-
Microencapsulation by spray drying of gallic acid with nopal
mucilage(Opuntia cus indica)
L. Medina-Torres a,*, E.E. Garca-Cruz b, F. Calderas a, R.F.
Gonzlez Laredo c, G. Snchez-Olivares d,J.A. Gallegos-Infante c,
N.E. Rocha-Guzmn c, J. Rodrguez-Ramrez b
a Facultad de Qumica, Departamento de Ingeniera Qumica, Conjunto
E, Universidad Nacional Autnoma de Mxico (UNAM), Mxico, D.F. 04510,
Mexicob Instituto Politcnico Nacional, CIIDIR-IPN-Oaxaca, Hornos
No.1003, Santa Cruz Xoxocotln, Oaxaca 71230, MexicocDepartamento de
Ing. Qumica y Bioqumica, Instituto Tecnolgico de Durango., Blvd.
Felipe Pescador 1830 Ote., 34080 Durango, Dgo., MexicodCIATEC, A.C.
Omega 201, Fracc. Industrial Delta, CP 37545, Len, Gto, Mexico
a r t i c l e i n f o
Article history:
Received 7 March 2012
Received in revised form
17 July 2012
Accepted 24 July 2012
Keywords:
Nopal mucilage
Rheological behavior
Bioactive compounds
Gallic acid
Spray drying
a b s t r a c t
The spray-drying process has been previously used to encapsulate
food ingredients such as antioxidants.
Thus the objective of this work was to produce microcapsules of
gallic acid, a phenolic compound that
acts as antioxidant, by spray drying with an aqueous extract of
nopal mucilage (O), which acted as an
encapsulating agent. The rheological response and the particle
size distribution of the nal solutions
containing gallic acid at concentrations of 6 g/100 mL were
characterized along with the control sample,
no gallic acid added, to elucidate the degree of encapsulation.
The drying parameters to prepare the
microcapsules with extract of nopal mucilage were: inlet air
temperature (130 and 170 C) and speed
atomization (14,000 and 20,000 rpm). The rehydrated biopolymer
showed a non-Newtonian pseudo-
plastic behavior. The Cross Model was used to model the
rheological data. Values for m varied between
0.55 and 0.85, and for time characteristic, l, the range was
between 0.0071 and 0.021 s. The mechanical
spectra showed that the sample with gallic acid was stable long
term (>2 days) and presented a bimodal
particle size distribution. This study demonstrated the
effectiveness of nopal mucilage when utilized as
wall biomaterial in microencapsulation of gallic acid by the
spray-drying process.
2012 Elsevier Ltd. All rights reserved.
1. Introduction
Polyphenols are chemical compounds or phytochemicals with
diverse biological activities due to their antioxidant
capacity.
Ingestion of polyphenol-rich foods should be benecial to
human
health as factors associated with cardiac mortality in
developed
countries with particular reference to the consumption of wine
(St.
Leger, Cochrane, & Moore, 1979). Wine has antimicrobial
and
antifungal activity and may play a role in the etiology of
migraine.
Red wine may even protect against the common cold. Wine
contains polyphenols from the avonoid type, mostly as grape
tannins (about 35 g/100 g) and anthocyanin pigments (about 20
g/
100 g), not only present mostly in red rather than in white
grapes
(Takkouche et al., 2002), but also non-avonoid phenolics such
as
stilbenes and gallic acid. Gallic acid (acid
3,4,5-tri-hydroxy-ben-
zoic) and its derivatives are considered natural antioxidants
and
their effects and uses have been widely reported (Cho, Kim, Ahn,
&
Je, 2011; Pasanphan & Chirachanchai, 2008; Negi et al.,
2005).
Stabilization and application of polyphenols in foods and
nutra-
ceutical formulations can be improved by microencapsulation
technologies (Senz, Tapia, Chvez, & Robert, 2009).
Microencap-
sulation allows protection of bioactive compounds; i.e., an
active
material (nucleus) is embedded in a polymer matrix
(encapsulating
agent or wall material) to act as a protective barrier against
external
or environmental factors (Ahmed, Akter, Lee, & Eun,
2010;
Borgogna, Bellich, Zorzin, Lapasin, & Cesro, 2010; Senz et
al.,
2009).
Spray drying is a common technique for producing
encapsulated
food materials (Senz et al., 2009). Good microencapsulation
ef-
ciency during spray drying is achievedwhen themaximum amount
of core material is encapsulated inside the powder particles,
suc-
ceeding in microcapsule stability, volatile losses prevention,
and
product shelf-life extension (Seid, Elham, Bhesh, & Yinghe,
2008).
In spray drying, the operating conditions and the dryer design
used
depend on the characteristics of the material to be dried
and
the desired powder specications (Len Martnez, Mndez, &
Rodrguez, 2010). Studying the effect of operating parameters
* Corresponding author. Tel.: (52) 55 56225360/59703815; fax: 52
55
56225329.
