Food Control 43 (2014) 150e154
Contents lists available at ScienceDirect
Food Control
journal homepage: www.elsevier.com/locate/foodcont
Comparison of bacterial inactivation with novel agitating retort
and static retort after mild heat treatments
Mehmet Baris Ates a, b, *, Dagbjørn Skipnes a, Tone Mari Rode a, Odd-Ivar Lekang b
a
b
Nofima AS, Richard Johnsens Gate 4, P.O. Box 8034, N-4068 Stavanger, Norway
The Norwegian University of Life Sciences, Department of Mathematical Science and Technology, P. O. Box 5003, N-1432 Ås, Norway
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 17 September 2013
Received in revised form
21 January 2014
Accepted 8 March 2014
Available online 20 March 2014
Lower thermal load on foods is desirable for food producers and consumers as the food gets higher
quality. With reduced thermal load, the investigation of food safety is of importance. In this study, microbial inactivation efficacy of a new retort process with high frequency longitudinal agitation was
compared to static retort process which was used as a benchmark. As a model, fish soup samples,
inoculated with approximately 108 cells/ml Listeria innocua, was exposed to mild heat treatments at 62,
65 and 68 C. Results clearly demonstrated that agitating mode can provide equivalent lethality to the
model organism L. innocua within significantly shorter heating times compared to static mode. Bacteria
were not detected on TSA-YE plates after 11.5, 6.8 and 5.5 min processing in agitating mode; 77, 67 and
52 min processing in static mode at 62, 65 and 68 C respectively. Bacterial inactivation in agitating mode
was generally correlated with estimated inactivation based on product core temperature, D- and z-values
for L. innocua. This may indicate that distribution of the heat load over the soup was enhanced through
agitation. Results showed that utilization of high frequency longitudinal agitation mechanism in retorts
is promising for reducing the thermal load on food products without compromising on food safety
related to non-spore forming pathogens.
Ó 2014 Elsevier Ltd. All rights reserved.
Keywords:
Agitating retort
Thermal inactivation
Listeria innocua
1. Introduction
Thermal processing in hermetically sealed containers is a
common method to produce foods with extended shelf-life utilized
historically since the Napoleonic era. Static retorts have been
widely used for industrial applications of thermal processing. Early
versions of these retorts used steam as the heating medium but
later on water, steam/air, raining and spray water systems were also
developed as heating media. In 1920s, agitating retorts were
introduced for the first time where agitation mechanism was based
on axial rotation (rolling of cans) (Eisner, 1988). Rotary retort was
later developed with end-over-end rotation principle (Clifcorn,
Peterson, Boyd, & O’Neil, 1950).
Development of agitating retorts was the outcome of a need to
overcome some weaknesses of conventional static retorts. The
weaknesses included differing temperature zones within heated
product, over-cooking, lack of consistency in texture and flavor in
processed products and slow heat penetration (Eisner, 1988). On
* Corresponding author. Nofima AS, Richard Johnsens Gate 4, P.O. Box 8034, N4068 Stavanger, Norway Tel.: þ47 96 95 27 94.
E-mail addresses: baris.ates@nofima.no, brsates@gmail.com (M.B. Ates).
http://dx.doi.org/10.1016/j.foodcont.2014.03.006
0956-7135/Ó 2014 Elsevier Ltd. All rights reserved.
the other hand, agitation of packed foods has enabled more uniform distribution of heat and process time reduction. These benefits often give higher quality food products while being only
applicable for liquid and semi-liquid foods (Rosnes, Skara, &
Skipnes, 2011). Furthermore, product consistency, headspace, fillin weight and rotation speed has to be strictly controlled to prevent under-processing as these parameters influence the heat
transfer effectiveness of agitating process (Awuah, Ramaswamy, &
Economides, 2007). Recently, an agitating retort with high frequency longitudinal agitation mechanism was developed in 2006
(Fig. 1). The new process allows rotation speeds beyond the 20e
40 rpm range with the help of reciprocating agitation mechanism
(Rosnes et al., 2011). Although critical factors for the new retort
process are believed to be same as rotary retorts, investigation of
food safety through microbial inactivation studies is of importance
with such novel processes (Walden, 2008).
