amylose–potassium oleate inclusion complex in plain set-style yogurt

E:FoodEngineering&PhysicalProperties

Amylose–Potassium Oleate Inclusion Complexin Plain Set-Style YogurtMukti Singh, Jeffrey A. Byars, and James A. Kenar

Abstract: Health and wellness aspirations of U.S. consumers continue to drive the demand for lower fat from inherentlybeneficial foods such as yogurt. Removing fat from yogurt negatively affects the gel strength, texture, syneresis, andstorage of yogurt. Amylose–potassium oleate inclusion complexes (AIC) were used to replace skim milk solids to improvethe quality of nonfat yogurt. The effect of AIC on fermentation of yogurt mix and strength of yogurt gel was studied andcompared to full-fat samples. Texture, storage modulus, and syneresis of yogurt were observed over 4 weeks of storage at4 °C. Yogurt mixes having the skim milk solids partially replaced by AIC fermented at a similar rate as yogurt sampleswith no milk solids replaced and full-fat milk. Initial viscosity was higher for yogurt mixes with AIC. The presence of3% AIC strengthened the yogurt gel as indicated by texture and rheology measurements. Yogurt samples with 3% AICmaintained the gel strength during storage and resulted in low syneresis after storage for 4 wk.

Keywords: amylose–fatty acid complex, rheology, storage, syneresis, texture, yogurt

IntroductionIn the presence of hydrophobic ligands such as fatty acids, amy-

lose undergoes conformational changes to form amylose–fatty acidinclusion complexes. The formation of amylose–fatty acids inclu-sion complexes has been extensively studied and recently reviewedin depth (Putseys and others 2010; Obiro and others 2012). Stud-ies of these types of amylose complexes have dealt mostly withtheir effect on the pasting properties of starch granules, structureof the complexes, thermodynamic properties (Ghiasi and others1982; Evans 1986; Biliaderis and Tonogai 1991; Eliasson 1994;Svensson and others 1998; Gelders and others 2006; Mira andothers 2007a, b), and their ability to retard retrogradation of starchin baked products (Keetels and others 1996). Amylose–lipid com-plexes have been proposed and examined as a means of deliveringligands with desired functional properties in food products. Oneimportant use is to deliver unsaturated fatty acids, nutraceuticals(Cohen and others 2008), and volatile flavor (Heinemann and oth-ers 2005; Wulff and others 2005; Conde-Petit and others 2006;Itthisoponkul and others 2007) or aroma (Jouquand and others2006; Tietz and others 2008) compounds while protecting themfrom oxidation.

Recently, we have been examining the preparation and proper-ties of starch materials containing amylose–sodium palmitate in-clusion complexes obtained by blending jet-cooked high-amylosecorn starch with aqueous solutions of sodium palmitate (Fanta andothers 2010; Byars and others 2012). At appropriate fatty acid saltconcentrations to effectively complex the amylose, a low-viscositydispersion results that displays no evidence of starch retrograda-tion upon standing for extended periods. These dispersions ex-hibit polyelectrolytic characteristics, and at high pH, electrostaticrepulsion between the anionic carboxylate head groups of the

MS 20131368 Submitted 9/26/2013, Accepted 12/30/2013. Authors are withUSDA, Agricultural Research Services, Natl. Center for Agricultural Utilization Re-search, 1815 N. Univ. St., Peoria, IL, 61604, USA. Direct inquiries to author Singh(E-mail: [email protected]).

Mention of trade names or commercial products in this publication is solely forthe purpose of providing specific information and does not imply recommen-dation or endorsement by the U.S. Dept. of Agriculture. USDA is an equalopportunity provider and employer.

complexed fatty acid salt stabilizes the amylose polymer in solu-tion and inhibits intermolecular interactions between the amylosemolecules. As the pH of the dispersion is lowered, the carboxylateanion is protonated and converted into its corresponding fatty acidthat reduces the electrostatic repulsion of the amylose complex.When this occurs, physical associations form between the amylosemolecules generating a stable 3-dimensional gel network (Byarsand others 2012).

