1 Microencapsulated Iron
2 for Drink Yogurt Fortification
5 S. J. Kim, J. Ahn and H. S. Kwak
6 Department of Food Science and Technology
7 Sejong University, 98 Kunja-dong, Kwangjin-ku,
8 Seoul, 143-747, Korea
11 Running head: Iron fortification in drink yogurt
13 Corresponding author : H.S. Kwak, Dept. of Food Science and Technology,
14 Sejong University, 98 Kunja-dong, Kwangjin-ku, Seoul, 143-747, Korea.
15 E-mail: email@example.com
16 Tel : (822) 3408-3226
17 Fax : (822) 497-8931
18 ABSTRACT : This study was designed to examine the effect of micro
19 encapsulated iron fortified drink yogurt and vit C as a bioavailable helper of
20 iron on chemical and sensory aspects during 20 d storage. Coating material
21 was PGMS, and ferric ammonium sulfate and vit C were selected as core m
1 aterials. The highest efficiency of microencapsulation of iron and vit C were
2 73% and 76%, respectively, with 5:1:50 ratio (w/w/v) as coating to core mat
3 erial to distilled water. Iron fortification did not affect to the fermentation ti
4 me required for the drink yogurt to reach pH 4.2. The addition of uncapsulat
5 ed iron decreased the pH during storage. TBA absorbance was significantly
6 lower in capsulated treatments than those in uncapsulated treatments during
7 storage. In sensory aspect, the yogurt sample added with uncapsulated iron a
8 nd vit C, regardless of capsulation, showed a significantly high score of astri
9 ngency, compared with those of control and other groups. A significantly str
10 ong sourness was observed in treatment containing capsulated iron and unca
11 psulated vit C at every time intervals. The present study provides evidence t
12 hat microencapsulation of iron with PGMS is effective for iron fortification
13 in drink yogurt.
14 Key words: Microencapsulation, Iron, PGMS, Yogurt, Vitamin C
15 Abbreviation key: PGMS = polyglycerol monostearate.
20 Yogurt has gained widespread consumer acceptance in the U.S. (Otto, 19
21 88) and other developed countries, primarily by women, children and teenag
1 ers, who consume yogurt as a luncheon or snack food. These populations ha
2 ve high calcium requirements and are also frequently deficient in iron (Dall
3 man et al., 1984). Even though yogurt is an excellent source of calcium and
4 protein (United States Department of Agriculture, 1982), it contains very litt
5 le iron (Blanc, 1981).
6 Fortification of iron in yogurt would help meet this nutritional need. Usin
7 g dairy foods as a vehicle for supplementing iron seems to be an advantage
8 because people who consume diets with low iron density usually consume
9 more dairy products (Hekmat and McMahon, 1997). Futhermore, iron-fortifi
10 ed dairy foods have a relatively high iron bioavailiability (Woestyne et al., 1
11 991). However, before any such fortification is undertaken in yogurt, the eff
12 ects of iron fortification on microbial physiology during manufacture and sh
13 elf-life of yogurt, oxidation of milk fat, and the effect of iron on sensory cha
14 racteristics must be ascertained.
15 Iron in food is absorbed by the intestinal mucosa and especially, nonhem
16 e iron, the major dietary pool, is greatly influenced by meal composition. It i
17 s well known that vit C is a powerful enhancer of nonheme iron absorption (
18 Lynch and Cook, 1980). Its influence may be pronounced in meals of iron a
19 vailability. Vit C facilitates iron absorption by forming a chelate with ferric i
20 ron at acid pH that remains soluble at the alkaline pH of the duodenum. Ho
21 wever, the addition of vit C influences on the quality of yogurt due to its hig
1 h acid. Therefore, iron and vit C need microencapsulation.
