Influence of starter culture type and incubation temperatures on rheology and microstructure of low...

ORIGINALRESEARCH Influence of starter culture type and incubation

temperatures on rheology and microstructure of low fat setyoghurt

HABIB ABBASI,1* MOHAMMAD EBRAHIMZADEH MOUSAVI,1

MOHAMMAD REZA EHSANI,1 ZAHRA EMAM D-JOMEA,1 MOHARAMVAZIRI,2 JAMSHID RAHIMI3 and SOMAYEH AZIZNIA4

1Department of Food Science and Engineering, Faculty of Biosystem Engineering, University of Tehran, Karaj, 2Depart-ment of Food Science and Technology, Azad Islamic University, Branch of Sanandaj, 3Department of Food Science andEngineering, Faculty of Agriculture, Urmia University, Urmia, Iran, 4Department of Food Science and Engineering,Faculty of Agriculture, Islamic Azad University of Shoudhtar Branch

*Author forcorrespondence. E-mail:[email protected]

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The effects of different cultures and incubation temperatures on the physical properties of low fatyoghurts were investigated. The samples were incubated with exopolysaccharide (EPS)-producing and

non-EPS-producing cultures at 37, 42 and 45�C. All measured parameters except firmness were influ-enced by culture type and incubation temperature. Firmness, G¢ and G¢¢ were maximised at 42�C for bothcultures. Increased incubation temperature and EPS culture led to a higher water-holding capacity but

lower syneresis, G¢ and G¢¢. The EPS treatment incubated at 37�C showed even lower syneresis thannon-EPS treatments incubated at higher temperatures.

Keywords Low fat set yoghurt, Rheology, Incubation temperature, Exopolysaccharide, Microstructure.

INTRODUCT ION

The physical properties (texture and rheology) ofset yoghurt are some of the main quality parame-ters that play an important role in consumeracceptance. Two major defects in set yoghurt arelow firmness and a high level of syneresis orwhey separation on the surface (Lee and Lucey2004). Fortification of liquid milk with dried dairyingredients of at least 150–160 g ⁄L is a commonpractice in yoghurt manufacturing (Shah 2003).The intention is to increase total solids, resultingin a firmer product with lower levels of syneresis.This implies that dried dairy ingredients arerequired to at least a level of 30–40 g ⁄L in thefortification-raising production costs (Amatayakulet al. 2005). Generally, the increase in total solidsof liquid milk causes an increase in density of theprotein matrix in the microstructure and the reduc-tion of syneresis (Kalab et al. 1983). There hasbeen an increasing trend of using yoghurt startercultures that are able to produce exopolysaccha-ride (EPS) during yoghurt manufacture. This isdue to their water-binding ability and texture-promoting properties (Broadbent et al. 2003). TheEPS-producing starter cultures can be categorisedinto two groups, capsular EPS-producing startercultures and ropy EPS-producing starter cultures(Cerning 1990). In some cases, bacteria can

produce both forms of EPS. Both types of EPS-producing starter cultures have been reported toreduce syneresis in set yoghurt significantly(Broadbent et al. 2003), although it was reportedthat capsular EPS and ropy EPS-producing startercultures affected viscoelastic properties of setyoghurt differently (Hassan et al. 2002). Hassanand Frank (1997) observed that set yoghurt madeusing EPS-producing starters had lower firmnessthan the control sample. The opposite result wasfound in the experiment carried out by Jaros et al.(2002). Ropy, thermophilic lactic acid bacteriastarter cultures for yoghurt production are com-monly used in some countries of the EuropeanUnion because the addition of stabilisers is pro-hibited in yoghurts (De Vuyst and Degeest 1999).It may be possible to reduce or replace the use ofdried dairy ingredients for yoghurt fortification bycombining dried dairy ingredients and EPS-pro-ducing starter cultures.Incubation temperature is another factor that has

major effects on the physical properties of yoghurt.The rheological properties of acid gels are affectedby different starter concentrations and incubationtemperatures, which directly affect the rate of acidi-fication (Lee and Lucey 2004). Kristo et al. (2003)reported that small deformation rheological proper-ties, such as G¢max, of fermented milk products,was affected by different inoculum concentrations

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and incubation temperatures. The G¢ values ofyoghurt gels increased with a decrease in incuba-tion temperature (Kristo et al. 2003). In contrastwith these results, it has been reported that yoghurtgels made at a lower incubation temperature exhib-ited lower G¢ values (Haque et al. 2001). Acidmilk gels made at a higher incubation temperatureexhibited greater whey separation than acid milkgels formed at lower temperature (Lee and Lucey2004). High incubation temperatures resulted in adecrease in fracture stress for glucono-d-lactone-induced gels and an increase in fracture strain(Lucey et al. 1997). Gels made at higher inocula-tion rates and incubation temperatures exhibitedhigher yield stress and maximum loss tangentvalues, respectively (Lee and Lucey 2004). As fewstudies on the combined effect of EPS cultures andincubation temperatures on physical properties andmicrostructure of low fat set yoghurt have beencarried out, the aim of this study was to investigatethe effects of these factors on the above mentionedproperties.

