African Journal of Biotechnology Vol. 11(22), pp.

6123-6130, 15 March, 2012

Available online at http://www.academicjournals.org/AJB
DOI: 10.5897/AJB11.4039
ISSN 1684–5315 © 2012 Academic Journals

Full Length Research Paper

Effects of stabilizers and exopolysaccharides on

physiochemical properties of fermented skim milk by
Streptococcus thermophilus ST1
Tiehua Zhang1, Zhuodan Zhang1, Haiyang Yan 1, Da Li2, Zhennai Yang2 and Mingruo Guo1,3*
1
College of Light Industry and Economics and Management, Jilin University, Changchun, 130062, China.
2
Center of Agro-food Technology, The Northeast Agricultural Research Center of China, Changchun, 130033, China.
3
Department of Nutrition and Food Science, The University of Vermont, Burlington, 05405, USA.
Accepted 17 February, 2012

In this study, the effects of exopolysaccharide (EPS) produced by Streptococcus thermophilus ST1 and
stabilizers on the textural and microstructural properties attributes of fermented skim milk were
investigated. ST1 had a high capacity to produce acids and EPS. Within 4.5 h, the pH dropped to 4.5, the
acidity reached 0.8%, and EPS reached 65.27 mg/L. ST1 was more effective at increasing viscosity as
well as water holding capacity and reducing spontaneous whey separation compared with control
sample (ST0). ST1 combined with carrageenan had the highest viscosity and the best water holding
capacity as well as the lowest spontaneous whey separation. ST1 combined with whey protein
concentrates showed better results with xanthan, but worse with carrageenan. The microstructure of
the fermented milk was examined using scanning electron microscopy. ST1 combined with
carrageenan resulted in compact and uniform structure, which is agreed with quality improvement of
fermented skim milk that used ST1 combine carrageenan as fat substitute.

Key words: Streptococcus thermophilus ST1, exopolysaccharide, fermented skim milk, texture.

INTRODUCTION

Yogurt is a popular fermented milk product and has been increase the firmness and prevent syneresis in yogurt (El-
a major part of people’s diet around the world. Low-fat Sayed et al., 2002). Carrageenan, synergistic with some
yogurts are increasingly popular due to their nutritional other gums, could increase the gel strength and water-
and potentially therapeutic characteristics (Aguirre- binding capabilities as well as modifying the gel texture
Mandujano et al., 2009). Fat reduction can cause some (Ertan et al., 2009). Whey protein concentrate (WPC)
defects in yogurt such as lack of flavour, weak body and affects the textural and physical properties of yogurts
poor texture (Guven et al., 2005). Several studies have (Sodini et al., 2005). Sandoval et al. (2004) found that
discussed the improvement of physical, textural, flavour reduced-fat yogurt with WPC showed similar texture
and rheological properties of low-fat yogurts by (tension, firmness, adhesiveness, cohesiveness, and
incorporating the stabilizers into the milk. This increases springiness) to full-fat yogurt.
the viscosity and reduces syneresis (Lucey, 2002). The exopolysaccharide (EPS) produced by low-fat
Xanthan gum has been used to improve the texture, yogurt starter cultures affect the textural and physical pro-
perties of yogurt and improve the sensory characteristics
such as mouthfeel, shininess, clean cut, ropiness and
creaminess (Folkenberg et al., 2006; Hassan et al., 2002;
*Corresponding author. E-mail: mguo@uvm.edu. Tel:
8026568168. Fax: 802656001.
Ruas-Madiedo et al., 2005; Ramchandran and Shah,
2009). Both capsular and ropy EPS possess high water
Abbreviations: ST, Streptococcus thermophilus; EPS, binding ability, resulting in increased water retention in
exopolysaccharide; WPC, whey protein concentrate; LAB, lactic yogurt (Hassan et al., 1996b). EPS has been reported to
acid bacteria; WHC, water-holding capacity. provide physiological benefits such as lowering of
6124 Afr. J. Biotechnol.

cholesterol, immunomodulation, and antitumor activity samples were stored at 4°C for 24 h for analysis.
(Welman and Maddox 2003). Therefore, using EPS
producing cultures when developing a low-fat yogurt with Texture analysis
physiological functions is necessary.
The objective of this study was to investigate the effect Fermented skim milk texture analysis was carried out with TA-XT2i
of EPS-producing culture and stabilizers on the textural (Texture Technologies Corp., Scarsdale, NY) using a 5 kg load cell.
and physical characteristic of fermented skim milk, and to A 35 mm diameter solid rod (A/BE35) was thrust into the test
reveal the mechanisms of these changes by micro- sample, a sample depth of 30 mm with crosshead speed of 1 mms-1
(Sandoval-Castilla et al., 2004).
structure of the fermented skim milk.

