JFS
S: Sensory and Nutritive Qualities of Food
Development, Stability, and Sensory Testing
of Microcapsules Containing Iron, Iodine,
and Vitamin A for Use in Food Fortification
RIT
A WEGMÜLLER, MICHAEL B
ITA
B.. ZIMMERMANN, V IVIANE G. BÜHR, ERICH J. WINDHAB, AND RICHARD F
F.. HURRELL
Introduction
I
odine, vitamin A, and iron deficiencies are important global public health problems, particularly for preschool children and pregnant
women in low-income countries (NHD/SDE/WHO) 2000). These deficiencies are mainly due to monotonous, poor-quality diets that do
not meet nutrient requirements (Tontisirin and others 2002). In countries where existing food supplies and/or limited access fail to provide
adequate levels of these nutrients in the diet, food fortification is a
promising approach. In many countries, iodization of salt is highly
effective in reducing or eliminating iodine deficiency disorders (IDD)
(WHO/UNICEF/ICCIDD 2001). In Central America, sugar has been
successfully fortified with vitamin A (Dary and Mora 2002). However,
there is no comparable, proven method for controlling iron deficiency anemia (IDA) in populations on a national level (Hurrell 2002b). In
addition, studies in animals and humans have shown that IDA impairs thyroid metabolism (Zimmermann and others 2000a, 2000b;
Hess and others 2002a, 2002b), and there is some evidence from both
experimental animal models and human studies that vitamin A deficiency may exacerbate anemia through impairment of iron metabolism (Semba and Bloem 2002). These micronutrient interactions
strongly argue for multiple micronutrient fortification.
Because salt is consumed daily at fairly steady levels, even by
population groups in poor remote areas, it could be a promising food
vehicle for fortification with iodine, iron (Fe), and vitamin A. However,
fortification of salt with all 3 micronutrients together is technically
MS 2005-0625 Submitted 10/18/05, Accepted 12/2/05. The authors are with
Human Nutrition Laboratory and Laboratory of Food Process Engineering, Inst. of Food Science and Nutrition, Swiss Federal Inst. of Technology,
Zürich, Switzerland. Direct inquiries to author Wegmüller (E-mail:
michael.zimmermann@ilw.agrl.ethz.ch).
© 2006 Institute of Food Technologists
Further reproduction without permission is prohibited
challenging. Most studies with salt dual-fortified with Fe and iodine
reported unacceptable color changes and iodine losses due to interactions of the iron compound with the iodine and salt impurities
(Madhavan Nair and others 1998; Venkatesh Mannar and Diosady
1998; Sivakumar and others 2001; Diosady and others 2002; Wegmuller and others 2003). To prevent the reaction of Fe and iodine
with the salt and with each other, a barrier could be formed by encapsulation. However, a recent stability study of salt dual-fortified with
iodine and 19 different encapsulated and nonencapsulated Fe compounds in West and North Africa suggested that currently available
encapsulation techniques do not allow successful salt fortification.
However, iodized salt fortified with nonencapsulated small particle
size ferric pyrophosphate with a mean particle size of 2.5 m resulted
in acceptable color change and iodine stability (Wegmuller and others 2003) and was effective in improving Fe and iodine status in children (Zimmermann and others 2004b). Adding vitamin A to salt is
particularly challenging because of its fat solubility and its instability
to oxygen and other oxidizing agents, particularly when it is exposed
to light and heat at the same time (BASF 2001). Encapsulation of vitamin A and iodine in an edible fat matrix could protect them from
interactions with salt impurities, light, air, and moisture. Fortification
of salt with a single dry mix containing iodine, Fe, and vitamin A
would be simpler and less expensive compared with separate addition of the 3 micronutrients to different food vehicles.
Spray cooling was chosen for the production of the microcapsules
because of the desirable coating characteristics produced by the technique and because spray cooling is currently the least expensive encapsulation technology (Gouin 2004). Fully hydrogenated palm fat was
chosen as the coating material because of its high melting point (63 °C),
which may allow the sprayed capsules to resist high temperatures enVol. 71, Nr. 2, 2006—JOURNAL OF FOOD SCIENCE S181
Published on Web 2/27/2006
S: Sensory & Nutritive Qualities of Food
ABSTRA
CT
odine
on deficiencies ar
e impor
tant public health pr
oblems in dev
eloping countr
ies
ABSTRACT
CT:: IIodine
odine,, vitamin A, and ir
iron
are
important
problems
developing
countries
and often coexist in vulnerable groups, such as pregnant women and young children. Food fortification can be a
sustainable, cost-effective strategy to combat these deficiencies. In remote, rural areas of subsistence farming, salt
may be 1 of few regularly purchased food items and is therefore likely to be a good food vehicle for fortification.
