Food Microbiology 30 (2012) 427e431

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Food Microbiology
journal homepage: www.elsevier.com/locate/fm

Thermal inactivation of Escherichia coli O157:H7 and Salmonella on catsh

and tilapiaq
Kathleen T. Rajkowski*
Food Safety and Intervention Technologies Research Unit, Eastern Regional Research Center, Agricultural Research Service, U.S. Department of Agriculture, 600 East Mermaid Lane,
Wyndmoor, PA 19038, USA

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 22 September 2011
Received in revised form
22 November 2011
Accepted 21 December 2011
Available online 17 January 2012

Thermal inactivation kinetics of individual cocktails of Escherichia coli O157:H7, or of Salmonella meat
isolates or seafood isolates were determined in catsh and tilapia. Determinations were done at 55, 60
and 65
C using a circulating-water bath and calculated using linear regression analysis. Salmonella
seafood and meat isolates D-10 values on the nsh were the same and ranged from 425 to 450, 27.1 to
51.4, 2.04e3.8 s (z 4.3
C) at 55, 60 and 65
C, respectively. The E. coli O157:H7 D-10 values ranged from
422 to 564, 45.2 to 55.5 and 3.3e4.2 s (z 4.3
C) at 55, 60 and 65
C, respectively. The only statistical
difference (P  0.05) was found when comparing the D-10 values for E. coli O157:H7 at 55
C on catsh
and tilapia. The other D-10 values for the Salmonella at all temperatures and E. coli O157:H7 at 60 and
65
C on the catsh or tilapia showed no statistical difference. D-10 values for the catsh and tilapia
were signicantly lower than the reported values in other food systems, but the z-values were within
the literature reported range. These D-10 values can be used to determine cooking parameters of nsh.
Published by Elsevier Ltd.

Keywords:
Finsh
Catsh
Tilapia
Escherichia coli O157:H7
Salmonella
Thermal D-values
Z-values

1. Introduction
Globally sh consumption reached 115.1 million tonnes in 2008
(17 kg/person) which can vary from 1 to 100 kg per capita
depending on geographical area and can even vary within the
individual country (FAO, 2007). Aquaculture contributed an estimated 50% of the available sh consumed and for some countries
this can mean an increase of imported sh (Greenlees et al., 1998).
Since 2001 aquaculture production has increased at an average
annual growth rate of 6.2% and in the United States sheries
production averages about 10% for the aquaculture products (FAO,
2007). Consumption of sh products has remained at about
23 kg/capita (1996e2006) in North America.
Fish, as dened in Section 21 of the United States Code of
Federal Register part 123.3 (d), means fresh or saltwater nsh,
crustaceans, other forms of aquatic animal life (including, but not
limited to, alligator, frog, aquatic turtle, jellysh, sea cucumber, and
sea urchin and the roe of such animals) other than birds or
q Mention of trade names or commercial products in this publication is solely for
the purpose of providing specic information and does not imply recommendation
or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.
* Tel.: 1 215 233 6440; fax: 1 215 233 6406.
E-mail address: Kathleen.rajkowski@ars.usda.gov.
0740-0020/$ e see front matter Published by Elsevier Ltd.
doi:10.1016/j.fm.2011.12.019

mammals, and all mollusks, where such animal life is intended for
human consumption (CFR, 2008). Another term used to describe
sh is seafood which is divided into three categories: nsh,
crustacean (shrimp) and mollusk (shellsh).
When the United States General Accounting Ofce (GAO) issued
a report on the seafood safety program in 2004, they stated that
80% of the consumed seafood (nsh, crustaceans and mollusk)
was imported and that eating contaminated seafood resulted in
about 15% of the reported food borne outbreaks in the U.S. which is
a greater percent than either meat or poultry even through meat
and poultry are consumed at 8 and 6 times the rate of seafood,
respectively (GAO, 2004). In 2006 the U.S. Center for Disease
Control classied food vehicles implicated in outbreaks into 17 food
commodities and determined that sh (47 outbreaks) was associated with most outbreaks (CDC, 2009).
Bacterial pathogens were listed as the cause of the seafoodrelated illnesses (GAO, 2004).
In particular Salmonella can contaminate seafood from harvest to
consumption and is the major cause of seafood-associated bacterial
outbreaks in the EU (EFSA, 2010), in the US (CSPI, 2009) and in other
countries worldwide. The United States Food and Drug Administration tested 11,312 imported and 768 domestic seafood samples
from 1990 to 1998 (GAO, 2004). They reported that overall 7.2% for
imported and 1.3% for domestic seafood were positive for Salmonella

