LWT - Food Science and Technology 69 (2016) 169e174

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LWT - Food Science and Technology

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Effects of salt concentration on Chinese sauerkraut fermentation

Tao Xiong a, b, *, Junbo Li a, b, Fan Liang c, Yanping Wang a, b, Qianqian Guan a, b,
Mingyong Xie a
a
State Key Laboratory of Food Science & Technology, No. 235 Nanjing East Road, Nanchang, Jiangxi, 330047, PR China
b
College of Food Science, Nanchang University, Nanchang, 330047, PR China
c
College of Food Science and Technology, Hunan Agricultural University, Changsha, 410128, PR China

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

Article history: The aim of the study was to determine the effects of salt concentration on traditional sauerkraut fer-
Received 1 October 2015 mented spontaneously. Lactic acid bacteria (LAB), fungi and Escherichia coli (E. coli) in the brine were
Received in revised form analyzed in the three kinds of sauerkraut. The contents of sugars (sucrose, glucose, fructose) and organic
21 December 2015
acids (lactic acid, acetic acid) in the brine and inside the cabbage were monitored by high-performance
Accepted 26 December 2015
Available online 29 December 2015
liquid chromatography (HPLC). In addition, the pH value was monitored in the brine. Results demon-
strated that sucrose and glucose were consumed and fructose was accumulated gradually during
fermentation. The whole fermentation process was dominated by LAB and a considerable accumulation
Keywords:
Chinese sauerkraut
of lactic acid was observed both in cabbage and brine at the end of fermentation. Salt concentration had a
Salt concentration significant effect on sauerkraut fermentation at early stage. The LAB population and metabolic rate was
Lactic acid bacteria reduced and the yield of lactic acid decreased with the increase of salt concentration. Suitable salt
Fermentation concentration can effectively inhibit the reproduction of fungi and E. coli. In comparison, high salt
Metabolism concentration delayed the maturation of sauerkraut and inhibited the metabolism of LAB.
© 2016 Elsevier Ltd. All rights reserved.

1. Introduction
It was recorded that Chinese sauerkraut (also known as “Pao
Cai”) originated from Zhou Dynasty 3000 years ago (Zhang, 1994)
and spread to South Korea in the 5th century (Ma, 2010). Chinese
sauerkraut, as a typical brine-salted vegetable fermented by lactic
acid bacteria (LAB), is widely consumed in China (Yan, Xue, Tan,
Zhang, & Chang, 2008). Unlike kimchi which uses direct salting to
withdraw juice from the cabbage (dry salting), traditional Chinese
sauerkraut is anaerobic, fermented in brine with a low salt con-
centration (2%e10%) by the indigenous microorganism on the raw
cabbage (Chen, 2007). LAB plays an important role during
fermentation, because they contribute to sensory characteristics
and preservation (Holzapfel, 1995). Fermentation of sauerkraut can
be divided into hetero-fermentation and homo-fermentation
phase, and species and quantity of LAB varies with fermentation
stage. The initial phase was hetero-fermentation dominated by
Leuconostoc citreum, Leuconostoc mesenteroides and Weissella
* Corresponding author. State Key Laboratory of Food Science & Technology, No.
235 Nanjing East Road, Nanchang, Jiangxi, 330047, PR China.
E-mail address: xiongtao0907@163.com (T. Xiong).
koreensis et al. (Park et al., 2010; Wiander & Ryha €nen, 2008), and
then gradually transited to homo-fermentation phase, dominated
by Lactobacillus plantarum, Lactobacillus brevis, Lactobacillus cur-
vatus, and Lactobacillus sakei et al. (Kim et al., 2002; Plengvidhya,
Breidt, Lu, & Fleming, 2007). It was also reported that the
fermentation process of Chinese sauerkraut with 4% salt also
experienced hetero-fermentative and successively homo-
fermentative phase (Xiong, Guan, Song, Hao, & Xie, 2012). Salt
concentration of sauerkraut had an effect on saline taste and mi-
crobial structure of brine so as to directly or indirectly affect the
quality and flavor of sauerkraut. High salt concentration can better
inhibit the growth of spoilage bacteria in brine, meanwhile, the first
hetero-fermentative phase was absent, due to the intolerance to-
wards salt of Leuconostocs (Cagno et al., 2009; Wouters et al., 2013).
Now, many researches about the effect of salinity on utilization
ratio of sugar and acid production during olive and cucumber
fermentation have been reported (Efstathios & Constantinos, 2006;
Frederico et al., 2005; Lu, Fleming, & Mcfeeters, 2001; McFeeters &
rez-Díaz, 2010). The water activity and osmotic pressure of brine
Pe
with different combinations of salt in Spanish olive fermentation
were described in detail (Panagou, Hondrodimou, Mallouchos, &
Nychas, 2011). However, there is little information regarding the
influence of salt concentration on the fermentation of Chinese

