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International Journal of Food Microbiology 97 (2005) 307 – 315

www.elsevier.com/locate/ijfoodmicro

Water activity affects heat resistance of microorganisms


in food powders
C. Laroche a, F. Fine a,b, P. Gervais a,*
a
Laboratoire de Génie des Procédés Alimentaires et Biotechnologiques, E.N.S.B.A.N.A., 1, Esplanade Erasme, 21000 Dijon, France
b
Unilever Bestfoods France, Amora-Maille, 48 quai Nicolas Rolin, 21000 Dijon, France
Received 23 July 2003; received in revised form 24 October 2003; accepted 27 April 2004

Abstract

To study the factors and mechanisms involved in microorganisms’ death or resistance to temperature in low-water-activity
environments, a previous work dealt with the viability of dried microorganisms immobilized in thin-layer on glass beads. This
work is intended to check the efficiency of a rapid heating – cooling treatment to destroy microorganisms that were dried after
mixing with wheat flour or skim milk. The thermoresistance of the yeast Saccharomyces cerevisiae and the bacterium
Lactobacillus plantarum were studied. Heat stress was applied at two temperatures (150 or 200 jC) for treatments of one of four
durations (5, 10, 20, or 30 s) and at seven levels of initial water activity (aw) in the range 0.10 to 0.70. This new treatment
achieved a microbial destruction of eight log reductions. A specific initial water activity was defined for each strain at which it
was most resistant to heat treatments. On wheat flour, this initial aw value was in the range 0.30 – 0.50, with maximal viability
value at aw = 0.35 for L. plantarum, whatever the temperature studied, and 0.40 for S. cerevisiae. For skim milk, a variation in
microbial viability was observed, with optimal resistance in the range 0.30 – 0.50 for S. cerevisiae and 0.20 – 0.50 for L.
plantarum, with minimal destruction at aw = 0.30 whatever the heating temperature is.
D 2004 Elsevier B.V All rights reserved.

Keywords: Heat; Water activity; Vegetative cells; HTST process

1. Introduction foods prefer to choose other technologies. Most de-


contamination processes involve heating, but these
Processes used for the decontamination of dried treatments induce severe damage to the products via
products, such as steam, microwaves, or Joule-effect the Maillard reaction (Fine and Gervais, 2003). To
treatments, often induce organoleptic degradation or limit this degradation, the use of very high temper-
achieve only a low destruction rate. Faced with the atures over short periods, followed by rapid cooling,
psychological barrier to and labeling obligations of has been patented in our laboratory (Gervais et al.,
irradiation technology, suppliers of dried powdered 2002).
The decontamination of food powders is difficult,
and the difficulty correlates with the presence of a
* Corresponding author. Tel.: +33-3-80-39-66-99; fax: +33-3-
specific microflora adapted to low water contents.
80-39-68-98. Both vegetative cells and spores are found in dried
E-mail address: gervais@u-bourgogne.fr (P. Gervais). products (Fine and Gervais, 2003).

0168-1605/$ - see front matter D 2004 Elsevier B.V All rights reserved.
doi:10.1016/j.ijfoodmicro.2004.04.023
308 C. Laroche et al. / International Journal of Food Microbiology 97 (2005) 307–315