MATER IALS AND METHODS

Starter culturesYoghurt starter, X-11(EPS-producing which con-sisted of Lactobacillus delbrueckii subsp. bulgari-cus and Streptococcus thermophilus) and CH-1(non-EPS-producing which consisted of Lactoba-cillus delbrueckii subsp. bulgaricus and Strepto-coccus thermophilus) were obtained from Chr.Hansen, Copenhagen, Denmark.

Preparation of yoghurtSkim milk powder (Pak Dairy Company, Tehran,Iran) was reconstituted and mixed with fresh creamto standardise the fat content to 15 g ⁄L. Total sol-ids of samples were 120 g ⁄L. The resulting recon-stituted milk was heat-treated in a batch pasteuriserat 90�C for 10 min. The heated milk was cooled to65�C and homogenised (APV Gaulin Lab60,Lubeck, Germany) at 200 MPa. It was then furthercooled to incubation temperature and portionedinto three equal batches. The batches were inocu-lated with 20 g ⁄L starter cultures (X-11 and CH-1)and incubated at different temperatures (37, 42 and45�C) until the pH of samples reached 4.6. Theyoghurt samples were cooled and stored at 4�C.

FirmnessThe firmness of yoghurt samples was measuredwith a Texture analyser, (Hounsfield H5KS, Red-hill England). A 34 mm diameter solid rod withconstant crosshead velocity of 0.5 mm ⁄ s wasplaced in the cylindrical containers (diameter ofcontainer was 3:1 compared to probe) to sampledepth of 35 mm holding the test sample. A 500 gload cell was used. The firmness was measured as

the maximum force (N) required to penetrate thesample to 35-mm depth.

SyneresisThe whey separation of yoghurt gels was deter-mined using the method of Lucey et al. (1998).After preheating, 220 g of milk was inoculatedwith working starter culture (X-11 and CH-1);inoculated milks were transferred to 250 mL glassvolumetric flasks. The milk samples were incu-bated in a temperature-controlled incubator at 37,42 and 45�C, until the pH of the milk reached 4.6.Four flasks were used for each treatment. Thewhey present on the yoghurt surface during fer-mentation was measured. The degree of whey sep-aration was calculated with the following equation:Whey (g ⁄100 g) = weight of whey ⁄ total weight

of milk · 100.

Water-holding capacityWater-holding capacity (WHC) was measuredusing the centrifuge method. A 50 g sample wascentrifuged at 1500 g for 20 min at 10�C. Thesupernatant was removed, and the pellet weightwas recorded. Water-holding capacity was calcu-lated as:Pellet weight ⁄ initial sample weight · 100.

Rheological propertiesRheological measurements were performed using aUDS-200 Paar Physica rheometer (Physica Mess-technik GmbH, Stuttgart, Germany). The measur-ing geometry consisted of two parallel plates witha gap size of 1 mm. Rheological properties werestudied using a dynamic frequency sweep experi-ment with the measurement of storage modulus(G¢) and loss modulus (G¢¢). Test conditions wereat a frequency of 0.1 to 50 Hz. Because there weredifferent treatments and each sample was differentfrom another before measurement of rheologicalproperties of each sample, the linear viscoelasticregion was determined by strain sweep test(Patocka et al. 2005). All the experiments werecarried out at 4�C.

MicrostructureSamples were viewed in a scanning electronmicroscope (XL Series, Model XL30; Philips,Eindhoven, the Netherlands) operated at 25 kVfollowing the method of Sandoval-Castilla et al.(2004) with some modifications. Samples ofyoghurt (0.3 g) were excised from approximately1 cm below the surface and mixed with 0.3 g of3 g ⁄100 mL aqueous agar solution at 45�C andthese mixtures were solidified by cooling to 20�C.The gelled samples were cut into 1 mm cubes andfixed in a 2.5 mL ⁄100 mL glutaraldehyde solutionin phosphate buffer (0.1 M, pH 7.2) as a primaryfixative to crosslink proteins at room temperature

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for 2 h, followed by 24 h at 4�C. The fixed sam-ples were washed with phosphate buffer (pH 7.2)and dehydrated in a graded ethanol series (30, 50,70, 80 and 90 mL ⁄100 mL), 1 h in each, and laterin absolute ethanol for 24 h, and then criticalpoint-dried in liquid nitrogen. Dried sections werefractured with a blade and fragments weremounted on aluminum Scanning Electron Micro-scope (SEM) stubs, vacuum gold coated for 540 sin a sputter-coater (type SCD 005; Baltec Inc.,Balzers, Switzerland) and observed at 25 kV.