Viscosity analysis
MATERIALS AND METHODS
The viscosity determination was based on Rawson and Marshall
Cultures (1997) method, with some modifications. The gel was broken by
stirring with a glass rod (10 times clockwise; 10 times
EPS-nonproducing strains Streptococcus thermophilus ST0 and anticlockwise). Rotational viscosity measurements were made
ropy exopolysaccharide-producing strains S. thermophilus ST1 using a Brookfield Viscometer (Model DV-Ⅲ; Brookfield
obtained from Culture Collection of Northeast Agricultural Research Engineering Laboratories, Stoughton, MA). N0 3 spindle was used,
Center of China (NARCC) were used throughout the study. The with about one third of the spindle immersed. Each measurement
strains were stored at -80°C in 10% (w/v) skim milk (Fonterra, New was made at room temperature at 100 rpm for 1 min.
Zealand) containing 30% (v/v) glycerol. S. thermophilus ST1 and
ST0 were propagated three times consecutively using a 3% (v/v)
inoculum in 10% skim milk at 42°C before use. Water-holding capacity analysis

The water-holding capacity (WHC) of fermented skim milk was

Determination of pH, titratable acidity and viable counts determined as described by Doleyres et al. (2005). Briefly, 10 g of
fermented skim milk was centrifuged at 5000×g for 10 min at 5°C.
The pH values were determined at 42°C. The titratable acidity was The resulting supernatant was carefully weighed to determine the
determined according to the method of Seo (2010). 10 ml of amount of excluded water (% wt/wt).
bacterial cultures and 20 ml of deionized water were mixed, and 0.5
ml of phenolphthalein was added into the mixture. This mixture was
titrated with 0.1 M NaOH. The acidity of the bacterial cultures was Spontaneous whey separation analysis
calculated as percent (%) lactic acid. Viable counts in fermented
skim milk were enumerated ST1 and ST0, respectively. S. Spontaneous whey separation was determined according to the
thermophilus was estimated by plating M17 agar for incubation at procedure described by Amatayakul et al. (2006). A cup of set
42°C for 48 h (Li, 2006). fermented skim milk was removed from refrigerator at 4°C, weighed
and kept at approximately 45°C to allow the whey on the surface to
be collected on the side of the cup. A needle connected to a syringe
was used to withdraw the liquid whey from the surface of the
Isolation and quantification of EPS
sample, and the cup of fermented skim milk was weighed again.
The process lasted for less than 10 s to avoid further leakage of
EPS was isolated from the fermented milk samples using a
whey from the curd. The syneresis was expressed as the
modified procedure previously described by Elin et al. (2010).
percentage weight of the whey over the initial weight of the
Briefly, trichloroacetic acid was added to the sample culture to a
fermented skim milk sample.
final concentration of 4% (w/v) and allowed to rest for 2 h at room
temperature. After centrifugation (10000×g for 30 min at 4°C) to
remove the precipitated proteins and bacterial cells, the supernatant
Microstructure analysis
was mixed with a double volume of cold ethanol and then stored at
4°C for 24 h. The precipitated EPS was collected by centrifugation
Fermented skim milk microstructures were examined as described
(10000×g for 30 min at 4°C), dissolved in deionized water and
by Sandoval-Castilla et al. (2004). Fermented skim milk samples
mixed with a double volume of cold ethanol and stored at 4°C for 24
(0.3 g) were excised from approximately 1 cm below the surface
h. EPS was precipitated with ethanol. It was recovered by
and mixed with 0.3 g of 3% aqueous agar solution at 45°C and the
centrifugation at 4°C 10000×g for 30 min. Total EPS (expressed as
mixtures were solidified by cooling at 20°C. The gelled samples
mg/L) was estimated in each sample by phenol–sulphuric method
were cut into 1 mm cubes and fixed in a 2% glutaraldehyde solution
(Dubois et al., 1956) using glucose as a standard (Torino et al.,
in phosphate buffer (0.1 M, pH 7.2) at room temperature for 2 h,
2001).
then held for 24 h at 4°C. The fixed samples were washed with
phosphate buffer and dehydrated in a graded ethanol series (30,
50, 70, 80 and 90%, 1 h in each) and afterwards in absolute ethanol
Fermented skim milk preparation for 24 h. These pieces were dried to critical point, and coated with
gold for 2 min by ion sputter (JFC-1600, JEOL, Japan). Samples
Several samples of fermented skim milk were manufactured using were viewed by a SEM (SEM, JEOL, Japan).
1.0% low fat milk, with various stabilizers: 0.01% (w/v) xanthan,
0.05% (w/v) carrageenan (kappa) and 0.1% (w/v) WPC-80,
dissolved at appropriate temperatures, pasteurized at 90°C for 10 Statistical analysis
min and cooled to 42°C. The samples were inoculated with 3%
starter cultures (ST0 or ST1) and fermented at 42°C for 4.5 h. The All analyses were done in triplicate. Statistical analyses were
 Zhang et al 6125