2 Microencapsulation, which shows potential as carriers of enzymes in the
3 food industry, could be a good vehicle for the addition of iron to milk (Jacks
4 on and Lee, 1991; Bersen’eva et al., 1990). Currently there is a considerable
5 interest in developing encapsulated flavors and enzymes. Among several fac
6 tors to be considered, choice of coating material is the most important and d
7 epends on the chemical and physical properties of the core material, the proc
8 ess used to form microcapsules, and the ultimate properties desired in micro
10 For microencapsulation – although several researchers have used coating
11 materials such as milk fat, agar, and gelatin, etc. responsible for enzyme, fla
12 vor and iron microencapsulation in foods (Braun and Olson, 1986; Magee a
13 nd Olson, 1981a,b), no study has measured the efficiency of iron microenca
14 psulation using fatty acid esters, and the stability of microcapsule itself and i
15 nside the body. Therefore, the objective of this study was to examine the eff
16 ect of microencapsulated iron and/or vit C added yogurt on chemical and se
17 nsory aspects during storage.
17 MATERIALS AND METHODS
20 For the microencapsulation of iron complex, polyglycerol monostearate (
21 PGMS) was used as a coating material. It was purchased from Il-Shin Emuls
1 ifier Co., LTD. (Seoul, Korea). As core materials, water-soluble iron comple
2 x, ferric ammonium sulfate (FeNH4(SO4) 2 4H2O) and L-ascorbic acid were
3 purchased from Sigma Chemical Co. (St. Louis, MO, USA) and Shinyo Pur
4 e Chemical Co. LTD (Osaka, Japan) and were in food grade.
6 Preparation of microcapsule
7 Microcapsules of iron were made by polyglycerol monostearate (PGMS),
8 which was selected as a major coating material from our previous study (K
9 wak et al., 2001). Also, ferric ammonium sulfate and L-ascorbic acid were s
10 elected (Kwak et al., 2002). Other experimental factors were as follows: the
11 ratio of coating material to core material was 5:1, and 50 mL distilled water
12 was additionally added because PGMS solution was highly viscous. The spr
13 ay solution was heated at 55C for 20 min, and stirred with 1,200 rpm for 1
14 min during spraying. An airless paint sprayer (W-300, Wagner Spray Tech.
15 Co., Markdorf, Germany) nebulized a coating material-iron emulsion at 45
16 C into a cyclinder containing a 0.05% polyethylene sorbitan monostearate (
17 Tween 60) solution at 5C. The diameter of the nozzle orifice was 0.33 mm.
18 The chilled fluid was centrifuged at 2,490 x g for 10 min to separate unwash
19 ed microcapsule suspension. Microcapsules were formed as lipid solidified i
20 n the chilled fluid. The microencapsulation of iron and ascorbic acid were d
21 one in triplicate.
2 Yogurt preparation
3 A commercial homogenized and pasteurized milk containing 3.4% fat a
4 nd 13.4% total solids was fortified with 2.7% (w/v) skim milk powder to inc
5 rease viscosity of yogurt and then homogenized (HC-5000 Homogenizer, M
6 icrofluidics Corp., Newton, MA, USA) at 150 kg/cm2 (60C) and cooled to
7 42C. A 0.2% commercial YC-380 starter culture (Chr. Hansen Pty. Ltd. Ba
8 yswater, Autralia) in freeze-dried direct-to vat set form containing Lactobac
9 illus delbrueckii ssp. bulgaricus and Streptococcus thermophilus was inocul
10 ated and fermented at 42C to be reached at pH 4.3. After fermentation, som
11 e yogurt samples were initially removed and incubated at 4C for 24 h. The
12 remaining samples were stored at 4C for 20 d to study the changes in chem
13 ical, microbial and sensory aspects during prolonged fermentation of yogurt
14 at 5 d intervals.
17 Five different groups in this experiment were as followed: 1) no addition
18 as control (Trt 1), 2) 20 ppm uncapsulated iron added (Trt 2), 3) 20 ppm cap
19 sulated iron added (Trt 3), 4) 20 ppm capsulated iron and 100 ppm uncapsul
20 ated vit C added, and 5) 20 ppm capsulated iron and 100 ppm capsulated ad
21 ded vit C.
2 Efficiency of microencapsulation
3 For iron measurement, the dispersion fluid was assayed for untrapped iro
4 n during microencapsulation. One milliliter of the dispersion fluid was taken
5 and diluted ten times and total iron content was measured at 259.94 nm wav
6 e- length by inductively coupled plasma spectrometer (ICP). Lactam 8440
7 Model spectrometer (Plasmalab, Victoria, Austrailia) was used. A sample m
8 easurement was run in triplicate.
