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Food Control 47 (2015) 1e6

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Survival of Salmonella enteric in skim milk powder with different


water activity and water mobility
Feng Lian a, Wei Zhao a, *, Rui-jin Yang a, Yali Tang b, Wendy Katiyo a
a
State Key Laboratory of Food Science & Technology, School of Food Science and Technology, Jiangnan University, No. 1800 Lihu Road, Wuxi 214122, China
b
School of Mechanical Engineering, Department of Packaging Engineering, Jiangnan University, No. 1800 Lihu Road, Wuxi 214122, China

a r t i c l e i n f o a b s t r a c t

Article history: Recently, the safety of low water activity (aw) foods started to become a major concern. It has been
Received 8 March 2014 observed that microorganisms may not grow in low-aw foods but can survive for rather long periods of
Received in revised form time, representing signicant risk. Most researchers have been concentrating on the role of water ac-
10 June 2014
tivity. However, little is known about the effect of water mobility on inuencing the survival of Salmo-
Accepted 17 June 2014
Available online 25 June 2014
nella in low-aw foods. In this study, water mobility of skim milk powder was manipulated using ultra-
high pressure to change tertiary structure, thus changing watereprotein interactions. Skim milk pow-
der with different levels of water mobility at similar aw level were obtained to evaluate how aw and water
Keywords:
Low-water activity foods
mobility inuenced the survival of Salmonella enteric in low-aw foods. Results showed that aw could
Water activity inuence the survival of S. enteric and the lower the aw, the higher the survival. Water mobility had little
Water mobility inuence on the survival of S. enteric when aw was 0.33 and 0.53. However, it inuenced its survival
when aw was increased to 0.81. The survival population of S. enteric was higher in the sample with low
water mobility.
2014 Elsevier Ltd. All rights reserved.

1. Introduction contamination continues, even in large multi-national companies


that employ experienced food microbiologists and risk managers.
Low-water activity foods are those with water activity (aw) It is known that aw is one of the basic properties of a food that
levels lower than 0.85 (Beuchat et al., 2013). Low-aw foods include exerts major inuence on microbial survival and growth (Beuchat
milk powder, egg powder, chocolate, peanut butter and so on. They et al., 2013; Farakos et al., 2013; Laroche, Fine, & Gervais, 2005).
are usually believed to have the advantages of controlling the Some research has been conducted in this aspect, but the conclu-
growth of pathogenic and spoilage microorganisms. Hence, their sions about the inuence of aw on microbial survival in low-aw
microbial safety is usually ignored by the public. Recently, a num- foods by different groups are inconsistent. Jung and Beuchat (1999)
ber of outbreaks associated with low-aw foods and pathogens concluded that Salmonella died more rapidly in higher aw egg white
occurred, resulting in the safety of these foods becoming a major powder than in lower aw powder. However, Mattick et al., (2001)
concern (Awuah, Ramaswamy, Economides, & Mallikarjunan, observed that the relationship between microbial survival and aw
2005; Beuchat et al., 2013; CDC, 2007; Farakos, Frank, & may change at different temperatures (Mattick et al., 2001). Their
Schaffner, 2013; Finstad, O'Bryan, Marcy, Crandall, & Ricke, 2012; study demonstrated that Salmonella at low aw (0.65) was more heat
Koch et al., 2005). The contamination of low-aw foods with Sal- tolerant at temperatures above 70  C than when at higher aw (0.90),
monella is not an unknown problem. It has been observed that but the reverse was true at lower temperatures. Laroche et al.,
foodborne pathogens may not grow in low-aw foods but can survive (2005) used Saccharomyces cerevisiae and Lactobacillus plantarum
for rather long periods of time once the food is contaminated, thus as test organisms. The microorganisms exhibited different survival
representing signicant risk even at low levels. However, current ability in the low-aw foods (wheat our and skim milk) when they
practices appear inadequate to address this challenge, as were adjusted to the same water activity. There was a range of aw
for greatest heat resistance for each microorganism and low-aw
food across all temperatures. Moreover, some researchers (Hills,
Manning, Ridge, & Brocklehurst, 1997) indicated that the molecu-
* Corresponding author. Tel./fax: 86 510 85919150.
E-mail addresses: zhaow@jiangnan.edu.cn (W. Zhao), ruijinyang@yahoo.com.cn
lar mobility of water in low-aw foods is an important factor in
(R.-j. Yang). microbial survival. Microbial survival in low-aw foods did not