er
How ev
tification of salt is challenging due to the white color and highly rreactiv
eactiv
e impur
ities
ever
er,, for
fortification
eactive
impurities
ities,, and added
micronutrients often cause color changes. Encapsulation may prevent or reduce these reactions. Potassium iodate, retinyl palmitate, and ferric pyrophosphate were microencapsulated in hydrogenated palm fat by spray
cooling. The size and morphology of the sprayed microparticles and losses of iodine and vitamin A during spraying
were analyzed. The microcapsules were added to local salt in Morocco. During storage for 6 mo, color change in the
able to the iodiz
ed salt
iple for
tified salt ((TFS)
TFS) was acceptable
er
e appr
oximately 20% compar
tr
acceptable,, and iodine losses w
wer
ere
appro
comparable
iodized
triple
fortified
(IS). Stability of retinyl palmitate was excellent, resulting in losses of only about 12% after 6 mo of storage. Sensory
tests were performed with typical Moroccan dishes cooked with either TFS or IS by triangle testing. No sensory
difference was detectable, and overall acceptability of the salt was good. Encapsulation by spray cooling produces
highly stable microcapsules containing iodine, vitamin A, and iron for salt fortification in Africa. Such capsules
may also be used to for
tify other dr
y matr
ices (for example
fortify
dry
matrices
example,, sugar
sugar,, flour).
Keywords: fortification, salt, micronutrients, microencapsulation, spray cooling
Microcapsules of Fe, iodine, & vitamin A . . .
countered during storage and transport of salt in tropical climates, and
because of its hydrophobic properties, which prevent the entrance of
water and reduce reactions between different core ingredients. In addition, fat is an ideal matrix for fat-soluble vitamin A due to the stabilization and the delay of oxidation of the vitamin (Dary and Mora 2002).
For the production of the microcapsules, ferric pyrophosphate was
chosen as the iron source because cool spraying of the better bioavailable compounds ferrous sulfate and ferrous fumarate in palm fat
resulted in unacceptable color change when microcapsules were
added to salt (Jermann 2003). KIO3 was chosen over KI due to less
reaction with the ferric form of iron, and an oily form of vitamin A was
used due to its solubility in the fat matrix, its higher stability, and its
lower costs compared with dried forms (Dary and Mora 2002).
Materials and Methods
Microcapsule components
The coating material used for the encapsulation process consisted
of fully hydrogenated palm fat with a melting point of 63 °C (Nutriswiss, Lyss, Switzerland) and 1% lecithin (Centrolex F-IP soya pure
lecithin, Univar AG, Zürich, Switzerland). The lecithin was added to
the molten palm fat together with the Fe to reduce the viscosity of the
suspension and enable a capsule:substrate ratio of 60:40. Small particle size ferric pyrophosphate (FePP) (about 21% Fe) with a mean
particle size (MPS) of 2.5 m (Dr. Paul Lohmann GmbH, Emmerthal,
Germany) was used. Reagent-grade potassium iodate (KIO3) (Riedelde Haen, Hannover, Germany) was chosen as the iodine source. The
KIO3 was ground to a smaller particle size (<10 m) before spraying
using a laboratory bead mill K8 (Bühler, Uzwil, Switzerland). The KIO3
was ground at 92 °C for about 90 min in molten palm fat at a ratio of
1:2. After grinding, the MPS of the KIO3 was approximately 6 m,
measured by laser diffraction spectrometry (Malvern MasterSizer X,
Malvern Instruments Ltd., Malvern, U.K.; lens 45 mm; wavelength
633 nm; output 2 mW). The vitamin A fortificant used was liquid retinyl palmitate 1.7 M IU/g, stabilized with 10 mg of BHT/million IU
(BASF ChemTrade GmbH, Burgbernheim, Germany).
Production of the microcapsules
S: Sensory & Nutritive Qualities of Food
The particle size of the microcapsules was set considering the
following factors: (1) the average particle size of the Moroccan salt
(approximately 1.5 mm); a MPS for the microcapsules of approximately 100 m was chosen to reduce segregation in the salt; (2) the
need to maintain an adequate volume-surface ratio to protect the
ingredients, but not interfere with release kinetics of the nutrients
from the capsules to maintain bioavailability.
