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TECNOCIENCIA CHIHUAHUA, Vol. XVII (1) e 1140 (2023)
https://vocero.uach.mx/index.php/tecnociencia
ISSN-e: 2683-3360
Artículo de Revisión
Recent developments on wall materials for the
microencapsulation of probiotics: A review
Desarrollos recientes en materiales de pared para la
microencapsulación de probióticos: Una revisión
*Correspondencia: luismt@unam.mx (Luis Medina-Torres)
DOI: https://doi.org/10.54167/tch.v17i1.1140
Recibido:: 09 de enero de 2023; Aceptado: 18 de abril de 2023
Publicado por la Universidad Autónoma de Chihuahua, a través de la Dirección de Investigación y Posgrado
Abstract
In recent decades a surge in demand for better and healthier foods has sprung up. One category of
products under such increases in demand is probiotic products, both in the form of foodstuffs and
dietary supplements. These are living microorganisms that when consumed provide a variety of
health benefits to the host, regarding the health of the gastrointestinal tract. The main technological
hurdle this presents is to provide them alive in enough quantity. Therefore, microencapsulation
methods are often employed to enhance their survivability. A critical point in the design of the
encapsulation processes is the adequate selection of an encapsulating agent, which must comply
with a series of requirements such as being food grade, being able to envelop the probiotic, and being
of low cost to name a few. Thus, this presents an area of opportunity regarding the formulation and
exploration of different wall materials. In this paper, some of the developments regarding new wall
materials for microencapsulated probiotics are presented and discussed.
Keywords: microencapsulation, probiotic, wall material, Lactobacillus, mucilage, gum
Resumen
En las últimas décadas ha surgido un aumento en la demanda de alimentos mejores y más
saludables. Entre ellos, los productos probióticos, ya sea en forma de productos alimenticios o como
suplementos dietéticos. Los probióticos son microorganismos vivos que cuando se consumen en
cantidades adecuadas brindan una variedad de beneficios para la salud del huésped, en particular,
José Gabriel Montoya-Soto1, Rubén Francisco González-Laredo1, Luis Medina-Torres2*, Olga
Miriam Rutiaga-Quiñones1, José Alberto Gallegos-Infante1, Luz Araceli Ochoa-Martínez1,
1 Tecnológico Nacional de México/IT de Durango. Felipe Pescador 1830 Ote., 34080 Durango, Dgo., México.
2 Universidad Nacional Autónoma de México. Facultad de Química. Circuito Exterior S/N, Coyoacán, Cd.
Universitaria, 04510 Ciudad de México, CDMX.
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a la salud del tracto gastrointestinal. El principal obstáculo tecnológico que esto plantea es
proporcionarlos vivos en cantidad suficiente. Por ello, a menudo se emplean métodos de
microencapsulación para aumentar su capacidad de supervivencia. Un punto crítico en el diseño de
los procesos de encapsulación es la selección adecuada de un agente encapsulante, el cual debe
cumplir con una serie de requisitos como ser grado alimenticio, poder envolver al probiótico y ser
de bajo costo, por mencionar algunos. Por lo tanto, esto presenta un área de oportunidad en cuanto
a la formulación y exploración de diferentes materiales de pared. En este artículo, se presentan y
discuten algunos de los desarrollos relacionados con nuevos materiales de pared para probióticos
microencapsulados.
Palabras clave: microencapsulación, probiótico, material de pared, Lactobacillus, mucílago,
goma.
1. Introduction
The importance of probiotics in several sectors such as the pharmaceutical and food
industries has resulted in an ever-increasing interest in its application to both food systems and food
supplements and drugs. A microorganism is considered a probiotic by the United Nations Food and
Agriculture Organization (FAO) and World Health Organization (WHO) if it provides measurable
and verifiable health benefits to the host when it is administered in a sufficient dose. A sufficient dose
is considered to be around 106 CFU per milliliter or gram (although this may vary from individual to
individual) (FAO/WHO, 2002, 2006). Ensuring that the right amount of living cells is administered is
one of the challenges that technologists and engineers face when working with probiotics due to the
harsh conditions during both processing and delivering into the gastrointestinal tract.
Microencapsulation is the group of technologies in which a sensitive but biologically active
component is enveloped using a much more resistant material known as wall material. Some of the
features of the encapsulated products are consumer safety, such as the “generally recognized as safe
(GRAS)” label given by the Food and Drug Administration (FDA); ability to envelop adequately the
active material, preserving its bioactive and/or organoleptic features; protection against adverse
environmental conditions such as humidity, temperature changes, or UV radiation; and controlled
release of the active material after its consumption (Kandasamy and Naveen, 2022). Thus, one of the
main concerns when designing a probiotic microencapsulation process is the adequate selection of
the encapsulating material (wall material) because it must comply the aforementioned characteristics
and be compatible with the probiotic physiological characteristics, site of action, preferred release
mechanism and the encapsulation technique used.
