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Survivability of Salmonella cells in popcorn after microwave oven and

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Article in Microbiological Research · February 2008

DOI: 10.1016/j.micres.2006.03.010 · Source: PubMed

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 ARTICLE IN PRESS
Microbiological Research 163 (2008) 73—79

www.elsevier.de/micres

Survivability of Salmonella cells in popcorn after

microwave oven and conventional cooking
I. Anaya, A. Aguirrezabal, M. Ventura, L. Comellas, M. Agut

IQS Technical College, Ramon Llull University, 08017 Barcelona, Spain

Accepted 16 March 2006

KEYWORDS Summary
Salmonella;
The survivability of Salmonella cells in popcorn preparation was determined for two
Corn kernels;
distinct cooking methods. The first method used a standard microwave oven. The
Popcorn;
second method used conventional cooking in a pan. Prior to thermal processing in
Thermal treatment;
independent experiments, 12 suspensions in a range between 1  103 and 8  106
Microwave
colony-forming units (CFU) per gram of Salmonella cells were inoculated in both raw
microwave popcorn and conventional corn kernels. The influence of the initial
concentration of Salmonella cells in the raw products and the lethal effects on
Salmonella by thermal treatments for cooking were studied. Survival of Salmonella
cells was determined in the thermally processed material by pre-enrichment and
enrichment in selective medium, in accordance with the legislation for expanded
cereals and cereals in flakes. Viable experimental contaminants were recovered
from the conventionally cooked popcorn with initial inoculation concentrations of
9  104 cells/g or greater. Salmonella cell viability was significantly reduced after
microwave oven treatment, with recoveries only from initial concentrations of
2  106 cells/g or superior.
& 2006 Elsevier GmbH. All rights reserved.

Introduction (Uyttendaele et al., 1998; Bemrah et al., 2003).

Salmonellosis is the most frequently reported
cause of foodborne illness in the world. It is a
bacterial disease caused by members of the genus
Salmonella. This pathogen is widely found in the
environment and in animals, particularly poultry
Corresponding author. Tel.: +34 932 672 000.
E-mail address: ivananayab@iqs.es (I. Anaya).
Salmonella was detected with a frequency between
8% and 13% in laboratory analyses of the hygienic
quality of raw popcorn (Anaya et al., un-published
data). Consumption of popcorn products could be a
risk when they are contaminated and/or when good
hygienic practices are not followed during their
preparation. Processing methods are likely to
affect bacterial viability in the finished popcorn.
Therefore, care must be taken to ensure that