A specifically designed stainless-steel spraying tower was manufactured by the mechanical workshop of the Food Process Engineering
Laboratory at the Swiss Federal Inst. of Technology, Zürich. A 2-fluid
nozzle with hot air as the 2nd medium from SSCO-Spraying Systems
(Pfäffikon SZ, Switzerland) was used for the atomization (specification:
SUE 28B: fluid cap PF 35100, air cap 122281-60 ° (spraying systems); bore
width of the fluid cap: originally 0.95, widened to 1.1; bore width of the
air cap: 2.0; spraying angle: 60 °). Tubes transporting the fat suspension
to the spraying tower were double liner tubes, and the outer liner was
heated with water of about 90 °C from a water bath to avoid blockage
due to solidification of the palm fat at room temperature.
Ferric pyrophosphate (40% w/w) and lecithin (1% w/w) were
stirred into molten palm fat (80 °C to 90 °C) and than filled into a
heated tank above a rotary pump (NMOG 322, ibex pumps, Eastbourne, U.K.). It was constantly stirred with a vibro-mixer (Chemap
E1, Chemap, Volketswil, Switzerland) to avoid sedimentation of the
Fe particles, and then the iodine particles and retinyl palmitate were
added and mixed. The mixture contained the added functional comS182
JOURNAL OF FOOD SCIENCE—Vol. 71, Nr. 2, 2006
ponents at a ratio of Fe:iodine:retinol of 100 mg : 2 mg : 5 mg per g
mixture. To minimize losses of iodine and retinol due to heat, light,
and/or oxidation, once these ingredients were added, the final suspension was immediately sprayed into the pre-cooled spraying tower
through the 2-fluid nozzle with heated air of about 90 °C as the 2nd
medium. The pump pressure was set at 1 bar, and the air pressure for
the nozzle was set at 2.5 bar. Liquid nitrogen was sprayed into the
middle zone of the tower to cool and rapidly solidify the atomized
particles. They were collected at the bottom of the tower in a drawer
containing a polystyrene recipient laid out with a plastic foil. The
capsule:substrate ratio of the produced microcapsules was 60:40.
Viscosity experiments
The effect of varying processing parameters on the viscosity of the
molten palm fat suspension was studied and included (1) suspensions containing 25% (w/w) FePP with a MPS of 2.5 m heated to different temperatures (65 °C, 68 °C, 71 °C, 74 °C, 80 °C) and sheared
with increasing shear rates (10–1 – 103/s); (2) suspensions containing
0.5% lecithin (Centrolex F-IP soya pure lecithin, Univar AG, Zürich,
Switzerland) or 0.5% polyglycerol polyricinoleate (PGPR) (Danisco Ingredients, Copenhagen, Denmark) in addition to the 25% Fe particles sheared at 70 °C in the shear rate range of 10–1 to 103/s; and (3)
suspensions containing varying capsule:substrate (FePP) ratios, with
and without the 2 emulsifiers (Lecithin, PGPR) in varying concentrations sheared in the same shear rate range. Viscosity was measured
using a Physica MCR-300 rheometer with a Peltier-heated doublegap Couette geometry (Paar Physica, Stuttgart, Germany).
Particle size measurements
The particle size distribution of the microcapsules after spraying
was measured in air flow by laser diffraction using a Sympatec Helos
(Bühler AG, Uzwil, Switzerland). The number distribution Q0(x) was
calculated and the values for x10,0 (the diameter of 10% of the number
of particles that were smaller than x), x50,0 (the diameter of 50% of the
number of particles that were smaller than x), and x90,0 (the diameter
of 90% of the number of particles that were smaller than x) were read
from the size distribution. The microcapsule morphology was determined by optical inverse microscopy (Nikon Diaphot TMD, Nikon
Corp., Tokyo, Japan) and by scanning electron microscopy (Hitachi
S900, Hitachi, Tokyo, Japan).
Salt fortification with the microcapsules in Morocco
The salt fortification level chosen for the Fe compound was equivalent to 1 mg of Fe as ferrous sulfate per gram salt and was based on (1)
the estimated relative bioavailability of the FePP (approximately 50%)
compared with ferrous sulfate (Hurrell 2002b); (2) previous studies of
daily salt (approximately 10 g/d) and iron (approximately 12 mg/d,
97% as non-heme Fe from a highly inhibitory diet) intake in Moroccan
school children (Zimmermann and others 2003, 2004a); and (3) a goal
of supplying approximately the estimated daily iron requirement of
about 8 mg for this age group (Inst. of Medicine 2001). Therefore, ferric
pyrophosphate was added at a level of 2 mg Fe/g salt. The fortification
level for KIO3 was based on (1) salt intake in Morocco (Zimmermann
and others 2003); (2) supplying the estimated daily requirement of 120
to 150 g for children 9 to 18 y old (Inst. of Medicine 2001), and (3) anticipation of losses (approximately 50%) during spraying, storage, and
cooking (WHO/UNICEF/ICCIDD 1996). Therefore, KIO3 was added
in the double amount at spraying, assuming a final iodine content in
the fortified salt of about 20 g/g salt. The vitamin A fortification level
was based on (1) salt and vitamin A intake (approximately 250 g RAE/
d) in Morocco (Zimmermann and others 2003, 2004a); (2) estimated
losses during spraying (approximately 50%); and (3) the estimated
daily requirement of 400 to 600 g for children 4 to 13 y old (Inst. of
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Microcapsules of Fe, iodine, & vitamin A . . .