Fat plays a significant role in gel strength, texture, and synere-sis of yogurt. Stabilizers in low-fat yogurts are used to strengthenthe 3-dimensional network structure formed by casein micellesat low pH. Various nondairy ingredients such as starch, wheyprotein concentrates, gelatin, and hydrocolloids have been addedto yogurt as fat replacers and to modify the rheological prop-erties (Mistry and Hassan 1992; Keogh and O’Kennedy 1998;Guzman-Gonzalez and others 1999; Decourcelle and others 2004;Sodini and others 2004). The addition of whey protein concen-trates can lead to powdery taste, excessive acid development, ex-cessive firmness, higher syneresis, and grainy texture (Mistry andHassan 1992; Guzman-Gonzalez and others 1999). Addition ofstarch increases the viscosity of yogurt, but some starches impartan undesirable taste and promote phase separation. Addition ofinulin improved the texture of no fat yogurt but increased yogurtsyneresis (Pimentel and others 2011). In our previous studies, wefound that starch–lipid composites strengthened low-fat set-styleyogurts (Singh and Byars 2009; Singh and Kim 2009).

The objective of this study was to examine the suitability ofamylose–fatty acid salt complexes as stabilizers in nonfat yogurt.We chose potassium oleate instead of sodium palmitate as used inour previous studies for nutritional superiority. These complexedstarches can be simply prepared on large scale using commerciallyavailable steam jet cookers and renewable low-cost commodityamylose-containing starches and fatty acid salts.

Materials and Methods

Preparation of potassium oleateHigh-amylose corn starch (AmyloGel 03003) containing 70%

apparent amylose and a moisture content of 11.45% was a prod-uct of Cargill, Minneapolis, Minn., U.S.A. Percent moisture was

C© 2014 Institute of Food Technologists R©E822 Journal of Food Science � Vol. 79, Nr. 5, 2014 doi: 10.1111/1750-3841.12378

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Starch–potassium oleate yogurt fermentation . . .

calculated from weight loss after drying at 100 °C under vac-uum, and all starch weights are given on a dry weight basis.Oleic acid, 99%, was purchased from Nu-Check Prep (Elysian,Minn.). Ethanol (95%) was purchased from Decon Laborato-ries, Inc. (King of Prussia, Pa., U.S.A.). Potassium hydroxide,>85%, pellets/certified ACS, was purchased from Fisher Chemical(Pittsburgh, Pa., U.S.A.).

The general procedure of de Mul and coworkers was used forthe preparation of potassium oleate (de Mul and others 2000).A solution of oleic acid (33.53 g, 0.118 mol) in 95% ethanol(130 mL) was prepared by stirring and warming to 50 °C. Tothe solution, 51 mL of 2.53 M KOH in 95% ethanol was slowlyadded while stirring. After addition, the solution was stirred anadditional 30 min at 50 °C and then removed from the heat andcooled to room temperature (approximately 22 °C). The solutionwas further cooled to 4 °C and allowed to crystallize undisturbedovernight. The resulting crystals were vacuum filtered in a Buchnerfunnel, washed with cold 95% ethanol, and vacuum-dried ina desiccator. The yield of potassium oleate obtained was 65.1%(24.5 g).

Preparation of amylose corn starch–potassium oleateinclusion complexes (AIC) by jet cooking

The general procedure described by Fanta and coworkers wasused to prepare the high-amylose corn starch–potassium oleatecomplexes (Fanta and others 2010). High-amylose starch (165.0g) was dispersed in 2700 mL of deionized water, and the slurry waspassed through a Penick & Ford laboratory model steam jet cooker(Penick and Ford, Ltd., Cedar Rapids, Iowa, U.S.A.) operatingunder excess steam conditions. Temperature in the hydroheaterwas 140 °C, the steam back pressure was 380 kPa, and the steamline pressure from the boiler was 550 kPa. The flow rate throughthe jet cooker was about 1 L/min. The hot, jet-cooked starchdispersion was collected. The percent starch solids in the cookeddispersion were determined by freeze-drying accurately weighedportions of this material. Over 95% of initial weight of starch wascollected in the jet-cooked dispersion.

