A Narrative Review On Microencapsulation

Food Reviews International
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A Narrative Review on Microencapsulation of

Obligate Anaerobe Probiotics Bifidobacterium,
Akkermansia muciniphila, and Faecalibacterium
prausnitzii
Yining Chen , Maninder Meenu & Xu Baojun
To cite this article: Yining Chen , Maninder Meenu & Xu Baojun (2021): A Narrative Review on
Microencapsulation of Obligate Anaerobe Probiotics Bifidobacterium,�Akkermansia�muciniphila, and
Faecalibacterium�prausnitzii , Food Reviews International, DOI: 10.1080/87559129.2020.1871008
To link to this article: https://doi.org/10.1080/87559129.2020.1871008
Published online: 18 Jan 2021.
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FOOD REVIEWS INTERNATIONAL
https://doi.org/10.1080/87559129.2020.1871008
REVIEW
A Narrative Review on Microencapsulation of Obligate Anaerobe

Probiotics Bifidobacterium, Akkermansia muciniphila, and
Faecalibacterium prausnitzii
Yining Chena, Maninder Meenua, and Xu Baojun a
a
Food Science and Technology Programme, BNU-HKBU United International College, Zhuhai, Guangdong, China
ABSTRACT KEYWORDS
Probiotics have been reported to exhibit various potential health and nutri- Microencapsulation;
tional benefits. However, the efficient delivery of these probiotics to the bifidobacterium; Akkermansia
intestine for the health benefit of the host is of much interest. muciniphila; viability;
Microencapsulation came up as an efficient technique to protect probiotics stability
during gastrointestinal (GI) transit. There are many studies and reviews
related to microencapsulated probiotics, but no review has been published
on the microencapsulation of anaerobic probiotics especially the obligate
anaerobic probiotics Bifidobacterium genus. This review article aims to sum-
marize the microencapsulation of obligate anaerobe Bifidobacterium and
seek out the optimal encapsulating methods for strictly anaerobic microbes-
next-generation probiotics. The studies related to the microencapsulation of
strictly anaerobic bacteria especially Bifidobacterium, Akkermansia mucini-
phila and Faecalibacterium prausnitzii published in the last 5 years have
been reviewed. This review summarizes the encapsulants, techniques for
microencapsulation, the viability of probiotics during storage and their sta-
bility in GI.
Introduction
According to the International Scientific Association for Probiotics and Prebiotics (ISAPP) consensus
statement probiotics are defined as “a substrate that is selectively utilized by host microorganisms
conferring a health benefit”.[1] Most of the probiotics belong to the facultative anaerobic or strict
CONTACT Xu Baojun [email protected] Programme of Food Science and Technology, BNU-HKBU United International
College, 2000, Jintong Road, Tangjiawan, Zhuhai 519087, Guangdong, China.
#
Two authors have equal contribution
© 2021 Taylor & Francis
2 Y. CHEN ET AL.
anaerobic bacterium as they colonized in the intestine under a relatively anaerobic environment.
Among these classical probiotics, only the genus Bifidobacterium includes various Gram-positive non-
motile anaerobic bacteria which are relatively susceptible to oxygen. Those commonly studied strains
of bifidobacteria, considered as important probiotics, contains Bifidobacterium infantis,
B. adolescentis, B. animalis subsp. animalis, B. animalis subsp. lactis, B. bifidum, B. longum, and
B. breve.[2] Furthermore, the research has extended from “classical probiotics” to “next-generation
probiotics” leading the attention to cure the intestinal disorders by the means of manipulating certain
strictly anaerobic bacteria host gut microbiota.[3] Next-generation probiotics are normal components
of healthy human gut microbiota and reduction in their population in the gut is associated with
various disorders such as inflammatory disorders.[4] This group of potentially beneficial microbes
includes Bacteriodes thetatiotaomiron, Faecalibacterium prausnitzii, Akkermansia muciniphila,
Eubacterium halii, and B. uniformis, among others.[,3,5] A. muciniphila and butyrate-producing
bacteria F. prausnitzii are well known to exhibit anti-inflammatory effects among these bacterial
species.[6]
A few decades back, the concept of encapsulation was introduced to protect the micro-
bial cells from harsh environmental conditions and to provide suitable conditions for their
growth and metabolism. [7] Based on the resultant polymeric beads two types of encapsula-
tion was reported, i.e., macroencapsulation and microencapsulation. [8] The size of the
polymeric bead ranges from few millimeters to centimeters in case of macroencapsulation.
However, microencapsulation lead to polymeric beads ranges from 1 to 1000 μm. The
polymeric beads with less than 1000 μm are preferred due to their mechanical robustness,
efficient diffusion of nutrients, oxygen and metabolites that lead to a high concentration of
cells within the beads. [7] Microencapsulation technique was reported to protect various
strains of Bifidobacterium through simulated gastrointestinal (GI) fluids and under the
acidic conditions. In addition, the size, morphology, color, hygroscopicity of microcapsules
were suitable to be incorporated into food products without interfering with the sensory
aspects of foods. [9] Whereas some oxygen-facultative probiotics like certain Bifidobacteria
are extensively being used in nutraceutical formulation or functional food, it is difficult to
guarantee that the viability of these probiotics is sufficient to manipulate or alter the
function of the intestinal system due to their great sensitivity towards oxygen and other
environmental factors. Microencapsulation of these anaerobes can not only efficiently
protect them from external stress like oxygen but also package them into a form that is
easier to be incorporated into a food product.
Although various researchers have reviewed the available literature related to the micro-
encapsulation of probiotics for their GI delivery, microencapsulation delivery system for
their long-term preservation as biotherapeutics agents, the impact of various microencap-
sulation technologies on the viability of probiotics and impact of coating on physiological
protection of probiotic microcapsules [10–13] but no review article has covered the micro-
encapsulation of the obligate anaerobe Bifidobacteria or other strictly anaerobic probiotics.
In order to better summarize the microencapsulation techniques and their effects on the
classical obligate anaerobe genus Bifidobacterium and further seek out the optimal micro-
encapsulation methods for the next-generation probiotics, this paper has reviewed the
research papers published on the microencapsulation of Bifidobacterium and also reviewed
the research papers related to the A. muciniphila and F. prausnitzii in recent 5 years. We
have also discussed and compared the encapsulants (wall materials), techniques for micro-
encapsulation, particle size, viability during storage and stability through simulated GI
condition followed by the conclusion of this review article with some possible future
trends in this field.
FOOD REVIEWS INTERNATIONAL 3
Principles and methods for microencapsulation

Various techniques have been employed for the microencapsulation of probiotics in recent years.
Based on the functions, the microencapsulation process consists of two typical stages including
initial microencapsulation and drying. For the initial microencapsulation, the methods can be
divided into gelation (gelification), coacervation, and polymerization based on the core mechan-
isms. To control the morphology of microcapsules, two typical techniques including extrusion or
emulsification are commonly utilized. At the drying stage, various drying techniques such as
spray-drying and freeze-drying were employed to produce a product with optimal water content
and long shelf life. As mentioned before, Bifidobacterium and other obligate anaerobe probiotics
are extremely sensitive to oxygen, thus as compared to other aerobic probiotics or facultative
anaerobic probiotics, the whole process involving culturing, fermentation, following microen-
capsulation process, and drying process has to be carried out in oxygen-free environment. Thus,
all of these mentioned operations are generally carried out in an anaerobic system and all
materials used in this process has to be preferably placed under anaerobic environment
one day before the experiment.
Methods and techniques employed during initial microencapsulation