Thus, one of the food engineers’ main concerns is seeking new wall materials sources that fulfill
technological features. Among them, meeting GRAS requirements, good thermal, rheological, and
physicochemical in addition to other effects such as prebiotic potential or anti-inflammatory
properties (Macías-Cortes et al., 2020). The objective of this review is to collect works about the
different materials used for the microencapsulation of probiotics; with an emphasis in novel or
previously unexplored materials such as mucilage, gums, vegetable proteins.
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2. Probiotics
As stated in Probiotics in Food: Health and nutritional properties page 2, the FAO and WHO
(2002), define a probiotic as "live microorganisms that, when administered in adequate amounts,
confer a health benefit on the host." The use of probiotics in food systems is quite old, dating back
centuries, mainly for the production of fermented milk products such as yogurt and kefir. Some of
the microorganisms responsible for the production of these food products include several genera of
lactic acid bacteria such as Lactobacillus, Streptococcus, Lactococcus, and yeasts such as some species of
the genus Kluyveromyces. In broad terms, the idea behind the consumption of probiotics is to change
the composition of the normal and potentially harmful microbiome into one that provides benefits
to its host. This is due to multiple mechanisms by which probiotics benefit their host, as shown in
Figure 1. These include enhancing the epithelial barrier, increasing adhesion to the gastrointestinal
mucosa, inhibition of pathogen adhesion, competitive exclusion of pathogens, secretion of
antimicrobial substances, and modulation of the immune system (Bermudez-Brito et al., 2012)
Figure 1. Probiotic’s mechanisms of action.
Figura 1. Mecanismos de acción de los probióticos.
2.1 Common probiotics
2.1.1 Lactic acid bacteria
Lactic acid bacteria are a group of facultative anaerobic gram-positive bacteria, commonly
found in human mucosal surfaces and fermented foods, such as some dairy products and fermented
vegetables (Vinderola et al., 2019). These include Lactobacillus, Lactococcus, Streptococcus, etc. Lactic
acid bacteria have been used for at least a century in the production of products such as fermented
dairy foods like yogurt, cheese, and kefir, and fermented vegetables such as pickles, sauerkraut, or
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kimchi, and some fermented meats like salami. Some species of Lactobacillus used as probiotics are
Lactobacillus acidophilus, Lb. rhamnosus, Lb. casei, Lb. helveticus (Azad et al., 2018). Regarding their
morphology, they can be classified into bacilli and cocci. According to their metabolism they can be
separated into homofermentative, bacteria that produce almost exclusively lactic acid, and
heterofermentative which can produce other metabolic products such as ethanol, acetic acid, and
CO2. Figure 2 shows a diagram of the main metabolic pathways from which homofermentative and
heterofermentative bacteria obtain energy.
Figure 2. Embden-Meyerhoff (left) and Phosphate pentose (right) metabolic pathways.
Figura 2. Rutas metabólicas Embden-Meyerhoff (izquierda) y pentosas fosfato (derecha).
Lactobacilli are rod-shaped bacteria often found in food such as dairy and fermented vegetables. In
the same way lactobacilli can be classified by their metabolism as homofermentative and
heterofermentative.
Homofermentative bacteria’s main characteristic is that the primary product of their fermentation is
lactic acid, with little to no presence of other metabolites such as CO2, acetic acid, or ethanol. This is
due to a preference of species within this classification for the Embden-Meyerhoff pathway that uses
glucose as its main substrate, ending with pyruvate as final product which then acts as an acceptor
of protons by reduced nicotinamide adenine dinucleotide (NADH) and leads to the production of
lactate and NAD+ (Poltronieri et al., 2017). While strict homofermentative bacteria exist within the
Lactobacillus genus, they are fewer in number than heterofermentative species. Some
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homofermentative species within the genus are Lb. acidophilus, Lb. delbrueckii, Lb. helveticus, Lb.
salivarius (Vinderola et al., 2019).
Heterofermentative includes all lactic acid bacteria that produce other metabolites aside from lactic
acid while fermenting sugars, this includes CO2, ethanol, and acetic acid. Bacteria within this group,
have a predilection for the pentose phosphate pathway that uses sugars (e.g., glucose) as a substrate
to produce NADPH, pentoses, and ribose (used for the synthesis of nucleotides), and the final
product is xylulose, which is metabolized into ethanol, acetate, and lactate by its catabolism. Within
this classification exist both obligate heterofermentative and facultative heterofermentative.
Lactobacillus species such as plantarum, sakei, curvatus, and casei, are considered facultative
heterofermentative; while species such as, fermentum, pontis, reuteri, brevis, and buchneri, are
considered obligate heterofermentative. These bacteria have shown several probiotic activities such
as immune system modulation, production of antimicrobial substances and direct competition with
pathogens (Vinderola et al., 2019).