http://dx.doi.org/10.1016/j.lwt.2015.12.057
0023-6438/© 2016 Elsevier Ltd. All rights reserved.
170 T. Xiong et al. / LWT - Food Science and Technology 69 (2016) 169e174
sauerkraut.
The aim of this study was to determine the effect of salt con-
centration on sauerkraut fermentation. The changes of pH, LAB,
fungi and Escherichia coli in brine as well as the contents of organic
acid, sugar, and sucrose in cabbage and brine under different salt
concentrations were examined.
2. Materials and methods
2.1. Materials
Fresh cabbage and other auxiliary materials were purchased
from a local supermarket in Nanchang, Jiangxi Province, China.
2.2. Preparation of sauerkraut
Cabbages were cut into small pieces (2e3 cm
6e8 cm), then
the pieces of cabbage were washed and drained as the raw material
of sauerkraut. Fermentation were carried out in 5 L ceramic jars,
each containing 1 kg sliced cabbage pieces and auxiliary materials,
including crystal sugar (4%), hot red pepper (4%), garlic (3%), ginger
(2%) and Chinese prickly ash (1.5%) (All percentages were calculated
by the volume of sterile water). Salt (2%, 5%, and 8%, w/v) and sugar
(4%) were dissolved in 2000 mL sterile water, saline solutions at the
three concentrations were prepared as mentioned above. Finally
cold sterile water was added into sauerkraut jar that was then
water sealed. The sauerkraut jars were kept at ambient tempera-
ture (20e25  C) during experiments.
2.3. Sampling
During the fermentation, brine (10 mL) and cabbage (10 g)
samples were withdrawn aseptically every 12 h for 7 days, the
sauerkraut jars were shaken before each sampling. A part of the
brine was used for measurements of pH value and analysis of
microbiological changes, the other part was stored at 20  C for
HPLC analysis. The cabbage samples were pulped and diluted 10
times, 5 mL diluent was taken and then stored at 20  C for HPLC
rez-Díaz, 2010).
analysis (McFeeters & Pe
2.4. Analytical methods
2.4.1. Microbiological analysis
1 mL brine was aseptically added into 9 mL sterile saline (0.85%
NaCl, w/v), appropriately diluted, 100 mL brine of 3 suitable gradient
dilutions were respectively coated on the following flat plate, each
with a parallel coating. Violet Red Bile Dextrose agar (VRBDA) for
Enterobacteriaceae, the agar media were incubated at 37  C for
24 h, LAB on MRS incubated at 37  C for 48 h (Efstathios &
Constantinos, 2006; Wang, Ren, Liu, Zhu, & Wang, 2013), Fungi
on Yeast Extract Peptone Dextrose Medium agar (YPD) incubated at
25  C for 72 h. To avoid bacterial growth, YPD was supplemented
with chloramphenicol (0.1 g L1; SigmaeeAldrich) (Wendy, Ilenys,
& Perez, 2012).
2.4.2. Determination of organic acids, sugar and pH value
HPLC (Model 1200, Agilent, USA) was used to determine the
concentration of sugars and organic acids. For HPLC analysis, the
brine and cabbage slurry samples were thawed and centrifuged at
10000
g for 10 min, then filtered through 0.22 mm membrane
