Received: 24 November 2020
Revised: 21 February 2021
Accepted: 22 February 2021
DOI: 10.1002/btpr.3138
REVIEW
Yeast cells for encapsulation of bioactive compounds in food
products: A review
Elahe Dadkhodazade1 | Elham Khanniri1 | Nasim Khorshidian2
|
3
4
Seyede Marziyeh Hosseini | Amir M. Mortazavian | Ehsan Moghaddas Kia5
1
Student Research Committee, Department of
Food Science and Technology, National
Nutrition and Food Technology Research
Institute, Faculty of Nutrition Sciences and
Food Technology, Shahid Beheshti University
of Medical Sciences, Tehran, Iran
Abstract
Nowadays bioactive compounds have gained great attention in food and drug industries owing to their health aspects as well as antimicrobial and antioxidant attributes.
Nevertheless, their bioavailability, bioactivity, and stability can be affected in differ-
2
Food Safety Research Center (Salt), Semnan
University of Medical Sciences, Semnan, Iran
3
Department of Food Science and Technology,
Faculty of Nutrition Sciences and Food
Technology/National Nutrition and Food
Technology Research Institute, Shahid
Beheshti University of Medical Sciences,
Tehran, Iran
4
Food Safety Research Center, Shahid
Beheshti University of Medical Sciences,
Tehran, Iran
ent conditions and during storage. In addition, some bioactive compounds have
undesirable flavor that restrict their application especially at high dosage in food
products. Therefore, food industry needs to find novel techniques to overcome these
problems. Microencapsulation is a technique, which can fulfill the mentioned requirements. Also, there are many wall materials for use in encapsulation procedure such as
proteins, carbohydrates, lipids, and various kinds of polymers. The utilization of foodgrade and safe carriers have attracted great interest for encapsulation of food ingredients. Yeast cells are known as a novel carrier for microencapsulation of bioactive
5
Department of Food Science and Technology,
Maragheh University of Medical Science,
Maragheh, Iran
Correspondence
Seyede Marziyeh Hosseini, Department of
Food Technology, Faculty of Nutrition
Sciences and Food Technology/National
Nutrition and Food Technology Research
Institute, Shahid Beheshti University of
Medical Sciences, Tehran, Iran.
Email: sm_hosseini@sbmu.ac.ir
Amir M. Mortazavian, Food Safety Research
Center, Shahid Beheshti University of Medical
Sciences, Tehran, Iran.
Email: mortazvn@sbmu.ac.ir
Funding information
Shahid Beheshti University of Medical
Sciences
1
|
compounds with benefits such as controlled release, protection of core substances
without a significant effect on sensory properties of food products. Saccharomyces
cerevisiae was abundantly used as a suitable carrier for food ingredients. Whole cells
as well as cell particles like cell wall and plasma membrane can act as a wall material
in encapsulation process. Compared to other wall materials, yeast cells are biodegradable, have better protection for bioactive compounds and the process of microencapsulation by them is relatively simple. The encapsulation efficiency can be improved
by applying some pretreatments of yeast cells. In this article, the potential application
of yeast cells as an encapsulating material for encapsulation of bioactive compounds
is reviewed.
KEYWORDS
bioaccessibility, carrier, cell wall, Saccharomyces cerevisiae, stability
them are 5–500 μm in diameter.2,3 Furthermore, microencapsulation
I N T RO DU CT I O N
of food ingredients can provide extended shelf life of the final prodMicroencapsulation has been as an efficient technology used in the
ucts.1,4,5 Microencapsulation can change physical characteristics of
food industry for about 70 years.1 Microencapsulation can be defined
material to handle it easier; also, it can provide a diluted sample of
as getting a core material surrounded by a wall material usually named
original substance's concentration, in cases that we need to use that
as shell, membrane, coating, carrier, matrix, or encapsulating material.
substance in small amounts.5,6 It has been mentioned that for applying
Size of microcapsules ranges from 5 to 5000 μm, but normally most of
microencapsulation in food industry considering consumers requests,
Biotechnol Progress. 2021;e3138.
https://doi.org/10.1002/btpr.3138
wileyonlinelibrary.com/journal/btpr
© 2021 American Institute of Chemical Engineers.
