JFS:

Food Microbiology and Safety

Thermal Inactivation Kinetics of

Salmonella and Listeria in Ground
Chicken Breast Meat and Liquid Medium
R.Y. MURPHY, B.P. MARKS, E.R. JOHNSON, AND M.G. JOHNSON

ABSTRACT: Thermal inactivation of Listeria innocua and 6 Salmonella serotypes in ground chicken breast meat
was compared to that in peptone (0.1%) - agar (0.1%) solution. Inoculated samples were packed in a thin-wall metal
tube and submerged in a water bath at temperatures ranging from 55.0 to 70.0 C. For Salmonella and Listeria, the
D values in ground chicken breast meat at 55 to 70 C were higher (p 0.0001) than those in peptone-agar solution;
however, the z values were not significantly different. Complete first-order inactivation models, with Arrhenius
temperature dependency, were developed for each inoculum and medium.
Key Words: bacteria, poultry, cooking, lethality, modeling

Introduction

HE U.S. D EPARTMENT OF A GRICULTURE F OOD S AFETY AND

FoodMicrobiologyandSafety

Inspection Service (USDA-FSIS) has published a final rule

intended to improve the safety of meat and poultry products. In
the background statement, the agency states: performance
standards spell out the objective level of performance establishments must meet during their operations in order to produce
safe and nonadulterated products, but allow the use of plantspecific processing procedures, other than those prescribed in
the current regulation. (FSIS 1999). Quantitative information on
lethality of pathogens is required for any processing schedule, to
show that it meets the lethality performance standard. The
knowledge of thermal inactivation (death) kinetics of potential
pathogens in commercial products is essential for proper thermal
process design and operation.
The heat resistance of pathogens in meat is influenced by
meat species, muscle type, pH, fat content, and other environmental factors (Ghazala and others 1995; Veeramuthu and others
1998). Thermal resistances of some bacteria were higher in
cooked meat broth than in conventional 0.05 M phosphate buffer at pH 7.0 (Bell and Delacy 1984). D-values ranging from 1.99 to
26.42 min were cited by Ghazala and others (1995) for Streptococcus faecium heated under pasteurization conditions in different
heating media, such as brain-heart infusion broth, luncheon
meat emulsion, ham broth, normal saline, nonfat milk, infant
food, and buffalo milk.
However, much published information on the inactivation kinetics of Salmonella and Listeria is based on limited experimental
studies conducted with nutrient medium broth (Smith 1995),
meat slurries (Abdul-Raouf and others 1993), or via external inoculation (on the surface) of meat (Manu-Tawiah and others 1993;
Nychas and Tassou 1996; Fu and others 1995a, 1995b; Kim and
others 1994). Most thermal inactivation kinetic data for Salmonella and Listeria were developed with liquid media (Cole and
others 1993; Stephens and others 1994; Pruitt and Kamau 1993;
Membr and others 1997). One consequence is that they have
little direct application to real poultry products in commercial
processes.
The kinetic values for thermal inactivation of Salmonella and
Listeria have not been reported in ground chicken breast meat
products, although a z value of 6.4 C for Salmonella Senftenberg
in chicken la king was reported (Angelotti and others 1960). In

706 JOURNAL OF FOOD SCIENCEVol. 65, No. 4, 2000

turkey thigh meat, Veeramuthu and others (1998) obtained D

values of 211.35, 13.24, and 3.43 min at 55, 60, and 65 C, respectively, and a z value of 5.4 C for the same organism. Goodfellow
and Brown (1978) reported a z value of 5.6 C for six Salmonella
serotypes in heated ground beef. Orta-Ramirez and others
(1997) reported a z value of 6.3 C for S. Senftenberg in ground
beef.
Due to the highly complicated structure and composition in
meat, thermal inactivation kinetics of microorganism within the
meat could differ from those in liquid media or on external surfaces (Rodriguez-Estrada and others 1997). Additionally, Liu and
others (1997) stated that the total process lethality, the cumulative effect of a given heat treatment on biological factors, could
be affected by meat composition. The kinetic studies into microbial inactivation in real products, as opposed to traditional liquid
culture, should provide a model system more representative of
the food environment.
The objectives of this study were to evaluate the thermal inactivation of Salmonella and Listeria in ground chicken breast
meat and to compare the thermal lethality kinetics of these
pathogens in ground chicken breast meat with those in liquid
medium.