Gelation
Gelation can be defined as the formation of a three-dimensional network by chemical or physical
cross-linking that include agglomeration, weak hydrogen bonds along with the ionic and hydrophobic
associations.[14] Ionic gelation is frequently applied in microencapsulation due to its capability to
crosslink polyelectrolytes in the presence of multivalent ions such as Ca2+, Ba2+ and Al3+.[15] The
interactions built up between the anionic carboxylic groups of polyelectrolytes and divalent metal
cation (such as Ca2+) contributes to the formation of strong hydrogels.[16] Encapsulation by ionic
gelation technique could be carried out externally or internally (Fig. 1). In external gelation, Ca2+ ions
diffuse from an external source into the polymer solution,[17] while suspension with calcium salt
(CaCO3) is added dropwise into the polymer solution in internal gelation method, which results in the
production of an aqueous-core calcium alginate capsules.[18] It is advantageous to encapsulate
probiotics within hydrogel beads. These microgels are generally engineered to encapsulate high
concentrations of probiotics and protect them from environmental stresses, such as acidic pH, bile
salts, and digestive enzymes.[19–21]
Extrusion is the most common technique relevant to gelation in microencapsulation due to its ease
of operation. Generally, the probiotic cells are mixed with the hydrocolloids solution and further
dripped via a syringe needle or nozzle spray machine in the form of droplets into the hardening
solution mostly calcium chloride.[10] To form droplets, coaxial flow and electrostatic field are
employed alternatively. For instance, Bifidobacteria were encapsulated within alginate microgels
using an extrusion–gelation method,[19] in which sodium alginate solution was mixed with probiotic
suspended in physiological saline, and aliquots of probiotic/alginate solution were injected into
calcium chloride solution to form probiotic/alginate beads. Owing to the limitation of the materials
used for the ionic gelation-extrusion method, the nature of alginate microgels is fragile especially
under acidic environment, which makes it fail to sustain protective effect in the gastric condition when
the single method was employed for microencapsulation.[19,20] Despite this, although extrusion is easy
to perform, the low productivity of these techniques restrict its application on an industrial scale.[22–23]
Emulsification is another frequently used alternative related to ionic gelation. Generally, emulsifi-
cation is carried out by homogenization of the discontinuous phase in a large volume of continuous
phase with the assistant of surfactant molecule that results in the formation of a water-in-oil emulsion.
Along with the formation of water-in-oil emulsion, the water-soluble polymer is crosslinked to form
particles within the oil phase followed by harvesting of beads via filtration.[11] In short, emulsification
provides the emulsion system to provide the shape to the microcapsules while gelation offers the hard
4 Y. CHEN ET AL.
Figure 1.
shell for the microcapsules. Ionic gelation used in the emulsion system can further be classified as
internal gelation and external gelation. External gelation is generally performed with calcium chloride
solution in a uniform emulsion;[24] whereas, in case of internal gelation, calcium carbonate suspension
was added with sodium alginate solution before forming emulsion.[9] Previously, sodium alginate
mixed with CaCO3 suspension and rapeseed oil was used to form water-in-oil microparticles, and
Tween 80 was used as an emulsifier to improve the emulsion condition for microcapsules containing
Bifidobacterium BB-12.[9] Another study conducted emulsification with alginate and various starches
such as wheat starch, rice starch and Hylon starch as well as chitosan or poly-L-lysine coating for
enhancing the survival of Lactobacillus casei and Bifidobacterium adolescentis. In both the studies
calcium chloride was employed for external gelation.[24] Different emulsions produced by employing
various kinds of emulsification approaches present significant variations in their physiochemical
performance and possess a significant impact on the microencapsulation of probiotics. No matter
internal gelation or external gelation applied with emulsification, the microencapsulation efficiency
shown in mentioned studies were higher than 80%. Also, particle size under this gelation-
emulsification paradigm was ideal that was below 100 μm[9,24] which was much smaller compared
to the particle size produced by gelation-extrusion.[19–21] Either external or internal gelation has been
employed in both extrusion and emulsion. It is difficult to justify whether external or internal gelation
demonstrates better protective effect by merely relying on the viability of probiotics from data of
various studies. For Bifidobacterium, regardless of the variation in strains, it might be suggested that
internal gelation in emulsion exhibited better protection on probiotics than external gelation in
emulsion based on their viability during storage. Holkem et al.[9] applied emulsification and internal
gelation to Bifidobacterium BB-12 and only about 1.5 log units reduction was observed after 120 days
storage at −18°C. However, referred to Zanjani et al.,[24] emulsification and external gelation were
conducted on Bifidobacterium adolescentis ATCC 15703 with various types of starch coating and
about 6 log units reduction in viability was reported after storing at −20°C for100 days.
Coacervation
Coacervation is a simple and widely employed technique in microencapsulation. Coacervation
technique involves the development of immiscible phases while mixing core material, coating material
(for instance, differently charged polyelectrolytes, referred to Fig. 2) and continuous liquid phase
followed by the development of encapsulating layer around the probiotics by regulating several
parameters including pH, temperature, the proportion of coating materials and ionic strength,
followed by the solidification of microcapsules by employing desolvation, heating, or cross-linking
methods.[25] Depending on the number of polymers involved in the process coacervation can be
classified as simple coacervation (involves single biopolymer) and complex coacervation (involves two
or more biopolymer).[26]
Recently, optimal soy protein isolate (SPI) and ι-carrageenan (IC) complex coacervates were
designed for the encapsulation of B. longum. Mao et al.[27] mixed SPI and carrageenan with varied
proportion (10:1, 15:1, and 20:1) to make complex coacervates at gradient pH from 2.5 to 4.5.
Involving ratio of wall materials, pH setting, zeta-potential analysis, and equivalence point determina-
tion were the determining factor for selection of optimal proportion of SPI and carrageenan as well as
pH range for feasible microencapsulation. In order to obtain optimal microencapsulation effect, the
impact of pH on positive charges and negative charges of SPI and IC, was also primarily confirmed. In
addition, the exact mixing ratio of SPI and IC towards the strongest electrostatic interaction was
further studied. Therefore, pH<3.5 and the zeta-potential above 10 mV for all the mixtures were
reported to be best for the physical stability when the microencapsulated Bifidobacteria was applied to
the acidic environment. It was also revealed that the coacervates with lowest IC content (10:1)
exhibited the highest coacervate yield and entrapment efficiency. Most importantly, this coacervate
obtained the best efficacy of microencapsulation with a least loss in viability (by 1.62 log units)
compared to the unencapsulated one (by 2.58 log units) as well as the one with more IC ratio. It has
also been reported that the difficulty of coacervation lays in the production of capsules of small sizes
leading to less attention towards the production of probiotic-loaded microcapsules.[12]
Polymerization
Although no study has mentioned the application of polymerization for the microencapsulation of
strict anaerobes, however interfacial polymerization is another mechanism employed following the
emulsification step. Interfacial polymerization involves the presence of two monomers, one in oil
phase and the other in water phase, dissolved and dispersed separately. Microcapsules are formed due
to the thin polymeric film-forming at the interface between the two solutions.[28] Since chemical
Figure 2.
6 Y. CHEN ET AL.
reactions are generally involved in polymerization which may arise food safety concern thus it is not
suggested to be used in microencapsulation of anaerobic probiotics.
Drying techniques
Various drying techniques commonly used for the microencapsulation of Bifidobacterium are spray-
drying,[29] freeze-drying,[30] spray freeze-drying, spray-chilling[31] and electrospray drying .[32]
However, various drying techniques presented a positive or negative impact depending on the
processing principles.
Spray-drying
Among all drying techniques, spray-drying is the most popular drying technique. This technique is
economical, rapid, and also mentioned as flexible because of its ability to efficiently dispose heat to the
large amounts of liquid feed cultures in a relatively short time, meanwhile, its energy consumption is
also reported to be 6 to 10 times lower than that of freeze-drying.[11,33] Most importantly, under
continuous operation, the characteristics of powder particles can be managed easily for the uniform
spherical shape, size distribution, and even the residual moisture content while using spray
drying.[34,35]
Inevitably, spray-drying also presented few drawbacks especially the application of high tempera-
ture may reduce the viability of probiotics. Previously, it has been reported that during spray drying
the probiotics endure multiple stresses such as thermal stress, dehydration, atomization stress, osmotic
and oxidative stress.[36] Particularly, heat stress and dehydration were reported as the two dominant
factors that exhibit high impact on the viability of probiotics. Heat stress, in the form of high outlet
temperature, was mentioned as a critical parameter that affects the viability of probiotics.[33]
Freeze-drying
Considering the heat sensitivity of probiotics, freeze-drying is another widely employed technique that
is focused to remove the frozen solvent of feed solution via sublimation.[10] The high yield of
microencapsulated powder and high viability of probiotics was observed after freeze-drying compared
to the spray-drying. This improved performance due to freeze-drying is attributed to its mild
processing conditions. Whereas, the lower powder yield during spray-drying is mainly attributed to
the loss in the drier and cyclone separator.[37]
However, it was also reported that the ice crystal formed during freezing lead to damage of cell
membrane and osmotic stress that in turn lead to the inactivation of the probiotics.[11] The damage
caused by the freezing can be diminished by the addition of cryoprotectants such as skim milk powder,
whey protein and glucose. However, freeze-drying is much more time-consuming and expensive than
spray drying. It was mentioned that the different encapsulant materials exhibit a wide range of glass
transition temperature that determines the duration of initial drying stage from a few hours to even
several days.[26]
Spray freeze-drying
The spray freeze-drying is the combination of processing steps common to spray drying and freeze-
drying. Spray freeze-drying is an alternative drying technique conducted under sub-ambient condi-
tions and suitable for heat-sensitive probiotics. This technique is also reported to be four times less
time-consuming compared to the spray freeze-drying. Until now, no study has been carried out for the
microencapsulation of strictly anaerobic probiotics by using spray freeze-drying. However, spray
freeze-drying has been previously applied for the microencapsulation of bioactive compounds.[11]
Spray-chilling
Spray chilling involves the injection of cold air that enables the solidification of particles. In this
technique, fat matrices are mainly used as a carrier.[11] Recently, spray chilling was employed to
microencapsulate B. bifidum and similar survivability of probiotics under the simulated gastric system
was observed as in case of spray drying. However, better protection effect in simulated intestinal
environment and heat resistance test were presented by the microcapsules prepared by spray
drying.[38] Fig. 3 presents the processing steps involved in the spray-drying, spray-chilling, and
spray freeze-drying.
Wall materials for microencapsulation