Medicine 2001) and on the maximum safe intake of 3000 g retinol
equivalents per day for pregnant women (WHO/MI 1998). Therefore,
vitamin A was added at double the amount at spraying to achieve a
final concentration of about 50 g vitamin A/g salt.
Local Moroccan salt prepared from drying ponds fed by a salty
spring was used to prepare the fortified salts. The salt was unwashed and unground, and has a moisture content between 1% to
4% depending on the season. To prepare the iodized salt (IS), iodine was added to the salt as reagent-grade KIO3 (Sigma & Aldrich,
Buchs, Switzerland) at a level of 25 g iodine/g salt. To prepare the
triple-fortified salt (TFS), salt was fortified with the microcapsules
at a level of 2 mg Fe/ ⬇20 g iodine/ ⬇50 g vitamin A per g salt.
The compounds were mixed into the salt in 2 steps. First, a concentrated 2-kg premix of the salts was prepared in a small electric rotating drum mixer (RRM MINI 80, Engelsmann, Ludwigshafen, Germany) that mixed at 26 rpm for 10 min. The mixture was then
transferred to a larger barrel mixer (ELTE 650, Engelsmann); 4 more
kg of salt were added and further mixed at 30 rpm for 5 min.
Iodized salt and salt fortified with the microcapsules were stored as
2-kg batches in closed transparent low-density polyethylene bags for
6 mo in a clean, ventilated room out of direct sunlight. At mixing and
after 2, 4, and 6 mo of storage, aliquots of 30 g (n = 3/salt) were taken
and placed in tightly sealed plastic containers, wrapped with aluminum
foil, and frozen until analysis. The iodine concentration was measured
in the IS and TFS, and the vitamin A concentration in the TFS. The
color of the 2 fortified salts was determined, and the color of TFS was
compared with that of IS. Iron content was verified at mixing.
Four commonly-consumed northern Moroccan meals—couscous
(semolina), white bread, bissara (fava bean-based soup), and chaaria
(semolina noodles in milk)—were prepared with both iodized salt and
salt triple-fortified with the microcapsules. Three of the meals (couscous, bread, chaaria) have a neutral taste and smell, as well as a pale
color. The sensory tests were carried out using the triangle test (Meilgaard and others 1999) and a non-trained panel of 18 local adults per
meal. The panel was asked to taste each of the 3 meals and to select the
sample that differed from the other 2. To estimate the overall acceptability of the salt, 50% of the households using either the iodized (n =
41) or triple-fortified salt (n = 30) were interviewed about the color and
taste acceptability after 10 mo of salt consumption.
Laboratory analysis
The fortification level of iron in the triple-fortified salt at mixing
was analyzed by the standard addition method using flame atomic
absorption spectroscopy (SpectrAA-400, Varian, Mulgrave, Australia) after sample dissolution and filtration. Iodine content of the IS
was measured after salt aliquots were dissolved in deionized water
in an ultrasound bath (Branson 5210, Branson Ultrasonic Corp.,
Danbury, Conn., U.S.A.) using a modification of the SandellKolthoff reaction originally described for the determination of urinary iodine (Pino and others 1996). This method could not be used
for the TFS due to incomplete digestion of the microcapsules, so
iodine content of the TFS was measured using inductively coupled
plasma-mass spectrometry (Haldimann and others 2003). Retinyl
palmitate was extracted with hexane from the fortified salt. Samples
were filtered and measured at an extinction wavelength of 331.6
nm and an emission wavelength of 481 nm by fluorescence spectrophotometry (Luminescence Spectrometer LS 50B, Perkin Elmer,
Wiltshire, U.K.) using an external calibration curve.
Color was determined by colorimetry (Chroma-Meter CR-310, Minolta AG, Dietikon, Switzerland) as described in an earlier publication
(Wegmuller and others 2003) using the Hunter Scale. The color of the
DFS and IS at each time point was compared with IS at baseline and
color lightness (L value), and color difference (E) was calculated.