E-mail address: [email protected] (L. Medina-Torres).
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http://dx.doi.org/10.1016/j.lwt.2012.07.038
LWT - Food Science and Technology 50 (2013) 642e650
-
on the physical properties of powder helps to identify the
optimum
operating conditions of spray dryers and their effect on
powder
characteristics (Chegini & Ghobadian, 2007; Wang, Lu, Lv,
& Bie,
2009). The main factors in spray drying that must be
optimized
are feed temperature, air inlet temperature, and air outlet
temperature (Liu, Zhou, Zeng, & Ouyang, 2004; Wang et al.,
2009).
Feed temperature modies the viscosity of the emulsion and
thus,
its capacity to be homogenously sprayed. When the feed
temper-
ature is increased, viscosity and droplets size should be
decreased
but high temperatures can cause volatilization or degradation
of
some heat-sensitive ingredients. The rate of feed delivered to
the
atomizer is adjusted to ensure that each sprayed droplet
reaches
the desired drying level before it comes in contact with the
surface
of the drying chamber (Zbicinski, Delag, Strumillo, &
Adamiec,
2002). Inlet air temperature is determined by the
temperature
that can be used safely without damaging the product or
creating
operational risks, and comparative costs of heat. Air inlet
temper-
ature is directly proportional to the microcapsule drying rate
and
the nal water content. An air inlet temperature low causes a
low
evaporation rate, the formation of microcapsules with high
density
membranes, high water content, poor uidity, and easiness of
agglomeration. However, a high air inlet temperature causes
an
excessive evaporation and results in cracks in the membrane
inducing subsequent premature release and a degradation of
encapsulated ingredient or loss of volatiles (Zakarian &
King, 1982).
The temperature at the end of the drying zone or air outlet
temperature can be considered as the control parameter of
the
dryer. The outlet temperature depends on inlet temperature, and
it
has been reported to vary from 50 to 80 C for the
microencapsu-
lation of food ingredients with phenolic compounds such as
green
tea (Fang & Bhandari, 2010; Gharsallaoui, Roudaut,
Chambin,
Voilley, & Saurel, 2007).
For encapsulation purposes, modied starch, maltodextrin, gum
or other substances are hydrated to be used as the wall
materials.
Maltodextrins has been used to encapsulate extracts of black
carrots, which contain anthocyanins (Ersus & Yurdagel,
2007);
maltodextrin-gum arabic has been used for procyanidins from
extract grape seeds (Zhang, Mou, & Du, 2007); chitosan has
been
used as a wall material in spray drying for olive leaf
extract
(Kosaraju, Dath, & Lawrence, 2006); Chiou and Langrish
(2007)
used citrus fruit ber as an encapsulating agent for
anthocyanin
complexes extracted from Hibiscus sabdariffa L.; colloidal
silicon
dioxideemaltodextrinestarch for soybean extract (Georgetti,
Casagrande, Souza, Oliveira, & Fonseca, 2008); another
wall
material used for encapsulation of polyphenol was sodium
caseinateesoy lecithin emulsion, which has been used in
spray
drying for grape seed extract, apple polyphenol extract and
olive
leaf extract (Kosaraju, Labbett, Emin, Konczak, & Lundin,
2008). The
mucilage from Opuntia cus indica is an interesting and
promising
alternative due to its emulsifying properties (Medina Torres,
Brito
De La Fuente, Torrestiana Snchez, & Katthain, 2000). It is
used as
an additive in the food industry, specically as an edible
coating to
extend the shelf life of food products (Del Valle, Hernndez
Muoz,
& Galotto, 2005). Previous studies have shown that
chemical
composition of O. cus-indica mucilage is a complex mixture
of
polysaccharides such as L-arabinose, D-galactose, D-xylose and
L-
rhamnose, and D-galacturonic acid, which represent up to 10
g/
100 g of total sugars (Medina Torres et al., 2000; Senz,
Seplveda,
& Matsuhiro, 2004). Multiple applications have been
developed for
this material ranging from a thickener of foods to a
turbidity
remover in contaminated water. The usefulness of this
hetero-
polysaccharide of high molecular weight (2.3 104 g/mol) relies
on
its physicochemical properties, which have been described by
many research groups; emphasizing its electrolyte thickener
capacity and its ow characteristics (Crdenas, Higuera Ciapara,
&
Goycoolea, 1997; Medina Torres et al., 2000). High moisture
content in the mucilage limits its applications, generating the
need
for previous treatments such as spray drying (SD) to increase
its
potential uses. The rheological properties of food products
sub-
jected to SD are important and can be used in quality
control,
storage and processing, stability measurements, and the nal
texture prediction of the dehydrated product. Rheological
studies
are useful, especially when related to the mechanical response
and
to the micro-structure of the materials (Abu-Jdayil, Banat,
Jumah,
Al-Asheh, & Hammad, 2004).