2.2.1 Other bacteria
Even when the most studied probiotics are lactic acid bacteria, other genera such as
Propionibacterium, or Bifidobacterium can be found inhabiting the same places. In addition, other
genera typically associated with the human gut as Escherichia and Clostridium, may have probiotic
strains (George Kerry et al., 2018; Crook et al., 2019; Guo et al., 2020).
2.3.1 Yeast
Yeast is a heterogeneous denomination given to single-celled organisms belonging to the
fungi kingdom. They are widely used in the food industry and are involved in the production of
many food products including wine, beer, bread, kefir, cider, sake, cocoa, etc. Some species of yeast
that have shown potential as probiotics include Saccharomyces cerevisiae, S. cerevisiae var. boulardii,
Kluyveromyces marxianus, K. lactis, Pichia kluyveri, P. pastoris, Debaromyces spp., Torulaspora spp.,
Hanseniaspora spp., etc. These have shown various activities such as denaturing Clostridium difficile’s
toxins and modulation of cytokines production (Gut et al., 2018; Staniszewski and Kordowska-
Wiater, 2021).
3. Microencapsulation
This is the name given to technologies whose final goal is to envelop on a microscopic scale
any given active material (often called core material) in a layer that protects it from reactions with
the environment, increasing its shelf life, stabilizing, and ensuring a gradual release of the active
material when consumed. All microencapsulation technologies have three steps: the wall must
envelop the core material, the shell must maintain its integrity, and finally, the crust must subside at
the right moment (and right place) ensuring the release of its contents at an adequate rate (Macías-
Cortes et al., 2020). The release of the active material inside the microcapsule is as important as its
microencapsulation. There are different mechanisms, as shown in Figure 3. The microcapsules
release their content mediated by factors such as temperature, pressure, and concentration gradient,
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and subjected to the adequate stimulus, the enveloping material will dissolve, expand or rupture
(Hu et al., 2017). There are different methods of microencapsulation, the most common are
mentioned ahead.
Figure 3. Different release mechanisms of the active component in a microcapsule.
Figura 3. Diferentes mecanismos de liberación del componente activo de una microcápsula.
3.1 Extrusion
This technique typically involves mixing the probiotic along with a hydrocolloid such as a
carbohydrate dispersion. Thereafter, it is extruded through a nozzle producing a small droplet,
afterwards, these droplets fall into a bath containing a solution that hardens the wall material
enveloping its core. The main advantage of this procedure is that it does not involve the use of either
high temperature or solvents, thus ensuring a high survival rate for the probiotic. The most common
material used to microencapsulate with this method is sodium alginate. However, the main
disadvantage for this process to be used at an industrial scale lies within its inability to produce large
quantities of microcapsules, the relatively high particle size and its higher costs compared with other
methods (Lee et al., 2019; Yang et al., 2020).
3.2 Coacervation
The definition of coacervation is the separation into two liquid phases of a colloidal solution.
There are two main forms of coacervation, simple and complex. Simple coacervation involves the
use of a single polymer and a salt or dissolving agent, such dissolving agents can be either alcohol
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or acetone. In complex coacervation, two polymers with opposing charges interact producing two
immiscible phases of liquid, the dense phase, which is polymer-rich, and the continuous phase which
is not. This method often uses animal proteins such as gelatin, whey protein or sodium caseinate.
Even though this technique provides advantages over other methods such as very stable shells, with
very high encapsulation efficiency and great controlled release of the core material, it poses several
disadvantages mainly due to the time required to encapsulate and its cost. This is a relatively new
technology, and it is considered to still be in experimental phase (Dhakal and He, 2020; Yang et al.,
2020).
3.3 Liposomes
This encapsulation technique requires the formation of a bilayer, typically of a phospholipid,
in an aqueous solution to which agitation, and heat are applied to form vesicles. Since phospholipids
are amphiphilic molecules, the liposomes can trap polar active substances in an aqueous solution
with their polar ends. It is also possible as well to trap nonpolar substances with the lipophilic end
of the phospholipid, making them more suitable for an aqueous delivery system. A special
application of this technique is the entrapment of core materials that require high water activity such
as enzymes or probiotics. Although one of the main disadvantages of this method of encapsulation
is the low resistance of the encapsulating material, being a phospholipid, it is prone to oxidation and
hydrolysis as well as sensitive to changes in pH and temperature (Dhakal and He, 2020; Mehta et al.,
2022).
3.4 Spray drying
Spray drying is one of the most widely spread microencapsulation techniques in use due to
its short processing time and the overall quality of the encapsulated product, mainly uniform particle
size, and defined morphology (see Figure 4). Spray drying is a technology that consists in the
pulverization or atomization of a suspension or solution into a chamber filled with hot gas and
finally recover it in the form of powder. The way in which spray drying microencapsulation works
is to prepare a dispersion of both the active and enveloping materials in an adequate solvent,
pumping the dispersion into the drying chamber, wherein it is atomized, and the solvent is quickly
evaporated. The dehydrated product is collected either in powder or agglomerated form from a
cyclone (Ceja-Medina et al., 2020). This method consists of the next main steps: preparation of the
dispersion, homogenization, atomization, dehydration of the atomized particles and collection.