Microbial inactivation studies with artificially inoculated foods
are typically used for food safety studies with novel processes.
Lower number of survivors than the hazardous level in the food
product over a determined shelf-life period after thermal processing is desirable (NACMF, 2010). Traditionally, process lethality
calculations have been based on thermal resistance data for
M.B. Ates et al. / Food Control 43 (2014) 150e154
151
over the whole food product with agitating retort process in
comparison to static process which was used as a benchmark. This
was done by conducting bacterial inactivation experiments
through a large set of heat treatments with fish soup samples
inoculated with L. innocua model organism. The product was
intended to have limited shelf life at refrigerated temperatures
lower than 3.3 C.
2. Materials and methods
2.1. Fish soup preparation
Fig. 1. Principle for the new retort system: Products (1) within the basket are agitated
in longitudinal direction. The corresponding patent can be referred to for descriptions
on each number shown in the figure modified from (Walden & Ferguson, 2007).
bacteria and spores. Thermal resistance has been mathematically
expressed by decimal reduction time (D-value) and z-value. D- and
z-values are based on the assumption that thermal inactivation of
bacteria follows log-linear kinetics. D value is the duration of heat
treatment at a specific temperature necessary to kill 90% of the
microbial population and z value is the temperature change
required to shift D value by 1 log unit (Stumbo, 1973). Other
available thermal inactivation models for microorganisms have
been reviewed by (Smelt & Brul, 2014) for interested readers.
Milder heat treatment is generally applied on foods designed to
have short shelf-life under refrigeration temperatures. For such
foods, Listeria monocytogenes contamination is a large problem as
the bacterium can cause lethal diseases. Compared to other nonspore forming food-borne pathogens, Listeria is generally reported to have higher heat resistance as well as being able to grow
at temperatures from 1.5 C up to 44 C (Hudson & Mott, 1993).
Furthermore, L. monocytogenes has been reported to grow in foods
from aw of 0.91e0.93 and pH value of 4.2 (FAO/WHO, 2004). It is
generally agreed that sufficient pasteurization can eliminate
L. monocytogenes. Mild heated products are required to be heated
for at least 2 min at 70 C (at the coldest point) in order to achieve
6-log kill effect on L. monocytogenes (FAO, 1999, p. 34; Rosnes et al.,
2011).
In research studies, Listeria innocua is proposed as a potential
surrogate microorganism for L. monocytogenes. This is because
L. innocua is safer to work with as well as having major phenotypic
similarity with L. monocytogenes (Kamat & Nair, 1996; Lorentzen,
Ytterstad, Olsen, & Skjerdal, 2010; Miller, Gil, Brandão, Teixeira, &
Silva, 2009). In a recent review, Milillo et al. (2012) recommended
more precise selection of surrogate microorganisms for
L. monocytogenes based on experimental conditions. Although
several strains of L. innocua have been found to be more heat
tolerant than L. monocytogenes (Friedly et al., 2008; O’Bryan,
Crandall, Martin, Griffis, & Johnson, 2006; Sorqvist, 2003), these
results may sometimes vary with process conditions and product
matrix (Murphy, Duncan, Beard, & Driscoll, 2003). Lorentzen et al.
(2010) compared the survival of L. innocua ATCC 33090,
L. monocytogenes NCTC 11994 and No. 4006 and found ATCC 33090
to be the most heat tolerant one. L. innocua is apparently a useful
model organism for inactivation studies but should not be directly
used for thermal validation purposes.
To the best of our knowledge, there are no studies published
regarding microbial inactivation efficacy of the retort process with
high frequency longitudinal agitation mechanism. Therefore,
objective of this study was to investigate bacterial inactivation
A common recipe for making fish soup was used. Ingredients
consisted of approximately 2% fish bouillon, 8e8.5% fat (from butter, milk and cream), 0.66% salt, and the rest being mainly water.
The soup was cooked, packed and treated with a sterilization pro10C 3 min based on core temperature. As a next step,
gram of F121
C
the soup was packed in polypropylene plastic trays (Promens,
Kristiansand, Norway) with dimensions 9 4 13.2 cm and sealed
with a plastic film. Samples were then stored at 1 C until the day of
experiments.