In the present work, an antioxidant compound (gallic acid)
was
encapsulated using aqueous extracts from O. cus-indica (O)
mucilage as wall material by spray drying; the thermal
(differential
scanning calorimetry, DSC) and scanning electron microscopy
(SEM) analysis were used to evaluate the effectiveness of
wall
material as an encapsulating agent. The response through DSC
coupled and the release of the microcapsules was evaluated as
to
assess the feasibility of this encapsulating process. The
biome-
chanical response in simple shear and oscillatory ow and the
particle size distribution (PSD) were evaluated as quality
measure
of microcapsulation. The microcapsules obtained represent an
interesting option for incorporation of food antioxidants
and
additives into functional foods applications.
2. Materials and methods
2.1. Materials
Cladodes of nopal (O. cus-indica) (O) of approximately 6-
month-old plants, with 92.21 g/100 g dry solid, moisture
content,
were collected randomly from the same plantation (August
2010),
at Milpa Alta, Mexico City. The moisture content of fresh
cladodes
was determined with an infrared balance (AND, model
AD-4714A).
Cladodes were washed thoroughly with water at 25 C, using
a plastic bristle brush. Cladodes were macerated (500mL
deionized
water per kg of material) to facilitate the extraction of
mucilage.
The material was let to stand 24 h, and the solid material
separated
by decantation. Extract was ltered to 149 mm pore size, and
the
remaining ne particles were separated with nylon canvas and
using a centrifuge Dinacclay at 11,000g for 15 min (Medina
Torres
et al., 2000). This will be called mucilage extract from here
on.
Mucilage extract was stored in refrigeration containers at 4 C
and
its Brix measured using a manual refractometer with
temperature
compensation (WestoverRHB-32ATC model).
2.2. Aqueous dispersion previous to the spray-drying process
The mucilage extract was diluted in deionized water at 1
Brix,
due to its initial high viscosity and solids content it was not
possible
to spray drying. The encapsulated samples were prepared with
0.3 g of gallic acid/L mucilage extract (E1eE5) to analyze the
effect
of spray drying. All samples were homogenized at constant
stirring
for 30 min using a mechanical shaker.
2.3. Spray drying
A pilot scale spray dryer with co-current ow Niro atomizer
(Production Minor Spray Dryer, Niro Inc., Denmark) (Niro,
Copen-
hagen, Denmark), equipped with rotary atomizer (TS-Minor,
M02/
A) was used to spray drying. Distilled water at room
temperature
(25 C) was used to stabilize the equipment. The mucilage
extract
was fed into the drying chamber using a peristaltic pump
(WatsoneMarlow 505S/RL). A 22 factorial design was used to
evaluate the effect of the independent variables: inlet air
temper-
ature (130 and 170 C), and atomizer speed (20,000 and
L. Medina-Torres et al. / LWT - Food Science and Technology 50
(2013) 642e650 643
-
14,000 rpm) on the encapsulated properties of samples E1eE4
(Table 1). The drying conditions for control samples (with
no
gallic acid added) B1 were 130 C and 14,000 rpm, while for
B2,
170 C and 20,000 rpm. Samples E5 and B3 (control) were
double
processed (dried, reconstituted and dried once again) at 130 C
and
14,000 rpm. All the experiments were carried out in
duplicate.
2.4. Reconstituted solutions of control and encapsulated
samples
Reconstituted solutions at a concentration of 6 g/100 mL
were
used for all rheological measurements, at this concentration
could
make out clearly the effect of the variables; the powders
were
dispersed in deionized water (pH w5.6), using a magnetic
stirrer
(Lighting mark) at 500 rpm for 2 h at 25 C. The pH of the
solution
was taken with a Thermo Orion 420 Apotentiometer Plus.
2.5. Rheological measurements
Rheological characterization was performed in simple and
oscillatory shear ow, using a controlled stress rheometer
(Model
AR-G2 TA Instruments) with the concentric cylinders geometry
(21.96 mm outer cylinder diameter, 20.38 mm inner cylinder
diameter, 59.50 mm height, and 500 mm gap), maintaining
a constant temperature (25 C) with a circulatory water bath
(Cole
Parmer Polystat and a Peltier AR-G2).
2.5.1. Steady-shear viscosity measurements
Steady-shear viscosity measurements were monitored as
a function of increasing shear rate h _g over the range 0.1e300
s1.
Experimental data were adjusted properly to the Cross model,
expressed in the Eq. (1)
h hN
h0 hN
1
1 l _gm (1)
where h is the shear viscosity (Pa s), g is the shear rate (s1),
l is
a relaxation time (s),m is the dimensionless index ow [m 1
n],
and hN and h0 are the limit viscosities at high and low shear
rates,
respectively (Kirkwood & Ward, 2008).
