Received: 4 February 2020 Revised: 2 April 2020 Accepted: 20 April 2020

DOI: 10.1111/jfpe.13436

ORIGINAL ARTICLE

Microencapsulation of Lactobacillus plantarum by spray drying

with mixtures of Aloe vera mucilage and agave fructans as wall
materials

Luis Isaac Ceja-Medina1 | Rosa Isela Ortiz-Basurto1 | Luis Medina-Torres2 |

3 2
Fausto Calderas | Maria Josefa Bernad-Bernad |
Ruben Francisco González-Laredo4 | Juan Arturo Ragazzo-Sánchez1 |
1 5
Montserrat Calderón-Santoyo | Marisela González-ávila |
Isaac Andrade-González6 | Octavio Manero7
1
Laboratorio Integral de Investigación en Alimentos, Departamento de Estudios de Posgrado e Investigación, TecNM / Instituto Tecnológico de Tepic, Tepic, Nayarit,
Mexico
2
Facultad de Química, Universidad Nacional Autónoma de México, Mexico city, Mexico
3
Laboratorio de Reología y Fenómenos de Transporte L7-PP Unidad Multidisciplinaria de Investigación Experimental (UMIEZ), Facultad de Estudios Superiores-
Zaragoza, Universidad Nacional Autónoma de México, Iztapalapa, Ciudad de México, Mexico
4
Departamento de Ingeniería Química y Bioquímica, TecNM / Instituto Tecnológico de Durango, Durango, Mexico
5
Centro de Investigación y Asistencia en Tecnología y Diseño del Estado de Jalisco, Guadalajara, Jalisco, Mexico
6
Departamento de Estudios de Posgrado e Investigación, TecNM / Instituto Tecnológico de Tlajomulco, Tlajomulco de Zúñiga, Jalisco, Mexico
7
Instituto de Investigaciones en Materiales, Universidad Nacional Autónoma de México, Mexico city, Mexico

Correspondence
R. I. Ortiz-Basurto, TecNM/Instituto Abstract
Tecnológico de Tepic, Laboratorio Integral de In this work, a spray-drying process is used to encapsulate a probiotic strain of Lacto-
Investigación en 12 Alimentos.
Av. Tecnológico # 2595, Col. Lagos del bacillus plantarum with mixtures of Aloe vera mucilage (AVM) (Aloe barbadensis Miller)
Country, Tepic, Nayarit C.P. 63175, México. and agave fructans of high degree of polymerization (AFHDP). Physicochemical prop-
Email: riobasurt@ittepic.edu.mx
erties of the powders reveal moisture contents lower than 10% and water activity
L. Medina-Torres, Facultad de Química, between 0.195 and 0.3, suggesting stability during storage. A non-Newtonian shear-
Universidad Nacional Autónoma de México,
México, 04510, México. thinning behavior arises in the reconstituted powders under steady shear flow and
Email: luismt@unam.mx viscosity is shown to depend on the concentration, pH, and temperature. A predomi-
nant viscous behavior is exhibited in the viscoelastic properties under small amplitude
oscillatory flow with equal values of the elastic and viscous moduli at high frequen-
cies (G´ = G´´), suggesting a random coil conformation. Scanning electron microscope
observations reveal a spherical microcapsule morphology possessing homogeneous
surfaces with modal particle-size distribution (D [4,3] =21.3 μm). The addition of ara-
bic gum to the AVM-AFHDP mixtures induces a shift in the glass transition tempera-
ture (Tg) to 150
C. Preserved stability of the AVM-AFHDP functional groups with the
probiotic after spray drying reveals the effective encapsulation of the microorganism,
as corroborated by transmission electron microscopy and Fourier-transform infrared.
Enhanced microorganism survival rate of 70% in the mixture is recorded, representing
an alternative for probiotic encapsulation.

J Food Process Eng. 2020;e13436. wileyonlinelibrary.com/journal/jfpe © 2020 Wiley Periodicals LLC. 1 of 12

https://doi.org/10.1111/jfpe.13436
2 of 12 CEJA-MEDINA ET AL.

PRACTICAL APPLICATIONS: Nowadays, the use of mixtures of prebiotic biopoly-

mers as encapsulating wall materials is highly appreciated by the food and pharma-
ceutical industry. This research demonstrated that mixtures of Aloe vera mucilage and
agave fructans are suitable for the microencapsulation of L. plantarum through studies
on their rheological, morphological, and calorimetric properties. High survival rates
and stable powders are obtained in samples subjected to spray drying. Results of this
investigation may help to develop new delivery drug systems, which are able to pro-
tect bioactive compounds or probiotic cells through the gastrointestinal tract. Increas-
ing health benefits, including probiotic and symbiotic effects, are expected with the
intake of dietary fibers.