The methods employed for the microencapsulation depend on the functionalities of polymers. In
addition, the molecular weight of each material significantly impacts the outcome of microcapsules. In
addition, external factors such as pH and temperature also play an important role in the development
of microcapsules. Table 1 presents the fundamental parameters such as molecular structure and
properties of polymers used for the microencapsulation of Bifidobacterium that need to be considered
during the selection of wall materials and microencapsulation methods.
Alginate
Alginate is one of the most popular polysaccharide materials used for microencapsulation and other
food applications. The extensive use of alginate in the food industry is attributed to its low cost,
biodegradability, good compatibility with various food systems, ease of gelation and coacervation.[19]
Although alginate is widely used for the microencapsulation of probiotics, it is not an ideal material
for the obligate anaerobes because the alginate hydrogel exhibit relatively large pores that allow the
penetration of oxygen, bile salts, or digestive enzymes into the microgels. That in turn lead to the
inactivation of entrapped anaerobes.[39] Alginate, a linear copolymer of D-mannuronic and
L-guluronic acids, is unstable at low pH condition.[11,40] Thus, the destruction of cell structures is
ascribed to the decomposition of alginate at low pH.[41] In order to overcome this drawback of
alginate, it is usually incorporated along with other materials or even added with antacid agent[20]
to further enhance the viability of probiotics under harsh environment.
Alginate-Chitosan
Calcium alginate gel is formed in the presence of Ca2+. Thus, the chelating agents of calcium ions such
as phosphates, acetates, lactates and citrates may lead to the deconstruction of calcium alginate
capsules.[11,24] Thereby, the semipermeable layers of chitosan coating around the negatively charged
calcium alginate capsules can enhance the physical and chemical stability of the capsules and protect
against the deteriorative effects of chelating agents of calcium ions. [42,43] Moreover, it was reported
that chitosan-coated alginate beads were capable to enhance the mucoadhesive properties of probiotic
bacteria that are beneficial for colonization of probiotics in the intestine.[19]
Figure 3.
8
Y. CHEN ET AL.
Table 1. Common wall materials employed for the microencapsulation for strict anaerobes.
Main func-
Wall tional
materials Source Monomer Methods groups Physicochemical and nutritional properties References
[26,76,77]
Alginate Brown algae or bacterial β-D-glucuronic and α-L-mannuronic acids Extrusion Carboxylic Physicochemical: Hydrophilic; GRAS (lack of toxicity); strong
sources (1→4) group capacity to be cross-linked and the different mild gelling
characteristic which change with the molecular weight and
ratio between M and G acids; with negative charge when
above its pKa (sensitive to acidic media leading to rapid
dissolution behavior in stomach conditions);
Nutritional: Regarded as essentially non-digestible in GI tract,
which can be classified as poorly fermentable soluble
fibres→ reduce the rate of small intestinal absorption of
nutrients thus reduce likelihood of cardiovascular diseases
and the onset of type II diabetes
Chitosan Shells of crustaceans, Glucosamine units (are able to polymerise Coating; Amine Physicochemical: A cationic polyelectrolyte with amine residues [12,78,79]
molluscs, cell walls of via cross-linking in presence of extrusion presents at a pKa around 6.5 and a positive charge in solution
fungi and the cuticle polyanions like sodium alginate of pH below than that; resistance to acidic media; capable to
of insects maintain the integrity and to reduce permeability of
microcapsules when used as a coating; inhibitory effect
against some bacteria;
Nutritional: Able to increase faecal fat excretion and even
accelerate weight loss when following a low calorie diet;
reduce serum cholesterol
[29,51,80,81]
Gum Arabic Acacia senegal and Galactose (~40%), arabinose (27%-46%), Coacervation Carboxylic Physicochemical: Molecular mass ranges from 380,000 to
acacia seyal rhamnose (4%-13%) and glucuronic acid group 850,000; readily soluble in water with a pH of about 4.5;
(6.5%-14.5%) reduction of the solution viscosity owing to charge screening
cause by its electrolyte property and undissociated carboxyl
groups at low pH; act as an emulsifier;
Nutritional: As a non-digestible fibre with prebiotic effects;
retard glucose absorption, increase stoll mass, and trap bile
acids etc.
(Continued)
Table 1. (Continued).
Main func-
Wall tional
[11,24]
Starches Corn, potato, rice α-D-glucose forming linear amylose and Emulsification Carboxylic
[11,44,82]
Resistant branched amylopectin Emulsification group The sum of starch and products of starch degradation products
starch not absorbed in the small intestine of healthy individual;
improve digestive and glycaemia health; as best substrates
for butyrate production; low water-binding capacity; help
probiotics with delivery to intestine via providing surface for
the adherence of the probiotic cells to the starch granules
[26,55]
Dextrins Spray drying Modified starches with various dextrose equivalent value;
(modified (Maillard water-soluble; dextrins with same DE values perform distinct
starches) reaction) functionalities based on various type of starch source
[26,29,30]
Maltodextrins Spray drying Dextrins with dextrose equivalent value below 20; higher DE
(MS) value of MD contributes to lower molecular weight and
higher solubility whilst more hydrophilic groups causing
higher moisture content of final product; capable to diminish
oxygen permeability of wall matrix;
[72,83]
Xanthan The bacterium β-D-glucose backbone with a trisaccharide Extrusion Carboxylic Anionic polyelectrolyte; with chitosan forming physically
Xanthomonas side chain (two mannose and one group crosslinked hydrogels with reversible ionic linkages
campestris glucuronic acid) on every other glucose
at C-3 (1 → 4)
[27,37,84]
Carrageenan Red seaweeds Galactose and 3,6-anhydrogalactose Coacervation; Sulfate High molecular weight linear polysaccharide (commercial

spray drying kappa-carrageenan extracts are between 400 and 560 kDa;
(Maillard soluble in hot water while only the sodium salts of kappa and
reaction) iota are soluble in cold water; solutions lose viscosity and gel
strength when heated in systems with pH values below
about 4.3 whilst kappa 2 and iota carrageenans do not
hydrolyse as rapidly and these materials tolerate acid
processing better; interacts with positively charged amino
acids in proteins
(Continued)
9
10
Y. CHEN ET AL.
Main func-
Wall tional
[81,85]
Gelatin Bovine, porcine, fish, Amino acids (Free α-chains, β-chains, γ- Coacervation Amino Physicochemical: All gelatins are derived from collagen, Type
poultry chains) groups A gelatins having more or less identical amino acid
compositions to their parent collagen thus with similar
average isoelectric point in the range 7–9.4 while Type B lack
many of the non-ionizable glutamine and asparagine
resigdues for conversion into carboxyl forms leading gelatins
to be more acidic thus with average isoelectric points
ranging from 4.8 to 5.5; with GRAS status and excellent
biocompatibility strict control of the viscosity of the gelatin
mass used for encapsulation is very important;
Nutritional: A high-quality source of protein, free of
cholesterol and sugar and contains practically no fat →
enrich protein content while reduce carbohydrates, salt
concentration and fat amount in low-fat products; as a carrier
for vitamins; may have a preventive and regenerative effect
on the skeleton and locomotor system
[26,37,86]
Soybean Soybean Amino acids Coacervation Amino Physicochemical: Ability to form gel, bind water, emulsify and
protein groups; work as surfactant;
Nutritional: Provide nutrient protection against oxidation; the
combination of soy protein isolate with polysaccharides as an
encapsulating material offers better protection, oxidative
stability and drying properties
[26,55]
Whey Milk Amino acids Coacervation; Amino Physicochemical: Excellent thermal gelling properties;
protein spray drying groups isoelectric point is pH at about 4.5; good emulsifying effect;
foaming properties;
Nutritional: Protective role against the development of tumor
in the GI tracts as well as selectively inhibition on cancer cell
growth
Chitosan is also a widely used polysaccharide wall material for microencapsulation of