2.5.2. Activation energy at shear rate ow
Viscosity-temperature dependence was observed from 25 to
45 C at a constant shear rate of 10 s1, and data were adjusted
to
the Arrhenius equation (Eq. (2)) (Medina Torres et al., 2000;
Sengl,
Ertugay, & Sengl, 2005)
h Aexp
Ea
R
1
T
(2)
2.5.3. Steady oscillatory ow measurements
The viscoelastic properties, storage modulus (G0) and loss
modulus (G00) were determined through small amplitude oscil-
latory shear ow experiments at frequencies ranging from 1 to
100 rad s1. Prior to any dynamic experiments, a strain sweep
test at a constant frequency of 10 Hz was performed, xing
the
upper limit of the linear viscoelastic zone at a strain value of
30%
(which was used in all dynamic tests). All rheological
measure-
ments were carried out in duplicate. The experimental rheo-
logical data were obtained and analyzed directly from the TA
Rheology Advantage Data Analysis software V.5.7.0 (TA
Instru-
ment Ltd., Crawley, UK).
2.6. Particle size distribution of resuspended solutions
(PSD)
Particle size distributions (PSD) of samples (6 g/100 mL)
were
quantied with a Master-sizer 2000 laser diffraction particle
analyzer (Malvern Instrument Ltd, UK). The dispersant was
deionized water (particle R.I. 1.336, and dispersant R.I.
1.33).
2.7. Differential scanning calorimetry (DSC)
DSC analysis was performed in a DSC-7 calorimeter (Perkin
Elmer, Norwalk, CT, E.U.A.), previously calibrated with
Indium
(melting temperature 156.6 C, melting heat 28.45 J/g) and
equipped with Perkin Elmer DSC pan cells No. 02190062. An
empty
pan was used as reference to develop the baseline from 20 to
140 C. The sample (18 0.6 mg) previously weighted in
aluminum
pans, was initially heated to 80 C for 30 min in the
corresponding
thermocell of the DSC. In all stages the heating rate used was 5
C/
min. Temperatures for the different transitions (i.e., the
onset
temperature, T0; peak temperature, Tp; ending temperature,
Te)
were determined using the rst derivative of the heat
capacity
calculated from the DSC program library and by comparison to
the
baseline.
2.8. Scanning electron microscopy (SEM)
Detailed sample preparation for SEM measurements has been
described elsewhere (Medina Torres, Brito De-La Fuente, Gmez
Aldapa, Aragn Pia, & Toro Vzquez, 2006). Essentially, the
sample
was placed onto an aluminum slide using electrically
conductive
tape (Bal-Tec, Frstentum Liechtenstein), and coated with gold
at
10 mbar for 90 s (Polaron SC-7610, Fisson Instruments, CA,
USA).
The images were obtained with an electron microscope Leica
Stereoscan S420i (Cambridge, England).
2.9. Controlled release of gallic acid from microcapsule
The release of the microcapsules of sample E5 was carried out
in
Franz cells with a membrane of 0.22 mm HV in a water bath (37
C)
with constant stirring (300 rpm). The sample was resuspended
to
6 g/100 mL in buffer at pH 5 in order to try to simulate the
condi-
tions of the intestinal tract. The concentration of gallic acid
liber-
ated was used in a spectrophotometer at an intensity range
of
1.0e0.8 counts (Sez, Hernez, & Lpez, 2003). The
calibration
curve of gallic acid ranged from 5.5 105 to 5.0 106. The
sampling was carried out with 2 mL of the receiving cell
(Franz
cells) which were recovered with the solvent (buffer pH 5).
Results
were analyzed at a wavelength of 273.71 nm (Ferk et al.,
2011).
Dilutions were performed 0.05 g/mL. Measurements were per-
formed at least two times for accuracy.
3. Results and discussion
3.1. Effects of spray-drying conditions on steady-shear rate
ow
The effect of each SD factor on the viscous behavior was
studied
graphically, comparing the samples with one degree of
freedom
Table 1
Samples drying conditions.
Treatment Ti (C) Sa (rpm)
E1 130 14000
E2 130 20000
E3 170 14000
E4 170 20000
E5 130 14000
B1 130 14000
B2 170 20000
B3 130 14000
L. Medina-Torres et al. / LWT - Food Science and Technology 50
(2013) 642e650644
-
(L 1), i.e., temperature, pressure or rotor speed. Drying
temper-
ature and speed atomizer were found as the factors that
inuence
the most on the sample viscous behavior.
3.1.1. Effect of inlet air temperature
Drying inlet air temperature (Ti) was shown to affect the
viscosity of reconstituted samples, by increasing Ti, the
viscous (h0)
response at low shear rates _g < 10 s1 was found to decrease
as
shown in Fig. 1(A), which shows ow curves from samples B1,
E1
and E3 (microcapsules of mucilage with 0.3 g/L gallic acid).