Results and Discussion

Raw product composition
The total water content of the ground breast meat was about
78% (w/w, wet basis), using an oven drying method at 110 C for
24 h. The total protein content was about 96% (w/w, dry basis),
using the Kjeldahl method. The total lipids content was about
0.12% (w/w, dry basis), using the Soxhlet method. The total ash
content was about 2.1% (w/w, dry basis), using a gravimetric
method and heating the sample at 550 C in a muffle furnace for
24 h.

Thermal history
Thermal history was monitored during treatments (Fig. 1). The
heating lag time, required for the samples to reach within 0.5 C of
the bath temperature, was taken into consideration in the calculations of the kinetic parameters, per Eq. 1 and 2. Conversely, the
cooling lag time was not considered, because the center temperature of each sample dropped to 23 C within just a few seconds.
2000 Institute of Food Technologists

Survival of Salmonella and Listeria in chicken

breast meat

Table 1Mean D values for Salmonella and Listeria in chicken breast

meat and peptone (0.1%) - agar (0.1%) at 55 to 70 C.

Analysis of uninoculated controls revealed no Salmonella or

Listeria initially present in the meat samples used in this study.
The initial inoculum range of 7.0 to 7.5 log 10(CFU/g) was attained
in all trials.
Survivor curves were constructed by plotting recovered CFU/
g of sample versus heating time. As expected, as heating temperature increased from 55 to 70 C, survival of Salmonella and Listeria decreased (Fig. 2 and 3). In general, semilogarithmic survivor
curves showed a linear decline in population over heating time.
However, some of the survival curves exhibited possible shouldering. Kotrola and Conner (1997) reported that shouldering
could be caused by the poor heat transfer through the heating
medium. Nonetheless, the curves for the most part illustrated a
logarithmic destruction of cells, which allowed for reliable calculation of mean D values.

Culture

Salmonella. The average D values for Salmonella in chicken

meat (Table 1) were calculated from the survival curves (r2
0.95). Kinetic rate constants (approximately 2.303/D) of 0.076 to
9.68 min -1 were obtained for Salmonella at a temperature range
of 55 to 70 C. The z value was 6.53 C, with a correlation coefficient of 0.993 (Fig. 4). The activation energy (E) and the

Fig. 1Center temperatures of small (8.5 g) chicken meat samples at

various bath temperatures.

Fig. 2Survival of Salmonella in chicken meat at different bath temperatures

Listeria

55.0
57.5
60.0
62.5
65.0
67.5
70.0
55.0
57.5
60.0
62.5
65.0
67.5
70.0

30.1
12.9
5.88
2.51
1.16
0.358
0.238
50.8
27.2
5.02
2.42
1.71
0.400
0.187

0.95
0.97
0.96
0.99
0.99
0.99
0.99
0.92
0.97
0.97
0.96
0.97
0.87
0.99

Peptone-Agar Solution
D (min)
r2
22.8
8.70
4.09
1.71
0.577
0.260
0.154
20.3
6.86
3.51
0.783
0.252
0.180
0.103

0.88
0.82
0.99
0.98
0.99
0.99
0.89
0.95
0.85
0.95
0.95
0.94
0.98
0.83

Arrhenius constant (a) were 311.9 kJ/mol and 3.31 1048 min -1,
respectively (Fig. 5).
In comparing our results with the limited previous literature,
Veeramuthu and others (1998) tested S. Senftenberg on ground
turkey thigh meat and obtained D values of 227.18 min at 55 C,
13.55 min at 60 C, and 3.08 min at 65 C, on phenol red sorbitol
agar plate. They reported a z value of 5.4 C. Orta-Ramirez and
others (1997) reported that D values of S. Senftenberg in ground
beef ranged from 53.0 to 0.22 min at temperatures of 53 to 68 C,

Fig. 3Survival of Listeria in chicken meat at different bath temperatures

Fig. 4Logarithm of D values for Salmonella in chicken meat and

peptone-agar

Vol. 65, No. 4, 2000JOURNAL OF FOOD SCIENCE

707

FoodMicrobiologyandSafety

Thermal Inactivation Kinetics in Chicken Breast

Meat

Salmonella

Temperature Chicken Breast Meat

(C)
D (min)
r2

Salmonella and Listeria in Chicken . . .