1 | I N T RO DU CT I O N glass transition temperature (Tg), improving viscoelasticity and poly-

electrolytic properties, as well their bioactive functions (e.g., prebiotic,
The encapsulation of probiotics is a process intended to protect these anti-inflammatory, symbiotic). There are different techniques to
microorganisms during the passage through the gastrointestinal tract, encapsulate products like spray-drying, presenting advantages such as
thus ensuring that the metabolically active probiotics reach the colon low cost, continuous production, availability of equipment and easy
of the host. Therapeutic benefits with a minimum amount of 106 CFU scaling-up (Drusch, 2007; Paradkar, Ambike, Jadhav, &
are expected. In addition, encapsulated probiotics have a high shelf- Mahadik, 2004). Microcapsule stability and spray-drying
storage life since the wall materials provide a physical barrier to resist (SD) efficiency depend entirely on the wall material (Zbicinski,
adverse environmental conditions (Alehosseini et al., 2019). Lactic acid Strumillo, & Delag, 2002). The conformational structure of the wall
bacteria are considered safe probiotics in the food industry (Coghetto, material ensures that the nucleus of an encapsulated matrix is pre-
Flores, Brinques, & Záchia Ayub, 2016). Furthermore, Lactobacillus pla- served at the inlet temperature during short residence times (less than
ntarum strains present remarkable capabilities for fermentation and 3 s) under spray drying (Medina-Torres et al., 2016b; Santiago-Adame
probiotic effects in the host, ranging from production of anti- et al., 2015; Zhu, Luan, Zhang, Zhang, & Hao, 2016).
inflammatory metabolites to inhibition of pathogenic bacteria In this work and for the first time, mixtures of Aloe vera muci-
(Rajam & Anandharamakrishnan, 2015a). Biopolymers are innocuous lage (hetero-polysaccharides) and agave fructans of high degree of
materials used for the microencapsulation of products of interest in polymerization, were spray-dried to successfully encapsulate pro-
the food industry, ranging from bioactive extracts to probiotic micro- biotics. Properties were assessed by rheometry, microscopy,
organisms (Coghetto et al., 2016; Dias, Ferreira, & Barreiro, 2015). particle-size distribution (PSD), differential scanning calorimetry
Aloe vera is a source of hydrocolloids with promising applications, and infrared spectroscopy, with the intention to evaluate the effec-
possessing high molecular-weight hetero-polysaccharides, which can tiveness of the material to encapsulate probiotics
withstand high temperature processing conditions (as the spray-drying (e.g., L. plantarum). The use of novel mixtures of biopolymers to
process), maintaining their internal structure and functional properties encapsulate bioactive materials is complemented with the analysis
(Cervantes-Martínez et al., 2014; Medina-Torres et al., 2019b; of rheological and microscopic properties. Various techniques to
Minjares-Fuentes et al., 2017a). Enriched agave fructans with high select suitable encapsulating systems for applications in the food
degree of polymerization stands as a convenient wall material for the industry are presented, thus adding new options to aloe and agave
encapsulation of bioactive compounds due to its lyo-protectant and cultivators for diversifying markets and crop uses.
proven prebiotic properties, including good physico-mechanical
advantages (García-Gamboa, Gradilla-Hernández, Ortiz-Basurto, Gar-
cía-Reyes, & González-Avila, 2020; Ortiz-Basurto, Rubio-Ibarra, 2 | M A T E R I A L S A N D M ET H O D S
Ragazzo-Sánchez, Beristain, & Jiménez-Fernández, 2017; Ramos-
Hernández et al., 2018; Rodríguez Furlán, Aldrete Herrera, Pérez 2.1 | Materials
Padilla, Ortiz Basurto, & Campderrós, 2014). Aloe vera mucilage (AVM)
and agave fructans mixtures are new wall materials used to encapsu- Aloe vera leaves were provided by plants grown under controlled irri-
late probiotics. In this study, it is shown that Aloe vera alone does not gation in a greenhouse. Leaves selected were 70–90 cm long,
possess sufficient advantages to reach gastric conditions, and there- 9–10 cm wide, and 6–8 cm thick, spotless, with bright green color,
fore agave fructans with high degree of polymerization are considered growing in the rims of plants 12–24 months old. A gel was extracted
here as reinforcing wall material to protect bioactive compounds at after separation of the outer layer of the leaves and cooled to 4
C to
prolonged liberation times under gastric conditions. The mixture of maintain a semi-solid condition when processed in a commercial food
these two wall materials provides enhanced efficiency, increasing extractor (Nutribullet Veggie bullet, 102,281). Mucilage was filtered in
CEJA-MEDINA ET AL. 3 of 12

300, 150, and 75 μm stainless steel sieves (U.S.A. Standard Test Sieve) Denmark). The encapsulation was carried out using a 5:1 w/w ratio
to separate the suspended solids. The clarified mucilage was stored in related to weight of wall material (AVM-AFHDP) and weight of


sterile bottles at low temperature (4 C). Characterization of pH, degrees L. plantarum biomass (De Prisco, Maresca, Ongeng, &
Brix, solid content, and moisture was performed with the methodology Mauriello, 2015). The mixture components were added one by one
described by Medina-Torres et al. (2019b). The powdered native agave and mixed at 500 rpm using a Braun mixer (Braun MQ725) during
fructans (Fiber Prime) was provided by Best Ground International S.A. de 10 min at 25
C. Mixtures were dried in an LPG5 rotary disc spray