The
viscous response of B1 is the highest of all; h in E1 is greater
than in
E3. The effect of Ti may be attributed to material thermal
degra-
dation when exposed to high temperature, as Kha, Nguyen, and
Roach (2010) reported previously, stating that an increase in
inlet
drying temperature results in thermal degradation and
oxidation.
The evidence is the fact that the shape of the ow curves does
not
essentially change, at high shear rates _g > 10 s1 all
acquire the
same shear thickening slope and most of the curves overlap
except
for E2. Spray drying (SD) may be causing the decrease in
viscosity
due to thermal effects and shear stress experienced by the
uid
since typical shear rates for spray drying range from 103 to 104
s1
(Barnes, 2000). McGarvie and Parolis (1981) and Medina
Torres
et al. (2000) reported molecular effects due to partial
hydrolysis
caused by thermal effects and the pH in the O mucilage
components, generating a higher concentration of
galacturonic
acid, causing a structural reconguration. Abu-Jdayil et al.
(2004)
observed that thermal effect alters structure of pectic
substances
mainly by hydrolysis. Pectic and other carbohydrate polymers
can
be largely hydrolyzed by heat resulting in smaller molecules.
High
temperature (>170 C) has been reported to cause thermal
degra-
dation of the mucilage molecular structure and a low
viscosity
(Len Martnez, Rodrguez Ramrez, Medina Torres, Mndez
Lagunas, & Bernad Bernad, 2011). The effect of thermal
degrada-
tion on viscosity was not observed for samples prepared at
high
spray speed (20,000 rpm): E2 (Ti 130C) and E4 (Ti 170
C). In
fact, E2 showed the lowest viscosity of all samples and does
not
overlap at high shear rates. In this case, the PSD had a
dominant
effect on the sample viscosity, samples E2 and E4 showed the
most
dispersed PSD (broadest distribution) of all samples, with PSD
of E2
broader than for E4 which directly affected viscosity, this is
also an
evidence of poor encapsulating effect for this sample, so
20,000 rpmwas considered as a non favorable process condition
for
encapsulation purposes.
3.1.2. Effect of air pressure (rotor speed)
Viscous response was also found to be affected by spray
speed
(Sa), where a high speed (20,000 rpm) caused the uid fed into
the
dryer to exhibit a decrease in viscosity at low shear rates (h0)
as
shown by the ow curves of B1, E1 and E2 samples on Fig.
1(A).
Again, the viscosity of the control sample is the highest (B) of
all
and the viscosity of sample E1 (14,000 rpm) is higher than that
of
E2 (20,000 rpm), this effect was not observed for samples at
high
inlet temperature (E3 and E4, 170 C) which is, attributed to
differences in PSD. Theoretically, rotor speed is proportional
to the
particle size distribution of mucilage powders obtained. This
means
that at a higher fragmentation rate, the greater the contact
surface
between the drop and hot air, the thinner and more porous
parti-
cles are obtained by the incorporation of air with lower
moisture
content. A similar effect was studied on O mucilage (Len
Martnez et al., 2011) and spray drying of milk (Walton &
Mumford, 1999), where higher spray pressure decreases
particle
size. Hill and Carrington (2006) suggest that viscosity
increases due
to the presence of very small particles, causing more
particleeparticle interactions and increasing the ow
resistance,
especially at higher shear rates, of course this is also
affected by
particle concentration and has to be considered carefully.
3.1.3. Activation energy at shear rate ow
Inuence of temperature from 25 to 45 C on viscous response
of encapsulated samples and control samples at concentration 6
g/
100 mL are shown on Table 2, where Ea represent the
activation
energy, A is a factor of Arrhenius equation and R2 is the square
of
the correlation coefcient. The viscosity of liquids
generally
decreases as temperature increases (Sengl et al., 2005).
This
relationship can be represented by the Arrhenius equation,
where
high activation energy (Ea), indicates a more rapid change
in
A
B
Fig. 1. Effect of spray-drying conditions on: A) Viscosity
curves and B) Storage (G0) and
loss (G00) modulus. (C B1, ; B2, - E1, A E2, :E3, E4) // Cross
Model. Filled
symbols are G0 , blank symbols represent G00 .
Table 2
Arrhenius equation parameters for encapsulated and control
samples.
Treatment Ea (kcal/mol) A (Pa s) 105 R2
E1 1.068 3.2 0.978
E2 1.124 1.8 0.982
E3 1.156 3.1 0.978
E4 1.130 2.1 0.980
E5 1.095 2.0 0.978
B1 1.056 3.8 0.975
B2 1.091 2.9 0.994
B3 1.083 1.1 0.997
L. Medina-Torres et al. / LWT - Food Science and Technology 50
(2013) 642e650 645
-
viscosity with temperature. Hassan and Hobani (1998) have
re-
ported that the intermolecular forces and wateresolute
(inter-
phase) interactions restrict the molecular motion and inuence
the
viscosity of a solution. Therefore, as temperature increases,
the
thermal energy of the molecules increases and the
intermolecular
distances raise as a result of thermal expansion (Koocheki,
Mortazavi, Shahidi, Razavi, & Taherian, 2009).