FoodMicrobiologyandSafety

with a z value of 6.25 C. Goodfellow and Brown (1978) calculated

D values in ground beef inoculated with 6 Salmonella serotypes
(without S. Senftenberg) and obtained D values of 61 to 62, 3.8 to
4.2, and 0.6 to 0.7 min at 51.6, 57.2, and 62.7 C, respectively, with
a z value of 5.56 C.
Because of the difference in testing material and strains, it
was expected that D and z values in this study would vary from
the previous published data. It was previously reported that S.
Senftenberg was more heat resistant than the other five types of
Salmonella commonly used in thermal destruction tests (Murphy and others 1999). This greater resistance is reflected in the
larger D values in the literature for S. Senftenberg, as compared
to the cocktail in this study. These differences emphasize the importance of test material, pathogen serotype, and environment
in determining parameters for kinetic models used in food safety
programs.
Listeria. The average D values for Listeria in chicken meat (Table 1) were calculated from the survival curves, with correlation
coefficients ranging from 0.87 to 0.99. The kinetic rate constants
(approximately 2.303/D) were 0.045 to 12.32 min1 at 55 to 70 C.
The z value was 6.29 C, with a correlation coefficient of 0.958
(Fig. 6). The activation energy (E) and the Arrhenius constant (a)
were 352.2 kJ/mol and 5.06 1054 min1, respectively (Fig. 7).
In previous studies with L. innocua, Moody and others (1998)
estimated thermal inactivation at 70 C for a liquid thermal process and obtained D values of 0.0195 and 0.0232 min for bath
and continuous processes, respectively. In their study, paired
equivalent isothermal exposures (PEIE) and equivalent point
(EP) methods were used to estimate the Arrhenius kinetic parameters from the data obtained by continuous flow process. D
values of 0.0243 and 0.0228 min were obtained respectively from
PEIE and EP calculations. The z values from their study, 4.5 to 5.1
C, were lower than our value (6.29 C).
With L. monocytogenes, Fain and others (1991) reported a D
value of 1.2 min at 63 C. In their study, less than one logarithm
reduction was obtained for L. monocytogenes in ground beef at
52 C for 100 min (Fain and others 1991). D values of L. innocua
were reported to be 1.5 3 times greater than those of L. monocytogenes (Foegeding and Stanley 1991). The z values of 6.8 to
6.9 C were obtained, respectively, for two L. innocua cultures in
buffer solution at a temperature range of 56 to 66 C (Foegeding
and Stanley 1991). A z value of 5.3 C was obtained for L. innocua
PFEI in skim milk heated at 56 to 66 C. The z values in chicken
meat from our study were approximately 8% lower than those determined in buffer solution by Foegeding and Stanley and 16%

higher than those in skim milk. Our activation energy for L. innocua in ground chicken meat of 352.2 kJ/mol is in the range of
319.0 to 405.3 kJ/mol reported for L. innocua in phosphate buffer
and skim milk, respectively (Foegeding and Stanley 1991).
Although our results are in general agreement with others, the
differences between D and z values obtained in this study and
those from previous literature may reflect the impact that different food materials can have on thermal inactivation kinetics.

Fig. 5. Natural logarithm of k (min-1) for Salmonella in chicken meat

and peptone-agar solution at 55 to 70 C

Fig. 7Natural logarithm of k (min-1) for Listeria in chicken meat and

peptone-agar solution at 55 to 70 C

708 JOURNAL OF FOOD SCIENCEVol. 65, No. 4, 2000

Comparison of chicken meat with liquid medium

The D values of Salmonella and Listeria in chicken meat were
higher (p 0.0001) than those in peptone-agar solution at each
respective temperature (Table 1). However the z values in peptone-agar solution (6.26 and 6.36 C for Salmonella and Listeria,
respectively) were not significantly different from those in chicken meat (Fig. 4 and 6). A protective effect of medium composition
on thermal lethality, as reflected in the D values, was also reported in other foods. Fain and others (1991) reported that D values
of L. monocytogenes for fatty beef were double those for lean beef
at 57 and 63 C and that different z values of L. monocytogenes
were obtained between fatty (6.3 C) and lean ground beef (5.2
C). Line and others (1991) determined D values of E. coli
0157:H7 in ground beef and concluded that D values in fatty
ground beef exceeded those for lean ground beef at 52, 57, and

Fig. 6Logarithm of D values of Listeria in chicken meat and peptone-agar

Materials and Methods

Raw material
Ground and formed chicken breast patties (114.3 mm dia
14.8 mm thick, avg 53 g) were obtained from a commercial processor. Six original patties were used to determine moisture,
protein, fat, and ash contents according to AOAC (1990).
Prior to the thermal treatments, the patty samples were
screened, per FDA methods (Andrews and others 1995; Hitchins
1995), for the presence of naturally-occurring Salmonella and
Listeria and were found free of both. The same batch of meat
(approximately 10 kg) was used throughout the study. Prior to
experiments, the patties were thawed for 16 h at 4 C and deformed using a sterilized spatula in a beaker. During chicken
meat handling, care was taken in order to avoid contamination,
and the meat was kept at 0 to 4 C prior to inoculation.