Several authors have studied the destruction of temperatures close to 110 – 120 jC for Bacillus
microorganisms by heat, sometimes in conditions of coagulans, Bacillus stearothermophilus, and C. bot-
low water activity (Riemann, 1968; Van Cauwenberge ulinum spores. Similar results were reported by
et al., 1981; Kirby and Davies, 1990; Archer et al., Angelotti et al. (1968) for Bacillus subtilis spores.
1998). However, most of these studies were performed In contrast, Corry (1975) noted that the thermal
in liquid media using solutes to depress the water resistance of bacterial vegetative forms, notably Sal-
activity (Gibson, 1973; Sumner et al., 1991; Chiruta, monella typhimurium, is maximal for aw in the range
1997; Manas et al., 2001). Particular attention has been 0 –0.2 at temperatures in the range 125 –160 jC,
paid to spore-forming organisms, rather than nonspore- above which thermal resistance decreased with in-
forming species (Murrel and Scott, 1966; Angelotti et creasing water activity.
al., 1968; Lubieniecki et al., 1975; Mazas et al., 1999) The aim of this study was to test a new process for
because of their greater resistance to heat stresses, and decontaminating powders and to show the factors and
also to foodborne pathogens such as Listeria mono- mechanisms involved in microorganisms’ death and
cytogenes (Linton et al., 1996) and Escherichia coli resistance to heat when placed in a low-water-activity
O157:H7 (Dock et al., 2000). powder. Two microorganisms were chosen: the yeast
Murrel and Scott (1966) reported that thermal resis- Saccharomyces cerevisiae and the bacterium Lacto-
tance of spores and vegetative cells is more important bacillus plantarum. These microorganisms do not
in dry than in liquid media; for microorganisms such as produce sporulated forms and always remain in a
Clostridium botulinum type E and Bacillus megate- vegetative form. These microorganisms were mixed
rium, there was a substantial decrease in decimal and then dried alive with milk or wheat– flour pow-
reduction time at 110 jC as the aw value approached ders, to study the effects of further heat treatment and
1.00. It is well known that the availability of water has a to compare the influences of this treatment on two
pronounced influence on heat resistance in microor- dried powdered food supports.
ganisms, and that the resistance of dried microorgan-
isms is many times higher than the resistance of the
same microorganisms in an aqueous solution. There is, 2. Materials and methods
however, very little information about the resistance of
vegetative cells as a function of water activity. Our 2.1. Strains and cultivation conditions
work is therefore intended to study the effect of
temperature on the viability of dried vegetative cells, Two microorganisms were used in this study:
with specific attention to the influence of water activity.
Moreover, water availability has also a great impact on – S. cerevisiae strain CBS 1171 cells were maintained
the transfer of heat to microorganisms. on Petri dishes with modified malt Wickerham
The influence of water activity on microorganisms medium, supplemented with 20 g/l agar (VWR
is complex, combining intrinsic factors (nutritive International, France). The yeast were grown
potential, pH, and antimicrobial compounds like aerobically, as previously described (Gervais and
SO2, nitrates, and nitrites) and extrinsic factors Martı́nez de Marañon, 1995), in 250-ml conical
(temperature, oxygen, chemical treatments, and irra- flasks containing 100 ml modified malt Wickerham
diation), which vary as a function of the kinds of medium, made up of 10 g/l glucose (VWR
foods and microorganisms. Studies have shown that International), 3 g/l pancreatic peptone (VWR
the heat resistance of microorganisms increases as International), 3 g/l yeast extract (Institut Pasteur,
their water content decreases (Brown and Melling, France), and 1.5 g/l NaH2PO4 (VWR International).
1971; Corry, 1973; Daemen, 1981; Bera et al., 1988), The pH was adjusted to 5.35 by the addition of
and that an optimum level of resistance occurs orthophosphoric acid (Sigma, France), before
between aw = 0.20 and 0.50, depending on the mi- sterilization by autoclaving at 121 jC for 20 min.
croorganism studied. Murrel and Scott (1966) have The flasks were shaken at 250 rpm on a rotary
shown that decimal reduction time (D) reaches a shaker (New Brunswick Scientific, USA) at 25 jC
maximum for water activities in the range 0.2 –0.4 at for 48 h. An aliquot (1 ml) of culture was
C. Laroche et al. / International Journal of Food Microbiology 97 (2005) 307–315 309