The Ea of encapsulated samples E1 and E3 (1400 rpm) is lower
than their corresponding samples E2 and E4 (2000 rpm) this
indicates a higher stability with temperature for samples
prepared
at low rotor speeds and is an evidence of the impact of high
shear
rates on the sample, this also indicates that at the
conditions
studied rotor speed has more inuence on sample integrity
than
the temperature. This also holds for control samples with Ea
for
sample B1 being lower than that for sample B2, while the effect
of
temperature cannot be distinguished here. Ea from control
samples
showed a similar trend to the 1.16 kcal/mol reported previously
for
O mucilage at 5 g/100 mL (Medina Torres et al., 2000).
3.2. Oscillatory shear curves on spray-drying conditions
The effect of drying conditions in storage (G0) and loss
(G00)
dynamic modulus, as a function of oscillating frequency of
samples
prepared with mucilage extract (B1, E1eE4), is presented in
Fig. 1(B). This data has been reported to be characteristic of
the
random coil conguration of polymeric networks (Medina Torres
et al., 2000). As shown on Fig. 1(B), at low inlet temperature
(Ti,
at 130 C), magnitudes G0 and G00 increase, while a decrease
is
observed with the addition of Gallic acid. However, for sample
E2
there is a slight solid-like response (G0 tending to be
frequency
independent while being lower than G00), implying a higher
phys-
ical interaction of components (mucilage extract-gallic acid)
and in
principle, a more stable matrix. The solid-like response has
been
reported elsewhere to conrm strong polymer matrix-disperse
phase interactions (Medina Torres, Calderas, Gallegos
Infante,
Gonzlez Laredo, & Rocha Guzmn, 2009). Len Martnez et al.
(2011) suggest a similar effect of spray-dried O mucilage due
to
partial hydrolysis of mucilage pectin chains.
Fig. 1(B) shows the evolution of G0 and G00 modulus showing
the
effect of spray speeds (Sa) maintaining a constant
temperature
(130 C). Its evident that the structure response modies (G0
decreases) as Sa increases. The encapsulated and dried sample
at
20,000 rpm shows a similar trend, more stable at longer times,
and
magnitude G0 is higher at lower frequency rates ( G0).
Viscoelastic behavior
of a biopolymer mixture (sodium alginate and hydroxypropyl
methyl cellulose, HPMC) used as excipient was reported with
G00
values larger than G0 (Borgogna et al., 2010) as observed in
this
study.
3.3. Analysis of simple shear and oscillatory curves at the
optimal
drying conditions
3.3.1. Analysis of simple shear curves
Simple shear ow curves [h vs _g] of double processedmucilage
samples: E5 and control (B3) have shown a non-Newtonian
shear-
thinning type (n < 1) behavior (Fig. 2(A)). Shear-thinning
behavior
is the resulting orientation effect of large polymer chains
aligned to
the ow direction caused by the shearing rate, showing less
interaction between adjacent chains and thus viscosity
decreases.
This behavior is typical of these macromolecules and has
been
previously reported (Medina Torres et al., 2000; Orozco, Daz,
&
Garca, 2007). At concentrations of 6 g/100 mL and lower
shear
rates (
-
represent macromolecular polysaccharide solutions with a
random
coil conguration similar to galactomannan and some other
gelling
polysaccharides such as dextran, l-carrageenan, and
cellulose
derivatives (Morris, Cutler, Ross-Murphy, & Rees, 1981), for
O
mucilage (Medina Torres et al., 2000), and Alyssum
homolocarpum
mucilage (Koocheki et al., 2009). Table 3 shows that viscosity
(h0) at
lower shear rates ( G0. In
this case (E5), the interaction between mucilage and gallic
acid
increases, and such change inuences the elastic modulus (G0),
this
effect is more evident at low frequencies (i.e., tendency to
solid-like
behavior). This was similar to a report for a gel system of
sodium
alginate and HPMC (Borgogna et al., 2010).