Potassium oleate (8.66 g, equal to 7.50 wt% of the weight ofamylose in the starch) sample was dissolved in 300 mL of deionizedwater at 95 °C, and the resulting clear solution was added to thehot starch dispersion immediately after it was collected from thecooker. The resulting dispersion was slowly stirred for 2 min, andthen transferred to a 4 L beaker and cooled in an ice-water bath to25 °C. The solids of final cooled dispersion was determined to be5.40 wt%. The materials were stored at 4 °C until use. A portionof the material was also freeze-dried and stored for later use.

Yogurt mix preparationNonfat milk powder containing 34.7% protein, 52.7% carbo-

hydrates, and 0% fat was purchased from local market (Carnationinstant nonfat dry milk; Nestle USA Inc., Solon, Ohio, U.S.A.).Full-fat milk powder containing 25.7% protein, 36.5% carbohy-drates, and 28.2% fat was purchased online (Nido instant full-fatmilk powder, Nestle, Netherlands).

The yogurt mixes were prepared by mixing nonfat milk pow-der, AIC (0%, 1%, 2%, and 3%), and deionized water, to a totalsolid content of 17%. Full-fat control yogurt mix was preparedsimilarly using full-fat milk powder. Mixes were heated to 80 °Cin a water bath, and then cooled to 40 °C. Stock culture wasprepared by dissolving of freeze-dried yogurt culture containingStreptococcus thermophilus, Lactobacillus delbrueckii subspecies bulgari-cus, Lactobacillus acidophilus, and Bifidobacterium (Yo-Fast 88; 200 U;

Chr. Hansen, Milwaukee, Wis., U.S.A.) in deionized water to aconcentration of 1 U/mL. Stock culture was added to yogurt mixat the rate of 1 U/L at 40 °C.

The inoculated yogurt mix was poured into 60 mL glass bottleswith lids to a level of 45 mL, and 50 mL centrifuge tubes leaving15 mm headspace. The set yogurts were refrigerated at 4 °C forfurther analysis. A part of the mix was saved prior to inoculationfor measurement of viscosity and pH. A part of the inoculatedsample was used for rheological studies. The inoculated yogurtmixes were incubated at 40 °C for 330 min for fermentation.

Rheology of yogurt during fermentationThe rheological properties of yogurt were characterized on a

Rheometrics LS1 controlled stress rheometer (TA Instruments,New Castle, Del., U.S.A.). Small-amplitude oscillatory shear flowmeasurements of the storage modulus, G′, the loss modulus, G′′,and the loss tangent, tan δ = G′′/G′, were obtained using a vanegeometry. A cup (34 mm diameter) was filled with mix to a depthof 44 mm, and the vane consisted of 6 radially symmetric paddles34 mm long and 18 mm diameter. The vane geometry allowsmeasurements to be taken without disrupting the gel formationand also prevents complications due to slip (Haque and others2001; Martin and others 2005). The temperature of the samplewas initially at 40 °C, and measurements were taken at a frequencyof 1 rad/s and 0.1% strain for 5.5 h. The sample was then cooledat 1 °C/min to 4 °C, and the frequency dependence of the moduliwas measured (ω = 10−2 to 102 rad/s). The response at 1 rad/swas then monitored for 16.5 h, followed by another measurementof the frequency dependence. The temperature was controlled towithin ±0.1 °C by a circulating water bath, and humidity coverswere used to prevent drying of the sample. For stored samples,the centrifuge tubes (27 mm diameter) were centered in the cup,which was filled with water to maintain the samples at 4 °C. Theviscosities of the mixes were measured in steady shear flow usingparallel plate geometry of 50 mm diameter.

Fermentation rateThe pH of yogurt mixes was measured using an Accumet X l50

pH meter equipped with an ATC probe for temperature effectcorrection. The pH of the inoculated yogurt mix was recordedevery 2 min during fermentation at 40 °C. The rate of lactosefermentation during yogurt was determined by plotting pH ofyogurt mix compared with fermentation time.

ColorColor of yogurt samples was measured using the LabscanXE

Hunter colorimeter (Hunter Associates Laboratories Inc., Reston,Va., U.S.A.). The Hunter L (lightness scale 100 = pure white,0 = black), a (red), and b (yellow) values were used to calculatethe total color �E = (L2 + a2 + b2)0.5.