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DADKHODAZADE ET AL.
technological aspects, and economic efficiency are major factors.4,7
GRAS. Moreover, there are some criteria that are effective in the
Therefore, it is crucial to find a low-cost carrier which needs simple
selection of encapsulating agents such as functionality of the core
technology to be used in encapsulation. Also, it should not be repel-
material in the final product, concentration of the core material, mech-
ling for consumers of the final product.
anism of release, stability, and cost limitations.3 These substances
Microencapsulation helps to protect useful and sensitive com-
should provide high protection degree for the core against environ-
pounds such as essential oils, vitamins, and antioxidants or to prevent
mental conditions during processing and storage, not react with the
undesirable interactions of some ingredients with each other besides
core and be easy to work with even at high concentrations.12 Figure 1
protection of active ingredients not to be affected by environmental
presents the most common wall materials used for encapsulation of
conditions.8,9 In addition to the protection role, it can provide con-
bioactive compounds in the food industry.16-18
trolled release of core substances in desired matrix or environment in
a specific period of time, thus spontaneously preventing degradation.
Microencapsulation may cause improved bioavailability of the core.10
In that case, we can obtain maximum benefit of food ingredient (core
3 | C O M M O N E NC A P SULA T I O N
M E T H O D S U S ED I N F O O D I N D U S TR Y
material) in gastrointestinal tract (GIT) by slowly releasing the core
from the capsules in GIT.11,12
Many foods need to undergo some processes in their preparation
steps, such as cooking, roasting, baking, frying boiling, and so on. These
Various encapsulation methods have been developed for encapsulation of food ingredients; the most common types are shown in
Figure 2 and are explained as follow:
processes may cause nutritional losses as many food components are
susceptible to the processing conditions. Therefore, encapsulation of
sensitive and unstable ingredients will help to protect them from harsh
3.1
|
Spray drying
processes. As sensory properties of food products are substantial, this
technique can help to mask undesirable flavors or regulate color and
Spray drying is one of the most popular techniques for encapsulation
texture and produce final products with improved quality.
in food industry and is a cost-effective, flexible, and fast process to
In food industries, there are various encapsulating materials such
produce powdered particles with a good quality.19 In spray drying pro-
as proteins, lipids, starches, phospholipids, waxes, and some microor-
cess, a solution-containing wall and core materials for encapsulation is
ganisms such as yeast cells.2,13 Since yeasts are recognized as Gener-
pumped into the heat chamber and rapid atomization of the solution
ally Recognized As Safe (GRAS), they are used in human food
particles occurs at high temperature by a spray nozzle. The atomized
formulations abundantly. Many commercial strains of yeast are avail-
droplets fall in the heat chamber of the spray drier and the droplets
able for simple use. Among them, Saccharomyces cerevisiae has been
are exposed to hot air flow with high temperature (160–220 C).
used in bakery and brewing industries for many years.14
Therefore, the water from these droplets evaporates rapidly and they
Yeast cells are key components of fermented foods like bever-
are dehydrated. Then, dried end product is separated from the drying
ages, bakery products, and cereals. In fermentation industry and pro-
air with a proper outlet temperature.20 Spray drying is a simple and
duction of metabolites via biotechnology, using yeast cells have been
relatively easy method for industrial settings. However, it has some
a major part of these processes; yeast cells play an important role in
drawbacks for temperature-sensitive molecules (protein carriers) that
alcohol production, manufacture of single cell proteins (SCPs) as a
may degrade at high drying temperatures and nonenzymatic browning
nutritional feed, production of many enzymes, and also wastewater
can happen in the system.21,22 Also, high inlet temperatures could
recycling. However, the bland taste, color, and low cost of yeast cells
affect activity of chemical bioactive compounds as well as probiotic
make them attractive in food industry. Yeast microcapsules (with any
bacteria.23 Yeast cells are successfully applied as a carrier material by
food ingredients) can be used in bakery and confectionary products,
spray drying.24,25 In a study by Sultana et al. (2017), it was observed
chewing gum, sauces, semi-ready foods, and cereals. Microcapsules
that the inlet air temperature of 200 C had no effect on the amount
can be made in tablet or powder forms, keeping the core materials
of encapsulated ethyl hexanoate with dried S. cerevisiae cells by spray
safe and release them by hydration.14 Also, in pharmaceutics, cells of
drying.26 Ruphuy et al. encapsulated curcumin and ibuprofen drugs in
S. cerevisiae have been used for microencapsulation of acyclovir and
yeast glucan particles by spray drying and investigated the effect of
berberine.2,15 This article reviews the encapsulation potential of yeast
initial solid content and atomizing droplet size on encapsulation effi-
cells for bioactive compounds in the food industry.
ciency (EE). Their research indicated that encapsulated drugs in comparison with the micronized crude drugs had faster dissolution rates.