3.3.3. Analysis of shear rate and oscillatory tests curves using
the
CoxeMerz relationship
Applicability of the CoxeMerz relationship was investigated
for
encapsulated E5 and control B3 samples. Fig. 2(C) shows the
CoxeMerz rule for double processed samples: control (B3) and
encapsulate (E5), where the relationship h*h h holds for low
shear
rates (
-
phase transition. Glass transition temperature (Tg) was taken at
the
midpoint of the glass transition zone. The samples used as
control
had a Tg of 48C, this value increased upon the addition of
gallic
acid to 60 C. Len Martnez et al. (2010) reported a Tg for
Opuntia
mucilage of 45 C, which closely resembles the value estimated
in
this study. Gonzlez Campos, Prokhorov, Luna Brcenas, Fonseca
Garca, and Snchez (2009) reported a transition temperature
of
51 C for chitin and 59 C for chitosan. This value is associated
with
the extensive characteristic hydrogen bonding for
polysaccharides
and polypeptides, signicant thermal disruption of H-bonding,
and
the onset of main chain molecular motions, which are
probably
closely related (Gonzlez Campos et al., 2009). The results of
this
study also suggest that the mucilage encapsulation increases
the
transition temperature. The latter effect is associated to the
pres-
ence of encapsulated gallic acid, which somehow restricts
molec-
ular chain mobility, possibly by the creation of
encapsulated
structures where gallic acid is surrounded bymucilage
components
and thus reducing mobility while enhancing the rheological
properties and PSD. This is in agreement with Senz et al.
(2009),
who observed that mucilage gum showed afnity to encapsulate
different bioactive composites. This behavior is associated
with
stickiness, which reduces performance because material adheres
to
the drier chamber. However, the outlet temperatures from
spray
drier were observed between 77 and 86 C for the encapsulated
and
control samples, respectively, therefore the encapsulated
product
cannot have a rubbery behavior output under these
conditions.
Chiou and Langrish (2007) explained that spray drying
produces
mainly amorphous products which, when heated above Tg,
become
a gummy and sticky material. This transformation usually occurs
at
20 C above Tg. These results suggest that encapsulated
products
should be stored at room temperature and in dry conditions
to
maintain the moisture content (less than 10 g/100 g dry solid)
due
to the hydrophilic characteristic of mucilage. Water sorption
in
polysaccharides is usually a non ideal process leading to
plastici-
zation, the presence of water increases the amount of
hydrogen
bonds producing an increase in cooperative motion. The
mucilage
may be readily hydrated, forming macromolecules with rather
disordered structures (Gonzlez Campos et al., 2009). DSC
analysis
suggests that the thermal degradation starts above 140 C.
Gonzlez Campos et al. (2009) reported that the thermal
degra-
dation process of chitosan (w170 C) can occur by a pyrolysis
of
polysaccharides, which starts by a random split of the
glucosidic
bonds, followed by a further decomposition.
3.6. Scanning electron microscopy
Scanning electron microphotographs for the O (B3) and gallic
acid (E5) systems were evaluated at two water activities
(0.2 < aw < 0.4) shown in Fig. 4. The microphotographs 4a
and 4b
clearly show themucilagemicrocapsules alone, andwith the
added
gallic acid, respectively. The morphology of microcapsules
with
encapsulating agents was irregularly spherical in shape with
an
extensively dented surface. The formation of these dented
surfaces
on spray-dried particles was attributed to the shrinkage of
the
Temperature (C)20 40 60 80 100 120
Hea
t fl
ow
, (J
/g)
0.00
0.05
0.10
0.15
0.20
0.25
0.30
Fig. 3. Heat ow vs temperature of double processed samples, C
B3, 7 E5.
Fig. 4. Micrographs of control single processed sample B1 and
double processed sample B5 at 1000, aw 0.2 (A and C), hydrated aw
0.4 (B and D). Samples of treatment B1 are A
and B, to E5, C and D.
L. Medina-Torres et al. / LWT - Food Science and Technology 50
(2013) 642e650648
-
particles during the drying process. Similar morphology was
observed in microcapsules of cactus pear cultivars (Opuntia
lasia-
cantha) pigments with maltodextrin (Daz, Santos, Kerstupp,
Villagmez, & Scheivar, 2006), Amaranthus using maltodextrin
of
different dextrose equivalents (Cai & Corke, 2000), and
b-carotene,
using modied tapioca starch and maltodextrin as
encapsulating
agents (Loksuwan, 2007). Nevertheless, smooth spheres have
primarily been observed in microcapsules of black carrot
pigments
(Daucuscarota L.) with maltodextrin (Ersus & Yurdagel,
2007).
Gharsallaoui et al. (2007) mentioned that changes in
morphology
are related to inlet temperature during the drying process.
The
microphotographs of the mucilage presented a macromolecular
dispersion that became less agglomerated by the addition of
gallic
acid. The intermolecular mucilageegallic acid interactions
become
favorable and thusly, considerably reduce the size of the
aggregates.
The results conrm the encapsulation by mucilage. It is
interesting
to note here that the chemical compositions of Opuntia
mucilage
have been described by several research groups (Senz et al.,
2009).
On the other hand, in the early 2000s, some authors
presented
evidence on the neutral character of the mucilage, but more
recent
reports have shown that it has acidic residues and,
therefore,
polyelectrolyte behavior (Medina Torres et al., 2000).