Some of the advantages the final product provides when working with spray drying is an increased
shelf life due to its low water activity, thus reducing the need of refrigeration, cutting costs in both
storage and transport. The main elements present in spray drying equipment (see Figure 5) are a
feeding pump, an atomizer, a heating device, a drying chamber, and a cyclone. Spray drying uses a
variety of compounds from which polysaccharides such as starches with varying grades of
modification, gums, and plant-based mucilage are of particular interest. This technique’s main
disadvantages are due to the high temperature involved. Because of this a wall material that is highly
resistant to heat, has high water solubility and a relatively low viscosity such as Gum Arabic,
modified starches, maltodextrin, and plant mucilage (Macías-Cortes et al., 2020; Yang et al., 2020).
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Figure 4. SEM micrography of Lb. plantarum microencapsulated in an Aloe vera mucilage/agave
fructans/gum Arabic microcapsule
Figura 4. Micrografía por SEM de Lb. plantarum microencapsulado en una microcápsula de mucílago
de Aloe vera/fructanos de agave/goma Arábiga (Ceja-Medina et al., 2020).
3.5 Spray chilling
Spray chilling, also known as spray cooling, is typically employed to encapsulate
hydrophilic materials into a hydrophobic shell. The wall material is most often a lipidic material
such as waxes, with a relatively high melting point, and similarly to spray drying is atomized into a
chamber filled with cool gas, which causes a fast solidification of the lipidic material around the core.
This technique is typically used in the encapsulation of water-soluble vitamins, enzymes, and flavor
agents. It is also possible to encapsulate hydrophobic core materials with hydrophobic wall materials
such as the encapsulation of liposoluble vitamins with fats, waxes, and oils as wall materials. The
main disadvantage of this method lies in the melting point of the material used as it should be low
enough as to not thermally kill the probiotic and high enough to not melt at room temperature. For
this reason, mixtures of waxes and other materials such as polysaccharides are under study
(Choudhury et al., 2021).
3.6 Spray freeze-drying
This is a combination of spray chilling and lyophilization in which a mixture of both the
encapsulating agent and the core material is sprayed into a cooling chamber in which it is instantly
frozen, producing a current of tiny ice spheres in which both materials are contained. Thereafter, the
ice particles are freeze-dried through regular lyophilization. Lyophilization is the removal of
moisture from a frozen matrix without going through the liquid phase, through a process known as
sublimation. Sublimation involves the use of very low pressure to turn ice into water vapor without
raising its temperature to the melting point. Its main use is to dry materials that are particularly
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sensitive to high temperature. Lyophilization consists of the next phases, the initial freezing phase,
and two drying phases. The initial phase in lyophilization is freezing, wherein most of the moisture
is frozen. Afterwards during the first drying step, frozen free moisture is removed by sublimation.
The two parameters that play a crucial role during this step are the shelf temperature and the
chamber pressure. The second drying phase cycle involves the elimination of unfrozen bound water
through desorption. The wall materials needed for this technique are similar to those needed in spray
drying, with the exception of resistance to high temperature (Kandasamy and Naveen, 2022).
Figure 5. A typical arrangement of spray drying equipment.
Figura 5. Un arreglo típico de un equipo de secado por aspersión.
3.7 Fluidized bed coating
It is like spray drying technology, although with some modifications. It consists of three
stages, the absorption of the core materials onto a support material, a solid porous material, which
is being fluidized; the coating which is done by spraying the liquid wall material into the fluidized
bed; and finally, the hardening of the shell by either vaporization of the wall material solvent or by
chilling, being air the most common gas used to both fluidize and cooling. This method provides
flexibility in wall materials using both water soluble materials such as protein and polysaccharides
and lipophilic materials such as waxes (Mehta et al., 2022).