(Xiong, Li, Guan, Peng, & Xie, 2014). The pH value of the brine
samples was measured using a pH meter (PHS-25, Shanghai Pre-
cision Scientific Instruments Company, China).
2.4.3. Statistical analysis
Data was represented as mean values (n ¼ 4) ± standard devi-
ation of means. Analysis of variance (ANOVA) was performed on the
data obtained every 12 h, followed by Student's t test using SPSS 20.
Differences were considered significant at p < 0.05. Origin8.6
software was used for mapping.
3. Results and discussion
3.1. Changes of pH value during Chinese sauerkraut fermentation
T, F, E represent for 2%, 5%, 8% salt concentration sauerkraut,
further referred to as T, F, E. Error bars represent the standard
deviation.
The pH is a critical indicator of fermentation progress, and its
drop occurred mainly due to lactic acid, the metabolism by LAB
(Adams, 1990; Kandler, 1983). As shown in Fig. 1, the initial pH
values of sauerkraut with different salt concentrations (2%, 5%, 8%,
w/v) were between 6.35 and 6.50. The pH values decreased sharply
at first and followed by a slowly decrease to a stable level, reducing
to 4 in the 1st, 2nd and 3.5th day, respectively. Salt had a significant
(P < 0.05) influence on pH values at the first 48 h in fermentation,
the lower the salt concentration was, the faster the pH decreased,
which may be because the acid producing ability of LAB was
restrained gradually with the increasing of salt concentration
(Rodríguez-Go  mez et al., 2012). In contrast, salt had no significant
(P > 0.05) effect on the changes of pH at the end of fermentation,
but the lower salt concentration resulted in the lower pH.
3.2. Microbiological changes during fermentation
As shown in Fig. 2A, the original population of LAB were
3.14e3.34 log CFU/mL and then sharply increased at the first day in
three fermentation, the concentration of T and F exceeded
log8.0 CFU/mL at 1st and 1.5th day respectively. However, the
growth of LAB in E was relatively slow, only reaching to 8.02 log
CFU/mL in the 3rd day, probably due to the initiating strain of
fermentation mainly was hetero-fermentative LAB with short
metabolic cycle, poor salt tolerance and acid resistance (Wouters
et al., 2013; Xiong et al., 2012). In the mid-late fermentation, the
amount of LAB remained stable above 8.0 log CFU/ml, probably
because the dominant LAB was homo-fermentative with strong
salt-tolerance and acid-resistance (Chorianopoulos, Boziaris,
Stamatiou, & Nychas, 2005; McFeeters & Pe rez-Díaz, 2010).
Therefore, salt had a significant inhibitory effect on the growth of
LAB in brine at early stage of fermentation, but the effect was not
6.5
T
F
6.0
E
5.5
5.0
pH
4.5
4.0
3.5
3.0
0 24 48 72 96 120 144 168
Fermentation time (h)
Fig. 1. Changes of pH during the fermentation of sauerkraut with three different salt
concentrations.
 T. Xiong et al. / LWT - Food Science and Technology 69 (2016) 169e174 171