Bifidobacterium. Various researchers have employed chitosan-coated alginate or chitosan as part of
coatings with alginate and other materials to provide better protection for certain probiotics.[19,24,32,44]
Alginate-Starch
Natural starch, resistant starch, and modified starch including dextrins and maltodextrins have also
been widely used for the microencapsulation. Different sources of starch have distinctive constituents
that contribute towards their distinct properties, for instance, Hylon maize starch exhibit high-
amylose content and demonstrate higher resistance against the high temperature and digestive
enzymes compared to the low-amylose starches such as rice or wheat starch.[24] Resistant starch,
a non-digestible starch provides great intestinal delivery feature along with an excellent adhering
surface for the probiotics.[11] Additionally, maltodextrin, a hydrolyzed starch incorporated with
alginate for the encapsulation of probiotics improve the emulsifying effects and reduce the oxygen
permeability.[26] Thereby, a uniform and homogenous complex can be produced by combining
alginate and starch from various sources that in turn contribute towards the enhanced viability of
probiotics during storage and while exposing to the harsh environment in GI tract.[24]
Alginate-milk (casein)
Another strategy to conquer the susceptibility of alginate microparticles towards the acidic conditions
is the incorporation of milk or milk-based matrix.[11] According to a recent study, milk proteins act as
a filler to seal the porous structure of alginate. The alginate-milk-based microcapsules provided better
protection to the microencapsulated bacterial cells. Also, the high buffering capacity of cow milk or
goat milk reported to protect the probiotics from the acidic environment of simulated gastric juice.[41]
Milk
Milk with buffering function has been regarded as an effective preservative agent for
probiotics through fabrication of protective film over the cell wall proteins of probiotics
and by stabilizing the membrane’s constituents. Thereby, bacterial strains are effectively
protected from the destructive effects of harsh GI condition. [45,46] Furthermore, another
possible underlying mechanism is the mutual interaction of denaturing whey proteins
when milk is above 60°C and associate with the casein micelles that form aggregates
through hydrophobic interactions and disulfide bonds that in turn lead to probiotics
entrapment. [47] Studies have also revealed that milk fat also protects the viability of
probiotics under the acidic environment. This protective effect of milk fat was attributed
to the low diffusion of hydrogen ion, organic acid and O 2 . [48,49]
A recent study also mentioned that B. longum 51A microencapsulated with skim milk by spray
drying as an ideal choice to ensure the viability and capability of probiotics under simulated gastric
and intestinal conditions compared to the microencapsulation of probiotics with alginate-chitosan or
alginate-resistant starch.[44] Another study encapsulated B. longum subsp. infantis CCUG 52486 with
milk from various sources and casein hydrolysate. This encapsulation reported to result in
a considerable protective effects to B. longum subsp. infantis CCUG 52486 in simulated gastric fluid
and storage.[41] Similar outcomes were also mentioned in another study where goat milk and full-fat
goat’s milk powder was used to encapsulate the B. animalis subsp. lactis BB-12 and Bifidobacterium
BB-12, respectively.[48,50]
Gum Arabic
Gum Arabic belongs to the plant exudates gums and widely employed for the microen-
capsulation of probiotics, generally in combination with maltodextrin, gelatin, and alginate
by using various techniques including extrusion, emulsion, coacervation, and spray-drying
12 Y. CHEN ET AL.
etc. For instance, recently alginate and gum Arabic were employed to fabricate the micro-
capsules of Bifidobacterium. Gum Arabic was coated as a second layer to protect the
alginate from disintegration at low pH and subsequent escape of encapsulated probiotics.
This study well demonstrates the antacid property of gum Arabic. [51]
Whey protein isolate or concentrate

A recent study found that the addition of whey protein concentrate (WPC) into wall material is an
efficient method for the protection of bacterial cells from the acidic environment.[52] The better
protective effects exhibited by WPC are attributed to its ability to create microenvironment within
the hydrocolloid matrix surrounding the bacteria. This ability was further ascribed to the existence of
lipids and lactose in the whey protein concentrate as well as to the specific amino acid residues present
in the whey protein.[53,54]
Whey proteins are typically used in the fabrication of complex coacervates or even for
the generation of Maillard reaction products along with several polysaccharides to further
give rise to encapsulation matrix. [26,52,55,56] It was also reported that the pre-heated and
cross-linked β-lactoglobulin provide better preservative effects for the anthocyanins against
the gastric digestion as compared to the untreated proteins. [57] This finding indicated that
the pre-heated proteins demonstrate better physical properties for the encapsulation sys-
tem. Additionally, the higher antioxidant activity of pre-heated protein [26] was also
reported as one of the reasons for better antioxidant capacities of Maillard reaction
products generated with whey protein as compared to the original whey protein. [55]
Soy protein isolates (SPI)

SPI present remarkable physicochemical characteristics such as gel formation, emulsification, fat
absorption, water-binding capacity, and nutrient barrier against oxidation.[26] As a plant protein,
soy proteins exhibit a great hydrophobic property compared to animal proteins such as whey proteins.
In addition, they are reported to present less risk of allergy and less expensive than the animal-derived
proteins.[58]
There are abundant applications of SPI for the encapsulation of bioactive compounds, and thus its
potential for the microencapsulation of probiotics can also be ensured. Commonly, SPI were incor-
porated into polysaccharides such as carrageenan[27,37] as encapsulants due to their electrostatic
interaction that provides a better barrier against the external stress factors such as acid, oxygen as
well as the drying properties.[26,59]
Other novel materials or applied ingredients

Goat milk
Recently, goat’s milk has gained the attention of researchers to be used as a wall material instead of cow
milk or casein for the microencapsulation of Bifidobacterium.[48,50,60] It was reported that the goat’s
milk fat globules are less than 4 μm in diameter. However, in case of cow milk the fat globules were
observed to be more than 4 μm in diameter.[61] In addition, aggregation of fat in goat’s milk fails to
occur due to the lack of agglutinin that acts as an aggregator for fat globules in cow’s milk.[62] Thus,
smaller microcapsules with higher retention ability and viability of probiotics were produced by using
the goat’s milk as a delivery vehicle. This process was reported to avoid the coalescence and
agglomeration of the spray-dried powder due to the generation of smaller microcapsules.[50]
Maillard reaction products (MRPs)

Maillard reaction, also known as a non-enzymatic browning reaction or glycosylation reaction,
occurs between the unprotonated amino group of a protein and a carbonyl group of reducing
sugar. The complexes produced by Maillard reaction have gained much attention notably for the
microencapsulation of bioactive compounds due to the good emulsifying properties[63,64] and
antioxidant capacities of MRPs.[65] The MRPs were also capable to improve the mechanical
strength of microparticles when subjected to various stressors such as acidic condition, high
temperature, and high ionic strength which further illustrates that the probiotics encapsulated
within MRPs can be more resistant to the gastric digestion.[63] Refer to the studies conducted by
Mao et al.[27,37] individually in 2018 and 2019, microcapsules involving MRPs exhibited better
protective effect than the one with complex coacervation of same materials SPI and IC. Mao
et al.[37] has explored the ratios of SPI: IC (1:3, 1:2, 1:1, 2:1 and 3:1) and drying time or degree
of graft during drying to evaluate the MRP system revealing that microcapsules with a SPI: IC
ratio of 1:3 and 6 h dry heating after spray drying played the best protective role during storage
and significantly enhanced the viability of the bacteria (1.61 log units reduction) compared to the
free cells (5.58 log units reduction) in simulated gastric fluid.[37] Ratios of involved constituents
and condition of the drying technique were revealed to ultimately impact the protective effect of
MRPs system in this study.
In addition, whey protein isolate/dextrans conjugated systems obtained by Maillard reaction
were employed as a wall material to encapsulate B. animalis subsp. lactis INL1 that results in 0.5
to 2.5 log units of increase in the viability compared to the relatively naked one along with the
improved stability of microcapsules during the storage.[55] Loyeau et al.[55] employed dextrans
with various molecular weights (6, 70, and 450 kDa) to perform Maillard reaction with whey
protein isolate finding that M-WPI/DX 6 exhibited the best antioxidant capacity and compre-
hensively considered to be the best system for microencapsulation in that study. Additionally,
a previous study has also demonstrated that MRPs had prebiotic feature since they were not as
easy to be digested as those of unglycated proteins in the small intestine. Thus, present more
available dietary glycoconjugates for fermentation by the gut microbiota in the distal colon.[66]
Thus, based on the reported studies MRPs can be used as a potential wall material to encapsulate
the anaerobic probiotic microbes.
Agarose
Agarose is a structural polysaccharide present in various species of red seaweed. Its gel-forming ability,
high oxygen barrier properties, and other unexplored potentials allow it to be a good alternative for the
encapsulation material.[52]
Polyamino acids: poly-L-lysine (PLL)