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4. Wall materials
The selection of adequate wall material is essential given that it will determine both the
efficiency of encapsulation and the stability of the capsules. Some of the qualities that wall material
must possess are, non-reactivity towards the core material, it must be able to contain the core
integrally inside of the capsule, being economically viable, it must meet standards such as FDA’s
GRAS, and depending on whether its application is in food or not, it must not have any unpleasant
smells or flavors (Dhakal and He, 2020). While most of the commonplace materials nowadays meet
the criteria of being safe for consumption, some of the more common problems are that resistance of
capsules and the price of the material are often at odds. Another avenue for new sources of materials
is that some might have prebiotic effects or come from vegan or vegetarian sources. This opens new
avenues for development of new developments. A brief list of recent developments regarding
common wall materials can be seen in Table 1. There are different wall materials of
microencapsulation, the most common are:
4.1 Protein
Protein wall materials coming from both animal and vegetable sources have been used with
success to encapsulate probiotics, some of these sources range from dairy, gelatin, and various
legumes. Protein solubility varies according to a variety of extrinsic factors, like pH and temperature,
and intrinsic factors mainly regarding the structure of the protein and its amino acid profile. Their
molecular weight varies drastically ranging from around 10 kDa upwards to 50 kDa or more. The
capacity of proteins to form emulsions is variable depending on factors such as molecular weight,
source, structure, and adsorption capacity (Kim et al, 2020). Proteins are typically sourced from
animal byproducts such as gelatin, obtained from the thermal hydrolysis of collagen from waste
products of the meat and leather industry such as bones, horns, hooves, skins, cartilage. One of the
most used sources for microencapsulating proteins is milk, usually milk whey. Milk whey is the
liquid remaining from the curdling of milk during cheese elaboration. It contains a mix of minerals,
and proteins such as alpha-lactalbumin, beta-lactoglobulin, and lactose. It is mainly used along with
wall materials from other sources such as carbohydrates like maltodextrin, alginates, etc. (Bhagwat,
et al., 2020; Obradović et al., 2022). Due to the rise in demand of vegan and vegetarian ingredients,
advances in vegetable protein have also been made. Regarding vegetable protein works like
González-Ferrero et al. (2020) worked with soy protein isolate, and maltodextrin to produce
microcapsules loaded Lactobacillus plantarum CECT 220, using a chi spray dryer, with a survival
rate of 93 %. Or Qi et al. (2021) in which a microcapsule made by coacervation made using pea protein
isolate and sugar beet pectin yielded the best results in a gastrointestinal simulated digestion.
Nevertheless, the bulk of research on vegetable protein is centered around microencapsulating
materials like antioxidants, essential oils, and vitamins. Due to their origin and complex purification,
protein wall materials are typically of higher costs than some other materials such as carbohydrates.
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Table 1. Common wall materials, and recent developments on probiotic microencapsulation
Tabla 1. Materiales de pared comunes y desarrollos recientes en microencapsulación de probióticos
Monomeric
units
Encapsulation techniques
Temperature
°C (i=inlet,
o=outlet)
Encapsulation
efficiency %
Probiotic
Reference
Lactalbumin
and
lactoglobulin
(amino acids)
Spray drying (SD)
140(i)
60(o)
70.65+-1.84
Enterococcus
canintestini
Bhagwat,
et al., 2020
Hydrolyzed
collagen
(amino acids)
Emulsification/coacervatio
n
40
97.78
Lb.
plantarum
Paula et
al., 2019
Glucose
SD
130-150(i)
55+-2(o)
89.15
Lb.
acidophilus
Arepally
et al., 2020
Mixed flow SD
140(i)
80(o)
20.88±0.03
Lb.
rhamnosus
Jiang et
al., 2020
alfa 1-4 and
alfa 1-6 linked
Glucose
Extrusion
-
48.46 ± 0.98
Lb. casei
Ashwar
et al., 2018
Carboxy-
methyl
Glucose
Extrusion
-
94.7±0.78
Lb.
plantarum
Dafe et
al., 2017
Glucosamine
SD
120(i)
68(o)
91±0.33
K.
marxianus
Vanden
Braber et
al., 2020
Fructose
SD/Spray Freeze Drying
SD: 110(i), 62(o)
SFD: -80
SD: 89.21
SFD: 96.16
Lb.
plantarum
Yoha, et
al., 2020
4.2 Lipids
Lipids, which include fatty acids, fats, waxes, sterols, and phospholipids, are an eclectic
group of molecules used to designate substances with relatively low polarity, and thus low solubility
in polar compounds such as water. As such there are not many studies that work with the
encapsulation of probiotics with only lipids as an encapsulating agent. Nevertheless, there are some
studies in which an outer crust of materials such as beeswax and stearic acid is used to cover
microcapsules made with other materials such as resistant starch or alginate to increase their
resistance to moisture. Lipids also ensure a controlled release in the intestine by the way of lipase
action while being digested (Rodrigues et al., 2020).
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4.3 Carbohydrates
Carbohydrates are the group of biopolymers most widely used in the encapsulation of
probiotics. They can be identified in any number of ways by size, composition, refining grade, and
origin. Being classified regarding their composition in homopolysaccharides when their forming
monomers are the same, such as starches, maltodextrin, and inulin, and heteropolysaccharides,
when their forming units are non-homogeneous, such is the case of gums such as Arabic and guar
gums. Carbohydrate solubility in water varies depending on the degree of polymerization, and
crystallinity; being those with a smaller polymerization degree and less crystalline more easily
solubilized. While carbohydrates range in molecular weight from around 180 Da for average
monosaccharides to 480 kDa for an average polysaccharide, although some polysaccharides can
upwards to 788 kDa. The molecular weight of carbohydrates frequently used in microencapsulation
usually starts at around 20 kDa (Ushiyama and Shimizu, 2018).