C.V. and filtered at 20 Brix concentration in a tangential ultrafiltration dryer (CIMA Industries, China) at conditions reported by Medina-
system fitted with a 5 kDa MWCO membrane (Pellicon 2 Millipore, Mas- Torres et al. (2019) (i.e., flow rate, 0.8 L/hr; inlet air temperature,
sachusetts). A double filtration of the retention liquid gave 18
Brix con- 150
C; and atomization speed of 27,500 rpm). The outlet tempera-
centration. The fraction enriched with fructans of high degree of ture was 78–90
C and similar to studies (Medina-Torres et al.,
polymerization (AFHDP) was stabilized in a LPG5 rotary disc spray dryer 2013; 2016; 2019). A digital infrared thermometer Etekcity 1022d
(CIMA Industries, China) at pre-established conditions (inlet/outlet tem- (CA. U.S.A.) measured the powder temperature in the dryer collec-
perature, 110/90
C; spray rate, 27,500 rpm, as function of pneumatic tor container and the powders were stored in vacuum-sealed metal
pressure; feed rate, 1.5 L/hr) as previously reported (Medina-Torres bags to store them at room temperature in a desiccator. The per-
et al. 2019b; Ortiz-Basurto et al., 2017). The probiotic microorganism, a formance of the SD process was calculated according to
lyophilized L. plantarum 115 strain, was provided by CIATEJ (Jalisco, Equation (1):
México). Stored at −20
C, the probiotic strain was slowly tempered up
to room temperature and then spread at 1% w/v in 50 ml flask with Total dry solids in fed solution
%Spray Drying Yield ðSDYÞ = × 100
MRS broth (Sigma-Aldrich) incubated for 18 hr at 37
C under semi Dried powder weight after spray drying

anaerobic conditions (the flask cap was sealed). In a second spread, 2 L ð1Þ

of MRS broth were inoculated using 10 ml of the first spread and incu-
bated at same conditions for 24 hr (no aeration feed was applied into
the fermenter). All materials were sterilized in an autoclave at 121
C, The microparticles were suspended in a 0.84% w/v NaCl physio-
1.5 bar for 15 min. Cells were collected in an early stationary phase, logical solution. The release was performed by two steps, first by
followed by centrifugation at 10,000 rpm for 10 min at 4
C. After mechanical agitation at 50 rpm for 5 min and 25
C; immediately after,
removing the supernatant, cells were washed twice with a sterile 1% this dilution was homogenized at 6,000 rpm for 3 min as second step.
(w/v) sodium chloride solution. The count of microorganism was then performed by plate count on
MRS agar (incubated at semi anaerobic conditions) as described in
section 2.1 for both steps. The L. plantarum survival was calculated
2.2 | Preparation of mixtures and encapsulation of according to Equation (2) (Sánchez, Ruiz, Lasserrot, Hormigo, &
L. plantarum using spray drying process Morales, 2017):

 
The mixture contents and the experimental design are described in N
%Survival of microrganism = × 100 ð2Þ
N0
Table 1. Arabic gum, guar gum, and xantan gum are food grade and
were purchased in a local food additives store; whey protein con-
centrate (Lacprodan SP-8011) with an 80% w/w protein concen- where N is the final count of L. plantarum and N0 is the initial count of
tration was purchased from Arla Foods Ingredients (Sønderhøj, L. plantarum both in CFU/g.

TABLE 1 Physicochemical properties and powder yielda

Code AVM (w/w) AFHDP(w/w) pH M (d.b) (g/100 g) aw Y(%)

M1 80 20 4.43 ± 0.07ª 7.95 ± 1.63ª 0.195ª 92.5 ± 0.23ª
M2 60 40 4.52 ± 0.04b 9.5 ± 2.01b 0.225b 85.8 ± 0.37b
M3 50 50 4.6 ± 0.09b 10.7 ± 1.82b 0.254b 80.5 ± 0.74b
c c
M4 M1 + 10% AG 4.45 ± 0.04ª 7.38 ± 0.94 0.3009 91.9 ± 0.59a
M5 M1 + 5% GG 4.44 ± 0.06ª 7.9 ± 1.06ª 0.254b 79.5 ± 0.96b
b
M6 M1 + 1% XG 4.38 ± 0.07ª 7.58 ± 1.18ª 0.283 72.2 ± 0.11b
M7 M1 + 10% WPC 4.44 ± 0.04ª 7.34 ± 0.28ª 0.225b 94.8 ± 0.73a

Abbreviations: AVM, Aloe vera mucilage; AFHDP, agave fructans high degree of polymerization; M: moisture content; aw,water activity; Y, yield; AG, arabic
gum; GG, guar gum; XG, xantan gum; WPC, whey protein concentrate.
a
Values are means (n = 3); means in the same column not sharing a common superscript letter are significantly different (p < 0.05 ).
4 of 12 CEJA-MEDINA ET AL.

2.3 | Physicochemical properties of the spray dried 2.7 | Differential scanning calorimetry
powders
Differential scanning calorimetry DSC 250TA Instruments (New Cas-
2.3.1 | Moisture content (%, M) and water activity tle, DE, USA) measured the glass transition temperature (Tg) of the
(aw) of the powders capsules. Calibration employed an Indium standard (melting tempera-
ture: 156.6
C). A sample (2.5mg) of the powders obtained in the spray
Determination of the moisture content of microcapsules used the drying process was placed in an air-tight sealed aluminum capsule
AOAC 2011 gravimetric method, and reported as dry matter percent- with an orifice. Thermal events were recorded in a temperature range
age. All measurements were performed in triplicate and reported as from 0 to 200
C with a 10
C/min ramp under a nitrogen atmosphere.
percentage of dry matter (d.b.). Water activity (aw) was measured in
an Aqualab Series 3 device (Meter Group, Inc., Pullman, Washington).
2.8 | Fourier-transform infrared spectroscopy