SyneresisWeighed yogurt samples set in 50 mL centrifuge tubes in du-

plicates were centrifuged at 1000×g for 10 min at 8 °C (BeckmanCS-6KR). The separated whey was carefully decanted using atransfer pipette and weighed, and the centrifuge tube was alsoweighed to confirm the whey removed. Syneresis index was cal-culated as the weight of the whey separated per unit weight ofyogurt.

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Yogurt textureTexture of yogurts set in 4 oz bottles was measured using

TA XT2i Texture Analyzer (Texture Technologies Corporation,Scarsdale, N.Y., U.S.A.). Yogurt samples were evaluated in trip-licates using stainless steel ball probe (TA 18) set for a 10 cycletest. The test parameters were 5 mm/s test speed, 2 mm/s pretestspeed, 5 mm/s posttest speed, 10 g trigger force, and a distance of10 mm. All measurements were recorded as the force (g) of thepeaks. The maximum force for the 1st peak (g) was used to deter-mine firmness, whereas ratio of the maximum force of the tenthpeak to the maximum force of the 1st peak was used to evaluategel resiliency. All tests were conducted in duplicates at ambienttemperature with product temperature near 4 °C. Samples weretaken directly from refrigerator and placed on instrument stage forthe measurements.

Results and Discussion

Fermentation rateThe rate of fermentation measured as drop in pH due to con-

version of lactose to lactic acid by bacteria during incubation at40 °C of skimmed milk yogurt mixes with 0%, 1%, 2%, and 3%AIC and whole milk yogurt mix is presented in Figure 1. Addi-tion of AIC to yogurt mix did not affect fermentation of lactoseto lactic acid, as all samples reached typical end point pH (4.6)for fermentation at the end of the incubation period. All samplesdisplayed characteristic lag phase, logarithmic phase, and the slow-down acidification phase during fermentation. Similar results havebeen reported with the addition of starch (Williams and others2003; Oh and others 2007) and starch–lipid composites (Singhand Byars 2009; Singh and Kim 2009).

Rheology of yogurt during fermentationThe initial viscosity of yogurt mixes with AIC was considerably

higher than skim milk and full-fat milk samples (Table 1). Anincrease in initial viscosity was also observed on the addition ofstarch–lipid composites (Singh and Byars 2009). Singh and Byars

Time [min]

0 60 120 180 240 300 360

pH

4.0

4.5

5.0

5.5

6.0

6.5

7.0

full fat control

1%2%

skim control

3%

Figure 1–The pH change during fermentation of full-fat milk yogurt mixand various amylose–potassium oleate complex levels (0%, 1%, 2%, and3%) in skim milk yogurt mix.

Table 1–Summary of yogurt properties. The mix viscosity wasmeasured at 40 °C. G′ values were measured at 40 °C after 5.5h, and tan δ values were measured at 4 °C after 16.5 h of storageat 4 °C.

G′ at 1 rad/s tan δ (Pa) Yogurt mix(5.5 h) (16.5 h) viscosity Pa·s

Skim control 82 0.18 0.0019Full-fat control 418 0.21 0.0024

1% AIC 232 0.18 0.112% AIC 382 0.16 0.413% AIC 605 0.15 0.3

(2009) found that mix viscosity in itself did not affect the final gelstructure of yogurt.

Onset time of gelation was defined as the time when the storagemodulus exceeded 3 Pa. Fat content in yogurt mix significantlyaffected onset time of gelation (Figure 2). Full-fat milk yogurtmix had significantly lower onset time of gelation compared toskim milk yogurt mix. Removal of fat in yogurt mix delayed thegelation process during fermentation. Xu and others (2008) alsoreported low-fat samples needed more incubation time for com-mencement of gelation in comparison to full-fat milk. Additionof AIC induced earlier gelation relative to skim milk control yo-gurt, and at 3% AIC gel began to form almost as early as forfull-fat milk control yogurt. This indicates that AIC can replacefat without affecting the gelation of yogurt.