transferred into a conical flask containing the same 2.4. Thermal-stress treatment
medium and was allowed to grow to early
stationary phase at 25 jC for 48 h, to a final The dried samples were heated by blowing them
concentration of 1  109 cells/ml. with hot air (at 150 or 200 jC) from a hot-air
– L. plantarum strain 103151 T cells (Institut Pasteur generator (Vulcanic, France) for a short time (5, 10,
Collection) were maintained on Petri dishes with 20, or 30 s) and immediately cooled with a cold gas
MRS medium (Biokar Diagnostics, France) supple- (released CO2, 70 jC). To do this, samples were
mented with 20 g/l agar (VWR International). The placed in a spherical metallic grid, which could retain
bacteria were grown in 250-ml conical flasks powder particles of more than 0.5 mm in diameter.
containing 100 ml MRS medium at 30 jC for The sphere, held with pliers, was placed under the hot
18h without shaking. An aliquot (1 ml) of culture air flow and shaken slightly to distribute the particles
was transferred into a conical flask containing the homogeneously. After a residence time, the sphere
same medium and was allowed to grow to early was instantaneously placed under the 70 jC CO2
stationary phase at 30 jC for 20 h, to a final flow to cool. The temperature of the sample was
concentration of 1  109 cells/ml. followed during each experiment using a thermocou-
ple in the center of the sphere in contact with the
2.2. Drying of microorganisms on powders powders. Temperature data were recorded with an
acquisition card system linked to a computer. Tem-
Cultures of microorganisms in early stationary perature acquisition was recorded at increments of
phase were harvested (2000  g, 5 min), and cells 3.34 ms. From these data, heating and cooling rates
were washed twice in a binary water/glycerol solution, could be calculated and were found to be around 50
at a water activity of 0.992. The pellet was mixed with and 75 jC/s, respectively (Gervais et al., 2002).
30 g of flour or skim milk powder in a mortar to
produce granules with a diameter in the range 0.8 – 3.2 2.5. Viability measurements
mms. We used a drying method that has been devel-
oped and patented in our laboratory. This method After heating, 1 g of the treated powder was mixed
allows us to achieve a very high level of viability with 9 g of water/glycerol solution (water activi-
after rehydration (Gervais et al., 1994). The mixture ty = 0.992) and shaken for 30 min to reconstitute the
was then dried in a fluidized bed (Retsch, Germany) cellular suspension. Decimal dilutions were per-
located in a type 320H60/1.5 climatic chamber (Cli- formed and spread on malt Wickerham-agar medium
mats-Sapratin, France) coupled to a type MLC450 air- (for S. cerevisiae) or MRS-agar (for L. plantarum).
dryer (Munters, France) for a specific time that Viability was determined by counting colony-forming
depended on the water activity to be reached. A units (CFU) and related to the viability of the controls,
temperature of 5 jC and a relative humidity of 1% which were samples that had been dried to the same
were maintained in the chamber during drying. After water activity but not heated. Experiments were
drying, the samples were stored in aluminum bags performed at least three times, and mean values were
sealed under vacuum to prevent rehydration. calculated as well as 95% confidence intervals (CI) for
the means.
2.3. Water activity

Experiments were performed at various initial 3. Results


water activities (aw = 0.10, 0.20, 0.30, 0.40, 0.50,
0.60, or 0.70). During drying, changes in the water 3.1. Viability after drying
activity of the samples were monitored to determine
the duration of drying necessary in each case. The The aim of the first set of experiments was to
water activity of solutions and samples was checked produce dried and viable microorganisms in the two
using a dew-point osmometer (Decagon Devices, types of powders in sufficient quantities to use in heat-
USA) before and after heat-stress treatment. destruction experiments. For the two types of micro-
310 C. Laroche et al. / International Journal of Food Microbiology 97 (2005) 307–315

