter pasteurization. This prediction was consistent with ex-

TABLE 3. Results of the contrast analysis to compare survivors

of Listeria monocytogenes between 227-g and 454-g packaged
chicken breast strips
Time (min) x2 P . x2

5 0.86 0.3526
6 4.50 0.0339
FIGURE 6. Predicted log10 (CFU/g) reduction from the process
7 13.17 0.0003
lethality model for L. monocytogenes in fully cooked and vacuum-
10 61.18 ,0.0001
packaged chicken breast strips.
J. Food Prot., Vol. 66, No. 4
monocytogenes in fully cooked and vacuum-packaged
chicken breast meat products. The heat penetration rate was
affected by the thickness of the product. The thicker the
product was, the slower the heating rate. The process le-
thality model is an effective tool in determining up to 7
log10 (CFU/g) of thermal lethality for L. monocytogenes in
fully cooked chicken breast meat products during in-pack-
age pasteurization.
ACKNOWLEDGMENTS
This research was partially supported by grants from USDA-NRI,
USDA-CSREES, and USDA-ARS NAFS. The authors thank Tyson Foods,
Inc., Springdale, Ark., for products and G. Dwyer, E. Johnson, and K.
Story for their assistance.
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