http://dx.doi.org/10.1016/j.foodcont.2014.06.036
0956-7135/ 2014 Elsevier Ltd. All rights reserved.
2 F. Lian et al. / Food Control 47 (2015) 1e6

correlate to water activity, but did correlate to molecular mobility further change in weight. The aw of samples was measured using a
of the water. Vittadini, Chinachoti, Lavoie, and Pham (2005) pro- water activity meter (Hygrolab2, Rotronic, Switzerland).
vided evidence that microbial behavior was more closely associated
with molecular mobility in low-aw foods and aw provided good 2.3. Water mobility determination
predictions of microbial behavior only in high-aw foods. A recent
study (Farakos et al., 2013) determined and discussed how the A low-eld 1H Nuclear Magnetic Resonance analyzer (MicroMR-
physical state of water in low-aw foods inuences the survival of CL, Niumag Corporation, Shanghai, China) with a resonance fre-
Salmonella, employing whey protein powder with different water quency of 21.798 MHz and 0.55 T magnetic eld was used for
mobility at similar aw levels by pH adjustment and heat denatur- measurements of proton transversal relaxation time (T2). The
ation. The results demonstrated that aw signicantly inuenced the transversal relaxation time was measured with a
survival of Salmonella at all temperatures, survival increasing with CarrePurcelleMeiboomeGill (CPMG) pulse sequence. The experi-
decreasing aw. Water mobility did not signicantly inuence sur- mental parameters were as follows: the 90  pulse width was 3 ms,
vival independent of aw. In their study, the water mobility of whey the 180  pulse width was 7 ms, the Number of Scans (NS) was 16,
protein powder was manipulated using pH adjustments to change the Receiver Gain (RG) was set to 20 dB, the echo time (TE) was
the tertiary structure, thus changing watereprotein interactions. In 80 ms and the echo number was set to 1000. The values of T21
this way, the solutes for the low-aw foods with different water relaxation time were recorded.
mobility at similar aw levels are difcult to keep the same. It has
been evidenced that use of different solutes to achieve similar 2.4. Procedure for inoculating milk powder for storage experiments
water activities produces markedly different microbial survival
kinetics (Mattick et al., 2001). Salmonella enteric (JFM-125) isolated from powdered infant
In low-aw foods, most of the water is in glassy and rubbery states formula was a gift from Food Biotechnology Center of Jiangnan
so the water has limited mobility. Since water molecules must University. The cultures were maintained at 4  C on LuriaeBertani
contact the bacterial cell for interaction, the ease of transition be- (LB) ager and activated by transferring a loop of inocula into 150 mL
tween physical states, i.e. molecular mobility, should indicate the nutrient broth and cultured for 14 h at 37  C. Cultures were har-
potential for interaction between bacterial cells and water. In the vested by centrifugation (9000 rpm, 5 min), and pellets were
present work, water mobility of skim milk powder was manipu- washed twice in 150 mL of sterile 0.1% peptone water. Finally, the
lated using ultra-high pressure to change the tertiary structure of pellets were re-suspended in 3 mL sterile 0.1% peptone water. The
protein, thus changing watereprotein interactions. Skim milk suspension was poured into a sterile Petri dish and put in a desic-
powder, with different water mobility at similar aw levels and other cator for 3 days to ensure aw of below 0.10. The dried cells were
conditions (such as solutes), was obtained to evaluate how aw and ground with a mortar and pestle. The dried inoculum (0.01 g) was