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K.T. Rajkowski / Food Microbiology 30 (2012) 427e431

and the Salmonella isolated were species identied from both

domestic and imported sh and shellsh (Heinitz et al., 2000).
Amagliani et al. (2011) reported that Salmonella contaminated sh
and sh products are responsible for 1.4% of the outbreaks in the EU.
In their review of food borne microbial pathogens of seafood
aquaculture, Greenlees et al. (1998) identied Escherichia coli and
Salmonella as inhabitants in pond water, whereas, E. coli was
isolated only from nsh harvested from those ponds (Greenlees
et al., 1998; GAO, 2004). Andrews et al. (1977) surveyed retail
fresh and frozen channel catsh (Ictalurus punctatus) for Salmonella.
They isolated Salmonella from the samples and reported that the
number of positive samples from the farm-raised catsh were
seasonal with a 0.9% incidence for JanuaryeMarch versus 5.7% for
JulyeSeptember (Andrews et al., 1977). Huss et al. (2000)
reviewed the hazards of consuming seafood (nsh and mollusk)
and identied both Salmonella and E. coli O157:H7 as pathogenic
bacterial contamination on seafood. In a survey of sushi (raw
salmon) sold frozen at retail and raw at sushi bars Salmonella and
E. coli were isolated from the raw nsh used in sushi preparation
and that the prevalence of E. coli was higher in the fresh sh than in
the frozen sh (Atanassova et al., 2008). In their epidemiological
review of seafood-associated infections in the U.S., Iwamoto et al.
(2010) reported that from 1973 to 2006 there were 10 outbreaks
due to salmonellosis, As more reports on the pathogenic contamination of raw nsh become available, there will be increased
emphasis on proper handling and cooking of seafood.
The three different types of seafood (nsh, crustacean and
mollusk) would require different cooking parameters. In the FDA
Food Code (2009), the cooking parameters for retail establishment
gives different time/temperatures for the seafood types (sh, crustacean, mollusk) and state a cooking time for sh of 15 s at 63
C (FDA,
2009). In the NACMCFs (2008) report and Doyle and Mazzottas
(2000) review, thermal inactivation data for the individual human
bacterial pathogens on seafood, particularly nsh, is lacking. This
study was conducted to determine the thermal inactivation of
Salmonella and E. coli O157:H7 inoculated on fresh catsh and tilapia.

plating in duplicate on tryptic soy agar (TSA, Becton, Dickinson and

Co.) The cocktail (1079 CFU/ml) was used immediately to inoculate
the sh and discarded.
2.3. Sample preparation
Two nsh types were used to represent a high fat sh (catsh
e 7.6% total lipid, 79.1% water and 15.2% protein/100 g) and a low fat
sh (tilapia e 1.7% total lipid, 78.1% water and 20.1% protein/100 g)
(NND, 2009).
Fresh channel catsh llets (I. punctatus) were obtained from
the catsh genetic laboratory of U.S.D.A. Agricultural Research
Service, Stoneville, MS. The catsh were caught, lleted and shipped by overnight express for arrival the next day. Upon arrival, the
catsh llets were cut into smaller pieces before being homogenized in a sterile laboratory blender (Model 38BL54, Waring,
Torrington, CT). Instant quick frozen (IQF) tilapia llets were
purchased from a local supermarket, thawed and cut into smaller
pieces before being homogenized.
Ten g of the homogenized catsh or tilapia samples were
weighed into a re-closable plastic bag (Zip-Pak, Minigrip, Seguin,
TX), frozen and irradiated frozen (20
C) with a dose of 10 kGy
sufcient to remove background microora (Rajkowski, 2008). The
irradiation process was done in a self-contained 137Cs gamma
irradiator (Lockheed Georgia Co., Marietta, GA) with a source
strength of ca. 88,359 Ci (2.39 PBq). The samples were placed
within a uniform area of the radiation eld to minimize variations
in the absorbed dose, which is checked yearly for uniformity using
alanine dosimeters. Actual dose (dosimetry) was veried by
measuring the free-radical signal of 5 mm diameter alanine
dosimeter pellets (Bruker Biospin Corp. Billerica, MA) using
a Bruker EMS 104 EPR Analyzer. The irradiated samples were kept
frozen (20
C) until used. The pH of the thawed-irradiated sample
was measured using an Orion 520A meter (Orion Research Co.,
Boston, MA).
2.4. Thermal destruct values

