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 Büchi 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

Polymer

Monomeric

units

Encapsulation techniques

Temperature

°C (i=inlet,

o=outlet)

Encapsulation

efficiency %

Probiotic

Reference

Whey protein

Lactalbumin

and

lactoglobulin

(amino acids)

Spray drying (SD)

140(i)

60(o)

70.65+-1.84

Enterococcus

canintestini

Bhagwat,

et al., 2020

Gelatin

Hydrolyzed

collagen

(amino acids)

Emulsification/coacervatio

97.78

Lb.

plantarum

Paula et

al., 2019

Maltodextrin

Glucose

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

Resistant and

modified starch

alfa 1-4 and

alfa 1-6 linked

Glucose

Extrusion

48.46 ± 0.98

Lb. casei

Ashwar

et al., 2018

CMC

Carboxy-

methyl

Glucose

Extrusion

94.7±0.78

Lb.

plantarum

Dafe et

al., 2017

Chitosan

Glucosamine

120(i)

68(o)

91±0.33

marxianus

Vanden

Braber et

al., 2020

Fructans

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 (1→6),

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 (1→4)

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; López-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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