2.2. Culture preparation and inoculation into fish soup samples
L. innocua ATCC 33090 (Oxoid, Hampshire, U.K) was stored in
Microbank (Pro-Lab Diagnostics, Canada) at 80 C. L. innocua was
initially grown in Tryptic Soy Broth (Oxoid) supplemented with
0.6% w/w Yeast Extract (Merck, Darmstadt, Germany) (TSB-YE) at
37 C for 20 h at 150 rpm. The overnight culture was then subcultured in TSB-YE with 20 h incubation at 30 C, 150 rpm.
Resulting cell density was 108e109 cells/ml. In order to concentrate
the cells further, bacteria were centrifuged at 3500 g for 4 min
and cell pellets were collected and re-suspended in peptone water
(Merck) to obtain 1010e1011 cells/ml. Bacteria were then added to
fish soup samples to obtain an initial concentration of approximately 108 cells per ml fish soup. Finally, inoculated fish soup
samples, each having 350 g weight, were separately packed and
shaken thoroughly to distribute the bacteria evenly before subsequent heat treatments.
2.3. Heat treatments
A batch retort (Steriflow, Roanne, France) was used for all heat
treatments since it was possible to run the retort both in agitating
and static heating modes. The retort was previously calibrated
and checked for even heat distribution and the heat transfer
medium was steam and raining water. The range used in agitating
mode was 80e100 strokes per minute (spm). There were two
process batches where three replicates of inoculated fish soup
were heated in each (n ¼ 6). Core temperature histories of three
additional soup samples were recorded during treatments. A
negative control (without bacteria) was also processed and
analyzed in each process batch.
For a detailed assessment of bacterial inactivation pattern with
longitudinal agitating heating mode in comparison to static mode,
three different mild temperatures (62, 65 and 68 C) were selected
for investigation. Retort program phases were (1) come-up period
for retort water temperature; (2) heating; (3e4) cooling (Fig. 2).
Phases 1, 3 and 4 were always kept constant for each thermal
treatment. Only the effect of selected timeetemperature combinations for heating phase (2) on bacterial inactivation was studied.
For this purpose, time intervals analyzed in agitating mode were 4e
9.5 min (at 62 C), 3e4.8 min (at 65 C) and 1.5e3.5 min (at 68 C).
In static mode, time intervals 40e70 min (at 62 C), and 30e65 min
(at 65 C) and 25e50 min (at 68 C) were investigated. Additionally,
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M.B. Ates et al. / Food Control 43 (2014) 150e154
dynamic heating condition was the case for all treatments, timee
temperature history data was incorporated to isothermal heat
inactivation kinetics to calculate the lethality (L) of each thermal
treatment based on Equation (1) where Dref ¼ 2.4 min;
Tref ¼ 60 C; z ¼ 4.71 C; t and Tcore were treatment time (min)
and core temperature ( C) respectively (Monfort, Sagarzazu,
Gayán, Raso, & Álvarez, 2012):
L ¼
Fig. 2. Retort programs for thermal treatments in agitating and static modes (1: comeup period for retort water temperature, 2: heating period at constant retort temperature, 3e4: cooling periods).
pre-heating of retort water temperature was 2 min for agitating and
static heating modes for all treatments.
Detailed settings of phases in agitating and static heating setups
were as follows:
(1) Retort water heated up to set temperature (62, 65 or 68 C).
Process time kept constant as 2 min with 80 strokes per minute
(spm) shaking frequency in agitating mode whereas process
time was 2 min in static mode without shaking,
(2) various temperature-time combinations at 100 spm shaking
frequency in agitating mode and without agitation in static
mode,
(3) retort water cooled down to 30 C in 2 min at 100 spm
shaking frequency in agitating mode and in 3 min without
shaking in static mode,
(4) retort water further cooled down to 20 C within 5 min at
80 spm shaking frequency in agitating mode and within 15 min
without shaking in static heating mode
The reason for choosing a longer cooling time for static process
was to ensure fish soup samples were below ca. 45 C since cooling
was slower in static process compared agitated cooling. The retort
was otherwise too warm to touch before the samples could
immediately be placed on ice-water.