2. Materials and methods

2.1. Microorganisms
E. coli O157:H7 933, A9218-C1 and 45753.35 and Salmonella
enteritidis Enteritidis 13076, Senftenberg 8400, and Typhimurium
14028 (meat isolates) were obtained from the Eastern Regional
Research Centers culture collection. Salmonella Schwarzengrund
19535, Panama 19545, Bahrenfeld 19489 and Weltevreden 19493
were obtained from the U.S. Food and Drug Administration and are
seafood isolates (Zhao et al., 2006). Working stock cultures of each
strain were maintained in brain-heart infusion broth (Becton,
Dickinson and Co., Sparks, MD) and stored at 4
C.
2.2. Inoculation preparation
The day before the procedure the isolates, either Salmonella meat,
Salmonella seafood or E. coli O157:H7 for the individual cocktail were
grown separately overnight at 37
C in tryptic soy broth (TSB, Becton,
Dickinson and Co) to obtain an 18 h culture. The cocktail was made
by combining 5 ml of each overnight culture and centrifuging at
3600  g for 10 min (Sorvall Legend RT centrifuge, Kendro Laboratory Products, Newtown, CT). The pellet was re-suspended in
Butterelds phosphate buffer (BPB-6.8 pH; Hardy Diagnostics, Santa
Maria, CA) to the original cocktail volume. Three different cocktails,
E. coli - meat, Salmonella e meat and Salmonella e seafood, were
prepared. The cell density of the cocktail was determined by serial
dilution in 0.1% peptone water (PW, Becton, Dickinson and Co.) and

Fish samples (10 g) for the thermal destruction values study were
thawed to room temperature and mixed well with 0.1 ml inoculation
cocktail for a 1:100 dilution of the initial inoculum for a nal cell
concentration of 1067 CFU/g. One g sample was weighed into
stomacher bags (200 ml, Whirl-Pak lter bags, Nasco, Fort Atkinson,
WI) and the sh sample distributed in the bag to form a thin layer
before being vacuumed heat sealed (Model A300/16), MULTIVAC,
Sepp Haggenmller GmbH & Co. KG, Wolfertschwenden, Germany).
The thermal destruct method as developed by Huang (2009)
was used. The sample bags were placed in a rack constructed to
provide adequate contact with the hot water. All samples were
placed simultaneously in a re-circulating hot water bath (Model
ESRB-7, Techne, Burlington, NJ) which was tted with a temperature control unit (TU-20D, Techne). The temperature of the water
bath was monitored by inserting a temperature probe into the
water. The temperature of the water bath was set at one of three
temperatures: 55, 60 or 65
C and the pull time intervals were
determined during preliminary trials. A minimum of ve time
intervals were used: 0, 120, 360, 600, 720, 960, and 1200 s at 55
C;
0, 10, 20, 40, 60, 80, and 100 s at 60
C; and, 0, 2, 4, 6, 8, 10, 12 s at
65
C. The come-up time (lag time required for the food temperature to reach bath temperature) was 4 s (Huang, 2009). At the
determined time intervals (after correcting for the come-up time)
the sh samples were removed from the hot water bath and
immediately immersed in iced water to stop the heating process.
The sh samples remained chilled and recovery of survivors was
done immediately. The thermal destruct study on the catsh and

K.T. Rajkowski / Food Microbiology 30 (2012) 427e431

429

tilapia using the three cocktails at each temperature was repeated

two times.
2.5. Plating of samples
The bag containing the pre-weighed 1 g catsh or tilapia
samples was aseptically cleaned, opened and 9 ml buffered peptone
water (Becton, Dickinson and Co.) added obtaining a 1:10 dilution.
The samples were stomached for 2 min (Stomacher 400, Tekmar
Co., Cincinnati, OH) and serial diluted with PW before being surface
plated on TSA to determine survivors. The plates were incubated for
24 h at 37  1
C before being hand counted.
2.6. Thermal D-10 and Z-values
The thermal D-10 value is the time required to reduce the
microbial population by 90% at a specic temperature (Pug et al.,
2001). Regression analysis was done on a minimum of ve values
from the linear portion of the survival plot using the DMFit
program (Baranyi and Roberts, 1994). The thermal D-10 value was
calculated by taking the reciprocal of the slope (D-10 1/slope).
The Z-value is the change of temperature (
C) required for 1-log
cycle change in D-10 values and was calculated using the formula
(Pug et al., 2001): z (T2 e T1)/(log D1 e log D2)
2.7. Statistical analysis
The D-10 and z-values were analyzed by ANOVA to determine
the effects and interactions of the sh type and temperature (Miller,
1981).
3. Results and discussion
3.1. Thermal destruct procedure
Rajkowski (2008) reported that 10 kGy was sufcient to remove
background microora and that the irradiation process did not
affect the lipid content of the catsh or tilapia as indicated by TBAR
values. This decision to remove the background microora to
recover on TSA was supported by Clavero et al. (1998) who reported

Fig. 1. Thermal inactivation curves at 55
C for E. coli O157:H7 and Salmonella meat and
seafood isolates inoculated on catsh and tilapia.