2.4 | Rheological properties of the reconstituted The Fourier-transform infrared (FTIR) spectrum from the powder sam-
powders ples obtained by a FTIR Tensor 27 device (Bruker CO. Massachusetts)
covers the frequency range from 400 to 4,000 cm−1 with resolution
Powders were re-suspended in Mili-Q water with constant stirring using of 1 cm−1. Approximately, 2 mg of sample mixed with 200 mg of
a magnetic hot plate (CLS6795420 KIT Sigma, 5–550
C) at 250 rpm for potassium bromide (KBr) were compressed into pellets for


30 min at 25 C. Rheometric measurements at various concentrations, measurements.
temperatures and pH levels were performed in a controlled-stress hybrid
rheometer DHR-1 (TA Instruments) fitted with a Peltier system. The
geometry used includes a concentric cylinder fixture (21.96 and 2.9 | Statistical analysis
20.38 mm of outer and inner cylinder diameters, respectively; 59.50 mm
height, and 500 μm gap). Viscosity measurements under steady-state The single-factorial experimental design is described in Table 1, where
simple shear flow covered a range from 1 to 300 s−1. Viscoelastic prop- various ratios for each wall vector were considered, following the
erties (i.e., storage and loss moduli), under small amplitude linear oscilla- ANOVA Tukey test (α =0.05), using Statistica 7.0 (StatSoft) and the
tory flow (i.e., γ < 5%), cover the frequency range from 0.1 to 200 rad/s. Fisher's LSD test to identify homogeneous groups and the significant
differences among the mixtures.

2.5 | Morphology of the spray-dried powders

3 | RESULTS AND DISCUSSION
2.5.1 | Scanning electron microscopy
3.1 | Physicochemical properties of powders after
Scanning electron microscopy (SEM) JSM6300 (JEOLUSA, Inc., Pea- the spray-drying process
body, Massachusetts) revealed the morphology at 1000x magnifica-
tion of the particle surface, following the method reported by The physicochemical properties of powders after the spray-drying
Medina-Torres et al. (2016). process (Table 1) with L. plantarum at a 5:1 ratio (wall material-to-core
material ratio), show that the outlet temperature in the dryer and tem-
perature of the powders were the same for all mixtures (M1-M7)
2.5.2 | Transmission electron microscopy 85 ± 2
C and 55 ± 2.2
C, respectively, at the SD operating conditions
(Medina-Torres et al., 2019b). The surface temperature of the micro-
Transmission electron microscopy (TEM) (JEM 200; JEOL USA, Inc.) capsules is important because it is widely reported that the tempera-
revealed the presence of L. plantarum inside the microcapsules at a ture of the nucleus will be inferior after spray drying process. Similar
25,000x magnification. A drop placed on copper grid was covered by results were obtained by Zhu et al. (2016) through analyses of the
a Lacey carbon film. Once the drop dried, diagonal cuts performed by thermal resistance of L. plantarum BM-1, reporting that the cell reduc-
an ultra-microtome provided samples for microscopy. tion is less than 0.08 log CFU/ml after 1 min at 60
C, and the final
count after 10 min period is higher than 6 log CFU/ml.
A significant pH difference (p < 0.05) observed in mixtures M2
2.6 | Particle-size distribution and M3 is due to the increase in the AFHDP concentration at pH of
4.35–5.5, as related to the nonreducing carbohydrate nature of agave
PSD of the capsules was determined in a Mastersizer 3,000 analyzer fructans (Aldrete-Herrera et al., 2019; López, Mancilla-Margalli, &
(Malvern Instruments, UK) following the method reported by Medina- Mendoza-Diaz, 2003). This is likely a result of interactions of hydroxyl
Torres, Núñez-Ramírez, Calderas, Bernad-Bernad, et al. (2019). groups of the fructans through hydrogen bonds with the partially
CEJA-MEDINA ET AL. 5 of 12