2.4. Calculation of process lethality and core temperature data
acquisition
1
Dref
Zt
Tcore Tref
z
10
dt
(1)
0
2.5. Enumeration of survivors
Along with positive and negative controls, triplicate samples of
2 ml processed fish soup (taken from 350 g aseptically opened fish
soup packs) were diluted in 18 ml peptone water and vortexed.
Further ten-fold serial dilutions were prepared for subsequent
surface plating on Tryptic Soya Agar (Oxoid) supplemented with
0.6% yeast extract (TSA-YE). Additionally, dilutions were plated on
Brilliance Listeria Agar added with selective and differential supplements (Oxoid). The latter medium, that is selective for Listeria,
can give information about cell injury, as injured cells have difficulties to grow on this medium (Hansen & Knochel, 2001; Miller,
Brandão, Teixeira, & Silva, 2006). Eddy Jet spiral plater instrument
(IUL Instruments, Barcelona, Spain) was used for surface plating
procedure unless manual plating was necessary to count lower
amounts of bacteria. All plates were incubated at 30 C for 2e5
days.
2.6. Statistical analysis of data
L. innocua inactivation data was calculated as log10 (N0/N),
where N0 is the initial bacteria concentration and N number of
survivors on TSA-YE and Brilliance plates after heat treatment.
Detection limit was 102 cells/ml. If there were no survivors on
plates with lowest dilution, all bacteria were considered killed
after the heat treatment. Results for each data point were obtained by calculating the mean-value and standard deviation
from six replicates. The general linear modeling (GLM) and
Tukey’s HSD test were used to compare means at significance
level p < 0.05 using Minitab Statistical Software v15 (Minitab
Ltd., Coventry, UK).
3. Results and discussion
Process lethality was estimated only on agitating process
samples based on coldest spot. Lethality was not calculated on
static process samples since different temperature zones within
the product causes misleading results. Classical thermal death
model was used for process lethality calculations. Heat resistance
data for the L. innocua culture was previously obtained as
D60 C ¼ 2.40 min with a standard deviation (SD) of 0.04 and
z ¼ 4.71 C with an SD of 0.08 after experiments made in TSB-YE
medium. As a comparison, in previous studies D60 C was found
2.43 0.17 min for L. innocua ATCC 33090 in peptone water medium (Ahn & Balasubramaniam, 2007). Based on experiments
with various food media, z-values for L. innocua were obtained
5.8 0.8 C (Sorqvist, 2003).
Heat resistance data available for L. innocua culture was used
for estimating microbial inactivation (in log units) based on
lowest core temperature values (0.05 C accuracy). The temperature data was obtained via E-Val Flex thermocouple system
(Ellab A/S, Hilleroed, Denmark) integrated to PC software (Valsuite, Ellab A/S). Threshold temperature value was set to 50 C
where L. innocua inactivation was assumed to begin. Since
3.1. Heat penetration data
Agitating mode caused faster product heating than the static
mode for all experiments. As a representative for other heat
penetration curves, selected heat penetration values and simulated
core temperature data are shown (Fig. 3).
3.2. Microbial inactivation data
Results showed agitating heating mode shortens process time
needed to inactivate the model organism L. innocua compared to
static mode. No colonies were detected after 11.5, 6.8 and 5.5 min
processing in agitating mode compared to 77, 67 and 52 min processing in static mode at 62, 65 and 68 C respectively (Figs. 4 and
5). Another study concluded that the heat resistance of L. innocua in
liquid medium decreases at higher heating rates shown with nonisothermal heating experiments at 1.5, 1.8 and 2.6 C/min from 20
to 65 C (Miller et al., 2011). Similar cases were also reported for
L. monocytogenes (Quintavalla & Campanini, 1991) and Salmonella
M.B. Ates et al. / Food Control 43 (2014) 150e154
153
Fig. 3. Timeetemperature history of fish soup and retort water temperature during
agitating heating mode (62 C, 11.5 min process) and static heating mode (62 C, 72 min
process).
typhimurium (Mackey & Derrick, 1987). In the present study, the
phenomenon is likely a synergistic factor for microbial inactivation
since agitating heating mode provides faster heating rates in
comparison to static mode.