0944-5013/$ - see front matter & 2006 Elsevier GmbH. All rights reserved.
doi:10.1016/j.micres.2006.03.010
 ARTICLE IN PRESS
74
microwave or conventional cooking is capable of
eliminating pathogens such as Salmonella in order
to guarantee the safety of such processed food.
It is known that each popcorn kernel contains a
drop of water inside a mass of soft starch
surrounded by a hard outer surface. As the kernel
heats up, the water begins to expand, and pressure
builds against the hard starch. Eventually, this hard
surface fractures, and the soft starch inside inflates
and bursts, turning the kernel inside out. The drop
of water is vaporized and released, as the corn
kernel pops, causing Salmonella cell death under
the best-case scenario.
The thermal treatment, to reduce the presence
of Salmonella and other microorganisms in differ-
ent foods including pork, turkey, poultry meat, eggs
and corn flour, by use of water bath and dry heat
treatments is described in the literature by
(VanCauwenberge et al., 1981; Juneja et al.,
2001; Bemrah et al., 2003; Grijspeerdt and Her-
man, 2003; Marcy et al., 2004). Also, the use of
microwave radiation for the reduction of Salmo-
nella and others microorganisms in various foods:
chicken, turkey, beef, corn-soy-milk, eggs, frozen
food, poultry feed, poultry meat and rice salad is
described in the literature by (Craven and Lillard,
1974; Blanco and Dawson, 1974; Crespo et al.,
1977; Cunningham, 1978; Bookwalter et al., 1982;
Burdick et al., 1983; Aleixo et al., 1985; Evans
et al., 1995; Levre and Valentini, 1998).
Reports of Salmonella survivability in popcorn
processed from raw microwave popcorn or conven-
tional corn kernel products are not available in the
published literature and this work could complete
this lack of information regarding these products.
We report the survival characteristics of Salmonella
enterica in inoculated raw popcorn kernels that
were conventionally stove cooked in a pan and
cooked in a microwave oven to final internal
temperatures of 130.0 and 110.0 1C, respectively.
Materials and methods
Preparation of the standard calibration curve
A strain of Salmonella enterica, subspecies I,
serotype: Typhimurium 4,12:i:1,2; lysotype: 104,
previously isolated from raw microwave popcorn
(Anaya et al., 2004) was used to obtain a standard
calibration curve. Salmonella cells were grown on
trypticase soy agar (TSA) (MERCK) at 37 1C for 24 h.
After the incubation period, an inoculation loop-
ful of cells from a TSA culture was added to 9 ml of
sterile salt solution (0.85% NaCl) to obtain a cell
I. Anaya et al.
density equivalent to 2 on the McFarland scale. This
suspension was used to prepare serial standard
decimal dilutions in sterile salt solution (0.85%
NaCl).
Subsequently, absorbance readings of the serial
dilutions were taken using a spectrophotometer
(Helios Alpha, Unicam, UK) at 390 nm, with sterile
saline solution (0.85% NaCl) as the blank.
Viable counts of Salmonella cells present in these
serial dilutions were determined by superficial
inoculation on Hektoen enteric agar (Oxoid).
Exactly 0.1 ml of each serial dilution was placed
and spread onto an agar plate using a glass
spreader. The plates rested for some minutes in
the same position before they were incubated at
37 1C for 24 h. Colonies, which developed on
Hektoen enteric agar, were recognized and
counted. The total colony-forming unit (CFU) per
gram was obtained by multiplying the number of
colonies by ten.
Thermal treatment
Corn samples
Samples of corn kernels were purchased from a
local supermarket. The raw microwave popcorn is
manufactured using corn suitable for microwave
popping which is specially prepared with stable
vegetable fats, salt, flavourings and antioxidants.
This product is packed in a 100 g specially designed
paper bag, which can be placed in the microwave
oven.
On the other hand, the conventional corn kernels
for popcorn production were purchased as raw
products supplied in containers with selected
kernels that had been packed in a modified atmo-
sphere packaging.
Prior to the thermal treatment, the corn kernel
samples were screened by standard methods
(Pascual-Anderson and Calderón-Pascual, 1999) to
determine the presence of naturally occurring
Salmonella. Only samples free of Salmonella were
considered suitable for the assay.
Salmonella suspensions
In order to study the survivability of Salmonella
cells during both microwave oven and conventional
cooking, the same isolated Salmonella enterica
strain employed to prepare the standard calibra-
tion curve, was used to contaminate the samples
with suspensions of known concentrations. For each
trial, a 24 h culture of Salmonella was prepared
 ARTICLE IN PRESS
Survivability of Salmonella cells in popcorn after microwave oven and conventional cooking
individually at 37 1C by growing the organisms on
TSA. After this period, cells from the TSA culture
were added to 9 ml of sterile salt solution (0.85%
NaCl) in order to obtain the suspensions labelled
from S1 to S12. The optical density of all suspen-
sions ranged between one and five on the McFar-
land scale. The absorbance readings of the
suspensions were taken by use of a spectrophot-
ometer at 390 nm. A sterile salt solution (0.85%
NaCl) was used as the blank. Concentration values
for these inocula suspensions were extrapolated
from the empiric equation (Eq. (1)) obtained by
means of a standard calibration curve.
Since, turbidity measurements tend to lose
linearity with higher cell counts, the Salmonella
cell concentration for suspensions S1 through S12
were confirmed by preparation of serial standard
decimal dilutions in sterile salt solution (0.85%
NaCl) and spreading by superficial inoculation on
Hektoen enteric agar (Oxoid) plates incubated at
37 1C for 24 h.
The time lapse between Salmonella cell suspen-
sion (S1–S12) preparations and the inoculation of
the raw corn samples was approximately 30 min.
Microwave cooking
Independent contamination experiments were
performed on the raw microwave popcorn using
cell suspensions (S1–S12) of Salmonella. The
microwave popcorn inner bag was opened carefully
under aseptic conditions and each Salmonella
suspension was subsequently added to the bag
(0.04 ml/g). The inoculated product was mixed for
5 min to ensure even distribution of the organism,
by means of a sterile spatula. The microwave
popcorn bag was resealed again, and stored at
room temperature for 2 h to ensure a homogeneous
temperature within samples.
The microwave heating of the inoculated kernels
used a 2450-MHz microwave oven. The popcorn
kernel sample bag with the cell suspension was
placed in the centre of the oven and exposed to
microwaves at full power (700 W) for 3 min, reach-
ing a temperature of 130.070.5 1C in the centre of
the bag. The temperature was determined by
plunging a rapid-indicating mercury thermometer
(20–200 1C range) into the sample immediately
after irradiation, as suggested by Vela and Wu
(1979).
After thermal treatment, the samples were
removed from the oven, placed in a sterile
stomacher bag, broken into smaller segments by
hand while still in the bag, and stored at 4 1C for
concurrent examination.
75
Conventional cooking
Independent contamination experiments were
conducted on the corn kernels for conventional
popcorn production for each suspension (S1–S12). A
known weight of corn kernel sample (50 g) was
transferred to a sterile polyethylene bag and was
surface drop wise inoculated with a suspension of
Salmonella (0.04 ml/g). The sample was mixed for
5 min to ensure homogeneous distribution of the
microorganisms. Then, the inoculated corn kernels
were divided aseptically into 25 g portions and
stored at room temperature for 2 h to ensure a
homogeneous temperature within the bag.
Inoculated corn kernel samples were placed in a
sterile oil-drenched pan heated on a gas stove. The
samples were individually heated for 4 min until all
the kernels exploded, reaching a temperature of
110.070.5 1C in the centre of the pan. The
temperature was determined by plunging a rapid-
indicating mercury thermometer (20–200 1C range)
into the sample immediately after cooking.
After thermal treatment, the samples were
removed from the pan, placed in a sterile stoma-
cher bag, broken into smaller segments by hand
while still in the bag, and stored at 4 1C for
concurrent examination.
Salmonella detection and identification
After microwave and conventional cooking, Salmo-
nella detection was realized according to the method
recommended by the Spanish legislation (Pascual-
Anderson and Calderón-Pascual, 1999), in which the
presence of Salmonella is detected in the 25 g of
homogenized sample by use of non-selective pre-
enrichment, selective enrichment, and isolation
procedures. Strain identification was accomplished
by use of the API 20E test kit (bioMérieux, France).
Negative controls used 25 g sample bags of corn grain
inoculated with 1 ml of peptone water buffered (4%
w/v) without addition of Salmonella cells.
Non-selective pre-enrichment media
Into a sterile 500 ml Erlenmeyer flask, 25 g of
homogenized popcorn samples were added to
225 ml peptone water buffered (Merck) and mixed
well by swirling. The mixture was incubated at
37 1C for 16–20 h.
Selective enrichment media
10 ml of Rappaport–Vassiliadis broth medium
(Merck) was placed in a 50 ml test-tube and inoculated
 ARTICLE IN PRESS
76 I. Anaya et al.