Statistical analysis
Data processing and statistics were done using Excel (XP 2002,
Microsoft, Seattle, Wash., U.S.A.). Colorimetry results and iodine
and vitamin A content were expressed as means (SD) for IS and TFS
at 0, 2, 4, and 6 mo of storage. A 2-factor repeated-measures analysis of variance (ANOVA) was done to compare effects of the fortification × time interaction on salt color and iodine content. If the
interaction effect was significant (P < 0.05), t tests between groups
and paired t tests within groups over time were done.
Results and Discussion
Properties of the spraying suspension
Figure 1 shows the viscosity function of a palm fat suspension
containing 25% (w/w) FePP (MPS ⬇ 2.5 m) at different tempera-
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Vol. 71, Nr. 2, 2006—JOURNAL OF FOOD SCIENCE
S183
S: Sensory & Nutritive Qualities of Food
Figure 1—Viscosity
function of a palm
fat suspension
containing 25% (w/
w) small particle size
ferric pyrophosphate
(MPS ⬇ 2.5 ␮m) at
different temperatures
Microcapsules of Fe, iodine, & vitamin A . . .
tures as a function of the shear rate. At low shear rates, viscosity is
more temperature-dependent than at high shear rates. At shear
rates of · 200/s, viscosity increased with temperature. At shear
rates of · 200/s, this phenomenon reversed and viscosity decreased with increasing temperature. A possible explanation of this
flow behavior can be given if the competition between structure forces (interparticle forces) and hydrodynamic flow forces is considered.
At low shear rates the structure forces dominate the flow forces. In
the continuous fat phase, the particles experience strong attractive
interparticle forces due to their hydrophilic surfaces. This leads to
particle agglomeration. Consequently, temperature increase leads
to enhanced particle agglomeration and the related entrapment of
free fluid (melted fat) in the voids and pores of the particle agglomerates, causing an increase in the effective volume fraction. Consequently, the viscosity increases. In the high shear rate domain (here
· 200/s), the hydrodynamic forces dominate the structure forces,
leading to de-agglomeration of the structure. Consequently, only the
fluid viscosity that reduces with increased temperature is relevant.
This was confirmed with the small particle size FePP (MPS ⬇ 2.5 m),
showing a quick increase of viscosity when it was mixed into molten
palm fat. It was not possible to produce a suspension containing
more than 25% (w/w) of the iron compound (Windhab 2000).
The viscosity functions of suspensions containing 25% (w/w)
FePP (MPS ⬇ 2.5 m) with and without the addition of an emulsifier (0.5% lecithin or 0.5% PGPR) were compared. As shown in Figure 2, at low shear rates, samples containing emulsifiers had lower
viscosity, with PGPR showing a larger reduction in viscosity compared with lecithin. At high shear rates (for example, during spraying), the viscosity of the samples with emulsifiers was also lower
than those without emulsifier, while the viscosity of the 2 samples
with emulsifiers was comparable. These findings indicated the
benefit of emulsifier addition to the palm fat suspension, allowing
the substrate:capsule ratio to be maximized. Varying amounts of lecithin were added to increase the solid content of the suspension
and thereby reduce the amount of capsule material and costs at the
same time. Finally, a sprayable suspension containing 40% FePP
was achieved using 1% lecithin; and a final capsule:substrate ratio
of 60:40. A decrease in viscosity in the case of emulsifier addition can
be explained by the emulsifier functionality which acts in modify-
Table 1—Particle size distribution of 2 batches of
microcapsules
Particle size (µm)
X10,0a
Batch 1
Batch 2
35.2
28.9
X50,0
X90,0
138.1
132.3
305.2
428.7
a The diameter of 10% of the number of particles that were smaller than x.
ing the interparticle forces and as a spacer between particles and
thereby reduces agglomeration (Hugelshofer 2000). The emulsifier
may also stabilize specific crystal forms that can affect the diffusion
rate of water through the matrix (Gouin 2004).