water mobility inuence the survival of Salmonella in low-aw foods. mixed with 0.99 g of equilibrated skim milk powder to provide a
1.00 g sample in a polypropylene vial. It was assumed that the
2. Materials and methods addition of inoculum did not inuence aw of the milk powder
because the dose was too small to be signicant. The samples were
2.1. Modication of skim milk powder placed in retort pouches, then vacuum packaged. The vacuum
packaged samples were stored in desiccators at their corresponding
The water mobility of skim milk powder (Bright dairy corpora- relative humidity in an incubator at 37  C. The samples were taken
tion, China) was manipulated using ultra-high pressure adjust- at: 0, 3, 6, 12, 30 and 60 days for survival experiments.
ments to change the secondary and tertiary structure of protein,
thus changing watereprotein interactions. Skim milk powder 2.5. Enumeration of cultivable Salmonella
(500 g) and water (500 mL) were made into a solution. The solution
was then transferred into polyethylene bags and a vacuum sealer The plate count method was adopted to enumerate Salmonella
(A300/16, Multiuac, Germany) was used to remove most of the air. populations. Each inoculated sample (1.00 g) was assayed for
The sealed samples were stored overnight at 4  C. Ultra-high population of Salmonella at selected time intervals. All samples
pressure treatments were performed by ultra-high pressure were respectively dissolved in 9 mL sterile saline and homogenized
equipment (UHPF-800MPa-5L, Baotou Kefa Co., China) for 10 min at for 1 min with a vortex (Lab Dancer, IKA, Germany). After homog-
approximately 25  C. The temperature of the vessel was kept at enization, 1 mL dissolved sample was serially diluted using sterile
room temperature. The compression and decompression rate was test tubes containing 9 mL sterile saline to obtain the appropriate
25 MPa/s. The samples were treated at 100, 200, 300, 400 or degree of dilution. Then 1 mL appropriate dilution was transferred
500 MPa. The control sample was hydrated overnight at 4  C but to a Petri dish, and soon afterwards approximately 15 mL nutrient
was not treated by ultra-high pressure. After treatment, samples ager, with the temperature about 46  C, was added. When the
were then poured into sterile Petri dishes and frozen to 80  C nutrient agar (Sinopharm Chemical Reagent, China) solidied, the
overnight in a freezer (HFU 586 Basic, Thermal Scientic, Germany). petri dishes were inverted and placed in an incubator. The plates
The samples were then placed in a vacuum freeze drier (7948030, were enumerated after incubation at 37  C for 24 h.
Labconco, US) for 3 days to obtain aw levels below 0.10. Once freeze
dried, the samples were broken down to homogenous particles 2.6. Statistical analysis and curve tting
with a mortar and pestle.
Cultivability of S. enteric for each combination of water activity
2.2. Adjustment of the aw of re-dried samples and water mobility was performed. Each experiment was carried
out at least in triplicate. Data was analyzed in Microsoft Excel 2010
Re-dried samples were adjusted to the targeted aw values in (Microsoft Corporation, US). Initial data (CFU/g) was converted into
vacuum desiccators containing various saturated salt solutions of log of the survival of S. enteric at a given time. Comparison was
known relative vapor pressures. The targeted aw levels were: 0.33 made by SPSS software. Curves were tted using the Curve Expert
(Magnesium Chloride), 0.53 (Magnesium Nitrate) and 0.81 software (Version 1.3). This software contained 60 models. The
(ammonium sulfate). Equilibrium was assumed when there was no most appropriate model was chosen to describe the curves.
F. Lian et al. / Food Control 47 (2015) 1e6 3