with 0.1 ml of the pre-enrichment medium. The tube
was then incubated at 42 1C for 18–24 h.
Additionally, 100 ml of selenite–cystine enrich-
ment broth (Merck) was placed in a 250 ml
Erlenmeyer flask and inoculated with 10 ml of the
pre-enrichment medium. The flask was incubated
at 37 1C for 18–24 h.
Isolation
Each microbiological loop sample was inoculated
into a separate polyethylene plate, which had been
made previously to contain 25 ml of brilliant green
agar (Merck) or Hektoen enteric agar (Oxoid). The
plates were subsequently incubated at 37 1C for
24–48 h.
Identification of presumptive salmonella
colonies
Bacterial colonies which developed on the selective
agar cultures, brilliant green agar and Hektoen enteric
For the initial inoculation of the samples, the
equation described above is useful to calculate the
concentration of the Salmonella suspensions
S1–S12. Results are shown in Table 1.
We have found no reports in the literature
indicating Salmonella contamination levels in raw
corn material for microwave or conventional cook-
ing. The range of Salmonella contaminations
normally present on raw material would have an
important bearing on establishing safe cooking
procedures.
There is no exact infective dose of Salmonella,
but as few as 100 cells per 100 g of food have been
reported to make people sick (Jay, 1996).
The risk of infection is dependent upon age and
health of the host, and it also depends on the
bacterial strain. For safety reasons, European
regulation concerning the quasi-totality of food
0.07 y = 5.9E-06x + 1.2E-05
0.06 R2 = 0.9992
0.05
Absorbance