Fig. 2. Thermal inactivation curves at 60
C for E. coli O157:H7 and Salmonella meat
and seafood isolates inoculated on catsh and tilapia.

that the use of selective medii (sorbitol MacConkey agar supplemented with 4-methylumbelliferyl-b-D-glucouronid and modied
eosin methylene blue agar) were inhibitory in recovering
sub-lethally heat-injured E. coli O157:H7 cells. Therefore TSA was
used to recover E. coli O157:H7 and Salmonella after the thermal
processing.
3.2. Thermal destruct times and z-values for E. coli O157:H7
The thermal destruction curves for E. coli O157:H7 inoculated on
the catsh and tilapia at 55, 60 and 65
C are illustrated in Figs. 1e3.
There was no observed lag or tailing in any of the E. coli O157:H7
survivor curves and such linear curves suggested that the cocktail
population was homogeneous. Listed in Table 1 are the calculated
E. coli O157:H7 D-10 values obtained at 55, 60 and 65
C, and the
regression curves had an r2 values of >0.92. The E. coli O157:H7 had
a signicantly higher (P  0.05) D-10 value at 55
C on tilapia than
on the catsh which was not observed at the higher temperatures.
Ahmed et al. (1995) determined and compared the D-10 values for
E. coli O157:H7 inoculated on various meats (chicken, turkey beef

Fig. 3. Thermal inactivation curves at 65
C for E. coli O157:H7 and Salmonella meat
and seafood isolates inoculated on catsh and tilapia.

430

K.T. Rajkowski / Food Microbiology 30 (2012) 427e431

Table 1
Thermal destruct times in seconds and regression data for Escherichia coli O157:H7 isolates inoculated on catsh and tilapia as compared to literature values on ground beef and
chicken.
Temperature

E. coli

55

131

60

140

65

149

a
b

E .coli

Catsh

Tilapia

Ground beefa

Chickena

422  0.3b
r2 0.96
55.5  2.8
r2 0.97
4.2  0.09
r2 0.92

564  0.7b
r2 0.98
45.2  2.0
r2 0.98
3.3  0.04
r2 0.98

1267.8

710

190.2

98

23.4

22

Taken from Juneja et al. (1997).

Signicantly different at P  0.05.

and pork sausage) which had different fat content. They reported
that at 50 and 55
C, the higher fat-content meat samples had
a higher D-10 value than the lower fat content meats. In this study
at 55
C we obtained the opposite results. Comparison conrmed
a statistically higher (P  0.05) D-10 value at 55
C for the E. coli
O157:H7 inoculated on the tilapia which has a lower fat content
(1.7%) compared to catsh with the higher fat content (7.6%) even
though the pH of both nsh samples was 6.3 (NND, 2009). Ahmed
et al. (1995) reported that there was no signicant difference for the
D-10 values at 60
C for turkey or beef samples and we also did not
observe any difference with the catsh and tilapia samples at both
the 60 and 65
C.
It was reported that different D-10 values were obtained among
the strains of E. coli O157:H7 (Clavero et al., 1998). We were able to
compare our E. coli O157:H7 D-10 results using catsh and tilapia
with literature values for ground beef and chicken, since our
cocktail contained some of the same strains used by Juneja et al.
(1997) in their study. Also, the pH of both nsh was similar to the
pH of the ground beef and chicken (Juneja et al., 1997). For
comparison listed in Table 1 are their reported D-10 values using
ground beef and chicken. The D-10 values for the catsh and tilapia
were much lower. It took twice as long to inactive the E. coli
O157:H7 in the chicken compared to the nsh and about three
times as long to inactive in the ground beef sample (Juneja et al.,
1997). When researchers used different strains of E. coli O157:H7
to determine the D-10 value in beef and poultry, their results were
also higher than those reported here for catsh and tilapia (Ahmed
et al., 1995; Line et al., 1991).
The calculated z-values for E. coli O157:H7 on catsh and tilapia
was 4.3
C. When compared with the z-values for E. coli O157:H7
obtained using meat or poultry with the reported z-value obtained
using catsh and tilapia, the z-values were found to be within the
reported range of 4e6
C (Juneja et al., 1997; Line et al., 1991;
Srqvist, 2003) regardless of the E. coli O157:H7 isolate used.
3.3. Thermal destruct times and z-values for Salmonella
Comparison of data for the thermal destruct values of Salmonella
on nsh (catsh or tilapia) with published reports is lacking. Doyle