9 A 6
B T
F
5
8 E

4
7
(logCFU)/mL

(logCFU)/mL
3
6
T
F 2
5
E

4 1

3 0

0 24 48 72 96 120 144 168 0 24 48 72 96 120 144 168

Fermentation time (h) Fermentation time (h)

8
C
T
F
6 E
(logCFU)/mL

0 24 48 72 96 120 144 168

Fermentation time (h)

Fig. 2. Changes of LAB, fungi, E. coli during the fermentation of sauerkraut in three different salt concentrations.

significant on the late fermentation of sauerkraut (Choi et al., 2003).
It was reported that pectinase produced by fungi softened
vegetables and led to deterioration in flavor (Etchells, Bell, Monroe,
Masley, & Demain, 1958). Fungi was regarded as undesirable
microorganism in sauerkraut fermentation (Wouters et al., 2013;
Zhao & Ding, 2008). As shown in Fig. 2B, initial populations of
fungi were about 3.75e4.00 log CFU/mL and reduced to an unde-
tectable amount before the ripe of sauerkraut, but the specific
growth rate was affected by the amount of salt. It was found that
the fungi in T reached to 5.35 log CFU/mL in the 0.5th day, while
that in F reached to 4.67 log CFU/mL in the 1st day, then both
decreased gradually until disappeared. However, the amount of
fungi in E was maintained at 3e4 log CFU/mL for 5 days, then
rapidly decreased till uncountable in the 6.5th day. Hetero-
fermentative LAB and yeast consumed sugar to produce carbon
dioxide forming anaerobic environment in brine (Wendy et al.,
2012; Xiong et al., 2014). It is presumed that the anaerobic envi-
ronment, decreased pH, as well as elevated acidity may make fungi
disappear. Salt was found to have a significant (p < 0.05) influence
on the amount of fungi during fermentation. Compared with the
other two salt concentration, 5% (w/v) salt not only reduced the
peak of fungi, but also made fungi disappear firstly.
As shown in Fig. 2C, the initial content of E. coli in three kinds of
sauerkraut were 4.38e4.54 log CFU/mL, the growth curve of E. coli
was similar to the fungi. The amount of E. coli in T and F rose to the
peak in the 36th hour and then decreased gradually, but E. coli in F
passed through the peak and disappeared earlier than that in T.
E. coli in E were inhibited and had no significant changes in cell
population till the 5th day, and then sharply decreased. Results
showed that salt had an obvious inhibitory effect on E. coli in Chi-
nese sauerkraut, probably due to the combined effect of brine pH,
LAB and salt concentration. It was also reported that the growth of
E. coli was inhibited by lactic acid, bacteriocins and phenyllactic
acid produced by lactic acid bacteria (Kim, Song, Yook, Ryu, & Byun,
2004; Li et al., 2015).
3.3. Changes in levels of sugars and organic acids during
fermentation
3.3.1. Changes in levels of sugars during fermentation
Crystal sugar, mainly containing sucrose as well as a small
amount of glucose and fructose (Xiong et al. 2014), was added to
the fermentation as initial carbon source. As shown in Fig. 3A, the
content of sucrose in cabbage was quite different from that in brine,
sucrose in brine quickly decreased while the increasing concen-
tration of sucrose in cabbage was relatively low when fermentation
started. When the content of sucrose in brine decreased to the same
as that in cabbage, the content of sucrose inside and outside the
cabbage synchronously declined, and total sucrose was mostly
consumed in the end. However, salt had a significant (p < 0.05)
172 T. Xiong et al. / LWT - Food Science and Technology 69 (2016) 169e174

100
A Tb Fb Eb B
Tc Fc Ec 120
Tb Tc
80
Fb Fc
Sucrose concentration (mM)

100

Glucose concentration (mM)

Eb Ec

60 80

60
40

40

20
20

0 0
0 24 48 72 96 120 144 168 0 24 48 72 96 120 144 168

Fermentation time (h) Fermentation time (h)

100 C
Fructose concentration (mM)

80

60

40

Tb Tc
20 Fb Fc
Eb Ec

0
0 24 48 72 96 120 144 168
Fermentation time (h)

Fig. 3. Changes in the levels of sucrose, glucose and fructose during the fermentation in cabbage and brine with different salt concentrations. Tb, Fb and Eb represent 2%, 5% and 8%
salt concentration in brine, Tc, Fc and Ec represent 2%, 5% and 8% salt concentration in cabbage.