acetylated groups of the mannose units in the acemannan polysaccha- temperatures and concluded that low drying yields (≤ 8% w/w) are
ride, which is present in large amounts in AVM (Rodríguez-González obtained in treatments with longer residence times caused by a slow
et al., 2011). As reported by Medina-Torres, Calderas, et al. (2016), feed flow (1.5 L/hr) and high temperature gradients (150
C inlet,
the pH change in treatments M1-M7 is due to the carboxyl group ion- 67
C outlet). Moisture values lower than 10% and aw equal to or less
ization of the acemannan molecule, causing a saturation effect, a than 0.3 ensure the storage stability of the microcapsules, as observed
Newtonian plateau of the steady shear viscosity in the alkaline region, in all treatments, thus preventing microbial growth (Rajam &
and a pronounced increase of the viscosity between pH of 4 and Anandharamakrishnan, 2015a). Additionally, Quek, Chok, and
6. This behavior confirms the polyelectrolyte nature of the AVM and Swedlund (2007) reported that powders and foods with low aw values
AFHDP molecules. In the drying process yield, two groups with signif- (0.2–0.4) are considered stable to lipid oxidation, microbial growth
icant differences appear (p < 0.05 ), as observed in treatments M1, and hydrolytic and enzymatic reactions.
M4, and M7, with yields higher than 9% w/w. The remaining treat-
ments M2, M3, M5, and M6 with yields lower than 8% w/w have in
common a lower amount of total solids due to the concentration 3.2 | Rheological behavior of the reconstituted
effect of AVM, guar gum and xanthan gum. It is worth mentioning powder
that all mixtures were dried at the same operating conditions, and
therefore, the yield differences can be attributed to the stickiness in 3.2.1 | Simple shear flow: Effect of concentration,
the dryer chamber, the deposition in the collecting cone, and to the temperature, pH, and different additives
escape of fine particles or to the relative humidity variations during
the spray-drying process. The powder yield is affected by the mois- Simple shear flow tests results of the reconstituted powders are
ture content, since it is related to the total solid content present in shown in Figure 1a. At low shear rates, we observed a Newtonian
the solution, the amount of powder obtained and the water fraction. behavior (constant viscosity plateau). However, at high shear rate
Cervantes-Martínez et al. (2014) and Medina-Torres, Calderas, (>10 s−1) viscosity decreases with respect to shear rate (shear thinning
et al. (2016) studied the spray drying of AVM at different behavior). In fact, mixture M1 exhibits higher viscosity, indicative of

F I G U R E 1 Rheological behavior (steady shear viscosity) of reconstituted spray dried powders. (a) Concentration effect on AVM-AFHDP
formulations, filled symbols 0.06 g/ml, empty symbols 0.03 g/ml: M1 80–20% (■, □), M2 60–40% (▲, 4), M3 50% - 50% (◆, ◇). (b) Effect of
temperature on viscosity of M1: 10
C (●), 25
C (■), 37
C (▲) and 45
C (◆). (c) Effect of pH on viscosity of M1: pH 6 (□), pH 4.43 (
), pH 3 (◇),
pH 2 (4). AVM, Aloe vera mucilage; AFHDP, agave fructans high degree of polymerization
6 of 12 CEJA-MEDINA ET AL.

more complex structural arrangement attributed to the AVM content the elastic modulus (G') dominates. This behavior agrees with previous
(Medina-Torres, Calderas, et al., 2016), hence the selection to conduct reports (Cervantes-Martínez et al., 2014; Medina-Torres, Calderas,
the optimization of mixtures with food additives as a base mixture. et al., 2016) and suggests a disordered molecular arrangement or ran-
This high flow stability reflects optimum encapsulation abilities. The dom coil conformation of the polymer chains, thus producing weak
shear thinning behavior reflects the breakdown of the fluid internal gels with potential ability to encapsulate active materials
structure as molecular interactions weaken and particles orient along (e.g., probiotics).
the flow direction (Cervantes-Martínez et al., 2014). This behavior has The Cox–Merz rule holds (see Figure 2b) at low frequencies or
been previously reported in the literature for fresh and reconstituted low shear rate as the complex viscosity and the shear viscosity coin-
mucilage of Opuntia ficus (Ofi) by León-Martínez, Rodríguez-Ramírez, cide. This indicates a region where the structure is preserved with no
Medina-Torres, Méndez Lagunas, and Bernad-Bernad (2011) and flow alignment, such as the observed in mechanically stable samples.
Medina-Torres, Brito-De La Fuente, Torrestiana-Sanchez, and Thus M1 (AVM-AFHDP) has high stability, exhibiting a Newtonian
Katthain (2000). Additionally, temperature affects mixture M1 (see character at low shear and a shear thinning effect at high shear rate
Figure 1b), but the viscosity curves have the same shape at various where the Cox–Merz rule no longer holds, mainly due to flow align-
temperatures, suggesting structure stability. The flow activation ment and disruption of the fluid structure by shear forces.
energy is calculated (Ea = 2.121 Kcal/mol) according to the Arrhenius
equation. This value is comparatively lower than that of previous
reports in the literature (Medina-Torres et al., 2000; Medina-Torres, 3.2.3 | Effect of the addition of food additives to
Brito-De La Fuente, Gómez-Aldapa, Aragon-Piña, & Toro-Vazquez,- the AVM-AFHDP mixture
2006; Medina-Torres, Calderas, et al., 2016). Finally, the pH effect in
the range of 2–6 is depicted in Figure 1c, where the viscosity Figure 3 shows the flow curves of sample M1 (AVM-AFHDP) when
increases in the alkaline range due to macromolecular expansion. This adding a biopolymer; this causes an improvement in the mechanical
expansion is due to the ionization of the mucilage carboxyl groups as stability to flow and its encapsulation efficiency. The interaction of
reported in the literature (Medina-Torres, Calderas, et al., 2016), pro- M1 with other gums modifies the flow curve shape, causing a viscos-
moting the interaction with fructans at pH higher than 4.0 (isoelectric ity increase. In the case of M4 (M1 + arabic gum), the Newtonian vis-
point). cosity plateau increases up to 30 1/s, indicating a complex structural
arrangement and thus increased resistance to flow, larger than M1
(16.87 1/s). In the case of M5 and M6, the addition of guar and
3.2.2 | Small amplitude oscillatory shear test xanthan gum increased the viscosity (e.g., η > 8 Pa * s). However, the
change from Newtonian to shear-thinning behavior occurs at lower
The linear viscoelastic data (see Figure 2a) of the reconstituted pow- shear rate (M5 = 2.68 1/s, M6 = 1.871/s), indicating weak interactions
ders (6 g/100 ml) reveal a predominant viscous behavior (empty sym- of the chains in the mixture (León-Martínez et al., 2011; Medina-
bols) at low frequencies. As frequency increases, a crossover point is Torres, Santiago-Adame, et al., 2016). These results allowed selecting
apparent (e.g., G" = G') in all samples. Above the crossover frequency, mixtures M4, M5, and M7 as wall materials for the trails of