4.3.1 Starch
Starch is the name given to the reserve polysaccharides made by green plants. It is found in
foodstuffs such as cereals and tubers and it is one of the main sources of calories in modern human
diets. It is made up of glucose units linked together by alpha α (1 4) glycosidic bonds, forming
long chains, known as amylose, with ramifications of alpha α (1 6) glycosidic bonds known as
amylopectin. Starch is typically made up of around 1:3 up to 1:4 parts of amylose to parts of
amylopectin by weight. It is used both as an ingredient and raw material for different food products,
including modified starches and high fructose corn syrup. It has recently become of interest to
technologists the use of resistant starches as novel materials for the encapsulation of probiotics due
to their potential as a prebiotic. Resistant starches are starches resistant to enzymatic digestion by
intestinal amylase, this is due to a higher proportion of amylose which is less susceptible to these
enzymes due to its structure. The categories of resistant starch are as follows RS1) physically
inaccessible, RS2) native granules of non-gelatinized starch, RS3) retrograded amylose, RS4)
chemically modified starch (Bojarczuk et al., 2022). RS4 was studied by Ashwar et al., (2018; 2021)
using a rice-modified starch in an extrusion system.
4.3.2 Maltodextrin
Maltodextrin is a group of polysaccharides obtained from partial hydrolysis of starches. Like
starch, it is made up of glucose monomers bound to each other by α (1 4) bonds with occasional
α (1 6) bond ramifications. Maltodextrin is one of the most widely used and studied encapsulating
agents with works as recent as those made on survivability and stability by Arepally et al. (2020),
with novel forms of spray drying technology such as mixed flow spray drying by Jiang et al. (2020),
and its uses with other materials to yield better capsules such as whey protein by Bhagwat et al.
(2020).
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4.3.3 Cellulose
Cellulose is a structural polysaccharide found most abundantly in the cell walls of plants,
although it is also produced by bacteria such as that found in acetic fermentations. It is made up, like
starch, of glucose monomers, with the difference being that the bonds between subunits are β (16),
forming a much more resistant fibrillar structure. In its natural form, it is of little use as an
encapsulating agent due to its very low solubility in water and other common solvents, thus some
products derived from it such as methylcellulose, hydroxypropyl cellulose, and
carboxymethylcellulose (CMC), and other forms of such as micro and nanocrystalline cellulose are
used. Multiple works with both modified cellulose and nano/micro crystalline cellulose are at the
forefront of the study of new methods of probiotic encapsulation. Such as the study done by Wang
et al. (2022) where kelp nanocellulose was incorporated in an alginate microcapsule, leading to
increased survivability during gastrointestinal digestion simulation in comparison with a system
made exclusively with alginate. Regarding modified cellulose Tao et al. (2019), used skim milk along
with some polysaccharides including several modified celluloses such as CMC, hydroxypropyl
methylcellulose, methylcellulose as well as gum arabic and sodium alginate observing increased
survivability of Lb. paracasei, after spray drying compared to skim milk alone with encapsulation
efficiencies between 91 to 97 %.
4.3.4 Chitosan
Chitosan is a food-grade polysaccharide obtained from processing shrimp and other
crustaceans' exoskeletons with an alkali such as sodium hydroxide, it is the only carbohydrate used
in microencapsulation that is predominantly positively charged. It is composed of β (1 4) linked
units of both acetylated and nonacetylated D-glucosamine. It is widely used in the chemical,
pharmaceutical, cosmetic, and food industries (Pech-Canul et al., 2020). Chitosan has also been used
as an encapsulating agent to encapsulate different probiotics such as Lb. gasseri, Lb. rhamnosus, Lb
casei, Lb. acidophilus, Bifidobacterium animalis and, B. bifidum (Călinoiu et al., 2019).
4.3.5 Fructans
Although the bulk of forming units of fructans are as the name suggests fructose the
reducing end of the chain is a sucrose unit. There are five different types of fructans according to the
kind of bonds they present. The major kinds of fructans are inulin, levan, graminin and neo series
inulin and levan. In nature they are found in plants such as onions, garlic, artichokes, asparagus,
grasses, and agave. Fructans are widely used in the food industry mainly as a dietary fiber
supplement, because of their prebiotic properties (Wang and Cheong, 2023).
Fructans have recently been of interest as encapsulating agents in processes similarly to spray drying
such as the study done by Ceja-Medina et al. (2020) in which several food gums such as guar,
xanthan, and gum Arabic, as well as whey protein concentrate in several encapsulating systems,
made up from a mixture of Aloe vera mucilage and high molecular weight agave fructans. Being the
systems made with Aloe vera/fructans/whey and Aloe vera/fructans/gum Arabic, the ones with a
higher survival rate at about 70 %. Also, the work of Alvarado-Reveles et al. (2019) involved the use
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of both agave fructans and buttermilk proteins as wall materials yielding 1.08x1010CFU/mL against
3x109CFU/mL using buttermilk proteins alone.