agar, were tested to confirm correspondence with the

0.04
Salmonella species used in the contamination trials by
0.03
API 20E test kit analysis.
0.02
0.01
Serotyping
0.00
0.0E+00 2.5E+03 5.0E+03 7.5E+03 1.0E+04
Serological tests were performed to confirm the
CFU / g
biochemical profile of Salmonella, thereby distin-
guishing between potential natural and artificial Figure 1. Standard calibration curve of Salmonella cells.
contamination. Strains were sent to The Institute of
Health Carlos III Spanish Microbiology Reference
Laboratory, for serotyping. Table 1. Survivability of Salmonella cells in popcorn
after thermal treatments

Suspension Initial Salmonella recovery after

Results and discussion nomenclature Salmonella
cells (CFU/g)
Before laboratory inoculation of Salmonella cells, Microwave Conventional
raw corn samples (12 raw microwave popcorn, and 12 cookinga cookingb
conventional corn kernels for popcorn production)
were analysed to determine if they were naturally S1 8  106 + +
S2 5  106 + +
contaminated. Results show that two samples of raw
S3 2  106 + +
microwave popcorn presented naturally occurring S4 9  105  +
Salmonella enterica. Samples of conventional corn S5 7  105  +
kernels were free of Salmonella cells. S6 1  105  +
The standard calibration curve was made by S7 9  104  +
plotting the absorbance of each of the dilutions S8 6  104  +
versus the corresponding Salmonella cells counts S9 2  104  
(Fig. 1). Following linear regression analysis, the S10 7  103  
calculated R2 coefficient was 0.9992. The empirical S11 3  103  
equation obtained was: S12 1  103  