In addition, higher amount of initial solid and larger atomizing droplet
2 | COMMON ENCAPSULATING
M A T ER I A L S US E D I N F OO D I N D U S TR Y
size increased EE.24 In another study, the stability of encapsulated Dlimonene and ethyl hexanoate in S. cerevisiae and maltodextrin using
spray drying was evaluated. The authors announced that yeast cells
Several ingredients can be utilized as coating materials for entrapment
had higher retention capability for both types of flavor and oxidative
of liquids, solids, and gases with different properties.1 These sub-
products of flavors were formed in the spray-dried yeast powder less
stances should be certified for food applications and included as
than maltodextrin powder.18
3 of 12
DADKHODAZADE ET AL.
Wall materials
Polysaccharides
Gums:
Alginate
Guar
Pectin
Xanthan
Gum arabic
FIGURE 1
Proteins
Yeast cells
Carbohydrates:
Starches
Maltodextrin
Dextrins, Chitosan
Cellulose and their
derivatives
S. cervisiae
Plant based:
Y. lipolytica
Soy Proteins
Corn Proteins
Pea Proteins
Lipids
Animal based:
Waxes:
Milk proteins
Beeswax
Egg proteins
Carnauba wax
Others:
Phospholipids
Fractionated fats
Glycolipids
Mono- and diglycerides
Common wall materials for entrapment of bioactive compounds in microcapsules.7-14
Microencapsulation
techniques
Chemical
Interfacial
polymerization
Phase
separation
Coacervation
Physical/mechanical
Liposome
formation
Emulsification
FIGURE 2
3.2
|
Solvent
evaporation
Extrusion
Fluidized-bed
coating
Spray drying
Emulsification
Types of encapsulation methods used in food industry
Extrusion
and are solidified to capsules by chemical or physical process.28 Beads
produced by this technique may have various sizes, from micrometers
Extrusion technology is a basic encapsulation technique for micro-
to millimeters. The capsules with larger size are dispersed more diffi-
organisms, because the process can be performed at low tempera-
cult than smaller capsules in the food. Therefore, the large particles
27
in aerobic and anaerobic conditions. The extrusion process
are unfavorable in foods such as chocolate and condensed milk.29 In
involves extrusion of a biopolymer solution and bioactive substances
general, the effective factors on size and shape of the particles include
through a needle, which droplets are formed at the end of the needle
needle diameter and flow rate of the encapsulating material.30
ture
4 of 12
DADKHODAZADE ET AL.
Different polymers can be utilized by this technique. Grosso et al.
processes due to their resistance to heat resulting in higher stability of
reported the improved survival of probiotic bacteria (Lactobacillus aci-
flavor until the time of consumption. It seems that flavor encapsula-
31
dophilus and Bifidobacterium) by encapsulation in calcium alginate.
tion in yeast cells can solve concerns about flavor loss during high
Also, some authors mentioned that encapsulated cells have more
temperature processes of food production as well as long lasting
resistance to the acidic environments and thermal condition than free
release.42
cells and encapsulation by this technique improved their stability in
It has been mentioned that using yeasts as a coating in encapsula-
acidic media. Large-scale production by this method is difficult and
tion is highly cost effective because of simple process.14 However,
leads to low productivity. The size of particles is large and it is another
using fresh culture of yeast may increase expenses, but the procedure
issue, which makes it unsuitable for industrial application.13
of encapsulation is very much simpler than other carriers without
need of buying and using additional materials. Microorganisms
(S. cerevisiae) were recognized as a carrier in encapsulation process in
3.3
early 1970s.43 It has approximately 5 μm diameter in average cells.44
Coacervation
|
Some other strains that have been used for microencapsulation are
Coacervation is a modified emulsification method with up to 99%
Torulopsis lipofera, Saccharomyces bayanus, Endomyces vernalis, and
encapsulation yield. In this method, bioactive components are added
dairy yeasts like Candida utilis and Kluyveromyces fragilis14. S. cerevisiae
13
to a polymer solution and spherical droplets are formed.
According
can be considered as an ideal, applicable, and well-known container in
to Beikzadeh et al., after adding omega-3 fatty acids to S. cerevisiae
encapsulation technique used for microencapsulation of many bioac-
cells and β-glucan, the amount of loading capacity for yeast cells was
tive compounds. In a study by Karaman,45 plasmolysed (PYC) and non-
higher in comparison with β-glucan.