Statistical analysisA 2-factor 3 · 2 ANOVA with interaction was usedto investigate the effects of starter culture type andincubation temperatures on the physical and rheo-logical properties of yoghurt gels. Each experimentwas performed in triplicate. Level of significancewas established at P < 0.05. The statistical analysissystem, MINITAB version 14 (Minitab Inc., StateCollege, Pensylvania, USA), was used to performall statistical analyses.

RESULTS AND DISCUSS ION

SyneresisWhey separation refers to the spontaneous appear-ance of whey (serum) on milk gel surfaces and iscalled wheying-off (Lucey et al. 1998). Starter cul-ture and incubation temperature significantly(P < 0.01) affected whey separation, but the inter-active effect was not significant, (Table 1).Yoghurts incubated at 37 and 42�C as well as thoseincubated at 42 and 45�C were not statistically dif-ferent in syneresis. It was found that yoghurtsmade using EPS culture had a lower level of syner-esis than those produced with non-EPS culture atgiven temperatures (Figure 1). Similar results havealso been reported by other studies (Marshall andRawson 1999). Exopolysaccharide culture anddecreased incubation temperature decreased the gelsyneresis (Figure 1), in accordance to the findingsof Marshall and Rawson (1999). This might be due

to the high water-binding capacity of EPS(De Vuyst and Degeest 1999) as well as modifica-tions of yoghurt microstructure by EPS cultures(Hassan et al. 2002). In all treatments minimumsyneresis was obtained at 37�C. This was inagreement with other studies which showed thata lower incubation temperature led to lowersyneresis value (Lee and Lucey 2004). Limitedrearrangements in protein networks at lower tem-peratures probably led to less whey separation(Lucey 2002).

Water-holding capacityThe WHC of samples was affected by starter typeand incubation temperature but interaction of thesefactors was not significant (P < 0.05). There wasno significant difference between samples incu-bated at 37 and 42�C. However, differencesbetween samples incubated at 42 and 45�C as wellas between those incubated at 37 and 45�C werestatistically significantly different (P < 0.5). TheEPS treatments had higher WHC than non-EPStreatments (Figure 2). For both starter cultures, thehighest level of WHC was seen at 37�C. The dif-ference in the WHC of yoghurts can be explained

Table 1 Analysis of variance for rheological and physical parameters

Independent variables

S IT S · IT

df MS P df MS P df MS P

Synersis 1 0.73413 * 2 0.42743 * 2 0.02936 NS

WHC 1 25.514 * 2 42.677 * 2 0.338 NS

Firmness 1 0.02408 NS 2 0.19540 ** 2 0.07090 *

G¢ 1 357765 ** 2 32983 ** 2 8160 NS

G¢¢ 1 34133.3 ** 2 2186.3 * 2 902.3 NS

S, starter culture type; IT, incubation temperature; S · IT, interaction between starter culture type and incubation tempera-

ture; NS, not significant; WHC, water-holding capacity; MS, Mean square.

*,**Significantly different at P < 0.05 and P < 0.01, respectively.

Figure 1 Syneresis values of yoghurt samples produced with

different starter culture and incubation temperatures. : non-

EPS-producing starter culture at 37�C; : non-EPS-producing

starter culture at 42�C; : non-EPS-producing starter culture

at 45�C; : EPS-producing starter culture at 37�C; : EPS-

producing starter culture at 42�C; : EPS-producing starter

culture at 45�C. EPS, exopolysaccharide.


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by the presence of polysaccharidic material alone,as suspected by Hassan et al. (1996).

FirmnessFigure 3 shows the effect of different starter andincubation temperatures on the firmness of sam-ples. The firmness of samples was not affected bystarter type, but by the incubation temperature(P < 0.01) and interactive effects between the twofactors (P < 0.05). The maximum values of firm-ness for both starters were seen at 42�C. There wasno significant difference in firmness between sam-ples incubated at 37 and 42�C. However, the sam-ples incubated at 45�C were significantly differentfrom those incubated at 37 and 42�C.