Absorbance ¼ 5:9  106  ½CFU=g þ 1:2  105 . (+): positive recovery; (): negative recovery.
a
Total time: 3 min, Final temp: 130 1C.
(1) b
Total time: 4 min, Final temp: 110 1C.
 ARTICLE IN PRESS
Survivability of Salmonella cells in popcorn after microwave oven and conventional cooking
products stipulate a Salmonella contamination rate
of less than 1 bacteria per 25 g (Axelsson and Sorin,
1997).
In this study, Salmonella suspensions ranging
from 1  103 to 8  106 cells per gram, were used
to contaminate the corn kernel samples. These
values were chosen to simulate high-contaminated
samples levels that would be able to produce illness
after the consumption of popcorn.
Due to the different types of domestic micro-
waves ovens, the popcorn makers recommend in
the instructions, that using a 700 W unit, the
time required in order to explode the corn
grains is 3 min at full power (high). Under these
conditions, the centre of the bag reached
temperature values of 130.070.5 1C and was
favoured mainly by the packing type, which
concentrate a high quantity of water vapour,
and by the high content of vegetable fats. Follow-
ing microwave cooking for each of the 12 initial
suspensions, our experimental data showed
that Salmonella cells were recovered and detected
only when corn kernels were inoculated
with concentrations of Salmonella higher than
2  106 cells/g. The experiments in which Salmo-
nella cells were recovered and detected
are marked as positive (+) in Table 1, whereas the
experiments in which no Salmonella was detected
are marked as negative ().
The conventional heating process for raw corn
material does not have an established procedure
and the homemade form has many variations. After
different laboratory tests, it was demonstrated
that 4 min are necessary to completely explode
25 g of raw corn kernels in the pan. After the
4 min had elapsed, the temperature in the centre
of the finished product was 110.070.5 1C. To
achieve repetitive results during the conventional
thermal treatment, the raw corn kernels for
popcorn production were always cooked for 4 min.
Using this conditions, Salmonella cells were
recovered and detected only when corn kernels
were inoculated whit concentrations of Salmonella
higher than 9  104 cells/g. In Table 1, samples
marked as positive (+) are those in which Salmo-
nella was detected, whereas the experiments in
which no Salmonella was detected are marked as
negative ().
In this study, results demonstrate that the
microwave cooking procedure is useful to achieve
a 6-fold reduction of this pathogen. On the other
hand, conventional cooking is less efficient than the
microwave cooking process reaching only a 4-fold
reduction of Salmonella cells.
With considerations to the Salmonella concen-
tration in the raw material, it has been demon-
77
strated that Salmonella can survive after being
subjected to the thermal treatments typically
executed by end consumers. Likewise, it must be
taken into account that the time-temperature
relation is different in both cases, as with the
intensity and conditions of heating (microwave
oven: 3 min/130 1C; conventional cooking: 4 min/
110 1C).
The experimental data presented in Table 1 show
the differences in the Salmonella survivability
according to cooking type. The viability or
positive recovery of Salmonella was greater when
the raw popcorn was prepared by conventional
cooking. Although microwave heating was applied
for 1 min less, it resulted in a more intense heat
impact on Salmonella due to a higher end tem-
perature in the centre of the finished popcorn.
Thus, the lethal effects on Salmonella by micro-
wave cooking are greater compared with the
conventional cooking, and therefore Salmonella
survival is lower.
It is common knowledge that heat kills bacteria.
However, when evaluating process lethality, it is
essential to understand both the wide range of
product and process parameters, beyond just
temperature, that affect the process outcome.
Thermal inactivation or heat resistance of micro-
organisms is influenced by numerous intrinsic
factors. Kirby and Davies (1990), and Burns et al.
(2001) conclude that samples with low water
activity confer a higher thermal resistance to
Salmonella cells. In fact, the water activity (aw)
values of raw microwave popcorn and conventional
corn kernels for popcorn production are between
0.86 and 0.89. Additionally, as Fain et al. (1991)
had previously reported, the thermal resistance of
bacteria in food appears to increase with fat
content. However, the microwave bag is a sealed
package, allowing the high-temperature water
vapour and vegetable fats to remain in its interior
for more time, with increasing elimination of the
Salmonella cells.
The non-thermal effects of microwave processes
on microbial inactivation have not been confirmed
in the literature and appear insufficient in magni-
tude to be considered during development of
preparation procedure. Nevertheless, the food
ingredients such as ionized salts, vegetable fats,
flavourings and antioxidants interact with the
microwave oven electric field, increasing the
temperature in the bag and favouring Salmonella
cells death.
On the other hand, the conventional corn kernels
for popcorn production are exempt of preservatives
and the increment of temperature is only attained
by contact with the metallic material, which allows
 ARTICLE IN PRESS
78
Salmonella cell to survive the sub-lethal thermal
treatment.
Conclusions
We do not have knowledge of any reported cases
of salmonellosis due to the consumption of popcorn
from raw microwave or conventional corn kernels.
However, the ability of Salmonella cells to survive
the popcorn preparation, shows that the consump-
tion of products produced from contaminated
raw material may represent a risk if the initial
count of Salmonella cells is relatively high (approx.
104–106 cells/g).
Lower inoculums levels might yield a safe
product with the cooking procedures employed in
this study, either with microwave oven or with
conventional cooking. However, if levels of con-
tamination similar to those used in this study occur
in the commercial raw kernels (4104 cells/g),
popcorn cooking at home may represent a potential
food safety problem.
Due to the ability of Salmonella cells to survive
popcorn preparation by microwave and conven-
tional cooking, the data presented in this paper
may be interesting for popcorn producing enter-
prises when creating hazard analysis and critical
control point (HACCP) plans.
Acknowledgements
We acknowledge the support of Selecta S.A. for
the materials with which this study was under-
taken.
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