3. Results and discussion

3.1. The survival of S. enteric inuenced by water activity

The viability results for S. enteric in skim milk powder at three


levels of aw at 37  C are shown in Fig. 1. After adjusting to the tar-
geted aw and inoculating with S. enteric, the initial populations
were 9.90, 10.01 and 10.19 logs, in samples with aw of 0.33, 0.53 and
0.81, respectively. A reduction of about 3.96 logs occurred within
the rst month of storage, and about 0.27 logs in the second month
at aw 0.33. At aw 0.53, the reduction population during the rst
month was 3.89 logs, and it was similar to that at aw 0.33. Reduction
during the second month was 0.8 logs, and this was signicantly
higher than at aw 0.33 (p < 0.05). Reduction populations at aw of
0.81 were 4.69 and 1.16 logs, respectively. They were both signi-
cantly higher than that at aw 0.33 and 0.53 (p < 0.05). This indicates
that the death rate during the rst month was higher than the
second, at the three aw of skim milk powder. This phenomenon is in
agreement with observations by Licari and Potter (1970). These
researchers reported that Salmonella in skim milk powder died in a
two-stage process: rapid death during the rst several weeks fol-
lowed by slow death during the remaining shelf life. After storage
for two months, the reduction populations were 4.23, 4.69 and
5.85 logs at aw levels of 0.33, 0.53 and 0.81, respectively. This is
similar with the results of Jung and Beuchat (1999), who reported
that after storage of two months at 37  C, log populations in all the
samples were less than 1.00 log with an initial population of about
5.00 logs. It also indicates that survival is enhanced as the aw of
skim milk powder decreases. Vesterlund, Salminen, and Salminen
(2012) studied the effect of aw on the storage stability of pro-
biotics included in crushed axseed to identify the right aw level for
storage at room temperature. They observed that at the highest aw
tested (0.43), the probiotic product was unstable. Within 4 months
of storage, the reduction of viable cells was 3.70, 0.81 and 0.29 logs
at aw of 0.43, 0.22 and 0.11, respectively, demonstrating that lower
aw is more suitable for the survival of microorganisms in dried
foods.

3.2. Preparation of samples with different water mobility by ultra-


high pressure

Ultra-high pressure is classied as non-thermal processing


technique, using the uid medium (water or oil) for transmitting
pressure. Proteins or complex biopolymers subjected to ultra-high

Fig. 2. Continuous relaxation time spectra of samples at three aw and six water
mobility (water mobility 1: control, water mobility 2: protein denatured at 100 MPa,
water mobility 3: protein denatured at 200 MPa, water mobility 4: protein denatured
at 300 MPa, water mobility 5: protein denatured at 400 MPa, water mobility 5: protein
denatured at 500 MPa).

Fig. 1. Viability of S. enteric at 37  C and 3 water activities (aw) during 2 months of