3.7. Controlled release of gallic acid
The release of the microcapsules of mucilage with gallic
acid
was performed in Franz cells with a 0.22 mm membrane. The
sample E5 was double processed at 6 g/100 mL in buffer pH 5
in
order to try to simulate the conditions of the intestinal tract
(Ferk
et al., 2011; Sez et al., 2003). The results were analyzed
at
a wavelength of 273.71 nm. The controlled release is designed
with
the conditions of the small intestine as it is the place where
gallic
acid is absorbed (Sez et al., 2003). Sample follow-up was
per-
formed until no signal in the spectrum was shown. However,
after
3.3 days there was still an increase in the signal spectrum
respect to
mucilage without gallic acid. Fig. 5 shows the controlled
release of
gallic acid, which indicates that 65% is released in 2.47 days,
the
microcapsules showed high efciency (>60%) using mucilage
gum
this is attributed to microencapsulation conditions, which
showed
quasi-modal particle size and are, in principle, more stable
(Sez
et al., 2003).
New ndings suggest that mucilage may have both neutral and
acidic fractions depending on the extraction method used.
The
previously stated hypothesis, that mucilage might
encapsulate
gallic acid and that the interaction is only controlled by the
elec-
trostatic charge of the mucilage, is then supported by these
results.
Subsequently, the co-existence of two types of micro-structure
was
conrmed by SEM and controlled release of gallic acid, this
is
attributed to microencapsulation conditions (Walton &
Mumford,
1999).
4. Conclusions
This study has shown that using spray drying to process O.
cus-
indica mucilage extract produces a stable powder with small
particle size and, consequently higher viscosity, while also
exhib-
iting higher resistance to ow, mainly due to encapsulated
struc-
tures. Moreover, the viscous modulus G00 predominates over
the
elastic modulus G0 for the spray-dried samples at
concentrations
6 g/100 mL, and showed in some cases solid-like qualities,
indicating a strong biopolymeregallic acid interaction. Thus,
the
viscosity and viscoelastic properties (G0 and G00) were
signicantly
affected by high inlet air temperatures and behavior, under
steady
ow for all systems, was non-Newtonian shear thinning (n <
1).
This study showed that samples can achieve stability during
storage and subsequent usewith extract aqueous of mucilage,
dried
at 130 C and 14,000 rpm, as well as samples dried at 130 C
and
20,000 rpm. The rheological properties were affected inversely
by
the increase in inlet temperature and the atomizer speed,
and
directly by the increase of feed ow rate.
The nopal mucilage microcapsules described in this study
represent a promising food additive for incorporation into
func-
tional foods (gallic acid). The DSC analysis conrmed this
with
activation energy and glass transition temperature results.
Based
on the calorimetric and SEM data obtained, it is proposed
that
nopal mucilage serves as an effective encapsulating agent on
bioactive functional foods, providing additional structure.
Finally, the liberation proles of encapsulating principles
for
these systems are still under evaluation and it is observed that
the
cactus mucilage has a good ability to encapsulate, however
more
study and research is recommended over a longer and
continuous
time period in order to obtain more reliable and conclusive
results.
This study conditions may serve to understand properties of
encapsulated active ingredients (i.e., gallic acid) and their
stability,
as well as serve as a precedent for future investigations on
drying
yields and encapsulation efciency.
Acknowledgments
The authors would like to acknowledge the support received
by
Ivan Puente-Lee (Laboratorio de Microscopa, USAI, Facultad
de
Qumica, UNAM., Mexico., D.F.).
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L. Medina-Torres et al. / LWT - Food Science and Technology 50
(2013) 642e650650
Microencapsulation by spray drying of gallic acid with nopal
mucilage (Opuntia ficus indica)1. Introduction2. Materials and
methods2.1. Materials2.2. Aqueous dispersion previous to the
spray-drying process2.3. Spray drying2.4. Reconstituted solutions
of control and encapsulated samples2.5. Rheological
measurements2.5.1. Steady-shear viscosity measurements2.5.2.
Activation energy at shear rate flow2.5.3. Steady oscillatory flow
measurements
2.6. Particle size distribution of resuspended solutions
(PSD)2.7. Differential scanning calorimetry (DSC)2.8. Scanning
electron microscopy (SEM)2.9. Controlled release of gallic acid
from microcapsule
3. Results and discussion3.1. Effects of spray-drying conditions
on steady-shear rate flow3.1.1. Effect of inlet air
temperature3.1.2. Effect of air pressure (rotor speed)3.1.3.
Activation energy at shear rate flow
3.2. Oscillatory shear curves on spray-drying conditions3.3.
Analysis of simple shear and oscillatory curves at the optimal
drying conditions3.3.1. Analysis of simple shear curves3.3.2.
Analysis of the linear viscoelastic data3.3.3. Analysis of shear
rate and oscillatory tests curves using the CoxMerz
relationship
3.4. Particle size distribution (PSD)3.5. Differential scanning
calorimetry (DSC)3.6. Scanning electron microscopy3.7. Controlled
release of gallic acid
4. ConclusionsAcknowledgmentsReferences