Post on 16-Oct-2015
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: luismt@unam.mx (L. Medina-Torres).
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0023-6438/$ e see front matter 2012 Elsevier Ltd. All rights reserved.
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.).
References
Abu-Jdayil, B., Banat, F., Jumah, R., Al-Asheh, S., & Hammad, S. (2004). A comparativestudy of rheological characteristics of tomato paste and tomato powder solu-tions. International Journal of Food Properties, 7(3), 483e497.
Ahmed, M., Akter, M. S., Lee, J. C., & Eun, J. B. (2010). Encapsulation by spray dryingof bioactive components, physicochemical and morphological properties frompurple sweet potato. LWT e Food Science and Technology, 43, 1307e1312.
Barnes, H. A. (2000). A handbook of elementary rheology (1st ed.). Aberystwyth, UK:University of Wales, Institute of Non-Newtonian Fluid Mechanics.
Borgogna, M., Bellich, B., Zorzin, L., Lapasin, R., & Cesro, A. (2010). Food microen-capsulation of bioactive compounds: rheological and thermal characterisationof non-conventional gelling system. Food Chemistry, 122, 416e423.
Cai, Y. Z., & Corke, H. (2000). Production and properties of spray-dried Amaranthusbetacyanin pigments. Journal of Food Science, 65(6), 1248e1252.
Crdenas, A., Higuera Ciapara, I., & Goycoolea, F. M. (1997). Rheology and aggre-gation of cactus (Opuntia cus-indica) mucilage in solution. Journal of theProfessional Association for Cactus Development, 2, 152e159.
Chegini, G. R., & Ghobadian, B. (2007). Spray dryer parameters for fruit juice drying.World Journal of Agricultural Sciences, 3(2), 230e236.Fig. 5. Gallic acid release curve of double processed sample E5.
L. Medina-Torres et al. / LWT - Food Science and Technology 50 (2013) 642e650 649
Chiou, D., & Langrish, T. A. G. (2007). Development and characterisation of novelnutraceuticalswithspraydryingtechnology. Journal of FoodEngineering, 82, 84e91.
Cho, Y. S., Kim, S. K., Ahn, C. B., & Je, J. Y. (2011). Preparation, characterization, andantioxidant properties of gallic acid-grafted-chitosans. Carbohydrate Polymers,83, 1617e1622.
Cox, W. P., & Merz, E. H. (1958). Correlation of dynamic and steady ow viscosities.Journal of Polymer Science Part A: Polymer Chemistry, 28, 619e622.
Del Valle, V., Hernndez Muoz, G. A., & Galotto, M. J. (2005). Development ofa cactus-mucilage edible coating (Opuntia cus indica) and its application toextend strawberry (Fragaria ananassa) shelf-life. Food Chemistry, 91, 751e756.
Daz, F., Santos, E., Kerstupp, S., Villagmez, R., & Scheivar, L. (2006). Colourantextract from red prickly pear (Opuntia lasiacantha) for food application. Elec-tronic Journal of Environmental, Agricultural and Food Chemistry. Accessed 30.01.07.
Ersus, S., & Yurdagel, U. (2007).Microencapsulation of anthocyanin pigments of blackcarrot (Daucuscarota L.) by spray drier. Journal of Food Engineering, 80, 805e812.
Fang, Z., & Bhandari, B. (2010). Encapsulation of polyphenols-a review. Trends inFood Science & Technology, 21, 510e523.
Ferk, F., Chakraborty, A., Jger, W., Kundi, M., Bichler, J., Misk, M., et al. (2011).Potent protection of gallic acid against DNA oxidation: results of human andanimal experiments. Mutation Research, 715(1e2), 61e71.
Georgetti, S. R., Casagrande, R., Souza, C. R. F., Oliveira, W. P., & Fonseca, M. J. V.(2008). Spray drying of the soybean extract: effects on chemical properties andantioxidant activity. LWT e Food Science and Technology, 41, 1521e1527.