F I G U R E 2 (a) Frequency dependence of storage modulus G' (filled symbols) and loss modulus G" (empty symbols) and (b) Cox–Merz rule
(filled symbols η, empty symbols η*) applied to AVM-AFHDP formulations reconstituted at 0.06 g/ml. Key: M1 80–20% (●,
), M2 60–40% (▲,
4), M3 50–50% (■, □). AVM, Aloe vera mucilage; AFHDP, agave fructans high degree of polymerization
CEJA-MEDINA ET AL. 7 of 12

increase in survival of L. plantarum. Reported results by Rajam and

Anandharamakrishnan (2015b) reveal reductions of 3–3.5 log with
73% survival rate, using fructo-oligosaccharides and whey protein iso-
lates as additive agents with calcium alginate as the main encapsula-
tion material. The significant difference (p <0.05 ) between the
mechanical stirring and homogenization reveals that the micro parti-
cles do not release the total amount of L. plantarum until a strong
force is applied, and this is an important result that may lead to an
increased controlled release during industrial or food applications.

3.4 | Morphology studies using SEM and TEM on

the spray-dried powders

Figure 4a–d depicts the morphological features using SEM with mix-
F I G U R E 3 Effect of food additives: arabic gum (●), guar gum(▲),
xanthan gum (+) and whey protein concentrate (◆) on M1 (■) over tures M1 (AVM-AFHDP) and M4 (AVM-AFHDP-GA). These samples
flow curves on steady shear viscosity represent the lowest and highest survival rates in the encapsulation
process of L. plantarum, respectively, as well as higher yields after the
spray-drying process. The micrographs show spherical microcapsules
encapsulation of L. plantarum. Other works, using carbohydrates as with sizes between 15 and 25 μm with smooth and uniform surfaces;
encapsulating agents, have reported similar results (Medina-Torres similar results were reported by Dolly, Anisha Parvin, Joseph, and
et al., 2013; Medina-Torres, Núñez-Ramírez, Calderas, Bernad-Bernad, Anandharamakrishnan (2011) during probiotic drying with oligo-
et al., 2019). fructans. The capsule shape is a function of the feed flow, the water
evaporation rate, the inlet and outlet air temperatures of the drying
process and the atomization speed (Medina-Torres, Núñez-Ramírez,
3.3 | Survival of L. plantarum after the spray-drying Calderas, Bernad-Bernad, et al., 2019), thus, particles with spherical
process shape reflect adequate conditions of the spray-drying process. Stabil-
ity of the capsules is closely related to the increase in the glass transi-
M1, M4, M5, and M7 mixtures are selected to study the survival rate tion temperature (as seen in mixtures M1 and M4) and to the absence
of L. plantarum related to the spray-drying conditions, exhibiting of microcapsules aggregation (obtained with and without probiotics)
mechanical stability under the rheological tests. Results are shown in due to particle–particle electrostatic interactions and changes in the
Table 2. Each treatment was inoculated with 5.91 log CFU/g of lacto- biopolymer condition, as reported elsewhere (Rajam, Karthik,
bacillus. Mixtures with the best survival rates were M4 and M7, Parthasarathi, Joseph, & Anandharamakrishnan, 2012). Similar mor-
corresponding to samples with added arabic gum (AG) and those with phologies were observed in microcapsules of cactus pear crops (Opun-
whey protein concentrate (WPC), respectively. Results reveal a sur- tia lasiacantha), in pigments encapsulated with maltodextrin (Díaz-
vival rate up to 70% of the initial concentration of L. plantarum and Sánchez, Santos-López, Kerstupp, Ibarra, & Scheinvar, 2006), in Opun-
they are significantly different (p <0.05 ). This could be associated tia ficus indica and Aloe vera mucilages (Medina-Torres et al., 2013;
with the high degree of structural arrangement in these mixtures of Medina-Torres, Calderas, et al., 2016), in maltodextrin encapsulated
biopolymers, which was evidenced on the studies of rheological amaranthus and gallic acid (Cai & Corke, 2000), in gallic acid in malto-
behavior, where the Newtonian plateau extends, coinciding with the dextrin (Medina-Torres, Calderas, et al., 2016), in β-carotene

TABLE 2 Survival percentage of L.