Similar to the chitosan, PLL also forms a strong complex with the alginate hydrogels.[11] Until now, the
study on PLL as microencapsulating material is limited. A recent study mentioned the alginate-PLL -
starch complex but it has not explored the stability of this complex under simulated GI tract. Thus, it is
difficult to spell about its antacid property.[24] It was also revealed that the effect of PLL and chitosan
coating on alginate was insignificantly different. However, PLL was reported to form unstable
polyelectrolyte complexes with alginate whereas it exhibits higher binding capability towards alginate
compared to the chitosan. On the other hand, the chitosan is reported to exhibit higher binding
enthalpy than the PLL while binding to alginate. Thus, chitosan and alginate result in an extremely
stable complexes.[67]
Extracts from plant-based materials: mucilage and soluble protein

Recently, extracts from chia seed and flaxseed has also been used as materials for microencapsulation
of Bifidobacterium.[30] Another study reported the use of cress seed mucilage combined with sodium
alginate microcapsules for the encapsulation of curcumin.[68]
14 Y. CHEN ET AL.
Vegetal BM 297 ATO

Vegetal BM 297 ATO is a glyceryl distearate generated from vegetables. Vegetal is reported as safe for
human consumption and also used as a dietary supplement. Recently, Vegetal BM 297 ATO, a food-
grade lipid-based material extracted from vegetables, along with the poly-vinyl-alcohol, lactose and
inulin were used for the microencapsulation of B. longum LMG 13197 by emulsion.[69] However, until
now, no other study has been reported to analyze the effect of Vegetal BM 297 ATO as a potential
material for microencapsulation. Table 2 summarizes various techniques, materials, probiotics
employed for microencapsulation along with the efficiency of microencapsulation, particle size, and
shape of microcapsules, viability of probiotics during storage and their GI stability.
Materials with antioxidant property and their application

Bifidobacterium and most of the other novel probiotics like Akkermansia muciniphila are obligate
anaerobes, extremely susceptible to oxygen. Thus, the oxygen barrier or antioxygen feature of the wall
materials is a prime requirement for the microencapsulation of these probiotics. Table 3 demonstrates
the techniques and materials used for microencapsulation of A. muciniphila along with the particle
size/shape of microcapsule, viability of A. muciniphila during storage, and GI stability. Some of the
recent studies have also explored the anti-oxygen property of various materials such as whey protein
concentration and isolates, [52,55] SPI, [27] MRPs, [37,55] inulin, [48,50,51] agarose[52] and ascorbic acid[21]
while microencapsulation of Bifidobacterium. Interestingly, antioxidant capacity of the whey protein
isolate-dextrans conjugates (M-WPI/DX) obtained by Maillard reaction were determined in
a previous study[70] and the results showed that molecular weight of dextrans exerted significant effect
on both antioxidant capacity of system and viability of the target probiotics. As previously mentioned,
M-WPI/DX 6 (MW of DX is 6 kDa) with the best antioxidant capacity could be the most stable
microencapsulation system. However, it was also pointed out that the lower probiotic viability at room
temperature could be attributed to the higher rate fatty acids oxidation in bacteria’s cell membrane.
This phenomenon failed to be associated with the analysis of antioxidant capacity of the microcapsule
system, which is suggested to be improved in further study. Furthermore, no study has explored and
compared the oxygen permeability among these encapsulants while microencapsulating the anaerobic
probiotics except for a single study that was focused on the microencapsulation of bioactive
substances.[71]
Viability during storage

Viability of probiotics during storage depends on various factors such as microencapsulating techni-
ques based on various processing principles,[9,48,50,52] property of selected material,[20,24,37,41,44,55]
proportion of added materials,[27,37,48] temperature, and time of storage condition[9,37,50] and even
the strain of probiotics.[29]
Generally, at the same storage condition, the viabilities of different Bifidobacterium strains in
microcapsules produced by employing different materials and techniques are insignificantly different.
The storage conditions were found to be milder towards the viability of probiotics compared to the
gastric acid or high-temperature environment. The reduction in viabilities of probiotics was found to
be in an acceptable range of about 1 to 2 logs.[5,9,44,50,72]
Notwithstanding that the viability of probiotics has always been addressed to produce health
benefits, a new terminology named “para-probiotics” or “inactivated probiotic cells” has come into
sight and become popular in recent years. Para-probiotics refers to the use of inactivated microbial
cells or cell fractions to provide health benefits to the consumer.[73] This topic is attractive because the
growth condition of strictly anaerobic probiotics is difficult to handle especially due to oxygen
sensitivity. If para-probiotics can be verified for exerting equal health benefits as the probiotics, the
viability will no longer be a significant question.
Table 2. Recent studies related to the microencapsulation of Bifidobacterium.
Techniques or methods Materials Probiotics Microencapsulation Particle size/shape Viability (log CFU/g) during GI stability References
efficiency (%) (μm) storage
[69]
Double emulsion and freeze Vegetal BM 297 Bifidobacterium 88% Not mentioned Storage in yogurt- In SGF (simulated gastric
drying ATO (food longum LMG 13197 unencapsulated cells: 2.70 fluid):7.16 → 6.95 log CFU/
grade lipid- log unit reduction in mL (30 min) →7.30 log CFU/
based viability; encapsulated cells: mL (2 h); in SIF (simulated
material)) 0.9 log units increase intestinal fluid): about 8 log
CFU/mL within 6 h
Vegetal BM 297 82% 1.9 log units increase for In SGF: 5.93→ 5.87 log CFU/
ATO-inulin encapsulated cells mL (30 min) → 6.43 log
CFU/mL (2 h); in SIF:
continuous release of cells
above 6 log CFU/mL (about
8 log CFU/mL) within 6 h
[9]
Emulsification-internal Sodium alginate, Bifidobacterium BB-12 Ranged from 80% 77.84 ± 0.54 25°C: 8.36 ± 0.10 → Initial→ stomach (pH = 2,
gelation and freeze CaCO3, to 98% 7.88 ± 0.05 (60 d) → 90 min) →duodenum
drying rapeseed oil 2.10 ± 0.01 (120 d); 7 °C: (pH = 5, 110 min) →ileum
8.99 ± 0.04 → 8.31 ± 0.25 (pH = 6.5, 200 min)
(60 d) → 7.32 ± 0.12 (120 Free cells (log CFU/g): 14.53
d); → 11.49 → 11.32 → 9.07;
-18°C: 8.90 ± 0.05 → Encapsulated (log CFU/g):
9.14 ± 0.06 (60 d) → 11.91 → 2.54 → 7.07 →
7.319 ± 0.06 (120 d) 11.13
[44]
Emulsification Alginate- Bifidobacterium Not mentioned Not mentioned −20°C: 8.22 ± 0.05 → Not mentioned