storage in skim milk powder.
4 F. Lian et al. / Food Control 47 (2015) 1e6

pressure may have their tertiary and secondary structures modied


by disrupting hydrophobic and electrostatic interactions (Molina,
Papadopoulou, & Ledward, 2001). It has been widely used in the
modication of proteins. In this study, water mobility of skim milk
powder was manipulated using ultra-high pressure to change the
tertiary structure of proteins, thus changing watereprotein in-
teractions, that is water mobility. Skim milk powder with different
water mobility at similar aw levels and other conditions (such as
solutes) were obtained to evaluate the inuence of aw and water
mobility on the survival of Salmonella in low-aw foods.
LF 1H NMR has been used to investigate water mobility in ma-
terials and foods (Choi & Kerr, 2003; Fan et al., 2013). LF 1H NMR can
measure proton relaxation, thus can be used to study changes in
water mobility (Carneiro et al., 2013). Continuously distributed
exponential curve tting was performed on the obtained T2 relax-
ation time from samples. Dependence of the nature of skim milk
powder, the faster relaxation component which ranges from 0 to
10 ms in the following is called T21. In the present study, T21 rep-
resents the water which is closely associated with macromolecules
and microbial cells (Li et al., 2012). Fig. 2 shows the distributed T2
relaxation time spectra of skim milk powder submitted to different
treatments with ultra-high pressure. Table 1 shows the values of T21
detected by LF 1H NMR according to the different treatments of
skim milk powder. Comparison of the continuous distributed
curves, at three aw levels of 0.33, 0.53 and 0.81, reveals visible
differences between the treated skim milk powder and the control.
The treated samples mostly tended to exhibit a broader T21 distri-
bution than the control, which is likely due to the differences in
water distribution caused by ultra-high pressure. Fig. 2 shows
signicant differences in the distribution of water mobility be-
tween different treated samples. As shown in Fig. 2(a), a signicant
increase (p < 0.05) in relaxation time (T21) was observed in the
samples treated with pressure of 100, 200, 300 and 400 MPa. The
T21 distribution of the sample treated with 500 MPa pressure was
broader than the control. However, it was narrower than the rest of
the samples. This phenomena indicates that pressure ranging from
100 to 500 MPa affects the T21 distribution at aw 0.33. As shown in
Fig. 2(b), the curve of the sample at aw 0.53 is similar to that at aw

Table 1
Range of the LF 1H NMR obtained in skim milk powder, according to the different
treatments.

aw Water mobility T21 (ms)


a
0.33 0.05 1 0.187
2b 0.756
3c 0.498
4d 0.572
5e 0.498
6f 0.248
0.53 0.04 1 0.327
2 0.658
3 0.572
4 0.658
5 0.756
6 0.572
0.81 0.06 1 0.756
2 1.000
3 1.000
4 1.000
5 1.000
6 0.376 Fig. 3. Survival of S. enteric in samples at three aw and six water mobility (water
a
Control. mobility 1: control, water mobility 2: protein denatured at 100 MPa, water mobility 3:
b
Protein denatured at 100 MPa. protein denatured at 200 MPa, water mobility 4: protein denatured at 300 MPa, water
c
Protein denatured at 200 MPa. mobility 5: protein denatured at 400 MPa, water mobility 6: protein denatured at
d
Protein denatured at 300 MPa. 500 MPa).
e
Protein denatured at 400 MPa.
f
Protein denatured at 500 MPa.
F. Lian et al. / Food Control 47 (2015) 1e6 5