organisms, cell suspensions were mixed with wheat 3.2. Viability after heat stress
flour or skim milk at a concentration of about 6  108
cells per gram of dry matter. The aw variations during The experiments were performed at least three
drying are presented in Table 1. Mixing the micro- times, and mean values were calculated as well as
organisms with the powders induced a decrease in 95% confidence intervals (CIs) of the means. These
water activity to 0.89 for the milk and 0.96 for the CIs were found to be less than 15% of the mean
wheat flour. During drying, the viability of S. cerevi- viability.
siae decreased more rapidly than that of L. plantarum
in skim milk powder indicating a lower resistance of 3.2.1. Influence of time and temperature on treatment
the yeast to this kind of drying. The reverse phenom- Microorganisms dried in skim milk and wheat
enon was observed during wheat flour drying. Water flour were submitted to heat destruction experiments.
activity decreased rapidly during the first 30 min and Two temperatures (150 or 200 jC) and four treatment
more slowly in the second part of the drying period. durations (5, 10, 20, or 30 s of hot treatment followed
After 10 min, water activity was around 0.62 for the by 10 s of cold treatment) were tested. The temper-
two powders, and cellular concentration was 3.0  108 atures were clearly higher and the durations shorter
cells/g (on flour) and 2.3  108 cells/g (on milk) for S. than those of existing processes. Figs. 1 and 2
cerevisiae, and 2.5  108 cells/g (on flour) and describe the influence of heating temperature and
3.1  108 cells/g (on milk) for L. plantarum. After heating time on decontamination efficiency.
20 min of drying, the cellular concentration of the L. For all heating times and both strains, the higher
plantarum – milk mixture reached 1.3  108 cells/g the heating temperature, the greater was the destruc-
and did not vary further as a function of drying time, tion recorded. For each specific temperature and water
whereas the water activity of the powders continued to activity of the treated sample, a longer treatment time
decrease slowly. For the S. cerevisiae– milk mixture, achieved better destruction.
the cellular concentration was about 1.4  108 cells/g With this high-temperature short-time (HTST)
but continued to decrease for 10 min more before technology, an eight-log reduction of microbes could
stabilizing at around 2.5  107 cells/g. The reverse be achieved for wheat flour and skim milk, depending
phenomenon was observed with the flour, and S. on the time, the temperature, and the water activity,
cerevisiae appeared to maintain higher viability on while maintaining the organoleptic qualities of these
wheat flour, whereas L. plantarum better resisted products.
drying on skim milk. One hour of drying allowed
150 g of both mixtures to reach a water activity of 3.2.2. Influence of water activity level
0.04 for wheat flour and 0.06 for skim milk, with a
cellular concentration about 107 – 108 cells/g of mix- 3.2.2.1. Water activity evolution during heat
ture. This concentration was found to be sufficient to stress. The water activity of samples was determined
perform heat-stress experiments. before and after heat-stress treatments. The aw loss

Table 1
Number of cells per gram and water activity as a function of drying time
Drying Flour Milk
time (min)
Number of cells per gram Water Number of cells per gram Water
activity activity
L. plantarum S. cerevisiae L. plantarum S. cerevisiae
0 6.75  108 6.00  108 0.959 6.00  108 5.82  108 0.896
10 2.47  108 2.97  108 0.633 3.07  108 2.27  108 0.616
20 1.37  108 1.31  108 0.253 1.31  108 1.34  108 0.330
30 3.53  107 1.07  108 0.113 1.02  108 4.05  107 0.203
40 2.03  107 1.21  108 0.068 1.10  108 2.09  107 0.114
50 2.48  107 1.35  108 0.050 1.19  108 3.01  107 0.071
60 2.12  107 1.28  108 0.045 1.25  108 2.40  107 0.062
C. Laroche et al. / International Journal of Food Microbiology 97 (2005) 307–315 311

Fig. 1. Destruction of L. plantarum (a and c) and S. cerevisiae (b and d) dried on wheat flour at 150 jC (a and b) and 200 jC (c and d). Heating
times: ( )5 s, ( ) 10 s, ( ) 20 s, and ( ) 30 s.