chitosan; longum 51A 7.88 ± 0.17 (7 d) →
8.22 ± 0.11 (90 d);
Emulsification Alginate- Not mentioned −20°C: 9.42 ± 0.16 →
resistant 8.02 ± 0.27 (7 d) →
starch 7.87 ± 0.29 (90 d);
Spray drying Skim milk Polydisperse −20°C: 7.93 ± 0.35→
spheres with 7.83 ± 0.45 (7 d) →
sizes ranging 7.51 ± 0.25 (90 d);
from150 nm to
350 nm
(Continued)
15
16
Y. CHEN ET AL.
[24]
Emulsification-external Alginate Bifidobacterium 96.71 73 ± 4.47 −20 °C: 11→ 9.5 (20 d) → 5 Not mentioned
gelation; coating (various adolescentis ATCC (100 d)
types of starch & Alginate-wheat 15703 97.02 91 ± 3.21 −20 °C: 11.5 →10.5 (20 d)
chitosan/poly-L-lysine) starch- →7.5 (100 d)
chitosan
coating
Alginate-rice 98.23 95 ± 2.54 −20 °C: 11.5→ 9.5 (20d) → 6
starch- (100d)
chitosan
coating
Alginate-Hylon 97.42 94 ± 2.08 −20 °C: 11.5 →9.7 (20d) → 6
starch- (100d)
chitosan
coating
Alginate-wheat 97.36 95 ± 1.83 −20 °C: 11.5 →10.5 (20d)
starch-poly →7.3 (100d)
-L-lysine
coating
Alginate-rice 99.19 98 ± 2.43 −20 °C: 11.5 →9.3 (20d) → 6
starch-poly (100d)
-L-lysine
coating
Alginate-Hylon 96.93 92 ± 1.09 −20 °C: 11.5 → 9.7 (20d) → 6
starch-poly (100d)
-L-lysine
coating
[52]
Encapsulation and Agarose-whey Bifidobacterium Not mentioned Not mentioned 7 ~ 8 log CFU/mL before freeze Initial: 7.5 → SGF: 6.7→ SIF:
subsequent freeze drying protein pseudocatenulatum drying; 25 °C (35d): 2.8 log 6.5 (log CFU/g)
; oil-induced biphasic concentrate CECT 7765 units of reduction; 4 °C: less
hydrogel; particle than 1 log reduction
formation (precipitate of Agarose-alginate 7 ~ 8 log CFU/mL before freeze Not mentioned
agarose-based drying; 4 °C:1 ~ 2 log units
biopolymeric aqueous of reduction
solutions into a biphasic Agarose-gelatin 7 ~ 8 log CFU/mL before freeze Initial: 7.9 → SGF: 5.7→ SIF:
oil) drying; 25 °C (35d): 4 ~ 5 log ~4.0 (log CFU/g)
units of reduction; 4 °C:
3 ~ 4 log units of reduction
(Continued)
[37]
Freeze dried/spray dried Soy protein Bifidobacterium Not mentioned Spray dried 4 °C for 30 days: MRP microcapsules: SGF
isolate and longum powder: Spray-dried: 9.21 Log CFU/ (60 min):1.61 log units
I-carrageenan a cavity-like ml; freeze-dried: 9.00 Log reduction;
were spray- structure of CFU/ml Free cells:
dried to get MRP; SGF for 60 min: 5.58 log
Maillard Freeze dried units reduction
Reaction powder: the
Products flake-like
(MRP) structure of MRP
[30]
Spray drying Maltodextrin Bifidobacterium Not mentioned Not mentioned 9.86 (1 d) → 9.90 (45 d) 1.7 (2 h incubation in SGF)
Maltodextrin, infantis 9.47 (1 d) → 9.95 (45 d) Not mentioned
chia seed
mucilage
Maltodextrin, 10.87 (1 d) →10.44(45 d) Not mentioned
chia seed
mucilage and
chia seed
soluble
protein
Maltodextrin, 9.80 (1 d) →9.87(45 d) 4.8 (4 h incubation in SGF)
flaxseed
mucilage
Maltodextrin, 11.08 (1 d) →10.56(45 d) 6.7(6 h incubation in SGF)
flaxseed
mucilage and
flaxseed
soluble
protein
[55]

Spray drying Whey protein Bifidobacterium Not mentioned Not mentioned 8.27 ± 0.5 ~ 8.80 ± 0.5 After 90 min of simulated
isolate and animalis subsp. gastric digestion: 6.50
dextrans (DX lactis INL1
of 6, 70 and
450 kDa)
conjugates
obtained by
Maillard
reaction;
[29]
Spray drying Gum Arabic, Bifidobacterium Bb-12 74.31 to 79.73 (110° 8.75 8.38 ± 0.12 5.53 ± 0.06 (Esophagus/
maltodextrin, C-140°C) stomach 90 min/pH 2.0);
glycerol, 6.34 ± 0.06 (Ileum 90 min/
tween80 as pH 7.5)
feed solution;
(Continued)
17
18
Y. CHEN ET AL.
[48]
Spray drying Alginate, goat Bifidobacterium 87–91 (inulin at 279 ~ 341 9.44 ± 0.11 ~ 9.49 ± 0.08 8.11 ± 0.11 ~ 8.54 ± 0.06 (in
milk and animalis subsp. levels of 0, 0.5, 1, pH = 2 SGJ for 1 h);
inulin; lactis BB-12 1.5 and 2%) 8.07 ± 0.03 ~ 8.44 ± 0.10
(for 2 h)
[50]
Spray drying Full-fat goat’s Bifidobacterium BB-12 Not mentioned 2.01 ~ 19.10 Feed solutions: 9.22 ± 0.06; Not mentioned
milk powder Spray dried powders:
8.69 ± 0.02 → 8.2 (stored at
4°C for 120 days)
Full-fat goat’s 2.01 ~ 19.50 Feed solutions: 9.11 ± 0.20;
and inulin 8.58 ± 0.13→ 8.3 (stored at
4°C for 120 days)
and 8.13 ± 0.16 → 7.6 (stored at
oligofructose 4°C for 120 days)
milk powder, Spray dried powders:
inulin and 7.98 ± 0.05→ 7.8 (stored at
oligofructose 4°C for 120 days)
[87]
Spray drying Skim goat’s milk Bifidobacterium ~87% Not mentioned At 4 °C for 20–60 days: ~9.50 Not mentioned
or inulin animalis subsp. log CFU/g to ~9.30 log CFU/
added skim lactis BB-12 g; at 25 °C for 20–60 days:
goat’s milk ~9.50 log CFU/g to ~6.25
concentrate log CFU/g
[31]
Spray chilling Molten cocoa Bifidobacterium Not mentioned 44.4 (ranged from 7.4 ± 0.1 7.0 (in simulated gastric fluid
butter; animalis subsp. 1.6 to 126.9); for 2 h)
lactis spherical in
shape and with
irregular and
wrinkled walls
of the particles
(Continued)
[19]
Extrusion-external gelation Alginate; Bifidobacterium Not mentioned 135 to 185 for Extended cell viability of Not mentioned
CaCl2 longum (subsp. encapsulated B. infantis UMA 299 and 300
longum- UMA306, B. infantis; 149 by a few days; extended
318, 401, 402 & to 216 for viability of B. longum UMA
infantis- UMA298, encapsulated 401 cells by a week
299, 300, 305) B. longum
Extrusion-external gelation; Alginate beads Bifidobacterium Not mentioned 191 to 292 Only B. longum UMA 402 cells 8.40 ± 0.84 (in pH = 2.57
coating (CaCl2); longum (subsp. in chitosan-coated alginate gastric juice 0 h); 6.90 ± 0.04
chitosan longum- UMA401, bead with 2.4 log CFU (in pH = 2.57 gastric juice
402 & infantis- reduction higher than the 5 min)
UMA299, 300) naked (3–4 log CFU
reduction) and uncoated
one (7.2 log CFU reduction)
[72]
Extrusion; coacervation Xanthan- Bifidobacterium Encapsulation yield: Not mentioned Storage stability in yogurt at 4 In SGF (pH = 1.2) for 2 h: ~4.91
chitosan bifidum BB01 92.46 ± 0.03 °C for 21 days: 8.53 log CFU/ log reduction (to ~ 5.6 log
mL to 7.57 log CFU/mL CFU/g)
Xanthan- Bifidobacterium Encapsulation yield: Not mentioned Storage stability in yogurt at 4 In SGF (pH = 1.2) for 2 h: 3.77
chitosan- bifidum BB01 77.7 ± 0.02 °C for 21 days: 8.60 log CFU/ log reduction (to ~ 7 log
xanthan mL to 7.37 log CFU/mL CFU/g)
[41]
Extrusion; coacervation Sodium alginate- Bifidobacterium 94.9 ± 1.4 2.8 ± 0.3 mm 8.50 ~ 9.00 6.37 in SGJ (pH = 2) at 37°C for
cow milk; longum subsp. 2h
Sodium alginate- infantis CCUG 95.3 ± 1.6 3.1 ± 0.2 mm 8.50 ~ 9.00 5.19 in SGJ (pH = 2) at 37°C for
goat milk 52486 2h
Sodium alginate- 94.1 ± 2.7 2.4 ± 0.4 mm 8.50 ~ 9.00 4.00 in SGJ (pH = 2) at 37°C for
casein 2h
hydrolysate
[20]
Extrusion-external gelation Alginate solution Bifidobacterium Not mentioned 665 ± 8 Not mentioned 2 h gastric digestion: 1.0 log
containing pseudocatenulatum unit reduction in the