Particle size and morphology of microcapsules
Table 1 shows the results of the particle size analysis of 2 batches of
sprayed microcapsules. Capsule size ranged from several microns up
to several hundred microns. Comparing the distribution of the 2
sprayed batches, values for x10,0, x50,0, and x90,0 were comparable, with
the MPS of 138 and 132 m, respectively, indicating a good reproducibility. This MPS was close to the desired maximum MPS of approximately 100 m, chosen to reduce segregation of microcapsules in the
fortified salt. Spray cooling has the advantage that particles of a wide
particle size range can be produced (Gouin 2004); therefore, microcapsules can be adapted to the local salt of different countries or to other
food vehicles. However, the production process should be improved
to produce a narrower particle size range or the capsule product
should be classified. Figure 3 shows a light microscope image of the
microcapsules (100 × magnification). The sprayed particles are of
spherical shape with rather smooth surface, which is typical for spraycooled or spray-chilled products because there is no mass transfer by
evaporation as in spray drying (Shahidi and Han 1993). The image
demonstrates the relatively wide particle size range and the presence
of agglomerates likely due to insufficiently solidified particles during
settling in the spaying tower. Figure 4 shows a scanning electron microscopy (SEM) micrograph of the surface of microcapsules at 2 different magnifications. Fat crystals of the palm fat can be observed on the
capsule surface. Small capsules show fewer fat crystals on the surface
Figure 2—Viscosity
function of a palm
fat suspension
containing 25% (w/
w) small particle
size ferric pyrophosphate (MPS
⬇ 2.5 ␮m) with the
addition of 0.5%
lecithin, 0.5%
polyglycerol
polyricinoleate
(PGPR) and without
emulsifier at a
constant temperature of 70 °C
S: Sensory & Nutritive Qualities of Food
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JOURNAL OF FOOD SCIENCE—Vol. 71, Nr. 2, 2006
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Microcapsules of Fe, iodine, & vitamin A . . .
than larger ones, most probably due to shorter solidification time for
small capsules. To visualize the inner structure, microcapsules were
broken, and as shown in Figure 5, the large crystals of the palm fat can
be recognized on the surface of the cross-section. The individual nutrient components are not visible on the surface or in the cross-section
of the broken capsules. Techniques to visualize the distribution of the
different nutrients in and on the surface of the capsule are required for
more detailed characterization of the capsules.
Acceptability and sensory testing
There were no differences detected by the panelists using triangle tests in the 4 meals fortified with IS and TFS. After 10 mo of
household salt use (IS or TFS), the head of the household was interviewed about the acceptability of the salt. About half of the households used IS (n = 41) and the other half TFS (n = 30) for cooking.
There was no difference in the use of the salt, in color acceptability,
in salt taste in foods, and in overall acceptability between households using IS or TFS. A slight color change, mainly in egg and milk
dishes, was observed by 16% of the IS and 32% of the TFS heads of
household. However, this slight color change did not affect overall
acceptability and was not detected in the triangle tests also performed with dishes containing milk or eggs.
Stability and bioavailability of microcapsules
Table 2 shows the color and iodine content of IS and TFS, as well
as the retinol content of the TFS at baseline and after storage for 2, 4,
and 6 mo. Color determination showed no significant difference
between IS and TFS in color lightness (L value), and no significant
color change in the IS and the TFS over 6 mo of storage. The light
beige color of the TFS compared with the milky white color of IS resulted in an absolute color difference (E) of approximately 9. Although Wegmüller and others (2003) reported fortified salts with E
<10 compared with IS were generally considered acceptable during
interviews at local African markets, an improvement in salt color
could be a future aim in the refinement of the encapsulation process.
Ferric pyrophosphate with a whiter color than the 1 used (for example, reagent-grade material) would be a possibility, but would be
more expensive and more difficult to produce on a large scale. Because fats crystallize in various forms that exhibit very different crystal sizes, hydrophobicities and densities (Gouin 2004), refinement of
the crystallization during production and storage may also help in
preventing reactions of the Fe compound resulting in discoloration.
The spraying process resulted in iodine losses of approximately
40%. Losses after storage for 6 mo were additionally about 20% in
both salts, with no significant differences comparing TFS to IS. During spraying, approximately 30% of the retinol was lost. The retinyl
palmitate used in the experiments was surprisingly stable during
storage, with small losses of about 12% after 6 mo, presumably due
to the hydrogenated fat acting as an excellent barrier to oxygen.
These results, however, indicate that retinol and iodine losses during
production of the capsules are relatively high, and the encapsulation
process could be further improved to prevent these losses, particularly for retinol, which is expensive. Producing the microcapsules in
an oxygen-free area and without direct light could be a next step.
Besides the good stability of the microcapsules, the bioavailability
of nutrients from the capsule and thereby its potential efficacy in
human nutrition is an important consideration. Spray cooling is typically called “matrix” encapsulation because the particles are more
adequately described as aggregates of active ingredient particles
buried in the fat matrix, whereas “true” encapsulation is usually reserved for processes leading to core/shell type of microcapsules. A
matrix encapsulation process leaves a significant proportion of the
active ingredients lying on the surface of the microcapsules or sticking out of the fat matrix, thus having direct access to the environment
and generally releasing their content easily (Gouin 2004). However,
a strong binding of the ingredient to the fat matrix can prevent the
release of the ingredient, even though the fat matrix is melted and/
or damaged during processing (Gouin 2004). In a series of rat stud-
Figure 4—Surface of microcapsules analyzed by scanning
electron microscopy (SEM): (a) 700× magnified, picture width:
154 ␮m and (b) 5000× magnified, picture width: 21.6 ␮m
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Figure 5—Inner structure of a broken microcapsule analyzed by scanning electron microscopy (SEM) (700× magnified, picture with: 154 ␮m)
Vol. 71, Nr. 2, 2006—JOURNAL OF FOOD SCIENCE
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S: Sensory & Nutritive Qualities of Food
Figure 3—Sprayed microcapsules analyzed by light microscopy (100× magnification)
Microcapsules of Fe, iodine, & vitamin A . . .