during heating was not significantly influenced by the duration, but not of the initial water activity. There-
initial water activity and was clearly dependant on fore, we have chosen to represent cell mortality as a
temperature and duration of treatment. The average aw function of initial water activity, but the same kinds of
loss was calculated for each temperature and duration
of treatment, with associated confidence intervals of Table 2
the mean at the 95% level. These values are given in Average values for water activity loss as a function of temperature
Table 2 for flour samples. The results for milk samples and heating time for flour samples
have been omitted, because they were very close to Temperature (jC) Heating time (s) aw loss CI (95%)
the values for flour. For low initial aw level, the final 150 5 0.020 F 0.008
aw could not be determined as operating limitations 10 0.054 F 0.008
(aw < 0.05). 20 0.087 F 0.004
30 0.109 F 0.007
Measures of water activity of the samples after
200 5 0.057 F 0.008
treatment show that the evaporation of water can 10 0.099 F 0.003
induce a water activity loss of up to 0.152 for a 20 0.124 F 0.009
treatment of 30 s at 200 jC. This change in water 30 0.152 F 0.010
activity is a function of temperature and treatment CI (95%): confidence intervals of the means at 95% level.
312 C. Laroche et al. / International Journal of Food Microbiology 97 (2005) 307–315

curves could have been drawn as function of final water activity of 0.60, viability remained one to
water activity, although with slightly lower aw values. three log below that achieved at aw = 0.50. At
aw = 0.70, viability was similar or slightly less than
3.2.2.2. Viability. The viability results for L. planta- that achieved at aw = 0.60. Nevertheless, the lowest
rum and S. cerevisiae, in terms of initial water activity, viability occurred under conditions of low initial
at the four heating times and two temperatures are water activity (aw = 0.10).
shown in Figs. 1 and 2. The same phenomenon was observed for S. cer-
Unlike our observations of L. plantarum immo- evisiae with optimal heat resistance recorded for an
bilized on glass beads (Laroche and Gervais, 2003a), initial water activity value of 0.30 – 0.50. Lower
viability did not remain high and constant for all viability levels were observed for water activity levels
heating temperatures at a water activity of 0.30. of 0.10 and 0.70. When S. cerevisiae was mixed with
However, this initial water activity value corre- wheat flour, at 150 or 200 jC, viability was higher at
sponds to the optimal thermoresistance level of this aw = 0.30 –0.50 with maximal viability near aw = 0.50.
strain, both when mixed with flour or milk. For L. On the other hand, the viability of S. cerevisiae in
plantarum, in all cases, higher viability was ob- skim milk was always higher, in the range 0.30– 0.50,
served with a water activity close to 0.30. At a whatever the temperature tested, but this optimum

Fig. 2. Destruction of L. plantarum (a and c) and S. cerevisiae (b and d) dried on skim milk at 150 jC (a and b) and 200 jC (c and d). Heating
times: ( ) 5 s, ( ) 10 s, ( ) 20 s, and ( ) 30 s.
C. Laroche et al. / International Journal of Food Microbiology 97 (2005) 307–315 313