Rheological propertiesFigure 4 shows the storage modulus of yoghurtsamples produced with different starter cultures atdifferent incubation temperatures taken at 1 Hz.The effects of starter type and incubation

temperature on G¢ of yoghurt samples were signifi-cant (P < 0.01) but the interactive effect was not.Maximum and minimum G¢ for both cultures wereobtained by incubation at 42 and 37�C, respec-tively. Similar results have previously beenreported for yoghurt gels (Haque et al. 2001).Although G¢ obtained at 45�C was slightly higherthan that of 37�C, the difference was not statisti-cally significant (P < 0.05). In agreement with pre-vious studies, samples produced with EPS starterhad lower G¢ than samples with non-EPS starter(Hassan et al. 2003). When incubation temperatureincreased, there was an increase in hydrophobicinteractions which contributed to a more compactconformation and a contraction of casein particles.The increased G¢ for yoghurt gel incubated athigher temperature (42�C) could be due to

Figure 2 Water-holding capacity values of yoghurt samples

produced with different starter culture and incubation temper-

atures. : non-EPS-producing starter culture at 37�C; : non-


starter culture at 45�C; : EPS-producing starter culture at

37�C; : EPS-producing starter culture at 42�C; : EPS-

producing starter culture at 45�C. EPS, exopolysaccharide.

Figure 3 Firmness values of yoghurt samples produced with

different starter culture and incubation temperatures. : non-


starter culture at 42�C; : non-EPS-producing starter culture

at 45�C; : EPS-producing starter culture at 37�C; : EPS-

producing starter culture at 42�C; : EPS-producing starter

culture at 45�C. EPS, exopolysaccharide.

Figure 4 Storage modulus (G¢) values of yoghurt samples

produced with different starter culture and incubation

temperatures at frequency 1 Hz. : non-EPS-producing starter

culture at 37�C; : non-EPS-producing starter culture at

42�C; : non-EPS-producing starter culture at 45�C;: EPS-producing starter culture at 37�C; : EPS-producing

starter culture at 42�C; : EPS-producing starter culture at

45�C. EPS, exopolysaccharide.

Figure 5 Storage modulus (G¢) values of yoghurt samples


atures as a function of frequency. - - : EPS-producing starter

culture at 37�C; -d- : EPS-producing starter culture at 42�C;- - : EPS-producing starter culture at 45�C; -·- : non-EPS-producing starter culture at 37�C; -¤- : non-EPS-producing

starter culture at 42�C; -*- : non-EPS-producing starter cultureat 45�C. EPS, exopolysaccharide.



increased interaction between casein particles(Lucey 2002). The EPS and proteins had similarcharges at pH above the isoelectric point of the pro-teins (De Kruif and Tuinier 2001) during yoghurtfermentation, resulting in a repulsive force betweenEPS and proteins. This incompatibility betweenEPS and proteins might result in depletion-inducedattraction of casein micelles by EPS, leading to theformation of acid milk gel filled with EPS (DeKruif and Tuinier 2001). This might cause the dif-ference in the protein aggregation mechanisms andthe structure of protein network between yoghurtsmade using non-EPS and EPS-producing starters.The G¢ of different yoghurt samples as the functionof frequency is shown in Figure 5.Figure 6 shows G¢¢ values of yoghurt samples

produced with different starters and incubation

temperatures at a frequency of 1 Hz. The type ofstarter culture (P < 0.01) and incubation tempera-ture (P < 0.05) had significant effects on G¢¢. Inter-active effects, however, were not significant(P < 0.05). Samples incubated at 37 and 42�C hadsignificant differences, while the other treatmentswere not statistically significant. Figures 7 and 8show the G¢ and G¢¢ of yoghurt samples producedwith EPS and non-EPS cultures at different incuba-tion temperatures, respectively, as a function of fre-quency. All yoghurts exhibited typical behaviourcharacteristics of a weak viscoelastic gel, with G¢greater than G¢¢ at all frequencies, both showingsome frequency dependence. The higher the fre-quency, the higher was the G¢. Similar results havealso previously been reported (Amatayakul et al.2005).

MicrostructureYoghurt samples produced at a low incubationtemperature (37�C) showed a regular and compactnetwork with lesser and smaller pores (Figure 9:E37 and C37). In samples produced with EPS cul-ture, EPS strands were observed to be attached tothe cell body of starter bacteria as well as proteinnetworks (Figure 9: E37, E42 and E45). Exopoly-saccharide and small pores can influence waterabsorption in yoghurt gel networks, resulting inreduced syneresis and increased WHC of samplesproduced at 37�C (Figure 9: E37 and C37).Figure 9 (E42) shows the micrograph of yoghurtproduced at 42�C using EPS culture. Exopolysac-charide strands can be observed between and wasattached to the protein network. These strandsmight be responsible for the different behaviour ofthese yoghurts compared with yoghurt samplesproduced using non-EPS culture.