Released microorganisms (log CFU/g)
plantarum in function of wall material
formulationa Formulation Mechanical agitation Homogenization %S
aA aB
M1 (AVM-AFHDP) 2.67 ± 0.1 4.97 ± 0.44 33.96 ± 1.7a
M4 (AVM-AFHDP + AG) 3.43 ± 0.47bA 5.75 ± 0.18bB 67.92 ± 0.62b
abA bB
M5 (AVM-AFHDP + GG) 3.11 ± 0.26 5.4 ± 0.36 30.32 ± 0.43c
M7 (AVM-AFHDP + WPC) 1.59 ± 0.28cA 5.77 ± 0.09bB 71.03 ± 1.5b

Abbreviations: AVM, Aloe vera mucilage; AFHDP, agave fructans high degree of polymerization; AG, arabic gum; GG, guar gum; M: moisture content; XG,
xantan gum; WPC, whey protein concentrate.
a
Values are means (n = 3); means in the same column not sharing a common superscript lowercase letter
are significantly Different (p <0.05 ). Means between columns of encapsulated and release values not sharing a common superscript uppercase letter are
significantly different (p < 0.05).
8 of 12 CEJA-MEDINA ET AL.

F I G U R E 4 Morphology of powder
microcapsules. SEM images of
formulations: (a) M1 AVM-AFHDP. (b) M1
+ Lactobacillus plantarum. (c) M4: AVM-
AFHDP-AG and (d) M4 + L. plantarum.
TEM images of formulations where
L. plantarum was microencapsulated:
(e) M1; AVM-AFHDP. (f) M4; AVM-
AFHDP-AG. (g) M5; AVM-AFHDP-GG and
(h) M7; AVM-AFHDP-WPC, all TEM
images have a magnification of 2,500x.
AVM, Aloe vera mucilage; AFHDP, agave
fructans high degree of polymerization;
TEM, transmission electron microscopy

encapsulated with maltodextrin and modified tapioca starch reducing the air permeability that provides an adequate protection to
(Loksuwan, 2007), and in juices encapsulated in mixtures of native microorganisms.
agave fructans with maltodextrin (Jiménez-Sánchez et al., 2017). In In Figure 4d–h, the TEM micrographs of the microcapsules
addition, the micrographs reveal smooth surfaces with no fractures in obtained from the inoculated samples M1, M4, M5, and M7, respec-
the microcapsules containing L. plantarum (Figure 4b,d), thus con- tively, exhibit the protected L. plantarum inside the microcapsules
firming stability and adequate molecular interactions among the bio- (Figure 4g); it is possible to observe an internal amorphous wall with
polymers used in the mixtures. These interactions allow withstand the no cracks, together with encapsulated probiotics adhered to the inter-
expansion forces and swelling caused during the spray-drying process, nal wall (De Prisco et al., 2015). This is a new and interesting result,
CEJA-MEDINA ET AL. 9 of 12

since no reports exist on this type of encapsulation vectors in the lit- worth mentioning that Cervantes-Martínez et al. (2014) reported a Tg
erature, disclosing potential applications in the food industry. Overall, of 65
C in spray dried AVM with 12% humidity, which agrees with
these results confirm the encapsulation of probiotics in the mucilage- typical values of amorphous polymers such as the AVM. Here, the
fructans mixtures with no visible capsule surface damage. increase in Tg is due to an increase in chain rigidity caused by the addi-
tion of AFHDP, which has a Tg of 131
C (Espinosa-Andrews & Urias-
Silvas, 2012), and arabic gum with a Tg of 154
C (Michel-Barba &
3.5 | Particle-size distribution Rodriguez-Rodriguez, 2012) used in M4. These results ensure that
during the drying process the samples are stable and physically suit-
Particle size and PSD are important physical properties to assess the able to encapsulate probiotics.
suitability of the material to food formulations and the cohesiveness
and fluidity at storage conditions (Rajam & Anandharamakrishnan,
2015a, 2015b). Figure 5 depicts a predominant modal distribution, 3.7 | Fourier Infrared spectrophotometry
mechanically stable to flow, with a D [4,3] = 21.9 μm. Low polydisper-
sity with fine particles were produced in the spray-drying process, Spectra of the functional groups are depicted in Figure 7. Vibration of
decreasing particle–particle interactions and hence the viscosity. key bonds in functional groups of biopolymer are shown
Cervantes-Martínez et al. (2014) reported particle sizes smaller than corresponding to OH stretching (3,420 cm−1), CH stretching
15 μm with multimodal distributions when spray drying Aloe vera (in bands at 2923 cm−1), C O stretching of acetyl carbonyls
mucilage. The presence of a nonmodal PSD usually facilitates particle– (1760–1,740 cm−1), C O (1650–1,578 cm−1), COO-asymmetric
−1
particle interactions, while the presence of very small particles stretching (1,598 cm ), CH3 and COO-symmetric stretching
(<10 μm) increases the surface area and hence the viscosity. PSD is a (1,428 cm−1), C O C stretching of acetyl groups (1,248 cm−1),
strong function of the drying temperature (Chávez-Rodríguez C O C ether in sugars (1091–1,030 cm−1) and bands for glucans
et al., 2014; Farías-Cervantes et al., 2017), which explains the modal (1,031 cm−1). The peak intensity and width at 3420 cm−1 in samples
distribution of the mixtures. with L. plantarum indicates high water content due to the microorgan-
isms. These bands are present in the spray-dried samples, with
reduced magnitude, revealing a good encapsulation. According to sev-
3.6 | Differential scanning calorimetry eral studies, the acetyl groups of acemannans (in the AVM case) are
the main cause of the biopolymer interactions with other molecules,
In Figure 6, thermograms of samples M1 and M4 are shown, where facilitating the transport of bioactive compounds through the intesti-
survival of L. plantarum and high yield in the drying process are nal epithelium, thereby increasing their absorption (Minjares-Fuentes
observed confirming the observations by SEM. In the thermograms, a et al., 2016). The identification of strong bands at 1,078–1,036 cm−1