CaCO3; CaCl2 G7 number of viable bacteria
Alginate solution 540 ± 20 Not mentioned 2 h gastric digestion: a 1.5 log
containing Mg units reduction in the
(OH)2; CaCl2 number of viable bacteria
[51]
Extrusion and coating Gum Arabic, Bifidobacterium 92% Not mentioned; Not mentioned At stomach condition after 2 h,
alginate and bifidum, the mean the survivability was 88.29%
PLGA Bifidobacterium particle size of the initial population.
multiparticle animalis, and diameter for the
with inulin; Bifidobacterium produced inulin
lactis PLGA
nanoparticles
was
115.8 ± 82.7 nm
(Continued)
19
20
Y. CHEN ET AL.
[88]
Extrusion and coating; Sodium alginate Bifidobacterium from 80.33 to 1.21–1.72 mm At 4°C for 8 to 32 days: In pH = 2 SGJ for 1–3 h: 9.90 to
freeze-drying and zein bifidum 94.56% 9.69 ~ 10.02 log CFU/g 7.99 log CFU/g (minimum
(1,3,5,7, or 9% shifted to 6.01 ~ 8.28 log log reduction with 9% (w/v)
(w/v) coating) CFU/g after 32 days storage; zein coating); In bile salt
contained the one with 7% (w/v) zein solution for 1–4 h: 10.12 to
CaCl2 solution resulted in only 1.5 log units 8.56 log CFU/g (minimum
reduction log reduction with 7% (w/v)
zein coating)
[21]
Extrusion- external gelation Sodium alginate Bifidobacterium Not mentioned 1.7 ± 0.1 mm Stored in milk for six weeks at In pH = 2 SGJ for 2 h → in
and CaCl2 animalis subsp. about 6 °C: 0.4–0.6 log units pH = 6.8 simulated ileum
(addition of lactis Bb12 reduction (Free Bb12: 1.5–2 condition (ox bile and
inulin/ log units reduction) pancreatin) for 4 h: 0.9 ~ 2.8
ascorbic acid) log cycles reduction
Emulsion Reconstituted 204 ± 18 Stored in milk for six weeks at
skimmed milk, about 6 °C: 0.1–0.6 log units
rennet, CaCl2, reduction (Free Bb12: 1.5–2
sunflower oil log units reduction)
and soya
lecithin
(addition of
inulin/
ascorbic acid)
[81]
Coacervation; freeze drying Gelatin and gum Bifidobacterium lactis 86.04% (dry 203.32 (dry −18°C: 12.51 ± 0.10 → 10.67 ± 0.56 (Initial) →
Arabic microcapsules) microcapsules) 12.46 ± 0.15 (30d) → 8.94 ± 0.06 (Stomach) →
11.14 ± 0.07 (60d) → 8.76 ± 0.01 (Duodenum) →
6.60 ± 0.13 (120d); 7°C: 8.75 ± 0.05 (Ileum)
12.51 ± 0.10 → 10.84 ± 0.04
(30d) → 10.08 ± 0.08 (60d)
→ 6.42 ± 0.03 (120d); 25°C:
12.51 ± 0.10 → 12.08 ± 0.05
(30d) → 11.22 ± 0.14 (60d)
→ 3.67 ± 0.05 (120d);
[27]
Coacervation; freeze drying Soy protein Bifidobacterium Ranged from 20% Not mentioned 4°C: 7 (1d) → 6.8 (3d) → 6.0 SGF 60 min: 7 → 4.3; SIF
isolate and longum to 75% with (7d) → 5.7 (15d) →5.5 (30d) 60 min: 7 →3.5; Free cells:
carrageenan different ratios of 8.5 → 2.8 in SGF 60 min
complex SPI and IC at pH
from 2.5 to 4.5
(Continued)
[32]
Electrostatic spraying, Chitosan-coated Bifidobacterium (strain Not mentioned 200 7.87 log CFU/ml 7.61 log CFU/ml (in pH = 2.5
coating alginate name: TR17) gastric acid for 1 h); 7.51 log
microcapsule CFU/ml (in gastric acid for
loaded with 2 h)
in situ
synthesized
barium
sulfate;

21
22
Y. CHEN ET AL.
Table 3. Encapsulation of akkermansia muciniphila/faecalibacterium prausnitzii and related parameters and outcomes.
Techniques Microencapsulation Particle size/ Viability (log CFU/g) during
or methods Materials Probiotics efficiency (%) shape (μm) storage GI stability References
Double Sunflower oil, sodium caseinate and Akkermansia 97.5 24–25 Not mentioned 2 h: 6.6% survival compared to 0.4% of [89]
emulsion polyglycerol polyricinoleate muciniphila controlled group;
(PGPR) as emulsifier
[5]
Freeze Xanthan and gellan gum (XG); Akkermansia 64.3 ± 1.3 2.5 ± 0.2 mm Initial: 9.19 ± 0.08 Initial: 9.92 ± 0.08
drying cryoprotectant: sucrose & muciniphila 4 °C (Anaerobic storage): After stomach (pH = 2): 7.91 ± 0.06
trehalose 8.72 ± 0.34 (15 d) → After ileum (pH: 6.8–7.2): 7.06 ± 0.05
8.62 ± 0.03 (30 d)
25 °C (Anaerobic storage):
5.63 ± 0.12 (15 d) →
5.13 ± 0.19 (30 d)
XG; cryoprotectant: agrave syrup 76.2 ± 4.2 2.4 ± 0.3 mm Initial: 9.20 ± 0.02
8.97 ± 0.06 (15 d) →
8.36 ± 0.09 (30 d)
7.21 ± 0.09 (15 d) →
4.63 ± 0.09 (30 d)
XG; cryoprotectant: peptone & 12.1 ± 2.7 2.2 ± 0.2 mm Not mentioned
sorbitol
XG; cryoprotectant: skim milk, 68.2 ± 1.2 2.2 ± 0.2 mm Not mentioned
glucose, yeast extract; mannitol
[90]
Extrusion- Amidated low-methoxyl pectin Faecalibacterium Not mentioned Not 25 °C for 14 days: 3–5 log units of reduction when
ionic (ALMP) CaCl2 prausnitzii mentioned 9.9 ± 0.04 log CFU/mL → exposed to the stomach proximal
gelation 7.6 ± 0.66 log CFU/mL jejunum buffers for 30 min
Lipid based Gelucire® 43/01; gelatin capsules 25 °C for 14 days: 2 log units of reduction when exposed
coating 9.9 ± 0.03 log CFU/mL → to the stomach proximal jejunum
5.5 ± 0.03 log CFU/mL buffers for 30 min
Stability in gastrointestinal conditions

Microencapsulation of probiotics protects the probiotic bacteria from the harsh GI conditions.
Stability of the probiotics through the GI tract may be affected by various factors and most of them
are similar to factors that affect the viability of probiotics during storage. However, in this case, the
most critical point is to ensure the ability of encapsulants to resist the acidic conditions. It was reported
that even the microcapsules produced from a variety of materials with same technique present
different responses towards the stressors and the same was observed when alginate along with the
dairy-based material such as cow milk, goat milk and casein hydrolysates was used for encapsulation of
B. longum subsp. infantis CCUG 52486.[41] In that study, the microcapsules obtained by extrusion
were exposed to simulated gastric juice (pH = 2) at 37°C for two-hours acid-resistant test. The
probiotics encapsulated with alginate-cow milk demonstrated highest viability (6.37 log CFU/mL)
while those entrapped with alginate-casein hydrolysates showed the lowest viability (4.00 log CFU/
mL). Similar results were also found under refrigerated storage.
Recently, a ternary blend of chia seed mucilage, flaxseed mucilage, and flaxseed soluble protein was
used to encapsulate B. infantis. About 0.5 log reduction in the viability of probiotics were reported
during storage in the case of maltodextrin-flaxseed-mucilage encapsulated and maltodextrin-flaxseed
and soluble protein encapsulated probiotics. Nevertheless, probiotics encapsulated without flaxseed
soluble protein presented significant decreases in the survival rate of probiotics when exposed to
simulated gastric fluid.[30] Overall, most of the encapsulation methods result in an increase in the
viability of probiotics compared to the unencapsulated probiotics. However, proper selection of
materials can further enhance the viability of probiotics through harsh GI condition.
Table 4 indicates that even if microencapsulation provides ideal preservation for anaerobic pro-
biotics, certain dietary factors can further boom their colonization in gut. Therefore, it is worthwhile to
combine these beneficial dietary factors like prebiotic oligosaccharides and polyphenols with anaero-
bic probiotics to improve the quality of the core materials of microencapsulation so that the formula-
tion can be widely accepted by the people.
The tables and information above provide the essential basis to develop a better microencapsulation
strategy for strictly anaerobic probiotics. Comprehensively, the information in tables will help to select
and decide future microencapsulation paradigms for the anaerobic probiotics with expected results as
shown in Fig. 4.
Even though in the emerging field of para-probiotics, microencapsulation play an important role to
ensure the stability of bioactive compounds associated with these inactivated probiotic cells in GI tract.
Although only few articles mentioned microencapsulation of para-probiotics but no study has been
reported the microencapsulation of anaerobic para-probiotics. However, the microencapsulation of
para-probiotics is of prime importance especially during its delivery through GI tract as the external
stress may degrade bioactive compounds of para-probiotics.
Food matrices and encapsulated probiotics