pH profile (ST0)
pH profile (ST1)
7.0 Titratable acidity (ST0) 0.8 10.0
Titratable acidity (ST1)
Cell density (ST0) 0.7
Cell density (ST1) 9.5
6.5

0.6

Viable counts (log10 CFU/ml)

9.0

Titratable acidity(%)
6.0
0.5
8.5
pH

0.4
5.5
8.0
0.3

5.0
7.5
0.2

4.5 0.1 7.0

0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5

Time(h)
Figure 1. Changes in pH, titratable acidity and viable counts of fermented skim milk by ST0 and ST1 at 42°C.

Table 1. pH, EPS and viable counts of the culture at the end of fermentation

Culture pH EPS (mg/L) Viable counts (log10 CFU/ml)

ST0 4.49±0.01 6.64±0.12 9.58±0.05
ST1 4.50±0.01 65.27±0.09 9.58±0.02

performed with SPSS 16.0. Significant differences between stabilizer added are shown in Table 2. The results (Table
treatments were tested by ANOVA. 2) show the amounts of the stabilizers had a significant
impact on the texture of low-fat fermented skim milk. In
RESULTS AND DISCUSSION this study, firmness, consistency, cohesiveness and
resistance were the major indexes. As shown in Table 2,
Characteristics of culture samples with 0.01% xanthan, 0.05% carrageenan and
0.10% WPC had the highest firmness, as well as the
Results in Figure 1 and Table 1 show that the ST1 and highest cohesiveness and resistance, respectively.
ST0 strains produced acids fast and had the same
acidification rate. There was not a significant difference in
Textural characteristics
viable counts, and the only difference was that ST1
produced EPS. In 4.5 h, the pH dropped to 4.5, the
Fermented skim milk made using ropy EPS-producing
acidity reached 80°T. ST1 had not only high acidification
ST1 culture had the lowest firmness. Similar results were
rate but produced EPS. At 4.5 h, the amount of EPS
reported by others. Amatayakul et al. (2006) found that
produced by ST1 reached 65.27 mg/L.
the firmness of fermented skim milk made using capsular
EPS-producing or ropy EPS-producing cultures was
Level of stabilizers lower than that of fermented skim milk made with non-
EPS-producing starter cultures. The results (Table 3) also
Three different stabilizers were used as fat substitutes: show that the consistency and cohesiveness of fermen-
xanthan, carrageenan and WPC. The amounts of each ted skim milk made using ST1 were lower than those
6126 Afr. J. Biotechnol.