effect on sucrose content of sauerkraut in the early fermentation and increased comparatively slowly. There were two possible
stage. The lower the salt concentration was, the higher the content sources of glucose in the brine, one may be permeation from the
of LAB in brine was (Bautista, Arroyo Lo  pez, Dura
nQuintana, & cabbage to the brine; the other may be the transformation of su-
Garrido Ferna ndez, 2010). Hetero-fermentative LAB, which can crose in the brine (McFeeters et al., 2010; Chorianopoulos et al.,
produce high-activity dextransucrase, catalyzing decomposition of 2005). In comparison, the content of glucose in cabbage
sucrose (Hyun, Dong, & Nam, 2007), accounted for the majority of decreased the most but increased the least in Tb. These results
LAB in brine (Xiong et al., 2012). Sucrose content of Tb rapidly suggested that glucose was consumed by microorganism, which
decreased while that in Tc increased slowly, probably due to the grew the fastest among three fermentation. In the mid-late period
weak inhibition on the growth of microorganisms by high water of fermentation, the concentration of glucose tended to be stable
activity as well as the slow diffusion of sucrose from Tb to Tc caused and the concentration of glucose in the cabbage was slightly higher
by low osmotic pressure (Frederico et al. 2005; Panagou et al. 2011). than that in the brine. Although glucose is a preferred energy
In contrast, sucrose content in Fc and Ec with higher salt concen- source over sucrose and other monosaccharide by many microor-
tration increased rapidly at the initial 36 h. In addition, the ganisms (Lu et al., 2001), the residual glucose determined in the
consuming rate of sucrose slowed down in late fermentation, as a study was high, presumably because the presence of sucrose
result of the metabolism of homo-fermentative LAB, which was reduced glucose utilization (Fasina, Fleming, & Thompson, 2002).
inhibited by the accumulation of lactic acid and the decrease of The initial content of fructose in cabbage was much higher than
brine pH (Chorianopoulos et al., 2005; Sa nchez, Rejano, Montan ~ o, & that in the brine. The content of fructose decreased slowly
de Castro, 2001). At the end of fermentation, E had the lowest co- throughout the fermentation in cabbage while fructose concen-
efficient of sucrose utilization, and sucrose remained the most in- tration increased rapidly in brine at the first 60 h of fermentation
side and outside the cabbage. and then gradually leveled off. As shown in Fig. 3C, the sum amount
As shown in Fig.3B, at the early stage of the fermentation, the of fructose in cabbage and brine was 103.8e125.7 mM finally,
content of glucose in cabbage was 118.1 ± 4.2 mM and quickly which was higher than the starting amount 93.7 ± 2.0 mM. These
decreased, while glucose concentration in brine was 11 ± 0.5 mM results indicated that the utilization rate of fructose was relatively