9 Total vit C was analyzed spectrophotometrically using DNP (2,4-dinitrop
10 henyl hydrazine) test described (Korea Food Code, 2002). Samples were pre
11 pared immediately before analyses and kept cold and protected against dayli
12 ght during analysis. A vit C stock solution was prepared daily by dissolving
13 10 mg of vit C in 100 mL of deionized water (100g/mL). It was diluted wit
14 h deionized water to obtain the final concentration of 10, 20, 30, 40 and 50
15 g/mL. Total vit C was determined using the calibration graph based on conc
16 entration (g/mL) vs absorbance, prepared daily running fresh standard solu
19 Chemical analyses
20 pH and titratable acidity (TA)
21 pH and titratable acidity (determined by titration to pH 8.3) of the yogurt
1 samples were measured at a room temperature using pH meter (Sartorius, G
2 ermany). The TA was determined after mixing the 9 mL yogurt sample with
3 18 mL distilled water and titrating with 0.1N NaOH using a 0.5% phenolpht
4 halein indicator to an end point of faint pink color.
6 Thiobarbituric acid (TBA) test
7 Oxidation products were analyzed spectrophotometrically using the thiob
8 arbituric acid (TBA) test (Hegenauer et al., 1979). The TBA reagent was pre
9 pared immediately before use by mixing equal volumes of freshly prepared
10 0.025M TBA (brought into by neutralized with NaOH) and 2M H3PO4/2M c
11 itric acid. Reactions were terminated by pipetting 5.0 mL of yogurt sample c
12 ontaining iron microcapsules into a glass centrifuge tube and mixed through
13 ly with 2.5 mL TBA reagent. The mixture was heated immediately in a boili
14 ng water bath for exactly 10 min, and then cooled on ice. Then 10 mL cyclo
15 hexanone and 1 mL of 4M ammonium sulfate were added and centrifuged at
16 2,490 x g for 5 min at room temperature. The orange-red cyclohexanone sup
17 ernatant was decanted and its absorbance at 532 nm was measured spectrop
18 hotometically in an 1-cm light path. All measurements were run in triplicate.
21 Viscosity measurement was made with Bostwick consistometer (CSC Sci
1 entific Company, Seoul, Korea). Sample (100g) was placed and flow distanc
2 e (cm) for 1 min was expressed as viscosity.
4 Microbiological analyses
5 Lactic acid bacteria were determined from the colony counts on specific l
6 actic agar: MRS agar (pH 5.4) for Lactobacillus delbrueckii subsp. bulgaric
7 us and M17 agar for Streptococcus thermophilus. A 1-g yogurt samples stor
8 ed for 0, 5, 10, 15, and 20 d were diluted with 9 mL of sterile peptone and w
9 ater diluent. Subsequent serial dilutions of each sample were plated in triplic
10 ate and plated were incubated at 41C for 48 h.
12 Sensory evaluation
13 For the storage test, 10 mL drink yogurt containing capsulated or uncaps
14 ulated iron and vit C was stored at 4C for 0, 5, 10, 15 and 20 d. An eleven-
15 person panel, semi-experienced in judging dairy products were recruited fro
16 m faculty and graduate students in the Department of Food Science and Tec
17 hnology at Sejong University and evaluated the yogurt samples throughout t
18 he study.
19 The intensity of taste aspects (bitterness, astringency, and sourness) were
20 scored on a nine-point scale (1 = none, 3 = slight, 5 = moderate, 7 = strong a
21 nd 9 = very strong) and overall preference were scored on a nine-point scale
1 (1 = dislike extremely, 3 = dislike moderate, 5 = neither like or dislike, 7 = l
2 ike moderate, and 9 = like extremely). A randomized, balanced, complete bl
3 ock design was used (Cochran and Cox, 1957) that resulted in two replicatio
4 ns for all samples.
6 Statistical analysis
7 Data from each experiment were analyzed by analysis of variance (ANO
8 VA) using a SAS program (1985) and differences among treatments were de
9 termined by Student-Newman-Keuls comparison test at p < 0.05, unless oth
10 erwise stated.