and Mazzatta (2000) in their review stated that thermal resistance

of Salmonella can vary between serotypes and the food used to
determine the D-10 value. Therefore to overcome this difculty,
isolates of Salmonella from meat and seafood were used for the two
different cocktails to determine the D-10 values at 55, 60 and 65
C.
Representative curves of the two Salmonella cocktails (meat and
seafood) are given in Figs. 1e3 and listed in Table 2 are the D-10
values. There was no signicant difference (P  0.05) in the D-10
values between the meat isolate or seafood isolate cocktails, and
there was no signicant difference (P  0.05) between the Salmonella D-10 value between the catsh (pH 6.3) and tilapia (pH 6.3).
Plaza and Gabriel (2008) used S. Typhimurium inoculated oyster
meat (pH 6.0) and reported the D-10 value at 60
C of 23.04 s, which
is within the range observed in this study.
When the Salmonella D-10 values for both the meat and seafood
isolates on the nsh were compared with the reported values in
custard and chicken a la king, egg, liquids with D-10 values ranging
from 180 to 4890 s at 60
C (Angelotti et al., 1961; Doyle and
Mazzatta, 2000; Srqvist, 2003) our results were lower ranging
from 22 to 51 s at 60
C. Juneja et al (2001) reported a range of
289e399 s at 60
C for beef, pork, turkey and chicken, whereas we
found that the D-10 value at 60
C ranged from 22 to 51 s for the
nsh which is much lower. This wide range of reported D-10
values for Salmonella most likely is due to strain differences and
for that reason those strains isolated from seafood appear to be
less resistant to heat inactivation.
When liquids (egg, milk products, saline solutions, scalding
water from chicken and pork plants) were used to determine the
thermal destruct data, the reported z-value range varied from 3.24
to 9.5
C (Doyle and Mazzatta, 2000; Srqvist, 2003). The calculated
z-values for the Salmonella inoculated on the catsh and tilapia
were not different statistically (P  0.05) and there was no differences (P  0.05) between the two cocktail used. Since there was no
differences, the calculated z-values were averaged. The z-values for
the nsh calculated in this study ranged from 4.3 to 4.8
C with an
average value of 4.5
C and falls within the range reported for
liquids. However Juneja et al. (2001) reported the z-value ranging
from 5.77 to 6.91
C on meat samples and Angelotti et al. (1961)
reported z-values ranging from 9.3 to 13.75
C using custard and

Table 2
Thermal destruct times in seconds and regression data for Salmonella meat and seafood isolates inoculated on catsh and tilapia as compared to literature values on ground
beef.
Temperature

Meat isolates

55

131

60

140

65

149

Taken from Juneja et al. (2001).

Seafood isolates

8 strain cocktail

Catsh

Tilapia

Catsh

Tilapia

450  0.3
r2 0.96
51.4  2.2
r2 0.95
3.8  0.8
r2 0.98

425.5  0.3
r2 0.97
27.1  0.7
r2 0.97
2.04  0.03
r2 0.94

497.7  20.0
r2 0.97
29.5  2.1
r2 0.97
2.43  0.25
r2 0.98

337.3  5.7
r2 0.97
22.9  0.8
r2 0.97
1.62  0.06
r2 0.92

Ground beefa

328.8
40.2

K.T. Rajkowski / Food Microbiology 30 (2012) 427e431

chicken a la king to determine the D-10 value. In both of these

reports, the samples used had higher fat content that the nsh
used in this study.
4. Conclusions
Overall, the fat content between the catsh and tilapia did not
affect the D-10 values. The D-10 values for both E. coli O157:H7 and
Salmonella inoculated on nsh were lower than those reported for
other food systems, particularly meats. However the z-values,
which were low, did fall within the reported range.
Cooking, heat inactivation, is a way of destroying pathogens in
foods and remains the primary means of protecting against food
borne illnesses. Knowing the rate of destruction, further studies are
needed to obtain cooking parameters for nsh. These results can
be used to provide safe cooking instructions to the consumer.
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