4.3.6 Algae polysaccharides
Some of the most used heteropolysaccharides in the industry are derived from algae. Some
of the polymers which are currently under use in the food and pharmaceutical industries as
encapsulating material are those of the carrageenan family of polymers from which kappa, iota, and
lambda carrageenan are the most used. Another relevant polysaccharide obtained from algae is
alginic acid often found in its salt form as sodium alginate is a linear polymer with blocks of (14)
beta-D-mannuronate and alpha-L-guluronate. Another relevant polysaccharide derived from algae
is agar, it is most often associated with microbiological culture media, although not properly
microencapsulation since the particle size is bigger than 1mm developments such as the one done
by Albadran et al. (2020) which used chitosan to coat gelatin-agar particles to encapsulate Lb.
plantarum, demonstrating survival to a simulated gastric and intestinal digestion, demonstrate
possible new applications for agar as a potential microencapsulating agent
4.3.7 Gums and mucilages
Gum is a generic name given to a broad number of heteropolysaccharides that are soluble
and have the property of forming gels; gums are often found on the seed epidermis, the leaves, and
the bark of plants, although there are some, such as xanthan gum, that are of microbial origin. Gums
are a response to damage by some plants or unfavorable environmental conditions. Some of the most
common gums include guar, acacia (also known as Arabic), and tragacanth gums. Mucilages are
natural components of plant metabolism, they are very thick, viscoelastic, and usually do not have
as high solubility as gums, inside the plant they are often involved in water retention, calorie
reserves, as well as helping in seed germination (Amiri et al., 2021). A widely used gum is gum Arabic
which is a heteropolysaccharide obtained from the bark of Acacia senegal (L.), its constituents are
arabinose, galactose, rhamnose, and glucuronic acid. It has been thoroughly studied as an
enveloping material for probiotics such as the work of Arepally et al. (2020); in which a mixture of
maltodextrin and gum Arabic are used to encapsulate probiotics in a spray dryer, providing better
physical and physicochemical properties, as well as higher encapsulation yields when higher
concentrations of gum Arabic was used with a viability percentage higher than 80 % (around 7.3-9.9
log CFU/g). An alternative to gum Arabic that is currently under study is mesquite gum, which is
obtained from several species of trees under the Prosopis genus such as P. laevigata, P. juliflora, P.
velutina, and P. pubescens. Mesquite gum is made up mainly of monomeric units of L-arabinose and
D-galactose with trace amounts of D-xylose, D-mannose, and D-glucuronate, differing from acacia
gum because of its lack of L-rhamnose (Mudgil and Barak, 2020). There are few works regarding the
use of mesquite gum as a protecting agent for probiotics one of such is the work done by Rodríguez-
Huezo et al. (2014) a double emulsion process, in which Lb. plantarum cells were dispersed in canola
oil (continuous phase) and either sweet whey or "aguamiel" (sweet agave juice” were dispersed in
water, after that, it was further dispersed in a dispersion of gum Arabic, mesquite gum, and
maltodextrin. This emulsion was then integrated into the processing of Oaxaca cheese, exhibiting
survival rates of 8.2 and 8.15 log CFU/g for sweet whey and aguamiel respectively versus 6.8 log
CFU/g in cheeses prepared with free cells.
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Regarding mucilages, while there have been uses in the food industry for them before, it is only
recently that such polymers have garnered attention to their potential as new encapsulating
materials, although in some cases there has been more development towards the encapsulating of
antioxidants or other kinds of ingredients such as the work done by Medina-Torres et al. (2019),
which involved the encapsulation of gallic acid with nopal (Opuntia ficus-indica) and Aloe vera
mucilage via spray drying, obtaining a higher releasing percentage when encapsulating using Aloe
vera mucilage while nopal mucilage gave particles with a bimodal particle size distribution and a
prolonged release of the active ingredient. The work done by Jannasari et al. (2019) in which a
mixture of gelatin and cress seed mucilage was used to encapsulate Vitamin D using coacervation
as the encapsulation method obtaining up to 67 % of encapsulation efficiency. Cortés-Camargo et al.
(2017 and 2019), which used a mixture of mesquite gum and nopal mucilage to encapsulate lemon
essential oil obtaining the best overall results using a mix of both since nopal mucilage gave greater
encapsulating efficiency while mesquite gum allowed for a greater volatile oil retention. Alpizar-
Reyes et al. (2020) used tamarind seed mucilage to encapsulate sesame seed oil both showed
comparable results in peroxide value results for the oil, which was much lower than that of free oil
confirming the capabilities of these materials as good encapsulating vectors for essential oils.