Gharsallaoui, A., Roudaut, G., Chambin, O., Voilley, A., & Saurel, R. (2007). Appli-cations of spray-drying in microencapsulation of food ingredients: an overview.Food Research International, 40, 1107e1121.
Gonzlez Campos, J. B., Prokhorov, E., Luna Brcenas, G., Fonseca Garca, A., &Snchez, I. C. (2009). Dielectric relaxations of chitosan: the effect of water onthe a-relaxation and the glass transition temperature. Journal of Polymer SciencePart B: Polymer Physics, 47, 2259e2271.
Gunasekaran, S., & Mehmet, A. M. (2000). Dynamic oscillatory shear testing offoods-selected applications. Trends in Food Science & Technology, 11, 115e127.
Hassan, B. H., & Hobani, A. I. (1998). Flow properties of Roselle (Hibiscus sabdariffaL.) extract. Journal of Food Engineering, 35, 459e470.
Hill, A., & Carrington, S. (2006). Understanding the links between rheology andparticle parameters. American Laboratory News.
Kha, T. C., Nguyen, M. H., & Roach, P. D. (2010). Effects of spray drying conditions onthe physicochemical and antioxidant properties of the Gac (Momordicacochinchinensis) fruit aril powder. Journal of Food Engineering, 98, 385e392.
Kirkwood, D. H., & Ward, P. J. (2008). Comment on the power law in rheologicalequations. Materials Letters, 62(24), 3981e3983.
Koocheki, A., Mortazavi, S. A., Shahidi, F., Razavi, S. M. A., & Taherian, A. R. (2009).Rheological properties of mucilage extracted from Alyssum homolocarpum seedas a new source of thickening agent. Journal of Food Engineering, 91, 490e496.
Kosaraju, S. L., Dath, L., & Lawrence, A. (2006). Preparation and characterisation of chi-tosan microspheres for antioxidant delivery. Carbohydrate Polymers, 64, 163e167.
Kosaraju, S. L., Labbett, D., Emin, M., Konczak, I., & Lundin, L. (2008). Deliveringpolyphenols for healthy ageing. Nutrition & Dietetics, 65, S48eS52.
Len Martnez, F. M., Mndez Lagunas, L. L., & Rodrguez Ramrez, J. (2010). Spraydrying of nopal mucilage (Opuntia cus-indica): effects on powder propertiesand characterization. Carbohydrate Polymers, 81, 864e870.
Len Martnez, F. M., Rodrguez Ramrez, J., Medina Torres, L., Mndez Lagunas, L. L.,& Bernad Bernad, M. J. (2011). Effects of drying conditions on the rheologicalproperties of reconstituted mucilage solutions (Opuntia cus-indica). Carbohy-drate Polymers, 84, 439e445.
Liu, Z., Zhou, J., Zeng, Y., & Ouyang, X. (2004). The enhancement and encapsulationof Agaricus bisporus avor. Journal of Food Engineering, 65, 391e396.
Loksuwan, J. (2007). Characteristics of microencapsulated betacarotene formed byspray drying with modied tapioca starch, native tapioca starch and malto-dextrin. Food Hydrocolloids, 21, 928e935.
McGarvie, D., & Parolis, H. (1981). Methylation analysis of the mucilage of Opuntiacus indica. Carbohydrate Research, 88, 305e314.
Medina Torres, L., Brito De La Fuente, E., Torrestiana Snchez, B., & Katthain, R.(2000). Rheological properties of the mucilage gum (Opuntia cus indica). FoodHydrocolloids, 14, 417e424.
Medina Torres, L., Brito De-La Fuente, E., Gmez Aldapa, C., Aragn Pia, A., & ToroVzquez, J. (2006). Structural characteristics of gels formed by mixtures ofcarrageenan and mucilage gum from Opuntia cus indica. Carbohydrate Poly-mers, 63(10), 299e309.
Medina Torres, L., Calderas, F., Gallegos Infante, J. A., Gonzlez Laredo, R. F., & RochaGuzmn, N. (2009). Stability of alcoholic emulsions containing differentcaseinates as a function of temperature and storage time. Colloids and SurfacesA: Physicochemical and Engineering Aspects, 352(1e3), 38e46.