0.33. The samples treated with pressure ranging from 100 to water mobility has little inuence on the cultivability of S. enteric at
400 MPa had similar T21 distributions, indicating that they had this level of aw (p > 0.05). The cultivability of S. enteric at aw 0.81
similar water mobility. Fig. 2(c) shows the T2 distribution of skim after storage at 37  C was assayed in the treated and control skim
milk powder at aw 0.81. It was also discovered that the samples milk powder for up to two months (Fig. 3(c)). During the rst
treated with pressure ranging from 100 to 400 MPa had similar T21 month, the curve for the sample with water mobility 6 was similar
distributions, and as shown in Table 1, the T21 values of these to others'. However, in the second month, the S. enteric in the
samples were the same. The other signicant difference is that the sample with water mobility 6 had a reduction of 0.39 logs which
T21 value of the sample treated with 500 MPa is lower than the was signicantly lower (p < 0.05) than the reduction of approxi-
control, which suggests that its water mobility is lower. mately 1.28 logs for the other samples. The spectra of LF 1H NMR
(Fig. 2(c)) has indicates that water mobility of the sample treated
3.3. The cultivability of S. enteric inuenced by water mobility with 500 MPa is weaker (p < 0.05) than the rest. These results
suggest that water mobility has little inuence on the survival of
Fig. 3 shows the cultivability of S. enteric in skim milk powder S. enteric at low aw (aw < 0.53). However, it could inuence the
treated at different pressure at three aw. It was observed that about cultivability of S. enteric in skim milk powder at aw 0.81 (Fig. 3(c)).
5.00 logs of S. enteric were inactive after two months storage in all After two months storage, the decrease of microorganisms in the
the samples from Fig. 3(a). This indicates that water mobility has sample with water mobility 6 was about 5.00 logs. The rest of the
little inuence on the cultivability of S. enteric compared with the samples had about 6.00 logs decrease. This indicates that water
control at aw 0.33 (p > 0.05). This was also demonstrated by mobility may exert its effect at higher aw in low moisture content
Farakos et al., (2013). They revealed that water activity signicantly foods and the cultivability population of S. enteric is higher in the
inuenced the survival of Salmonella in low-aw foods (aw < 0.60), sample with lower water mobility. This level of aw is similar with
while water mobility had no effect independent of aw. Vittadini the aw (0.75e0.97) used by Pham, Vittadini, Levin, and Chinachoti
et al. (2005) investigated the correlation of microbial response in (1999), who reported that the germination time of the L-sorbose
model food systems with physico-chemical and mobility de- resistant strain of Aspergillus nidulans was highly dependent on
scriptors of the media. They studied the role of aw, macromolec- solid composition and aw (0.75e0.95) but correlation was best with
ular mobility and water molecular dynamics in multicomponent water mobility as indicated by 2H NMR T2 relaxation time.
model food (ranging from solid to liquid) systems in their corre- Vittadini, Dickinson, and Chinachoti (2002) reported that a strong
lation with microbial activity. It was found that a correlation be- mannitolewater interaction, leading to a decreased mobility,
tween cell death and increased 1H and 2H NMR mobility in low-aw played a role in protecting cells from death. The published litera-
foods (solid and semisolid media), indicating NMR molecular ture to date indicates little attempt to reveal molecular mecha-
mobility is a possible tool to describe water availability in solid and nisms involved in cell survival to discriminate water mobility from
semisolid systems (dry and intermediate moisture foods), while in aw. It was speculated that a higher water molecular mobility might
a high moisture system, the use of water activity remains a valid have allowed initiation but not completion of metabolic reactions
indicator for microbial activity. However, it is difcult to differen- leading to cells death (Vittadini et al., 2005). Further studies are
tiate the action of water mobility from that of aw because different needed to understand the metabolic response of the cell to water
water mobility with different aw were employed to correlate with mobility and aw.
microbial response. To further discriminate the inuence of mo-
lecular mobility on microbial survival behavior in low-aw foods, the 3.4. Fitting of inactivation models of S. enteric in samples with
present study prepared skim milk powder with different water different water mobility and aw
mobility at similar aw levels to evaluate how aw and water mobility
inuence the survival of Salmonella in low-aw foods. As shown in Farakos et al. (2013) developed models for non-fat food systems.
Fig. 3(b), all samples had similar reduction during the two months They observed that the survival data at 36  C could be described by
storage period, which was similar at aw 0.33. It also indicates that all models with the exception of the log-linear model. In this study,

Table 2
Statistical parameter, standard error (S) and relation index (r) of the model of Logistic model and Exponential association.