The microencapsulated Bifidobacterium and other strict anaerobes are suggested to consume in the
form of fortified foods such as yogurt, ice cream, and chocolates. Yogurt is an ideal food vehicle for
microencapsulated probiotics because yogurt itself is a widely consumed food item and cherished by
the consumers of every age for its palatable taste and nutritional value. Therefore, many of the
researchers have enriched the yogurt with microencapsulated Bifidobacterium.
Recently, emulsification and extrusion along with gelification were applied to entrap the
Bifidobacterium, and then these microencapsulated probiotics added into yogurt followed by sensory
evaluation and determination of change in pH or acidity levels of yogurt.[72,74] Researchers have
reported the drop in pH of yoghurt after the addition of unencapsulated cells that was owed to the
continuous release of acids by Bifidobacteria cells, while the matrices of microencapsulation signifi-
cantly reduce the alterations in acidity of yoghurt.[74] On the other hand, microcapsules were also
24
Table 4. Growth conditions (dietary factors) of various anaerobic probiotics and their effects on colonic metabolism.
Y. CHEN ET AL.
Anaerobic probiotics Growth condition Dietary factors Functions on Colonic Metabolism References
Bifidobacteria longum, Anaerobic bacteria; tolerance of Bifidobacterium Most Bifidobacterium species metabolize a wide Various functions carried out by bifidobacteria [91–93]
B. adolescentis, to acidic stomach conditions and bile is range of indigestible polysaccharides and genus involve production of nutrients like
B. pseudocatenulatum, strain specific. B. longum show the greatest oligosaccharides to acetic and lactic acids. vitamins B, antioxidants, and polyphenol,
B. infantis, B. animalis subsp. survival while in pH from 1.5 to 3.0 while Raffinose, stachyose, fructo-, isomalto- blocking the adhesion of pathogens to the
lactis, B. bifidum, B. longum B. adolescentis and B. breve survive poorly at galacto-oligosaccharides are effective for intestinal mucosa, and preservation of
subsp. infantis, pH levels (1.5 to 3.0) proliferation or resident or implanted immune homeostasis during life etc., while
bifidobacteria. they are strain-specific. One of the important
functions of bifidobacteria genus
contributing to gut homeostasis is the
production of acetate and lactate during
carbohydrate fermentation, organic acids
that can be further converted into butyrate
by other colon bacteria through cross-
feeding interactions.
[92,94–96]
Akkermansia muciniphila Strict anaerobes; mucin is used as the source of Polyphenols or polyphenol-rich foods such as As an abundant colonizer of the intestinal
carbon, nitrogen, and energy required for cranberry, lingonberry, non-absorbable mucus layer with a proficiency to degrade
growth. It inhabits the surface of the apple procyanidins, and grape polyphenols mucin, an important mediator of the gut
intestinal epithelium coated with mucin for (resveratrol significantly reduced the barrier function, A. muciniphila capable to
protection and maintenance of gut barrier A. muciniphila levels in mice) – the bloom of trigger a trophic mucin cross-feeding
functions and immune response. A. muciniphila caused by polyphenols cascade so that the overall equilibrium of the
depends on the baseline level gut bionetwork can be sustained via this
In addition, intake of fermented and keystone species. In addition, gut
unfermented herbal medicine such as Flos permeability can be reduced so that the
Lonicera, Rhizoma Atractylodis fortification of the enterocyte monolayer
Macrocephalae, Agumiel could lead to an integrity which is further reinforced by the
increase of A. muciniphila abundance in the production of short-chain fatty acids and
gut and it is widely reported that dietary extracellular vesicles.
fibers especially prebiotic fibers like
oligofructose boost the abundance of
probiotics
[94,97]
Faecalibaterium prausnitzii Strict anaerobes; higher population in the Inulin-type fructans, fructo-oligosaccharides, The metabolism of colonic bacteria depends
proximal colon than in the terminal ileum; polydextrose or soluble corn fiber largely on fibers that are not digested by
able to survive in the adjacent mucosa where supplementation and raffinose can lead to human enzymes in the upper
there is an oxygen influx from the gut increase abundance. gastrointestinal tract, work with fiber -free
epithelium; can grow on the host-derived and fiber-supplemented liquid diets found
sugar N-acetylglusamine, D-glucosamine and that F. prausnitzii populations and fecal
D-glucuronic acid. butyrate correlate with the fiber input.
Figure 4.
responsible to protect the probiotics from the adverse impacts imposed due to reduced pH.[72] The
viscosity of yogurt may also be affected by its acidity because of the fabrication of tiny sub-colloidal
molecular groups from the casein molecules, likely to further aggregate to form a network of hydrated
proteins leading to attain a peak viscosity, under acidic conditions.[75] Thus, these studies very well
described the ability of microencapsulation of Bifidobacterium to controls the pH of yogurt.
Ice cream is another commonly used functional food. Zanjani et al.[24] used alginate, starches from
various sources and chitosan or poly-L-lysine to microencapsulate B. adolescentis followed by the
addition of probiotics to the ice cream. After the addition of microencapsulated B. adolescentis, no
change was observed in the texture of ice cream. This may be due to the small size of capsules
produced via emulsification method.[24]
The microencapsulation of probiotics imposes a positive impact on the food matrices especially
dairy food. However, the selection of capsular materials may affect the interactions of microcapsules
and food matrices that can further influence the organoleptic properties of food. Therefore, the
alterations of the micro-structure of food matrices after incorporation of microcapsules with
Bifidobacterium is advised to be evaluated.
Conclusions
The most of encapsulating techniques and materials explored in literature are reported to provide
considerable protection to the anaerobic probiotics Bifidobacterium, Akkermansia muciniphila, and
Faecalibacterium prausnitzii. Pros and cons of various methods have been reviewed and presented in
terms of survival of encapsulated probiotics, however, limited studies are available regarding the
oxygen permeability of the microparticles which is of prime importance in case of strictly anaerobic
probiotics. Whereas, the addition of antioxidants in the encapsulating materials indeed helps to
increase the viability of cells. In order to seek out the optimal encapsulation methods for strictly
anaerobic probiotics, apart from considering the viability of probiotics under different storage con-
ditions and through the GI conditions, oxygen permeability is also an important parameter to be
considered.
Some of the studies have also focused on the incorporation of microencapsulated probiotics into
the food matrix, while the studies related to the change in the structure of the food matrix and
microcapsules are not available. Thus, more studies are suggested to be carried out related to the
molecular and structural changes in the final product after the addition of probiotics
microcapsules.
26 Y. CHEN ET AL.
Extensive research is advised to be carried out on the survival of strictly anaerobic probiotics
through GI conditions as well as during anaerobic and aerobic storage. The characteristics of each
specific strain of probiotics under these conditions are suggested to be explored along with the
physicochemical properties of wall matrixes such as oxygen permeability.
Acknowledgments
This project is jointly supported by one grant (project code: UIC201914) from Beijing Normal University-Hong Kong
Baptist University United International College and one research grant from Guangdong Education Bureau (Project
code: R5201911).
ORCID
Xu Baojun http://orcid.org/0000-0003-0739-3735
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Food Reviews International

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A Narrative Review on Microencapsulation of

Yining Chen , Maninder Meenu & Xu Baojun

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Principles and methods for microencapsulation

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