doi: 10.1111/j.1471-0307.2012.00836.

ORIGINAL
RESEARCH

Effects of poly-c-glutamic acid on the physicochemical

characteristics of skim milk yoghurt
SU-MIN LIM, 1 JAE-YONG SHIM, 2 SEJONG OH, 3 MINSUK RHEE, 4
MOON-HEE SUNG 5 , 6 and JEE-YOUNG IMM 1 *
1

Department of Foods and Nutrition, Kookmin University, Seoul, Korea, 2Department of Food and Biotechnology,
Hankyong National University, Anseong, Korea, 3Department of Animal Science, Chonnam National University, Gwangju,
Korea, 4Division of Food Bioscience and Technology, Korea University, Seoul, Korea, 5Department of Advanced Fermentation
Fusion Science and Technology, Kookmin University, Seoul, Korea, and 6Bioleaders Corporation, Daejeon, Korea

The physicochemical and sensory properties of skim milk yoghurts containing poly-c-glutamic acid
(PGA) at different levels (0.0025, 0.005 and 0.01%) were evaluated. Addition of PGA up to 0.01% to
reconstituted skim milk (11%, w v) did not affect the growth of lactic acid bacteria or the development of
titratable acidity in yoghurt, whereas full-fat control yoghurt had reduced acid production. No changes
were found in viable cell counts of PGA yoghurts during storage (4 weeks at 4 C). The addition of PGA
(0.005%) significantly decreased syneresis in skim milk yoghurt and did not cause any undesirable effects
in sensory acceptability.
Keywords Poly-c-glutamic acid, Yoghurt, Acceptability, Syneresis.

INTRODUCTION

*Author for
correspondence. E-mail:
jyimm@kookmin.ac.kr
 2012 Society of
Dairy Technology

Low-fat or non-fat products are one of the fastest

growing segments in the food industry, and high
consumer demand continues to exist for reduced or
non-fat dairy products. During the last decade,
yoghurt consumption has continuously increased,
which is probably due to the high organoleptic
quality, reduced lactose content and health-promoting effects.
Yoghurt is a gel matrix of casein micelles
formed at reduced pH, and the conversion of milk
to yoghurt is started by the accumulation of lactic
acid (Lucey 2004). As fat provides yoghurt with a
rich body and smooth mouthfeel, fat removal leads
to significant changes in textural characteristics
and sensory quality. Non-fat yoghurts usually suffer from poor flavour and texture as well as
increased syneresis (Brennan and Tudorica 2008).
Therefore, the preparation of non-fat yoghurt that
maintains good sensory qualities is a prominent
challenge for the dairy industry (Hess et al. 1997;
El-Sayed et al. 2002).
To improve organoleptic quality of non-fat
yoghurt, increasing total solid level and or the
addition of hydrocolloids was employed. The
increased solid content similar to that of full-fat
yoghurt using skim milk powder, Na-caseinate, or

whey protein concentrate resulted in a firm body

and grainy texture with increased syneresis
(Guzman-Gonzalez et al. 2000; Mistry and Hassan
1992). The addition of pre-biotics such as b-glucan
or inulin resulted in decreased sensory quality
(Sahan et al. 2008; Guven et al. 2005). In another
study, a fat replacer (Simplesse 100) that is produced by microparticulation of whey protein has
been applied to non-fat yoghurt. When fat replacer
was used at the same concentration as anhydrous
milk fat, yoghurt containing milk replacer did not
meet the textural quality of natural yoghurt by
showing a softer curd and increased syneresis
(Barrantes et al. 1994; Tamime et al. 1995).
Poly-c-glutamic acid (PGA) is a homopolyamide
composed of D- and L-glutamic acid units. PGA is
an edible biopolymer that contains amide linkages
between its a-amino and c-carboxylic acid groups,
and it is naturally found in the mucilage of traditional fermented soybeans in Japan (Natto) and
Korea (Chungkookjang) (Park et al. 2005). PGA is
widely used in many biological industries as a drug
carrier, biological adhesive, cryoprotectant and
bitterness-relieving agent (Shih and Van 2001).
In terms of physiological functionality, rats were
fed with PGA in a form of natto mucilage (20%
of diet) resulted in increased Ca solubility in the
small intestine (Tanimoto et al. 2001), and its Ca

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absorptionpromoting effect has been confirmed in post-menopausal women, especially those with lower Ca absorption than
average (Tanimoto et al. 2007). Sung et al. (2005) reported
that PGA administration improves antibody production and
tumour regression in a B16 tumour-challenged mice.
The high water-binding properties and physiological functionality of PGA led us to evaluate its performance in non-fat
yoghurt as a fat replacer. This study was conducted to examine
the effects of PGA on the quality characteristics of non-fat
yoghurt, including fermentation speed, viable cells, microstructure, syneresis and sensory attributes.
MATERIALS AND METHODS