Water activity Conguration Logistic model Exponential association

a b c r S a b r S

0.33 0.05 0.187 4.060 11.972 0.282 0.986 0.377 4.333 0.076 0.992 0.254
0.756 4.354 14.567 0.284 0.995 0.253 4.703 0.068 0.993 0.256
0.498 4.376 44.382 0.352 0.997 0.200 5.012 0.05 0.983 0.399
0.572 4.392 41.470 0.345 0.997 0.188 5.025 0.050 0.982 0.430
0.498 4.226 107.747 0.448 0.999 0.106 4.739 0.054 0.964 0.592
0.248 4.198 17.982 0.300 0.994 0.259 4.573 0.0646 0.988 0.323
0.53 0.04 0.327 4.151 13.728 0.293 0.990 0.329 4.479 0.072 0.990 0.289
0.658 4.644 14.282 0.318 0.984 0.470 5.046 0.075 0.988 0.356
0.572 4.395 21.277 0.343 0.987 0.413 4.784 0.0696 0.979 0.463
0.658 4.451 6.285 0.244 0.968 0.592 4.597 0.100 0.991 0.274
0.756 4.370 14.973 0.300 0.987 0.408 4.716 0.071 0.997 0.229
0.572 4.623 7.286 0.165 0.985 0.410 4.988 0.057 0.997 0.157
0.81 0.06 0.756 5.267 6.749 0.216 0.966 0.722 5.634 0.076 0.991 0.325
1.000 5.135 5.626 0.188 0.950 0.843 5.553 0.071 0.980 0.468
1.000 5.088 8.560 0.223 0.961 0.776 5.676 0.062 0.987 0.388
1.000 5.376 10.328 0.240 0.979 0.610 5.802 0.067 0.991 0.341
1.000 5.521 7.675 0.117 0.968 0.723 6.204 0.039 0.992 0.316
0.376 4.458 23.223 0.272 0.992 0.323 5.173 0.047 0.989 0.332
a, b, c
the parameters in equation, r relation index, S
standard error.
6 F. Lian et al. / Food Control 47 (2015) 1e6