Te s t o r g a n i s m s
Inoculation with several similar or dissimilar organisms
could give insight into possible microbial interaction; therefore, both Salmonella and Listeria were used in this study. Six
Salmonella serotypes (S. Senftenberg, S. Typhimurium, S.
Heidelberg, S. Mission, S. Montevideo, and S. California) were
chosen as the target microorganisms because of their potential
to occur in chicken products. S. Senftenberg (ATCC 43845) was
purchased from American Type Culture Collection (Rockville,
Md., U.S.A.). The other 5 Salmonella cultures were obtained
from Amy Waldroup (Department of Poultry Science, University of Arkansas, Fayetteville, Ark., U.S.A.). A nalidixic acid resistant culture of each serotype was prepared as previously described (Murphy and others 1999). Although, the acid resistance of the Salmonella cultures might have affected the heat
resistance, this effect was not quantified. Subcultures for use
as inocula were prepared from the stock culture as required.
Listeria innocua M1 was be used in this study as a model for
L. monocytogenes. Listeria innocua M1 was obtained from P.M.
Foegeding (Department of Food Science, North Carolina State
University, Raleigh, N.C., U.S.A. ). The Listeria culture was resistant to 50 ppm of rifampicin and 250 ppm of streptomycin.
The lyophilized culture was revived in tryptic soy broth (Difco,
Detroit, Mich., U.S.A.) for 24 h at 37 C before use.

Sample preparation
According to Heddleson and others (1991), the maximum
heat resistance of Salmonella occurs at 24 h (in stationary
phase). Therefore, for each trial, a 24 h culture was prepared
individually for each serotype in TSB (plus 200 ppm of nalidix-

in this study. Therefore, the practical implications derived from

our results concern the chemical nature of the food constituents,
which play critical roles in affecting the thermal inactivation of
pathogenic bacteria. The composition of the heating medium is
known to have a strong influence on thermal resistance in bacteria, which was confirmed in this study. The rate of pathogen thermal inactivation increases with decreasing solid content in liquid
foods (Annous and Kozempel 1998). Therefore, the prediction of
bacterial thermal inactivation in a certain food currently cannot
be reliably derived from data obtained from another food or
model system. Also, there may be variable influence of heating
medium on microbial inactivation, depending on the heating
temperatures and materials used. The resulting kinetic parameter should be useful in designing and estimating thermal processes for the poultry industry.

ic acid for the Salmonella) at 37 C. The count for each Salmonella serotype and the Listeria in those 24 h cultures was determined to be approximately 109 CFU/ml. Just prior to the thermal treatment, an equal-volume mixture (1.0 ml of each culture) was blended dropwise into ground chicken breast meat
(100 g, pH about 5.9), or a sterile agar (0.1%) peptone (0.1%)
aqueous solution (pH about 5.7), in a sterilized beaker to obtain uniform inoculation levels of 107 to 10 8 CFU/g. Diluted
agar solution was used in the liquid medium in order to increase the viscosity and minimize convection effects within
the aqueous solution. Four parallel tests were conducted to
ensure the consistency of the mixing procedure in the meat.

Thermal treatments
After mixing with the culture, samples (8.5 g of meat) were
loaded into thin-wall (0.7 mm) metal containers (8.23 mm dia
152.4 mm length) and immersed in a heated circulation water bath at 55.0, 57.5, 60.0, 62.5, 65.0, 67.5, or 70.0 ( 0.1) C.
After thermal treatment, the samples were immediately removed and placed in an ice-water cooling bath until the sample center reached 23 C (in a few seconds). The samples
were kept on ice less than 10 min before plating. The thermal
history was recorded (every 1 s) by a data acquisition system,
via thermocouples (40-gauge, type E) placed at the sample
center, sample surface, and in the heating and cooling baths.