first inflection point is observed around 100 C corresponding to evidences the presence of polysaccharide sugars such as mannose
humidity evaporation. A second inflection point close to 140
C in the and glucose in AVM and sucrose in the AFHDP sample. Similarly,
capsules containing L. plantarum (M1 + LP and M4 + LP) is associated bands at 1,740 cm−1, 1,598 cm−1, and 1,248 cm−1 are related to the
with the cell wall rupture. This confirms the encapsulation of the pro- stretching of the acetyl group of the bioactive acemannan
biotic, as this inflection point is absent in the mixtures without micro-
organisms. A third thermal transition (Tg) is observed at 150
C. It is

F I G U R E 6 Differential scanning calorimetry thermogram of

powder microcapsules: M1: AVM-AFHDP, M4: AVM-AFHDP-AG. LP:
F I G U R E 5 Particle-size distribution of powder microcapsules. Lactobacillus plantarum. AVM, Aloe vera mucilage; AFHDP, agave
Key: LP: Lactobacillus plantarum fructans high degree of polymerization
10 of 12 CEJA-MEDINA ET AL.

F I G U R E 7 Fourier-transform
infrared Analysis of powder
microcapsules (black line empty
microcapsules, gray lines
microcapsules with Lactobacillus
plantarum). (a) M1: AVM-AFHDP.
(b) M4: AVM-AFHDP-AG.AVM,
Aloe vera mucilage; AFHDP,
agave fructans high degree of
polymerization

polysaccharide (Medina-Torres, Núñez-Ramírez, Calderas, González- The mixtures of Aloe vera mucilage and agave fructans
Laredo, et al., 2019; Minjares-Fuentes et al., 2017). Thus, the initial dehydrated by the spray drying process (at drying conditions previ-
polysaccharide structure (predrying) is preserved during and after the ously studied: inlet air temperature 150
C, flow rate 1.5 L/hr, and
spray-drying process. It is important to highlight this result because atomizer speed 27,500 rpm) produced particles of sizes smaller than
previous studies (Lim & Cheong, 2015) have found that acemannan 20 μm and with homogeneous and modal distribution. The addition of
deacetylation increases when drying temperature increases arabic gum to this system produced high flow stability. This system
(e.g., > 170
C) and causes a solidification of nonhomogenized AVM represents an interesting and promising alternative to encapsulate
layers. Consequently, the spectra depict basically the peaks from the probiotics (e.g., L. plantarum-115) by spray drying, with potential appli-
encapsulating agent (i.e., wall material) without showing any absorp- cations in the food industry.
tion peaks corresponding to the probiotics (i.e., core material)
(Rajam & Anandharamakrishnan, 2015a) associated with an effective ACKNOWLEDG MENTS
encapsulation. The authors would like to thank Consejo Nacional de Ciencia y
Tecnología (CONACYT) for the scholarship number 434859 granted
to Ceja-Medina L.I. The authors also thank to Best Ground Interna-
4 | C O N CL U S I O N S tional SA de CV for Fiber Prime fructans donation.

Viscosity of the re-suspended powders of Aloe vera mucilage (AVM) CONFLIC T OF INT ER E ST
and agave fructans with high degree of polymerization (AFHDP) The authors would like to state that there is no conflict of interest of
decreased with shear rate, while the viscosity exhibited strong depen- any kind, and ethics approval was not required for this research. All
dency on the concentration, temperature and pH. Under small ampli- the authors listed made substantial contributions to the manuscript
tude oscillatory shear flow, samples were viscoelastic with a and qualify for authorship, and no authors have been omitted. We
predominant viscous behavior (G" > G') at low frequencies, and a pre- warrant that all the authors have agreed to this submission.
dominant elastic behavior at high frequencies, related to a slight ran-
dom coil chain conformation with a crossover point (G' = G´´). The Data Av ailability Statement
Cox–Merz rule was verified for these mixtures at low frequencies and The data that support the findings of this study are available from the
low shear rate indicating a mechanical stability to flow. corresponding author upon reasonable request.
The glass transition temperature of the mixture AVM-AFHDP
+ arabic gum showed an increase in comparison with the glass transi- OR CID
tion temperature of the mixture AVM-AFHDP, remarking its possible Luis Isaac Ceja-Medina https://orcid.org/0000-0002-7825-0670
application as an excellent wall material to encapsulate probiotics. Rosa Isela Ortiz-Basurto https://orcid.org/0000-0002-8284-4690
The FTIR analysis exhibited the preservation of AVM functional Luis Medina-Torres https://orcid.org/0000-0002-9963-821X
groups during and after the drying process. The analysis showed no Fausto Calderas https://orcid.org/0000-0002-3652-4223
indication of presence of bands specific to L. plantarum, which is asso- Juan Arturo Ragazzo-Sánchez https://orcid.org/0000-0002-2298-
ciated with an effective encapsulation of the probiotic, as confirmed 3306
by TEM. Octavio Manero https://orcid.org/0000-0001-6633-1070
CEJA-MEDINA ET AL. 11 of 12

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