140
A Tb Tc
Fb Fc
120
Eb Ec
Lactic acid concentration (mM)
100
80
60
40
20
0
0 24 48
Fermentation time (h)
Fig. 4. Change in the levels of lactic acid and acetic acid during fermentation of cabbage and brine with three different salt concentrations.
low and more fructose was transformed than consumed in the
brine. Fructose was not preferred carbon source of microorganisms
in Chinese sauerkraut, a similar result was reported by other re-
searchers in cucumber juice fermentation (Lu et al., 2001).
3.3.2. Changes in levels of main organic acids during fermentation
The stability of the strains was directly influenced by the con-
tent of lactic acid, the main organic acid in sauerkraut (Xiong et al.,
2014). As shown in Fig. 4A, the level of lactic acid increased slowly
in the first 48 h and accumulated rapidly in the following 96 h,
followed by a slow increase in the brine. An interesting phenom-
enon was observed that the content of lactic acid in cabbage was
higher than in brine at the first periods, but lower at the last. While
LAB reached a concentration of 108 CFU/mL in the second day and
sucrose was quickly consumed at the same time, the amount of
lactic acid was small. These results might be caused by two reasons,
one is that fermentation was dominated by hetero-fermentative
LAB at the early stage, which was poor in acid production; the
other is that some microbes in brine can utilize sucrose but cannot
produce lactic acid, such as yeast, mold and pathogenic bacteria
(Wendy et al., 2012). In contrast, the fermentation was dominated
by homo-fermentative lactic bacteria, which had better acid-
tolerance and acid-production ability in mid-late phase, but the
accumulation of lactic acid in the last day was slow. This may be
that the capacity of acid was affected by the accumulation of lactic
acid and Hþ and LAB need more energy to maintain the stability of
acid production (Lolkema, Poolman, & Konings, 1995; Wu et al.
2012). Salt had a significant impact on the production of lactic
acid throughout fermentation in sauerkraut, the higher the salt
concentration was, the lower the lactic acid production was (Zhao &
Ding, 2008).
Hetero-fermentative LAB produced equimolar amount of lactic
acid, CO2 and acetic acid under aerobic conditions via 6P-gloconate
pathway (Blandino, Al-Aseeri, Pandiella, Cantero, & Webb, 2003). It
was also found that a short acetic acid fermentation by acetic acid
bacteria in early stage of fermentation in Chinese sauerkraut
(Xiong, Peng, Li, Li, & Guan, 2015). Appropriate concentration of
acetic acid can effectively improve the sensory properties of
sauerkraut (Oliveira, Perego, Oliveira, & Converti, 2012). As shown
in Fig. 4B, the level of acetic acid changed slightly faster from the
1.5th day to 4th day, then tended to be stable until the end of
fermentation. The acetic acid content in cabbage was higher than
that in the brine at the first day, which might be that the cabbage
contains a high amount of acetic acid. Moreover, the content of
acetic acid was the highest in the brine with 2% salt and varied
T. Xiong et al. / LWT - Food Science and Technology 69 (2016) 169e174 173
B Tb Tc
40
Fb Fc
Eb Ec
35
Acetic acid concentration (mM)
30
25
20
15
10
5
0
0 24 48 72 96 120 144 168
72 96 120 144 168
Fermentation time (h)
depending on different concentrations of salt in sauerkraut. The
highest accumulation of acetic acid in T may benefit from its
highest concentration of LAB from the first day to 4th day, during
which fermentation was dominated by hetero-fermentative LAB
(Xiong et al., 2012). In addition, the combination of acetic acid and
ethanol, producing ethyl acetate, can enhance the flavor of
sauerkraut.
4. Conclusion
This study examined the impact of different salt concentrations
(2%, 5%, 8%, w/v) on the fermentation profiles of Chinese traditional
sauerkraut. Results showed that salt concentration mainly affected
the early stage of sauerkraut fermentation significantly. Different
salt concentrations resulted in the different osmotic pressure, wa-
ter activity and strains structure as well as microbial metabolism
and the rate of exchange substances (Wouters et al., 2013). Research
has shown that 2% (w/v) salt accelerated the maturation of the
sauerkraut, it can not effectively inhibit the growth of harmful
microorganisms. In contrast, 5% salt can make fungi and E. coli in F
passed through the peak and disappeared earlier. 8% salt in E not
only delayed the maturation of sauerkraut but also minimized the
utilization of sucrose and slowed down the metabolism of LAB.
Meanwhile, although the emergence of the peak of fungi and E. coli
was avoided, it failed to make them disappear rapidly. Taken
together, 5% salt concentration can improve the quality of sauer-
kraut in traditional fermentation. To provide a reliable basis for the
industrial production of Chinese sauerkraut, future researches in
the field will include detailed experimental designs that will assess
the effect of added salt on sensory, flavor and shelf life, in addition,
accelerate the demise of harmful microorganisms in low salt
sauerkraut by enhancing the hetero-fermentation.
Acknowledgments
The financial supports from the National Natural Science
Foundation of China (NSFC, Project No. 31560449) and the National
High Technology Research Development Key Program of China (863
Key Program, 2011AA100904), State Key Laboratory of Food Science
and Technology, Nanchang University (Project No. SKLF-ZZB-
201309 and No. SKLF-ZZA-201303) are gratefully acknowledged.
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