Although few, work regarding the encapsulation of probiotics using these gums and mucilages,
there have been some recent developments such as the works of Lai et al. (2020 and 2021). They used
flaxseed mucilage to encapsulate Lb. rhamnosus GG that yielded a reduction in cellular death during
storage between 120-135 % at 4°C and between 52-243 % at 25°C. The work done by Ceja-Medina et
al. (2020 and 2021), in which Aloe vera mucilage and agave fructans (along with some other
biopolymers) were used to successfully encapsulate Lb. plantarum with a survival rate of above 70 %
for the best mixes of polymers (gum Arabic and whey protein concentrate). Homayouni-Rad et al.
(2021) using Alyssum homolocarpum seed mucilage and inulin in spray drying encapsulation to
encapsulate Lb. casei obtaining a survival rate of around 67 % after gastric simulation as well as
showing a good capsule morphology with absent cracks in their walls. Bustamante et al. (2020)
encapsulating Lb. plantarum, Bifidobacterium longum, and B. infantis using chia and flaxseed mucilages
as well as inulin, which exhibited high viability after spray drying with around 98 % of viability and
high survivability after storage incorporated with an instant powder juice 10.5-11 log CFU/g for B.
infantis and between 7.3-8.9 log CFU/g for Lb. plantarum.
4.3.8 Prebiotics as encapsulating agents
Prebiotics are substances, typically carbohydrates, which when ingested promote the growth
of desirable bacteria groups within the gut they are often classified as dietary fiber. To be considered
a prebiotic a polysaccharide must meet certain criteria which include: 1) high resistance to orogastric
digestion which includes resistance to both the enzymes found in the mouth and stomach as well as
a low pH, 2) it is fermentable by gut bacteria, 3) provides a health benefit to the consumer, 4)
selectively stimulates the growth of certain bacteria, 5) stability in food systems. Some of the ways a
prebiotic might be incorporated into new products are, emulsifying agents, foam stabilizers, fat or
sugar substitutes, fiber supplements, and encapsulating agents (Behare et al., 2021; pez-Castejón
et al., 2021). The use of prebiotics as an ingredient in products with probiotics has been of interest in
recent times, naming such products as synbiotics. The importance of research in the realm of
symbiotics lies in the synergic effect that the prebiotic has on the probiotic, while not enhancing the
growth of other (potentially pathogenic) bacteria. Synbiotic show promise as effective tools in
managing health outcomes (Maftei, 2019). Typical prebiotics includes fructooligosaccharides (FOS),
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galacto-oligosaccharides (GOS), and trans-galacto-oligosaccharides (TOS) (Davani-Davari et al.,
2019) although some other substances such as xylooligosaccharides, pectic oligosaccharides,
resistant starch, and polyphenols are considered in some instances as such (do Nascimento and
Marostica Junior, 2021). Previously in this review, some of such materials have been mentioned as
being under study by different research groups as new sources of materials for the encapsulation of
probiotics, such as fructooligosaccharides and other fructans by Ceja-Medina et al. (2020, 2021),
Alvarado-Reveles et al. (2019); and resistant starches by Ashwar et al. (2018, 2021). Some kinds of
resistant starches have shown potential as prebiotics, by enabling the growth of lactobacilli and
bifidobacteria (Bojarczuk et al., 2022). Also, pectins have shown promising activity as probiotics such
as reported by Singh et al., (2020) and potential as new encapsulating materials such as reported by
Motalebi Moghanjougi et al. (2021). Aloe vera has shown to be a new possible source of prebiotics as
shown by the works of Tornero-Martinez et al. (2019) and Quezada et al. (2017) which show the
potential of Aloe vera’s polysaccharides as a possible substrate for probiotics to ferment, fermentation
that produces short chain fatty acids. Nopal (Opuntia ficus-indica) which has been used as an
encapsulating agent for other kind of bioactive materials has also shown potential as a prebiotic,
functioning as a substrate for lactobacilli and bifidobacteria (Cruz-Rubio et al., 2020).
Regarding new materials that are being studied as encapsulating agents with the potential of being
prebiotic components, materials such as gums, pectin, mucilages, and other biomaterials are a
promising frontier and an interesting alternative for new developments and satisfy the current
demand in the food industry.
Conclusions
Although the encapsulation of probiotics is not a new concept there is still much in the way
of developing better encapsulating materials. While some materials that are now commonplace in
the food and pharmaceutical industries, such as: starches, maltodextrins, and other polysaccharides,
which have already been extensively studied; there are still gaps in our knowledge of possible new
wall materials. One of such gaps is in the use of new refined proteins obtained from vegetable
sources such as soy, peas, and other plants. Another blind spot is the utilization of some gums and
mucilages such as those from tree sap (acacia and mesquite gums), seeds (flaxseed, and chia seeds
mucilages), and particularly some cactus and other succulents (dragon fruit, prickly pear cladodes,
and aloe).
Acknowledgments
Partial financial support from CONACYT is recognized (Fortalecimiento de Infraestructura-
CONACyT 2021, grant No. 317235). Financial support is recognized from TecNM (Project grant No.
17007.23-P).
Conflict of interests
All authors declare that they have no conflicts of interest.
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