Table 2—Color, iodine, and vitamin A concentration in iodized salt (IS) and triple fortified salt (TFS) after storage for 0,
2, 4, and 6 mo and fortification level before storagea
Vitamin A
Iodine f
µg /g salt
µg /g salt
TFS
Fortification
0 mo
2 mo
4 mo
6 mo
leveld
69.7
74.5
69.4
61.2
100
± 7.1
± 3.2
± 2.7
± 4.5
Color
IS
27.4
18.6
21.0
19.4
25
± 3.8
± 2.1
± 3.1
± 1.4
Eabc,e
Lightness b
TFS
25.7
22.2
26.5
20.6
IS
40
± 3.0
± 6.1
± 3.7
± 0.9
80.9
80.3
80.7
80.3
—
± 0.88
± 0.45
± 1.01
± 0.75
TFS
79.82
79.87
79.73
79.59
—
± 0.26
± 0.31
± 0.38
± 0.11
TFS/IS
9.01
9.17
9.02
9.02
—
± 1.05
± 0.07
± 0.28
± 0.52
aValues are means ± SD (n = 3).
b Lightness scale: 0 = black, 100 = white.
cE
ab absolute color difference between TFS and IS.
d Iodine and vitamin A added before spraying for TFS and iodine added at mixing for IS.
e Significant main effect of fortification, P < 0.001 (analysis of variance [ANOVA]).
fSignificant main effect of time, P < 0.001 (ANOVA).
S: Sensory & Nutritive Qualities of Food
ies (Hurrell 1985; Hurrell and others 1989), the relative bioavailability
(RBV) of encapsulated ferrous sulfate at a 40:60 capsule:substrate
ratio was comparable to that of nonencapsulated ferrous sulfate. A
study in children consuming salt fortified with ferrous sulfate encapsulated in partially hydrogenated vegetable oil (ratio 50:50) reported
that the encapsulated iron was highly effective in reducing the prevalence of IDA (Zimmermann and others 2003), suggesting encapsulation with a fat matrix had little or no effect on bioavailability. However, studies with encapsulated ferrous sulfate in hydrogenated
soybean oil and ferric ammonium citrate in hydrogenated palm oil
showed a reduction of RBV of about 20% to 25% at a capsule:substrate
ratio of 60:40 (Zimmermann 2004). In a recent rat study comparing
the RBV of small particle size FePP encapsulated with the method described in this article (fully hydrogenated palm oil at a
capsule:substrate ratio of 60:40) to the nonencapsulated compound,
a 40% decrease in RBV was found (Wegmuller and others 2004).
However, small particle size FePP encapsulated together with iodine
and retinyl palmitate in palm fat (60:40 capsule:substrate ratio) was
recently tested in a human efficacy trial of fortified salt in Morocco
and was shown to be highly efficacious in improving iron status (Zimmermann and others 2004a). Nevertheless, new WHO guidelines
(WHO 2005) recommend a capsule:substrate ratio of 50:50 due to
possible losses of bioavailability with greater ratios.
Although ferric pyrophosphate with a particle size of 10 m has a
relative bioavailability of only 20% to 70% compared with ferrous sulfate (Hurrell 2002a, 2002b; Wegmuller and others 2004), reducing its
particle size to 0.5 m (SunActive Fe, Taiyo Kagaku Co., Ltd., Mie, Japan) increases its bioavailability in humans to that of ferrous sulfate
(Fidler and others 2004). In a recent rat study, the reduction of MPS of
ferric pyrophosphate from 21 m to 2.5 m resulted in a nonsignificant
increase of RBV, from 59% to 69%, and further reduction to a MPS of 0.5
m increased RBV to 95%, comparable to ferrous sulfate (Wegmuller
and others 2004). Due to the high cost of commercial 0.5 m FePP,
which is coated with emulsifiers to make it water dispersible, the 2.5m compound was used in the present studies. The lower RBV of this
compound compared with ferrous sulfate (approximately 70% in rats)
was taken into account during microcapsule preparation and salt fortification, with a final amount of 2 mg Fe added per gram salt.