the Curve Expert software was used to nd a suitable model with frequency (RF) heating. Innovative Food Science and Emerging Technologies, 6(4),
396e402.
time as X-axis and log (N0/Nt) as Y-axis. The Logistic model (Equa-
Beuchat, L. R., Komitopoulou, E., Beckers, H., Betts, R. P., Bourdichon, F., Fanning, S.,
tion (1)) and Exponential association (Equation (2)) were more et al. (2013). Low-water activity foods: increased concern as vehicles of food-
suitable for the survival of S. enteric in comparison with other borne pathogens. Journal of Food Protection, 76(1), 150e172.
Carneiro, C. S., M 
arsico, E. T., Ribeiro, R. O. R., Jnior, C. A. C., Alvares, T. S., &
models.
Jesus, E. F. O. (2013). Studies of the effect of sodium tripolyphosphate on
frozen shrimp by physicochemical analytical methods and Low Field Nu-
(1) Logistic model clear Magnetic Resonance (LF 1H NMR). LWT e Food Science and Technology,
50(2), 401e407.
CDC (Centers for Disease Control and Prevention). (2007). Multistate outbreak of
a Salmonella serotype Tennessee infections associated with peanut butter e
y (1) United States, 2006e2007. CDC e Morbidity and Mortality Weekly Report, 42,
1 becx 516e517, 56:521e524.
Choi, S. G., & Kerr, W. L. (2003). 1H NMR studies of molecular mobility in wheat
starch. Food Research International, 36(4), 341e348.
(2) Exponential association Fan, D., Ma, S., Wang, L., Zhao, H., Zhao, J., Zhang, H., et al. (2013). 1H NMR studies of
starchewater interactions during microwave heating. Carbohydrate Polymers,
97(2), 406e412.
  Farakos, S. M., Frank, J. F., & Schaffner, D. W. (2013). Modeling the inuence of
y a 1  ebx (2) temperature, water activity and water mobility on the persistence of Salmonella
in low-moisture foods. International Journal of Food Microbiology, 166(2),
Table 2 shows the parameter details for these two models for all 280e293.
Finstad, S., O'Bryan, C. A., Marcy, J. A., Crandall, P. G., & Ricke, S. C. (2012). Salmonella
samples. It was observed that Exponential association is more and broiler processing in the United States: relationship to foodborne salmo-
suitable for the inactivation of S. enteric for all samples compared nellosis. Food Research International, 45(2), 789e794.
with Logistic model. Exponential association was therefore selected Hills, B. P., Manning, C. E., Ridge, Y., & Brocklehurst, T. (1997). Water availability and
the survival of Salmonella typhimurium in porous systems. International Journal
as the model to describe the inactivation of S. enteric. It was also of Food Microbiology, 36(2), 187e198.
observed that the parameters for the sample with aw 0.81 and T21 Jung, Y. S., & Beuchat, L. R. (1999). Survival of multidrug-resistant Salmonella
0.376 are different from other samples with aw 0.81. This may typhimurium DT104 in egg powders as affected by water activity and temper-
ature. International Journal of Food Microbiology, 49(1), 1e8.
indicate that water mobility may inuence the survival of S. enteric
Koch, J., Schrauder, A., Alpers, K., Werber, D., Frank, C., Prager, R., et al. (2005).
at aw 0.81. Salmonella Agona outbreak from contaminated aniseed, Germany. Emerging
Infectious Diseases, 11(7), 1124e1128.
Laroche, C., Fine, F., & Gervais, P. (2005). Water activity affects heat resistance of
4. Conclusions microorganisms in food powders. International Journal of Food Microbiology,
97(3), 307e315.
S. enteric could survive for a long period of time in skim milk Li, C., Liu, D., Zhou, G., Xu, X., Qi, J., Shi, P., et al. (2012). Meat quality and cooking
attributes of thawed pork with different low eld NMR T21. Meat Science, 92(2),
powder. The survival could be inuenced by water activity and 79e83.
water mobility. The higher the aw of skim milk powder, the lower Licari, J. J., & Potter, N. N. (1970). Salmonella survival during spray drying and
the S. enteric survival. When aw was at 0.33 and 0.53, water mobility subsequent handling of skimmilk powder. III. Effects of storage temperature on
salmonella and dried milk properties. Journal of Dairy Science, 53(7), 877e882.
had little effect. However, water mobility also inuenced the sur- Mattick, K. L., Jrgensen, F., Wang, P., Pound, J., Vandeven, M. H., Ward, L. R., et al.
vival of S. enteric when aw was increased to 0.81. The survival (2001). Effect of challenge temperature and solute type on heat tolerance of
population of S. enteric was higher in the sample with low water Salmonella serovars at low water activity. Applied and Environmental Microbi-
ology, 67(9), 4128e4136.
mobility. Molina, E., Papadopoulou, A., & Ledward, D. A. (2001). Emulsifying properties of
high pressure treated soy protein isolate and 7S and 11S globulins. Food Hy-
drocolloids, 15, 263e269.
Acknowledgments Pham, X., Vittadini, E., Levin, R. E., & Chinachoti, P. (1999). Role of water mobility on
mold spore germination. Journal of Agricultural and Food Chemistry, 47(12),
The authors gratefully acknowledge the nancial support pro- 4976e4983.
Vesterlund, S., Salminen, K., & Salminen, S. (2012). Water activity in dry foods
vided by Project 31101376 of the National Natural Science Foun-
containing live probiotic bacteria should be carefully considered: a case study
dation of China, the Program for New Century Excellent Talents in with Lactobacillus rhamnosus GG in axseed. International Journal of Food
University of Ministry of Education of China (Grant No. NCET-13- Microbiology, 157(2), 319e321.
Vittadini, E., Chinachoti, P., Lavoie, J. P., & Pham, X. (2005). Correlation of microbial
0834) and the Fundamental Research Funds for the Central Uni-
response in model food systems with physicochemical and mobility de-
versities (JUSRP51406A). scriptors of the media. Innovative Food Science and Emerging Technologies, 6(1),
21e28.
Vittadini, E., Dickinson, L. C., & Chinachoti, P. (2002). A study of 1H and 2H
References NMR molecular mobility and structural relaxation in xanthan and locust
bean gum mixtures: effect on microbial response. Carbohydrate Polymers,
Awuah, G. B., Ramaswamy, H. S., Economides, A., & Mallikarjunan, K. (2005). 49(3), 261e269.
Inactivation of Escherichia coli K-12 and Listeria innocua in milk using radio

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