remained less marked than for L. plantarum and siae. During drying, the cells have suffered many
closer to aw = 0.40. stresses (thermal, hydric, and ionic) and may have
Comparing strains, the viability of S. cerevisiae developed adaptation mechanisms, notably trehalose
was always lower than the viability of L. plantarum or heat-shock protein accumulation (Crowe et al.,
for water activities of 0.10 and 0.30, and for heating at 1984; Mager and Moradas-Ferreira, 1993; Siderius
200 jC, whereas at 150 jC, the destruction of S. and Mager, 1997), which could involve an increase
cerevisiae was similar to or slightly greater than that in yeast and bacterial thermotolerance (Trollmo et
of L. plantarum. At a water activity of 0.40, the al., 1988; Agab and Collins, 1992; Jørgensen et al.,
viability of S. cerevisiae was similar to or lower than 1995). Hence, compared with liquid products, higher
that of L. plantarum, but the trend was reversed for temperatures would be required to decontaminate
water activities of 0.50, 0.60, and 0.70, where the efficiently food powders.
viability of S. cerevisiae was similar to or higher than The results show that efficient microbial destruc-
that of L. plantarum. tion can be achieved with the HTST treatment devel-
oped (seven to eight log reductions), whereas
3.2.3. Influence of the dry medium destruction achieved with microwave or steam treat-
In Figs. 1 and 2, the results showed that L. ments that are usually used on an industrial scale are
plantarum was more thermoresistant on skim milk limited to two to four log reductions (Tisne, 1999;
than on wheat, especially for the long treatment times. Richard, 2000). However, marked variation in cell
Indeed, for 30 s of treatment at 150 jC and aw = 0.10, viability after heat treatment was observed as a
the destruction reached eight log in wheat flour, but function of initial water activity level, temperature,
only four log in skim milk. The reverse phenomenon treatment duration, and cell type. The viability of both
was observed for S. cerevisiae; under the same con- microorganisms was lower with longer treatment at
ditions, only 10 cells per gram of dry matter remained the two temperatures tested and with increased tem-
in skim milk, whereas 10,000 cells per gram of dry perature. Furthermore, for each strain, an initial water
flour were counted in flour. activity range (aw f 0.3 – 0.4) was noted over which
microorganisms are more resistant. Results also
showed that L. plantarum was more sensitive to
4. Discussion drying and heat treatment on wheat flour than on
skim milk. For S. cerevisiae, the reverse phenomenon
Experiments previously carried out in this labo- was recorded.
ratory have shown that heat destruction of micro- In relation to a previous study on glass beads
organisms in liquid medium depends strongly on (Laroche and Gervais, 2003a), microbial destruction
temperature and water activity (Martinez de Marañon was slightly lower. Microorganisms were distributed
et al., 1999). The temperature, at which the osmotic in thin-layer on glass beads, whereas powders par-
stress is applied, is also very important in the ticles were homogeneously contaminated. Conse-
prevention of cell death (Gervais and Marechal, quently, powder granulometry greatly affects
1994; Marechal et al., 1999), as are the kinetics of microbial destruction. Hence, when the time neces-
dehydration and rehydration (Laroche et al., 2001; sary for heat diffusion into the particles increased, the
Mille et al., 2002; Laroche and Gervais, 2003b). cells were exposed to less heat, and further time or a
However, for all those experiments, the cells were in higher temperature was required to achieve the same
a liquid medium. In this study, low water activity of decontamination level. Moreover, the lower destruc-
the microbial extract is achieved by drying process tion recorded in food powders could be also correlated
which led to skim milk and wheat flour powders with the nutrients available in the flour and skim milk
obtaining with high drying yields: dried wheat flour with which organisms could prevent the damage
had a microbial content of 2.1.107 CFU/g for L. caused by the drying process.
plantarum and 1.3.108 CFU/g for S. cerevisiae; dried The effects of heat stress are thought to result from
skim milk had a microbial content of 1.2.108 CFU/g the damage to proteins and the permeabilization
for L. plantarum and 2.4.107 CFU/g for S. cerevi- of membranes, particularly the plasma membrane
314 C. Laroche et al. / International Journal of Food Microbiology 97 (2005) 307–315

(Weitzel et al., 1987; Piper, 1993). A previous work of the product. Because color is a good indicator of
has shown that the death of yeast subjected to a heat degradation due to the Maillard reaction, it should be
shock might be related to the loss of membrane interesting to measure the colors of food samples,
integrity (Martinez de Marañon et al., 1999); when such as flour or dried milk, after treatment and to
temperature exceeded the physiological range, the determine the time – temperature combinations that
plasma membranes became ‘‘hyperfluid’’ and desta- allow a large decrease in microbial contamination
bilization of the lamellar phase occurred, producing a but the maintenance of the visual and functional
drastic leakage of ions from the cells and a rapid cell properties of the product.
death. It has been also postulated that the water that is
in close contact with proteins could be a factor
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