Table 2. Effects of different levels of stabilizers on texture of fermented skim milk by ST0

Firmness (g) Consistency (g.s) Cohesiveness (g) Resistance (g.s)

ST0 88e 2140g -39fg -60e
ST0-xanthan gum 0.01% 168h 3948m -97a -126a
g j b c
ST0-xanthan gum 0.02% 105 2302 -78 -82
ST0-xanthan gum 0.05% 62b 699b -25h -14h
e f g e
ST0-xanthan gum 0.10% 88 2082 -36 -60
ST0-carrageenan 0.01% 12a 255a -7i -2i
f k g ef
ST0-carrageenan 0.02% 97 2336 -38f -57
ST0-carrageenan 0.05% 102g 2165h -45cd -76d
c c ef d
ST0-carrageenan 0.10% 69 1713 -40 -73
d d de fg
ST0-WPC 0.05% 81 1899 -43 -54
g l c b
ST0-WPC 0.10% 105 2660 -48 -86
d e
ST0-WPC 0.15% 83 2075 -39fg -53g
e i ef e
ST0-WPC 0.2% 90 2198 -41 -59
a-m
Means within the same column with different subscriptions are significantly different (P < 0.05).

Table 3. Effects of different stabilizers on texture of fermented skim milk by ST1

Firmness (g) Consistency(g.s) Cohesiveness (g) Resistance(g.s)

ST1 54a 1391b -42e -67f
ST1-xanthan gum 0.01% 103cd 2483f -82b -151a
ST1-carrageenan 0.05% 89b 1716c -50c -102c
ST1-WPC 0.10% 52a 1169a -26g -40h
a–h
Means within the same column with different subscriptions are significantly different (P < 0.05).

made using ST0 (Table 2). Fermented skim milk structure Hassan et al., 1996a, 2003). These results may be due to
appears to have strong protein–protein interactions as a interaction between EPS and milk proteins resulting in
result of the fermentation process (acid development and the increase in viscosity (Ayala-Hernández et al., 2008).
protein interaction). The fermented skim milk gel Figure 2 shows the improvement of viscosity for the three
formation process was accompanied by EPS secretion, stabilizers indicating that each has a significant effect
and the EPS interfered with protein-protein interactions, compared to the control. Carrageenan leads to the maxi-
which resulted in a soft curd (Hassan et al., 2003; Ayala- mum fermented skim milk viscosity, carrageenan binds
Hernández et al., 2009). The added xanthan gum or more water than other stabilizers, the protein and sugar
carrageenan increased the firmness, consistency and components of the milk interacted to form a network. Free
cohesiveness of the low-fat fermented skim milk ST0 or water in the system was reduced, which significantly
ST1. Fermented skim milk supplemented with WPC increased the viscosity of fermented skim milk.
combined with ST1 had lower firmness, consistency and
cohesiveness than the control fermented skim milk ST1.
Water-holding capacity

Viscosity Fermented skim milk made with ST1 exhibited higher

water holding capacity, and fermented skim milk made
The viscosity of fermented skim milk is presented in with ST0 exhibited the lowest (Figure 3). These results
Figure 2. The viscosity of sample from EPS-producing confirm the ability of EPS to bind sufficient water to
culture ST1 was higher (P < 0.05) than that of ST0. significantly affect fermented skim milk consistency.
Several studies have found that fermented skim milk Hassan et al. (1996b) found similar results. With
made with ropy EPS-producing starter cultures have carrageenan in the system, fermented skim milk had the
higher viscosity values than those made with non- EPS- highest water holding capacity. The xanthan gum or WPC
producing starter cultures (Ayala-Hernández et al., 2009; did not show good water holding capacity.
 Zhang et al 6127

750
ST1
700 ST0

650

600
Viscosity(mPa.s)

550

500

450

400

350

300
control xanthan carrageenan wpc
Figure 2. Effects of different cultures and stabilizers on the viscosity of the fermented skim milk.