Materials
Skim milk and whole milk powder were purchased from Seoul
Milk Co. (Seoul, Korea). YC-X16 was obtained from Chr.
Hansen (Horsholm, Denmark) and used as a yoghurt starter.
PGA (Ca salt, MW: about 5000 kDa) was kindly provided by
Bioleaders (Daejeon, Korea). All other chemicals were
obtained from Sigma (Sigma Chemical Co., St Louis, MO,
USA) unless stated otherwise.
Starter culture
YC-X16 (0.02%), the mixed culture containing Streptococcus
thermophilus and Lactobacillus delbrueckii subsp. bulgaricus,
was inoculated into a sterilised skim milk medium (11% skim
milk powder) and incubated at 42 C. The starter culture was
freshly made prior to making the yoghurt.
Yoghurt manufacture
Skim milk powder (protein, 35%; carbohydrate, 52%; lipid,
1%; ash, 7.9%; and moisture, 4.1%) and whole milk powder
(protein, 25%; carbohydrate, 38%; lipid, 27%; ash, 6.2%; and
moisture 3.8%) were used for the preparation of non-fat and
full-fat yoghurts (11%, solid, w v), respectively. The milk powder (11%, w v) was reconstituted in distilled water and heated
at 100 C for 20 min. Fully solubilised PGA (0.0025, 0.005
and 0.01%, w w) was added to the reconstituted skim milk
prior to heating. The starter culture (YC-X16, 2.5%, w v) was
then inoculated, and the mixtures were stored at 42 C. When
the pH reached 4.6, the yoghurts were incubated at 4 C until
further analysis. At least three replicates of yoghurt preparation
trials were performed to obtain analytical data.
Titratable acidity and viable cell count
Titrable acidity (TA) was determined by the method of Dave
and Shah (1998). TA is expressed as gram of lactic acid 100 g
of yoghurt. Total lactic acid bacteria (LAB) were counted in
fresh and stored yoghurts (4 C, 2 and 4 weeks old) after cultivation on Elliker medium for 48 h at 37 C.
Syneresis
Syneresis was determined by the method of Achanta et al.
(2007). Yoghurt samples (100 g) were filtered through
424

Whatman filter paper (No.4, Whatman International Ltd.,

Madstone, UK) on the top of a funnel. After 2 h of drainage at
4 C, the volume of separated whey was measured in a graduated cylinder as an index of syneresis.

Cryo-FE scanning electron microscope (Cryo-FESEM)

A Hitachi FESEM (S-4700, Hitachi, Tokyo, Japan) was used to
observe the microstructure of the yoghurts. Yoghurt samples
were rapidly frozen in a jet freezing device (JFD 030, Bal-tec,
Balzers, Lichtenstein, Germany), after which frozen samples
were transferred (under vacuum at )140 C) to a cryochamber
using the high-vacuum cryotransfer system (VCT 100, Bal-tec,
Germany). The specimens were fractured and sputter-coated
with Pt (15 mA, 150 s). The coated specimens were then introduced to a microscope chamber where they were examined
under an accelerating voltage of 5 kV. The temperature of the
cryostage was maintained at )140 C during image processing.
Texture profile analysis
Compression tests were carried out using a TA.XT2 texture
analyzer equipped with a 50-kg load cell (Stable Micro Systems, Surry, UK). A cylindrical 25-mm-diameter probe was
used to measure the hardness of the yoghurt samples prepared
in 60-mL cups (5.5 cm diameter 5 cm height). The samples
(10 C) were placed under the probe, which then moved downwards at a constant speed of 2.0 mm s (pre-test), 1.0 mm s
(test) and 1.0 mm s (post-test). The averages of five replications were taken as the hardness values of the yoghurts.
Sensory evaluation
Non-fat yoghurt containing 0.005% PGA was compared with
full-fat yoghurt. The samples were prepared 1 day earlier than
the actual evaluations and stored at 4 C until served. Sensory
evaluation was performed by 50 untrained panellists (20 men
and 30 women, aged 2030 years). Samples coded with random three-digit numbers were provided to the panellists who
were asked to rinse their mouths with water after each tasting.
The panellists rated appearance, taste, texture and overall
acceptability using a hedonic 9-point scale, in which 9 means
most liked and 1 most disliked.
Statistical analysis
All analytical measurements were completed at least in triplicate, and statistical analysis was performed using SPSS ver. 14.0
(SPSS Inc. Chicago, IL, USA). When the analyses of variance
(ANOVA) revealed significant differences (P < 0.05), Tukeys
test was used for multiple comparison of the treatment means.
RESULTS AND DISCUSSION

Titrable acidity and viable cell counts

Changes in TA during incubation are shown in Figure 1. There
were no significant differences in TA, except in full-fat control
yoghurt. This result indicates that the addition of PGA did not
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109 cfu mL LAB after the completion of fermentation, and

there were no significant differences in viable cell count up to
4 weeks. This suggests that the addition of PGA did not result
in any undesirable effects on the growth and survival of the
starter culture for a possible expiration date (1 month). There is
no general consensus on the range of viable cell numbers in
yoghurts for exerting beneficial health effects in yoghurts,
although several countries including EU (EFSA 2010) have set
minimum LAB levels in yoghurts and or fermented milks.