Enumeration
Enumeration of Salmonella and Listeria was based on FDA
procedures (Andrews and others 1995; Hitchins 1995). Prior to
thermal treatment, 25 g of inoculated chicken meat (that is,
untreated control) was combined with 225 ml of sterile peptone solution (0.1%) in a sterile nylon-mesh-lined polyethylene bag and blended in a Stomacher (Lab Blender 400, Tekmar Co., Cincinnati, Ohio) for 2 min. For each thermally-treated sample, the entire sample (8.5 g) was combined with 0.1%
peptone solution (76.5 ml) and blended by the Stomacher for
2 min. In each case, the wash fluid was serially diluted, and 0.1
ml (for 10 CFU/g) or 1 ml (for 10 CFU/g) was spread-plated
over 2 or 3 plates, respectively, in duplicate for each dilution. A
total of 3 to 5 serial dilutions were plated for each treatment.
Salmonella was plated on TSB-N agar (containing 200 ppm of
nalidixic acid, sodium salt). Listeria was plated on TSB-YE-R-S
agar (containing 0.6% yeast extract, 50 ppm of rifampicin, and
250 ppm of streptomycin).
The plates were incubated at 37 C for 72 h for Salmonella
and for 96 to 144 h for Listeria, and the colonies were then
counted. The plates were returned to the incubator and re-

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63 C. Ababouch and others (1995) found that B. subtilis was

more heat resistant in oil than in buffer.
Additives (sodium chloride, sodium lactate, polyphosphate,
and fat) also may enhance thermal resistance of pathogens.
Kotrola and Conner (1997) observed this with E. coli O157:H7 in
turkey meat at 52 to 60 C and believed that this increase was
due to the reduction in water activity caused by the additives
binding water in the heating medium. Thermal inactivation of S.
Senftenberg in milk and milk by-products was reported to decrease in the presence of low-molecular-weight solutes (Kornacki
and Marth 1993). This protective effect could be due to the influence of low-molecular-weight solutes (lactose and salts) on osmolality, which in turn offers protection from thermal inactivation (Kornacki and Marth 1993).
Consistent isothermal heating temperatures were achieved

Salmonella and Listeria in Chicken . . .

counted until viable counts did not increase further. It should
be noted that, for the heated chicken meat samples, up to 144
h was required for the heat-injured Listeria to recover.

where N/N0 is the fraction of survivors, k is the destruction rate

(min1 ), a is the Arrhenius constant (min1), E is the activation
energy (J/mol); R is the universal gas constant (8.314 J/mol/K),
and T is the product temperature (K).

Survivor curves and primary models

Survivor curves were generated by plotting the logarithm of
survivor colony counts versus the heating time at each tested
temperature. The following linear primary model of Buchanan
and others (1997) was used to model the thermal destruction
of Salmonella and Listeria and to determine the decimal reduction times.
[t tL]
(1)
Xt X0
Xt X0 s (ttL)

[t tL]

(2)

where Xt log10 (cfu/g) at time t, X0 log10 (cfu/g) at time t 0,

s slope of the survivor curve, t time (min), and tL duration of lag period (min).
First-order kinetics and an Arrhenius equation were used to
estimate the kinetic parameters as follows:
N N0 ekt

(3)

k a eE/RT

(4)

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FoodMicrobiologyandSafety

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710 JOURNAL OF FOOD SCIENCEVol. 65, No. 4, 2000

Calculation of D, z, k, and E values

Triplicate thermal inactivation trials were performed at
seven temperatures from 55 to 70 C. The D (decimal reduction) values for Salmonella and Listeria at each trial temperature were calculated by taking the negative inverse of the
relevant s value (Ghazala and others 1995). The z values
(temperature change to change the D values 10-fold) were
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ln(N/N 0 ) in contrast to heating time plot at each tested temperature and could be estimated as 2.303/D. The activation
energy of thermal inactivation (E) was calculated from the
negative slope of the ln(k) in contrast to inverse temperature
(1/T) plot. The Arrhenius constant (a) was calculated from
the intercept of the ln(k) in contrast to 1/T regression. Slopes
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MS 19990616 received 6/11/99; revised 3/8/00; accepted 4/10/00.
This project was partially supported by a grant from the U.S. Poultry & Egg Association.

Authors Murphy and E.R. Johnson are with the Department of Biological
and Agricultural Engineering, University of Arkansas, Fayetteville, AR 72701.
Author M.G. Johnson is with the Dept. of Food Science, University of Arkansas. Author Marks is with Department of Agricultural Engineering, A.W.
Farrall Hall, Michigan State University, East Lansing, MI 48824-1323. Direct inquiries to Marks (E-mail: marksbp@msu.edu).