Processing costs to reduce particle size of FePP to 2.5 m tend to
approximately double the cost (Dr. Paul Lohmann GmbH, Emmerthal,
Germany) and could be a significant barrier for the use of small particle
size FePP in fortification programs in developing countries. Additional
costs for the encapsulation material as well as production costs must
also be considered. If microencapsulation provides the ingredient
with a unique property that is not achievable without encapsulation,
the cost-in-use is allowed to be slightly higher than that of the nonenS186
JOURNAL OF FOOD SCIENCE—Vol. 71, Nr. 2, 2006
capsulated ingredient (Gouin 2004). However, the price increment for
salt fortification, especially with vitamin A, tends to be high due to the
low baseline price of the salt. However, in many regions with subsistence farming in Africa and Indonesia, salt is 1 of few regularly purchased food items and therefore often is the only suitable food vehicle
for food fortification (Hess and others 1999; Melse-Boonstra and others
2000; Staubli-Asobayire 2000). Fortification of salt with iodine is highly
effective in reducing IDD (WHO/UNICEF/ICCIDD 2001) and some
food stuffs, such as oil (Favaro and others 1992; Johnson 1997), margarine ( Johnson 1997; Solon 1997a; Sridhar 1997), monosodium
glutamate (Solon and others 1985; Muhilal and others 1988), cereal
flours (Chavez 1997; Solon 1997b), and sugar (Mora and others 2000),
have been shown to be efficacious in reducing vitamin A deficiency.
But these fortification vehicles are often not widely distributed or not
consumed by the neediest population groups. Successful iron fortification has been demonstrated with infant cereals and formulas
(Walter and others 1990, 1998), sugar (Viteri and others 1995), curry
powder (Ballot and others 1989), and fish sauce (Thuy and others
2003), but not yet with cereal and corn flours (Hurrell 2002b). However,
the same problem of limited access by the neediest applies to Fe fortification with these food vehicles. Thus, triple fortification of salt with
a single compound containing all 3 micronutrients could be a useful
and simple new fortification strategy.
Conclusions
S
pherical microcapsules containing FePP, iodine, and vitamin A
for use in salt fortification were successfully produced by spray
cooling. Although iodine and vitamin A losses during production of
the microcapsules were relatively high, losses during storage after
addition to salt were low. Through the encapsulation, vitamin A added as retinyl palmitate was dissolved in the fat matrix before spraying and showed excellent stability in salt. Iodine and color stability
of salt fortified with the microcapsules were acceptable. By using a
small particle size FePP (MPS ⬇ 2.5 m) and a higher fortification
level, the low bioavailability of regular FePP was compensated. A
study with school-age children consuming salt fortified with the
microcapsules showed high efficacy of all 3 micronutrients in Morocco (Zimmermann and others 2004a). These findings indicate
that triple fortification of salt with a single compound containing all
3 micronutrients could be a useful and simple new fortification
strategy. However, process parameters and raw materials should be
further optimized to (1) decrease the capsule:substrate ratio of
60:40 to minimize possible losses in bioavailability of the encapsulated nutrients; (2) minimize color changes due to the off-white
ferric pyrophosphate and not tight enough capsules; (3) reduce
losses of iodine and especially of retinyl palmitate during spray
URLs and E-mail addresses are active links at www.ift.org
cooling; and (4) reduce costs because this could be a significant
barrier in fortification programs in developing countries.
Acknowledgments
This study was supported by the Swiss Federal Inst. of Technology
(Zürich, Switzerland). We thank Daniel Kiechl (Swiss Federal Inst. of
Technology, Switzerland) for technical assistance in building and
improving the spraying tower and in spraying the encapsulated compound; Dr. Paul Lohmann GmbH (Emmerthal, Germany) for providing the small particle size ferric pyrophosphate; BASF ChemTrade
GmbH (Burgbernheim, Germany) for providing the retinyl palmitate; Oskar Krois and Priscilla Fässler (Bühler AG, Uzwil, Switzerland)
for the help in the milling process and the particle size measurements; Max Haldimann (Swiss Federal Office of Public Health, Switzerland) for ICP-MS measurements of the triple-fortified salt; Rabie
Rahmouni (Brikcha, Morocco) and Christophe Zeder (Swiss Federal
Inst. of Technology, Switzerland) for assistance in sampling and mixing; Fabian Rohner (Swiss Federal Inst. of Technology, Switzerland)
for assistance in the sensory testing.
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Microcapsules of Fe, iodine, & vitamin A . . .