15 RESULTS AND DISCUSSION
18 In the present study, the yield of iron and vit C microencapsulation were
19 73% and 76%, respectively. In our laboratory, PGMS was appeared to be ha
20 rd to spray, therefore, we found the optimum ratio of PGMS to deionized wa
21 ter to reduce the viscosity of PGMS solution. In our previous study, the ratio
1 of PGMS to iron to distilled water was 5:1:50 (w/w/v), efficiency of the mic
2 roencapsulation was 75% as the highest value (Kwak et al., in press).
3 The size of microencapsulated iron or vit C with PGMS was irregular fro
4 m nano to micrometer, and the average size was in the range of 2 to 5 m (p
5 ictures not shown). Microscopic examination of microcapsules revealed sph
6 erical particles. Microcapsules containing iron or vit C had smooth surfaces
7 and evenly distributed pockets. The shape of the microcapsules was likely af
8 fected by encapsulated conditions.
9 Magee and Olson (1981a), and Braun and Olson (1986) found that lipid a
10 nd cooling fluid temperatures affected the shape of microcapsule by controll
11 ing the cooling rate of lipid coatings. They observed that microcapsules wer
12 e cylindrical when the lipid coating was rapidly cooled and spherical when t
13 he lipid was slowly cooled.
14 The change of pH and titratable acidity (TA)
15 Iron fortifications did not affect fermentation time required for the yogurt
16 mixes to reach pH 4.10 4.20 (Fig. 1). After 5 h fermentation, further trend
17 of pH changes during storage were also similar: the pH values of control an
18 d fortified samples reached 4.00 4.07 after 1 d and 3.95 4.07 after 20 d.
19 The treatment was divided into 5 different groups as followed: 1) no addi
20 tion as control (Trt 1), 2) 20 ppm uncapsulated iron (Trt 2), 3) 20ppm capsul
21 ated iron (Trt 3), 4) 20 ppm capsulated iron and 100ppm uncapsulated vit C
1 (Trt 4), and 5) 20 ppm capsulated iron and 100 ppm capsulated vit C (Trt 5).
2 The change of pH was shown as in Fig 1. pH was the highest in control g
3 roup among 5 different groups. pH was 4.20 at 0 d and decreased to 4.07 at
4 5 d and plateaued thereafter upto 20 d storage in control.
5 When compared with uncapsulated iron added group (Trt 2) and capsulat
6 ed iron groups (Trt 3), pH was significantly lower in Trt 2 at every time inte
7 rvals. Uncapsulated iron resulted in high level of acidity during fermentation
8 (0 d storage) and further storage, which indicating that iron capsulation sho
9 wed a profound effect on pH at every time intervals.
10 When compared with capsulated iron with uncapsulated vit C (Trt 4) and
11 capaulated iron with capsulated vit C (Trt 5), there was no difference at ever
12 y time intervals from the beginning to the end, especially, until 10 d storage.
13 In results, uncapsulated vit C showed a certain protective effect on pH decre
14 ase. Above result indicated that uncapsulated iron addition decreased the pH
15 of yogurt during storage. Addition of iron to skim milk led to a decrease in p
16 H. This decrease is related to the acidities of iron solution and to exchange b
17 etween iron ions and micellar bound H+ (Gaucheron, 2000).
18 Titratable acidity (TA) increased with the storage time (Fig. 2). The TA o
19 f control was the lowest and that of Trt 2 containing uncapsulated iron was t
20 he highest.
1 TBA test during storage
2 The effect of iron fortification in yogurt on chemical oxidation (as measu
3 red by the TBA test) during 20 d storage is shown in Fig 3. When compared
4 with uncapsulated (Trt 2) and capsulated (Trt 3) iron added group, TBA val
5 ue was slightly higher in uncapsulated iron added groups at 0, 5, and 20 d st
6 orage. The difference of TBA value between 2 groups increased dramaticall
7 y at 10 and 15 d storage.
8 When compared with capsulated iron with uncapsulated vit C (Trt 4) and
9 capsulated iron with capsulated vit C (Trt 5), the TBA value of Trt 5 was no
10 t significantly lower than that of Trt 4 in the early stage of storage (0, 5 and
11 10 d). However, the TBA value of Trt 5 containing capsulated vit C was sig
12 nificantly lower at 15 d storage.