Titratable acidity (%)

1.5

1.0

0.5
Full fat control
Non fat control
PGA yoghurt (0.0025%)
PGA yoghurt (0.005%)
PGA yoghurt (0.01%)

0.0
0

12

Time (h)

Figure 1 Effects of PGA addition on titratable acidity in yoghurts. PGA,

poly-c-glutamic acid.

affect the speed of acid production. The reduced acid production

of full-fat yoghurt was probably due to relatively lower lactose
and protein contents, as all yoghurt samples had the same total
nal et al. (2003) reported that TA of low-fat
solid content. U
yoghurts increases proportionally to the concentration of skim
milk solids, and higher acidities are found in yoghurts with a
greater amount of added protein (Modler and Kalab 1983).
A variety of factors affect the viable cell numbers in
yoghurts. Typically, acidity, chemical composition, inoculation
practice and storage conditions significantly affect viable cell
numbers (Donkor et al. 2006; Birollo et al. 2000).
Figure 2 shows the changes in the viable cell counts of the
yoghurts after the completion of fermentation as well as during
extended refrigerated storage. All yoghurts contained about

Full fat control

Non fat control
PGA youghurt (0.0025%)

PGA youghurt (0.005%)

PGA youghurt (0.01%)

10

Viable cells (log10 cfu/mL)

Syneresis
Syneresis is the spontaneous separation of whey in set yoghurts
and is considered a quality defect owing to its unattractive
appearance. The effects of PGA additions on syneresis are
shown in Table 1. First, the degree of whey separation was significantly influenced by fat level. Full-fat yoghurt resulted in
the lowest level of syneresis, whereas the non-fat control
yoghurt displayed the highest syneresis. Addition of up to
0.005% PGA to non-fat yoghurt significantly reduced syneresis, whereas no difference was found between PGA and full-fat
yoghurt. However, the addition of >0.005% PGA was less
effective at reducing syneresis in the non-fat yoghurt. Syneresis
occurs by continuous rearrangement of the casein matrix causing gel shrinkage (Lucey et al. 1998). Harwalkar and Kalab
(1986) reported that the pore size of the casein network is a critical factor governing the susceptibility of yoghurt to syneresis.
In the case of full-fat yoghurt, fat can be packed into the protein
network as an inert filler and thereby decrease porosity. Aziznia
et al. (2008) also suggested that positive interactions occur
between fat globules and the gel network in full-fat yoghurt.
The decreased susceptibility of syneresis in the PGA
yoghurts can be explained by the improved water-binding
effect of PGA. Increased syneresis at the 0.01% PGA might
have been caused by excessive bridging in the protein network.
The decreased uniformity and local aggregation of a protein
matrix can impair water-binding activity in a yoghurt protein
matrix. A similar trend was noted in the casein micelle and a
carrageenan mixture previously (Langendorff et al. 1999).
Considering that the effective concentrations of yoghurt stabilizers, such as locust bean gum, guar gum high methoxyl

Table 1 Effects of PGA addition on syneresis of yoghurts

4
Initial

Completion of
fermentation

Storage (Weeks)

Sample

Syneresis (mL 100 g)

Full-fat control
Non-fat control
PGA yoghurt (0.0025%)
PGA yoghurt (0.005%)
PGA yoghurt (0.01%)

41.0c
44.3a
42.1c
42.0bc
43.2ab

2
2
3
3
3

Each value is expressed as the mean SD (n = 20). Values with different

letters indicate a significant difference (P < 0.05). PGA, poly-c-glutamic
acid.

Figure 2 Changes in viable cell counts in yoghurts during the storage period.

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pectin, and gelatin, were in the range from 0.1 to 0.25%

(Koksoy and Kilic 2004), PGA effectively reduced syneresis at
much lower concentrations.