Bacterial inactivation data from TSA-YE plates and calculated
log kill (based on product coldest point and first order model)
after agitated processing was similar (Fig. 4). This may indicate
the thermal load was rather homogenously distributed over
the product in agitated process. Nevertheless, using traditional methods for thermal process validation is more convenient since the heat resistance among different bacterial strains
may vary.
L. innocua cells were sublethally injured after agitated processing for 8, 9, 9.5 and 10 min at 62 C; 5.5 min at 65 C; 4.5 min
at 68 C and after static processing for 47, 32 and 27 min at 62, 65
and 68 C respectively (Figs. 4 and 5). Occurrence of cell injury
was determined by the difference between colony counts on
TSA-YE and Brilliance plates (p < 0.05). Highest difference
observed was in the range of 4e5 log units suggesting that only
0.01e0.001% of the survivors were not sublethally injured in
those cases. The possible explanation is that under insufficient
heat treatment, injured cells appear to be able to repair themselves and grow on TSAYE medium but not on selective medium
as similar cases were reported in previous studies (Crawford,
Beliveau, Peeler, Donnelly, & Bunning, 1989; Mackey, Boogard,
Hayes, & Baranyi, 1994).
Competitive microflora, composition and temperature history of
a model food product should be considered for inactivation studies.
In the present study, potential effects from the competitive
microflora were knocked out by using sterile fish soup. However,
since Listeria has higher heat-resistance than other non-sporulating
bacteria, survival risk of other pathogens such as Salmonella spp.
and pathogenic Escherichia coli would be eliminated along with
Listeria under sufficient heat treatment (Farber, 1989). Furthermore,
cells may develop modified heat resistance based on food composition (high concentration of salt, acids, sugar and inhibitors) and
prior heat shocks which have been reviewed in the literature
(Doyle, Mazzotta, Wang, Wiseman, & Scott, 2001; Farber & Brown,
1990). This factor should be taken into account for such inactivation
studies. Finally, attention should be given when processing liquid
products with large solid particles. Underestimation of
L. monocytogenes inactivation in ground beef with log-linear and
Weibull model during dynamic heating was reported (Huang,
2009). In the present study, the product had neutral pH as well as
being absent of solid particles and excessive amounts of salt.
Fig. 4. Inactivation of L. innocua exposed to agitating heating at 62 C (a), 65 C (b)
and 68 C (c). Black bars: inactivation data (log10) obtained from TSA-YE plates; gray
bars: data from Brilliance plates; and white bars with dots show mathematically
calculated log inactivation based on lowest core temperature data. Data are means
from six replicate samples. Error bars represent standard deviation of each mean
value. Retort cooling times were 7 and 18 min for agitating and static modes (not
shown).
4. Conclusions
Results clearly demonstrated that agitating retort process could
deliver equivalent lethality to the model organism L. innocua within
significantly shorter times compared to static process. No colonies
were observed on TSA-YE plates after heat treatments of 11.5, 6.8
and 5.5 min in agitating mode; 77, 67 and 52 min in static mode at
62, 65 and 68 C respectively. Results could be relevant for food
producers interested in minimal food processing. Furthermore,
estimated bacterial inactivation was generally correlated with real
inactivation with samples treated in agitating mode. The result was
supportive of the assumption that the heat load through the soup
was homogenously distributed with the help of agitation. Apparently, further inactivation studies using more heat-resistant
L. monocytogenes strains (with 70 C/2 min process) and spores
are also needed for understanding the efficacy of the agitating
process at higher temperature ranges. Last but not the least,
154
M.B. Ates et al. / Food Control 43 (2014) 150e154
Fig. 5. Inactivation of L. innocua exposed to static heating mode at 62 C (a), 65 C (b)
and 68 C (c). Black bars: inactivation data (log10) obtained from TSA-YE plates, gray
bars show data from Brilliance plates; and white bars with dots show mathematically
calculated log inactivation based on lowest core temperature data. Data are means
from six replicate samples. Error bars represent standard deviation of each mean value.
Retort cooling times were 7 and 18 min for agitating and static modes (not shown).
samples should be checked for recovery risk of Listeria during a
refrigerated storage test.
Acknowledgments
Mehmet Baris Ates gratefully acknowledge his Ph.D. stipend
from Norconserv Foundation. We thank the Research Council of
Norway for their financial support through grant nr 210427.
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