Effect of AIC on formation of the yogurt gel at 40 °C is shownin Figure 3. The storage modulus, G′, was measured at a frequencyof 1 rad/s to monitor gel strength during fermentation. A longinduction time was observed for each sample, during which themodulus value was below the measurement threshold. The storagemodulus increased rapidly for each sample as gel began to form,and then continued to increase throughout the fermentation. Thelevel of starch complex affected both the time at which gel growthwas first observed and final value of storage modulus. The initialgrowth rate of the storage modulus was similar for each sample,but yogurts containing starch complex continued to increase in gel

AIC [%]

0 1 2 3 4

Tim

e [m

in]

0

60

120

180

240

AIC

skim control full fat control

Figure 2–Effect of fat content and amylose–potassium oleate complexlevels on skim milk yogurt formation at 4 °C.

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strength faster than the full-fat control yogurt. At the end of 330min fermentation period, 3% AIC yogurt mix formed strongergel than full-fat control (Table 1).

Storage and loss (G′′) moduli are shown for all samples inFigure 4 after holding in the rheometer at 4 °C for 16.5 h. Resultsfor each sample are characteristic of a gel, with G′ > G′′ at allfrequencies, and with both values showing very little frequencydependence. Values here are higher than those in Figure 3 primar-ily due to lower measurement temperature, but full-fat controlshowed a greater increase upon cooling and had the highest mod-ulus values at 4 °C. Frequency dependence of the moduli doesnot suggest any qualitative differences in the yogurts formed withstarch complexes. However, the loss tangent (tan δ = G′′/G′) de-

Time [min]0 60 120 180 240 300

G' [

Pa]

10-1

100

101

102

103

skim controlfull fat control1%2%3%

Figure 3–Effect of level of amylose–potassium oleate complexes in skimmilk on the onset time of gelation during yogurt fermentation. Onset timeis defined as G′ > 3 Pa.

ω [rad/s]10-2 10-1 100 101 102

[Pa]

101

102

103

104

skim controlfull fat control1%2%3%

Figure 4–Linear viscoelastic spectra after 16.5 h of storage at 4 °C. Thestorage modulus G′ is shown with solid symbols and the loss modulus G′ ′ isshown with open symbols.

creased for samples with starch complexes (Table 1). A lower valueof loss tangent indicates a firmer gel, so a firmer yogurt gel wasformed with starch complexes compared to either skim milk orfull-fat milk yogurts.

Storage modulus, G′ measured at a frequency of 1 rad/s for allyogurts samples during storage at 4 °C, is presented in Figure 5.All yogurt samples maintained gel strength during storage of 4 wk.Yogurt samples with fat (full-fat control) had significantly higherstorage modulus in comparison to skim milk yogurt control. Thestorage modulus increased with increasing AIC concentration inskim milk yogurt stored for 4 wk.

Color of yogurtTotal color of yogurt samples is presented in Figure 6. Full-fat

yogurt samples had higher total color values that were attributedto higher lightness (L∗). Addition of AIC to skim milk resultedin reduced total color attributed to lower lightness in yogurt.However, the difference in total color among yogurts was notobvious to naked eye.

Texture of yogurtInitial firmness of yogurt, as 1st peak force measured by tex-

ture analyzer during storage, is shown in Figure 7. As expected,full-fat milk yogurt was significantly firmer than skim milk yo-gurt during 29 d of storage, suggesting a positive interaction offat globules with the casein gel network in yogurt. Martin-Dianaand others (2004), Pereira and others (2006), Aziznia and others(2008), and Yazici and Akgun (2004) also observed that fat signif-icantly increased gel firmness. Addition of 3% AIC to skim milkyogurt mix significantly increased firmness of the yogurt. This isin agreement to the observations from rheology data describedabove. This confirms our assumption that AIC plays the role of fatduring yogurt fermentation.

Final firmness at the end of cycle as the 10th peak force of allyogurt samples followed a similar trend as initial firmness, but wassignificantly lower.

Time [day]

1 4 8 15 22 29

G' (

rad/

s) P

a ∙s

0

1000

2000

3000

4000

5000

6000skim controlfull fat control1%2%3%

Figure 5–Effect of storage time at 4 °C on linear viscoelastic spectra(storage modulus G′) for full-fat milk yogurt and yogurt various amylose–potassium oleate complex levels (0%, 1%, 2%, and 3%) in skim milk.