13 In this experiment, TBA absorbance was significantly lower in capsulate
14 d groups than those in uncapsulated group, regardless of iron and vit C, duri
15 ng storage. These data indicated that oxidation process may be faster in yog
16 urt samples containing uncapsulated iron than in those containing capsulated
18 Another study (Kwak et al., in press) showed the effect of iron fortificati
19 on in milk on chemical oxidation during 15 d storage. They reported that TB
20 A absorbance was significantly lower in capsulated group than that in uncap
21 sulated group at 15 d.
1 Jackson and Lee (1991) indicated that samples containing uncapsulated ir
2 on (ferrous sulfate and ferric chloride) showed 2-3 times high in fatty acid p
3 roduction, compared with those containing capsulated iron complex when m
4 ilk fat was used as a coating material. The reason why iron fortification caus
5 ed several modifications in milk and yogurt could be explained that added ir
6 on may interact with casein, resulting in iron-casein complexes and the pres
7 ence of O2 acts as a prooxidant, therefore, lipid oxidation in yogurt can be a
11 Change of Microbial counts during storage
12 The change of Lactobacillus delbrueckii ssp. bulgaricus in microencapsu
13 lated iron fortified drink yogurt at 4C for 20 d storage is shown in Table 1.
14 At 0 d, the mean counts of L. delbrueckii ssp. bulgaricus for control and oth
15 er groups were not significantly different. Also, the mean counts in all group
16 s showed a decrease trend during 20 d storage. L. delbrueckii ssp. bulgaricu
17 s counts were about 107 cfu/ml.
18 The change of viable cells of Streptococcus salivaries ssp. thermophilus i
19 n microencapsulated iron fortified drink yogurt at 4C for 20 d storage is sh
20 own in Table 2. At 0 d, the mean counts of S. salivaries ssp. thermophilus fo
21 r control and other groups were not significantly different. Also, the mean c
1 ounts in all groups did not show any change during 20 d storage. Meanwhile
2 , S. salivaries ssp. thermophilus counts were about 108 cfu/ml.
3 Hekmat and McMahon (1997) reported that counts of L. delbrueckii ssp.
4 bulgaricus and S. salivaries ssp. thermophilus after 1 d of storage in iron-for
5 tified skim yogurt were 7.0 x 108 cfu/ml, which were not significantly differ
6 ent from counts in unfortified yogurts. Counts decreased to 2.5 x 108 cfu/ml
7 and 1.9 x 108 cfu/ml for L. delbrueckii ssp. bulgaricus and S. salivaries ssp.
8 thermophilus, respectively, after 30 d storage. Fortifying yogurt with iron di
9 d not affect the growth of Pseudomonas flurescens or Escherichia coli.
12 When measured viscosity by consistometer, flowing longer distance indic
13 ated lower viscosity, as shown in Fig 4. Four treatments except Trt 2 showe
14 d a slightly decreasing trend of viscosity during 20 d storage. However, Trt
15 2 containing uncapsulated iron only showed no difference to other treatment
16 s until 10 d storage, however, a dramatic decreasing was found from 15 d up
17 to 20 d. The dramatic decrease of viscosity in uncapsulated iron fortified tre
18 atment (Trt 2) may be explained that an interaction of casein and whey prote
19 in with iron complex was developed in yogurt during storage (Sadler et al.,
1 Sensory analysis
2 The sensory characteristics of drink yogurts in five treatments were show
3 n in Table 3. For bitterness, it was not significantly different among treatme
4 nts during 20 d storage. However, in Trt 2, uncapsulated iron fortified yogur
5 t revealed a slightly higher score than others. Also, no difference was found
6 in all treatments during storage.
7 For astringency, uncapsulated or capsulated iron containing drink yogurt
8 (Trts 2 and 3) showed a higher score, compared with those of control and ot
9 her treatments at 0 d. At 5 d storage, groups containing uncapsulated iron (T
10 rt 2) and capsulated iron with vit C regardless of capsulation (Trts 4 and 5) s
11 howed a significantly higher astringency, compared with other groups. No d
12 ifference was found among groups thereafter.
13 For sourness, a significantly strong sourness was observed in Trt 4, whic
14 h was added with capsulated iron and uncapsulated vit C at every periods ex
15 cept 10 d storage. Sourness increased with storage time in all groups. If we c
16 ompared Trt 2 with Trt 3, we may find the effect of iron microencapsulation
17 on sourness score, and no significant difference was found.