Microstructure
The microstructures of the PGA yoghurts were observed by
Cryo-SEM (Figure 3). As shown in Figure 3(a) and (b), the microstructures of the whole and non-fat yoghurts were clearly
differentiated by the presence of fat globules. The addition of
PGA resulted in significant changes in microstructure. PGA
seemed to connect and fill the pores of protein chains and consequently forming a continuous network structure. Similar to
milk protein gel, the addition of PGA affected thickness and
strands in tofu network, and PGA was located inside of soy
protein network (Lee and Kuo 2011). A dense and less voidspaced interrelated protein network was found with 0.005%
PGA (Figure 3d). The yoghurt containing 0.01% PGA showed
some irregular network structure with larger void spaces (Figure 3e). These results correspond with the increased syneresis
of yoghurt as mentioned previously in Table. 2.

The microstructure of yoghurt can vary depending on the

type of stabilizer. Addition of gelatin (0.5%) resulted in no significant changes in yoghurt structure, whereas a fibrillar microstructure of large casein clusters was observed in the presence
of carrageenan (0.4%) (Kalab et al. 1975). Lee and Kuo (2011)
reported that increased electrostatic repulsion owing to the
negatively charged glutamic acid moiety of PGA (1000
1500 kDa, 0.10.2%) caused delay in tofu gelation. This, in
turn, weakened the tofu structure by reducing the number of
hydrophobic interactions between soy proteins. However, PGA
cannot impose significant electrostatic repulsion in yoghurt
structure formation considering the acidic pH of yoghurt.

Hardness
The effects of PGA addition on the hardness of yoghurt were
determined using a texture analyzer. As shown in Table 2, fat
content significantly affected the hardness of yoghurt. Non-fat
yoghurt demonstrated greater hardness than that of the full-fat
control. This result was consistent with a report of Yazici and
Akgun (2004). Sodini et al. (2004) reported that the firmness

(a)

(b)

(c)

(d)

(e)

Figure 3 Cryo-scanning electron micrographs of yoghurts. (a) Full-fat control yoghurt, (b) Non-fat control yoghurt, (c) PGA yoghurt (0.0025%), (d) PGA
yoghurt (0.005%), (e) PGA yoghurt (0.01%). PGA, poly-c-glutamic acid.

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Table 2 Effects of PGA addition on hardness values of yoghurts

Sample

Hardness value (g)

Full-fat control
Non-fat control
PGA yoghurt (0.0025%)
PGA yoghurt (0.005%)
PGA yoghurt (0.01%)

47.3c
65.2b
78.9ab
89.3a
76.2ab

5
4
9
9
3

Each value is expressed as the mean SD (n = 5). Values with different

letters indicate a significant difference (P < 0.05). PGA, poly-c-glutamic
acid.

of yoghurt is greatly influenced by total solid content and especially its protein content because protein would increase crosslinking in the protein network. The hardness value of non-fat
yoghurt further increased as the concentration of PGA was
increased up to 0.005%.
The interactions between PGA and casein can be observed in
Figure 3(d), and the reinforced gel internal microstructure
could be a reason for increased firmness. However, the hardness value of non-fat yoghurt containing 0.01% PGA was
lower than that with 0.005% PGA yoghurt. A similar trend was
reported by Maroziene and Kruif (2000). In this report, pectin
molecules adsorbed onto casein micelles formed a stable system at low concentrations. As the pectin concentration was
increased, the casein micelles became fully covered leading to
reduced flocculation.

Sensory quality
The acceptability of PGA yoghurt (0.005%) was compared
with that of full-fat yoghurt. As shown in Figure 4, no significant differences were found in appearance, flavour, texture and
overall acceptability between the samples. Although the addition of PGA resulted in increased hardness (Table 2), it did not

10
Full fat yoghurt
Non fat yoghurt (0.005% PGA)

Sensory score

0
Appearance

Flavor

Texture

Overall

Acceptability

have any negative effect on sensory acceptability. This result is

consistent with a report by Mitsuiki et al. (1998) that indicated
PGA did not exhibit its own taste.
Creaminess is one of the key attributes governing the overall
acceptability in low-fat non-fat yoghurt, and the creaminess
perception is inversely proportional to the fat content in yoghurt
(Alting et al. 2009). On the basis of the result, the perceived
creaminess could be improved in the presence of PGA in nonfat yoghurt.
Consumers continue to require healthy non-fat products.
PGA is a high MW natural biopolymer and has various physiological functionalities. The addition of PGA to non-fat yoghurt
did not impair quality characteristics such as fermentation
speed, viable cell counts and sensory quality. The syneresis of
non-fat yoghurt was improved by the addition of PGA, and the
high water-binding activity of PGA exerted a positive effect by
providing a creamy mouthfeel. Therefore, PGA has great
potential to replace conventional stabilizers such as gelatin in
premium non-fat yoghurts.
ACKNOWLEDGEMENT
This work was supported by a grant from the Next-Generation BioGreen 21 Program (No. PJ0083272011), Rural Development
Administration, Republic of Korea. This work was also supported
by a grant from Kookmin University received in 2010. The authors
are thankful for the financial support.

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