Morris, E. R., Cutler, A. N., Ross-Murphy, S. B., & Rees, D. A. (1981). Concentrationand shear rate dependence of viscosity in random coil polysaccharide solutions.Carbohydrate Polymers, 1, 5e21.
Negi, A. S., Darokar, M. P., Chattopadhyay, S. K., Garg, A., Bhattacharya, A. K.,Srivastava, V., et al. (2005). Synthesis of a novel plant growth promoter fromgallic acid. Bioorganic & Medicinal Chemistry Letters, 15, 1243e1247.
Orozco, A. C., Daz, S. D., & Garca, S. S. (2007). Extracto de Nopal: Reologa y secadopor aspersin. In VI Congreso Iberoamericano de Ingeniera de Alimentos (CIBIA VI)Guanajuato, Mxico, del 31 de Mayo al 1 de Junio (pp. 277e283).
Pasanphan, W., & Chirachanchai, S. (2008). Conjugation of gallic acid onto chitosan:an approach for green and water-based antioxidant. Carbohydrate Polymers, 72,169e177.
Senz, C., Seplveda, E., & Matsuhiro, B. (2004). Opuntia spp mucilages: a functionalcomponent with industrial perspectives. Journal of Arid Environments, 57,275e290.
Senz, C., Tapia, S., Chvez, J., & Robert, P. (2009). Microencapsulation by spraydrying of bioactive compounds from cactus pear (Opuntia cus-indica). FoodChemistry, 114, 616e622.
Sez, V., Hernez, E., & Lpez, L. (2003). Liberacin controlada de frmacos. Apli-caciones biomdicas. Revista Iberoamericana de Polmeros, 4, 111e122.
Seid, M. J., Elham, A., Bhesh, B., & Yinghe, H. (2008). Nano-particle encapsulation ofsh oil by spray drying. Food Research International, 41, 172e183.
Sengl, M., Ertugay, M. F., & Sengl, M. (2005). Rheological, physical and chemicalcharacteristics of mulberry pekmez. Food Control, 16, 73e76.
Servais, C., Jones, R., & Roberts, I. (2002). The inuence of particle size distributionon the processing of food. Journal of Food Engineering, 51, 201e208.
St. Leger, A. S., Cochrane, A. L., & Moore, F. (1979). Factors associated with cardiacmortality in developed countries with particular reference to the consumptionof wine. The Lancet, 1, 1017e1020.
Takkouche, B., Regueira-Mndez, C., Garca-Closas, R., Figueiras, A., Gestal-Otero, J. J., & Hernn, M. A. (2002). Intake of wine, beer, and spirits and the riskof clinical common cold. American Journal of Epidemiology, 155(9), 853e858.
Walton, D. E., & Mumford, C. J. (1999). Spray dried products-characterization ofparticle morphology. Education for Chemical Engineers, 77(Pt A), 21e38.
Wang, Y., Lu, Z., Lv, F., & Bie, X. (2009). Study on microencapsulation of curcuminpigments by spray drying. European Food Research and Technology, 229(3),391e396.
Xu, C., Willfr, S., Holmlund, P., & Holmbom, B. (2009). Rheological properties ofwater-soluble spruce O-acetyl galactoglucomannan. Carbohydrate Polymers, 75,498e504.
Zakarian, A. J., & King, C. J. (1982). Volatiles loss in the zone during spray drying ofemulsions. Industrial Engineering Chemistry Process Design and Development, 21,107e113.
Zbicinski, I., Delag, A., Strumillo, C., & Adamiec, J. (2002). Advanced experimentalanalysis of drying kinetics in spray drying. Chemical Engineering Journal, 86,207e216.
Zhang, L., Mou, D., & Du, Y. (2007). Procyanidins: extraction and micro-encapsu-lation. Journal of Agricultural and Food Chemistry, 87, 2192e2197.
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