Spontaneous Whey separation made with the different stabilizers. The fermented skim
milk made using EPS-producing culture ST1 had small
Figure 4 shows the changes in spontaneous whey and evenly distributed pores, and the protein network
separation of fermented skim milk. The use of ropy EPS- structure was thin (Figure 5A). The results of Figure 5
producing starter culture ST1 reduced the level of were associated with the presence of EPS, and EPS led
syneresis in fermented skim milk significantly, especially to this network structure. The fermented skim milk made
in the products made from ST1 combined with carra- with ST1 had high viscosity and good water holding
geenan. Only fermented skim milk made with xanthan capacity as well as a low level of spontaneous whey
gum showed a significant level of syneresis compared to separation. Figure 5B shows the fermented skim milk by
others. Similar results about the effect of EPS on the ST1 and carrageenan had closer and more uniform
reduction in syneresis of fermented skim milk have been network structure, and appeared to have higher water
reported by others (Marshall and Rawson, 1999; holding capacity and viscosity. ST1 combined with
Amatayakul et al., 2006). This may be due to high water- xanthan gum showed many flaps, and these flaps twist
binding capacity of EPS and reduce permeability of with casein and lactic acid bacteria, and did not integrate
serum through skim milk gel (Amatayakul et al., 2006). into the typical protein network (Figure 5C). This might be
Figure 4 shows that the control, samples with carra- because carrageenan has a much smaller molecular
geenan and WPC had no difference in the levels of weight compared with xanthan. The interaction between
spontaneous whey separation. the negative ions on the surface of carrageenan and the
positive ions on the surface of casein resulted in the tiny
net structure (Figure 5B). It binds more water preventing
Microstructure whey separation (Soukoulis et al., 2007), but the large
molecular weight of xanthan gum formed a network with
Figure 5 shows the microstructure of fermented skim milk large gaps and limited the number of caseins in the larger
6128 Afr. J. Biotechnol.

72
ST1
71 ST0

70

69
WHC(% wt/wt)

68

67

66

65

64

63

control xanthan carrageenan wpc

Figure 3. Effects of different cultures and stabilizers on WHC of the fermented skim milk.
WHC, Water-holding capacity.

18
ST1
16 ST0
spontaneous whey separation (%,w/w)

14

12

10

0
control xanthan carrageenan wpc
Figure 4. Effects of different cultures and stabilizers on spontaneous whey separation of
the fermented skim milk.
 Zhang et al 6129

Figure 5. Microstructure of the fermented skim milk (A) ST1; (B) ST1+carrageenan; (C) ST1+xanthan; (D) ST1+WPC. WPC, Whey protein
concentrate.

isolated intervals (Soukoulis et al., 2007). Lactic acid Conclusions

bacteria fermentation resulted in increased acidity and
casein aggregation. Larger particles precipitated, which Results indicate that exopolysccharides produced by ST1
caused lower water-holding capacity as well as more combined with exogenous stabilizers have a considerable
marked whey separation. Fermented skim milk made with effect on the physiochemical properties and the
ST1 combined with WPC (Figure 5D) was observed, and microstructure of fermented skim milk by ST1 compared
it is clear that casein particles did not form large aggre- with the samples using ST0. EPS-producing culture ST1
gates, but the particles interconnected to form filaments may be effective in improving the viscosity and the water
with the bigger interspace. This had a great impact on the holding capacity as well as reducing spontaneous whey
water-holding capacity of the network and its viscosity. separation. The microstructure of the fermented skim milk
The whey separation was also influenced to some extent. also showed the interactions between casein micelles
6130 Afr. J. Biotechnol.

and other components. Hassan AN, Frank JF, Schmid KA, Shalabi SI (1996a). Rheological
properties of yogurt made with encapsulated nonropy lactic cultures.
J Dairy Sci. 79: 2091-2097.
Hassan AN, Frank JF, Schmid KA, Shalabi SI (1996b).Textural
ACKNOWLEDGMENTS properties of yogurt made with encapsulated nonropy lactic cultures.
J. Dairy Sci. 79: 2098-2103.
The financial supports for this project are provided by the Hassan AN, Corredig M, Frank JF (2002). Capsule formation by
nonropy starter cultures affects the viscoelastic properties of yogurt
Earmarked Fund for Modern Agro-industrial Technology during structure formation. J Dairy Sci. 85: 716-720.
Research Systems of China (Nycytx-05-02), Post- Hassan AN, Ipsen R, Janzen T, Qvist KB (2003). Microstructure and
doctoral Funds of Jilin Province (2009100) and Research rheology of yoghurt made with cultures differing only in their ability to
produce exopolysaccharides. J. Dairy Sci. 86: 1632-1638.
Fund of Jilin University (20080017).
Lucey JA (2002). Formation and physical properties of milk protein gels.
J. Dairy Sci. 85: 281-294.
Marshall VM, Rawson HL (1999). Effects of exopolysaccharide-
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