Figure 6 Loss modulus (G¢¢) values of yoghurt samples


atures at frequency 1 Hz. : non-EPS-producing starter cul-

ture at 37�C; : non-EPS-producing starter culture at 42�C;: non-EPS-producing starter culture at 45�C; : EPS-produ-

cing starter culture at 37�C; : EPS-producing starter culture

at 42�C; : EPS-producing starter culture at 45�C. EPS,exopolysaccharide.

Figure 7 Storage modulus (G¢) and loss modulus (G¢¢) valuesof yoghurt samples produced with EPS-producing starter cul-

ture at different incubation temperatures as a function of fre-

quency, - - : EPS-producing starter culture at 37�C;-d- : EPS-producing starter culture at 42�C; - - : EPS-

producing starter culture at 45�C; -·- : non-EPS-producingstarter culture at 37�C; -¤- : non-EPS-producing starter

culture at 42�C; -*-: non-EPS-producing starter culture at45�C. EPS, exopolysaccharide.

Figure 8 Storage modulus (G¢) and loss modulus (G¢¢) valuesof yoghurt samples produced with non-EPS starter culture at

different incubation temperatures as a function of frequency,

- - : EPS-producing starter culture at 37�C; -d- : EPS-

producing starter culture at 42�C; - - : EPS-producing starter

culture at 45�C; -·- : non-EPS-producing starter culture at37�C; -¤- : non-EPS-producing starter culture at 42�C;-*-: non-EPS-producing starter culture at 45�C. EPS,exopolysaccharide.



The microstructure of yoghurts made at higherincubation temperatures (42 and 45�C) had largerpores with a less regular network. The higher thetemperatures, the larger were the pores (Figure 9:E42 and C42 compared to Figure 9: E45 andC45). Similarly, Lee and Lucey (2004) showedthat the microstructure of yoghurt gels made at ahigher incubation temperature (45.7�C) exhibitedlarger pores and a less interconnected or branchedprotein network than gels made at 40�C. At higherincubation temperatures, extensive rearrangementsin protein networks occurred, which promotedwhey separation related to the unstable gel net-work. However, in gels produced with EPS cul-ture, EPS could partially compensate forrearrangements of casein particles in the gel net-work, which were the driving forces responsiblefor whey separation. In other words, the highwater-binding capacity of EPS could decrease thesyneresis of gel samples produced using EPS-pro-ducing culture more than those produced usingnon-EPS culture.

Yoghurt gels incubated at 37�C exhibited a moreobviously branched and homogenous intercon-nected protein network. The gel network under-went less obvious structural changes than thosemade at 42�C and especially at 45�C (Figure 9).Moreover, in yoghurt gels made at 37 and 42�C,EPS could be seen obviously attached to the cellbody of starter culture cells and between proteinnetworks. The incompatibility between casein andEPS may be explained by observed differencesbetween gels produced using EPS and non-EPScultures. This incompatibility might also be respon-sible for lower G¢ and G¢¢ values in gels made withEPS culture compared with those made with non-EPS culture, as previously reported by other stud-ies (Hassan et al. 2003).

CONCLUS IONS

This study showed that the type of starter culturesand incubation temperatures are significant factorsaffecting the physical and rheological properties

Figure 9 Scanning electron micrographs of yoghurt samples produced with different starter culture and incubation tempera-

tures. E-37: EPS-producing starter culture at 37�C; C37: non-EPS-producing starter culture at 37�C; E-42: EPS-producing star-ter culture at 42�C; C-42: non-EPS-producing starter culture at 42�C; E-45: EPS-producing starter culture at 45�C; C-45: non-EPS-producing starter culture at 45�C. White ‹ shows the EPS strands as attached to cell body and between protein network

(E37 and E42) : lactobacilli, : streptoccocci. The higher the incubation temperature, larger are pores for both cultures espe-

cially at 45�C. Samples made at lower incubation temperature exhibited regular and more homogenous networks. EPS, exopoly-

saccharide.



and microstructure of yoghurt gels. Using EPS-producing starter culture resulted in decreased syn-eresis, storage and loss moduli and increasedWHC of yoghurt gels compared with the non-EPSculture. The use of an intermediate incubation tem-perature (42�C) may provide yoghurt with higherfirmness and storage moduli.

A C KNOWL EDG EMEN T S

We are deeply thankful to Mr. R. Rouhani, Mr. M.Rezaei and the rest of the staff in the pilot plant andR&D laboratory at Pak Dairy Company, Tehran, Iran.This study was funded by R&D section of Pak DairyCompany, Tehran, Iran.

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