18 The only difference we found was between Trt 4 and Trt 5, and it was ca
19 used by vit C encapaulation or not. Therefore, a dramatically high sourness
20 score in Trt 4 was resulted from not capsulated iron, but uncapsulated vit C i
21 n the drink yogurt.
1 For overall preference, control (Trt 1) and capsulated iron (Trt 3) and/or
2 vit C (Trt 5) containing treatments showed a high consumer preference in all
3 storage periods. The scores of Trts 2 and 4 (uncapsulated iron added, and ca
4 psulated iron and uncapsulated vit C added groups) were dramatically lower
5 compared with those of other three treatments. This result indicated that mic
6 roencapsulation process was very effective to mask off-taste and flavor of ir
7 on and vit C in this experiment.
8 The sensory quality of iron-fortified dairy foods has been shown to be eff
9 ective by the capsulation of both iron and vit C. Two major off-flavors have
10 been associated with dairy products: oxidized flavor resulted from catalysis
11 of lipid oxidation by iron, and sourness contributed by vit C.
12 Iron is known to catalyze lipid oxidation resulting in rancidity with devel
13 opment of an unpleasant odor and flavor. The TBA test has been extensively
14 applied to food in which the absorbance of TBA reaction products correlates
15 positively with sensory evaluation. Fortification with iron complex causes o
16 xidized off-flavor and high TBA number. To avoid oxidized and metallic fla
17 vors and color changes, microencapsulation techniques were needed. (Gauc
18 heron, 2000).
10 The present study demonstrated that the ratio of 5:1:50 (w/w/v) as coatin
11 g (PGMS) to core material (iron complex) to distilled water showed a high e
12 fficiency of microencapsulation of iron and vit C such as 73% and 76%, res
13 pectively. Our results indicated that lipid oxidation process measured by TB
14 A test was significantly slower in capsulated iron than in uncapsulated iron f
15 ortified yogurt. In sensory, we need to point out that no significantly adverse
16 effects was found in microcapsulated iron and vit C fortified drink yogurt du
17 ring 20 d in this experiment. Therefore, we may suggest that this study provi
18 de an important evidence that microcapsules of iron and vit C were an effect
19 ive means of fortification, and can be applied to drink yogurt without any ch
20 anges in sensory aspects.
10 This research was supported by the Small & Medium Business Administr
11 ation (SMBA) in Seoul, Korea.
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8 Figure Legends
9 Fig 1. Changes of pH in microencapsulated iron fortified drink yogurt stored at 4C
10 for 20 d. Trt 1, control (no addition); Trt 2, 20 ppm uncapsulated
11 iron; Trt 3, 20 ppm capsulated iron; Trt 4, 20 ppm capsulated iron and 10
12 ppm uncapsulated vit C; Trt 5, 20 ppm capsulated iron and 100 ppm
13 capsulated vit C.
14 Fig 2. Changes of titratable acidity (TA) in microencapsulated iron fortified drink
15 yogurt stored at 4C for 20 d. Trt 1, control (no addition); Trt 2, 20 ppm
16 uncapsulated iron; Trt 3, 20 ppm capsulated iron; Trt 4, 20 ppm capsulated
17 iron and 10 ppm uncapsulated vit C; Trt 5, 20 ppm capsulated iron and 100
18 ppm capsulated vit C.
19 Fig 3. Changes of TBA absorbance in microencapsulated iron fortified drink yogurt
20 stored at 4C for 20 d. Trt 1, control (no addition); Trt 2, 20 ppm
21 uncapsulated iron; Trt 3, 20 ppm capsulated iron; Trt 4, 20 ppm capsulated
1 iron and 10 ppm uncapsulated vit C; Trt 5, 20 ppm capsulated iron and 100
2 ppm capsulated vit C.
3 Fig 4. Changes of viscosity in microencapsulated iron fortified drink yogurt
4 stored at 4C for 20 d. Trt 1, control (no addition); Trt 2, 20 ppm
5 uncapsulated iron; Trt 3, 20 ppm capsulated iron; Trt 4, 20 ppm capsulated
6 iron and 10 ppm uncapsulated vit C; Trt 5, 20 ppm capsulated iron and 100
7 ppm capsulated vit C.