Resiliency of yogurt, as the ratio of final peak force to initialpeak force, during storage is shown in Figure 8. Fat content incontrol samples had an inverse relationship with resiliency of yo-gurt texture. Skim milk yogurt was more resilient and retainedits resiliency during storage in comparison to full-fat control. In-creasing the amount of AIC from 1% to 3% in skim milk yogurtmix increased resiliency of yogurts during storage. This affirmsour earlier assumption that AIC strengthens yogurt gel.

Syneresis of yogurt during storageSyneresis, a measure of rigidity of yogurt gels for all samples over

4 wk storage, is presented in Figure 9. Fat content significantlyaffected syneresis in control yogurt samples during storage. Full-fat

AIC [%]0 1 2 3

ΔΕ

60

70

80

90

100

AIC

skim control full fat control

Figure 6–Effect of fat content and amylose–potassium oleate complexlevel on the total color of skim milk yogurts.

Time [day]

1 4 8 15 22 29

Firm

ness

[g]

0

20

40

60

80

100skim control full fat control

3%

1% 2%

Figure 7–Effect of storage on the firmness of yogurts made full-fat milk andvarious amylose–potassium oleate complex levels (0%, 1%, 2%, and 3%)in skim milk.

yogurt gels were more rigid in comparison to skim milk yogurtsas is evident by lower serum expulsion by centrifugation. Thisis in agreement with Tamime and Robinson (2007) and Azizniaand others (2008) who attribute low fat as one of the reasonsfor syneresis in yogurts, but it is in contrast to Ruiz and others(2013) who observed lower whey separation in 1% fat yogurtsthan those with 3% fat. Addition of AIC to skim milk yogurtmix lowered syneresis by strengthening the gels. This could bedue to positive interaction of AIC with gel network. Syneresisfor yogurt samples increased storage. Similar observations havebeen reported by Sandoval-Castilla and others (2004), Salvadorand Fiszman (2004), and Singh and Byars (2009).

Time [day]

1 4 8 15 22 29

Res

ilien

cy [%

]

0

20

40

60

80

100

full fat control

2% 1%

3%

skim control

Figure 8–Effect of storage on the resiliency of yogurts made full-fat milkand various amylose–potassium oleate complex levels (0%, 1%, 2%, and3%) in skim milk.

Time [day]1 4 8 15 22 29

Syne

resi

s [%

]

0

5

10

15

20

25

30

1%skim control

2% 3%full fat control

Figure 9–Effect of storage on syneresis of yogurts made full-fat milk andvarious amylose–potassium oleate complex levels (0%, 1%, 2%, and 3%)in skim milk.

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Full-fat yogurt continued to have lower syneresis than nonfatyogurt during storage of 29 d. Yogurt samples with 3% AIC hadsignificantly lower syneresis than full-fat yogurt all throughout thestorage of 29 d. This suggests that AIC interacts with gel network,thus strengthening the gel structure and reducing the syneresisduring storage.

ConclusionYogurt mixes with skim milk solids replaced by amylose–

potassium oleate complexes (AIC) or milk fat, fermented lac-tose to lactic acid at a rate similar to those with no milk solidsreplaced. Positive interaction of AIC (3%) with yogurt networkstrengthened skim milk yogurt gels, reduced syneresis, and be-haved similar to full-fat yogurts. Yogurts with 3% AIC maintainedstrong gel structure during 4 wk of storage at 4 °C. AIC pro-vides an alternative method to strengthen low-fat yogurts. Thisstudy demonstrates that AIC can be added to replace fat in yogurtmix, without affecting structural characteristics and storability ofset yogurt. However, further study is needed to understand themechanism of interaction by which AIC induces earlier onset ofgelation with increased gel strength, without affecting the fermen-tation of lactose to lactic acid in yogurts.

AcknowledgmentTechnical assistance provided by AJ Thomas and Wilma Rinsch

during the course of this study is gratefully acknowledged.

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amylose–potassium oleate inclusion complex in plain set-style yogurt

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