32
In addition, the reported loading
plasmolysed S. cerevisiae yeast cells (NPYC) were used as
capacity for thymol and carvacrol of Zataria multiflora Bioss. essential
microcarriers for encapsulation of thymoquinone (black cumin seed
oil encapsulated in S. cerevisiae cells were 44.53 and 30.88%, respec-
oil). The results indicated that bioactivity of thymoquinone was
tively and no significant difference was observed in antibacterial activ-
protected better in PYC and the PYC samples showed the lowest deg-
33
by
radation ratio of thymoquinone (52.63%) during 8 days storage. In
coacervation can be achieved with simple and complex methods. In a
another study, Dadkhodazade et al. investigated the ability of
simple process, only one polymer such as alginate, gelatin, and pro-
S. cerevisiae cells for encapsulation of cholecalciferol (vitamin D3).
teins is used, while in complex method, two or more colloidal solu-
They reported that the spray dried and plasmolysed yeast cells
ity
of
essential
oil
after
encapsulation.
Encapsulation
tions are used. The complex coacervation is more suitable for
showed the highest EE (76.10 ± 6.92%) at initial vitamin D3 concen-
encapsulation of hydrophobic compounds.34,35 Coacervation has high
tration of 2.5 mg per gram of yeast cells.25 Cell wall and its eukaryotic
value for encapsulation of functional compounds, such as polyphe-
structure and plasma membrane made it special as a physical barrier
nols. However, the experimental parameters need to be carefully
against environmental components like oxygen or free radicals and
22
light radiation.30,37 Cell wall properties can result in sustained release
controlled.
of core in a way that dry yeast cells are a good protector of core
material.5,30 Two parts of yeast cells can be used for encapsulation,
4 | YEAST CELLS AS ENCAPSULATING
MATERIAL IN FOOD PRODUCTS
namely, cell wall and plasma membrane. Nguyen et al. explored stability of Hibiscus sabdariffa extract (anthocyanin source) encapsulated in
cells of S. cerevisiae. They optimized the process and an EE of 27%
Yeast cells are natural micro-containers for microencapsulation of
was obtained. Storage stability of encapsulated pigments was studied
both fat-soluble and water- soluble food ingredients.6,11 Firstly, it was
in water and buffer (pH 1.5) at different time and temperatures. The
mentioned that water soluble flavors can pass the yeast cell and
results showed that the stability of microparticles was higher in sam-
remain in it as a core material.36 Then, it was implied that fat soluble
ples with heat treatment compared to those without heat treatment.
substances can be entrapped in yeast cells with more than 70% lipid
It was related to enzymatic activity of yeast cells when cells were not
content.37 Finally, AD2 Ltd (1987) found that cells with low lipid con-
subjected to heat treatment. On the other hand, acidic pH had an
tent (<5%) can be used as micro-container in microencapsulation pro-
inhibitory effect on enzymatic activity and pigment degradation. They
cess without need of any treatment and also showing higher core
declared that yeast cells were a good carrier for colorant agents and
loading in comparison with previous patents.38 Fortunately, both
anthocyanin.46 Table 1 summarizes selected publications on encapsu-
hydrophobic and hydrophilic molecules can be loaded in yeast cells.
lation of food bioactive compounds by yeast cells.
38
There are examples of encapsulation of essential oils,
purslane seed
oil,39 resveratrol,10 chlorogenic acid,40 and some enzymes41 in yeast
cells.
4.1
|
Cell wall
Microencapsulation by yeast cells is an applicable method in food
industry. There is an investigation on the production of limonene
The main component of yeast cells is cell wall (Figure 3). It holds the
encapsulated by yeast cells (S. cerevisiae) and their application in
shape of the cell, protects protoplasm from lyses and surrounds some
instant noodles. These microcapsules protect flavor during harsh
protoplasmic enzymes to prevent their undesirable activities.47
Water/oil
solubility
Oil soluble
Oil soluble
Oil soluble
Water soluble
Oil soluble
Water soluble
Oil soluble
Water soluble
Oil soluble
Oil soluble
Oil soluble
Water soluble
Oil soluble
Oil soluble
Sunflower oil
Limonene
Oregano essential oil
Ascorbic acid
Cholecalciferol
Probiotic bacteria
Purslane seed oil
Berbrine
Resveratrol
Limonene
Menhaden fish oil
Chlorogenic acid
(CGA)
Limonene
Orange peel and
peppermint oil
Pretreatment by sodium azide
Plasmolysis (Patent EP0453316A1)
Plasmolysis by NaCl
Autolysis with ethyl acetate
Enzymatic hydrolysis with b-glucanase
Plasmolysis (Patent EP0453316A1)
Max EE 40%
EY 26.7%
Max EE 12.6%
Control 32.6 ± 2.8
-Autolysis 39.4
-Autolysis with ethyl acetate 44.6
-Hydrolysis with Glucanex R200 36.3
-Combination of autolysis and hydrolysis 45.3
EY 4.52%
LC 78%
—
Plasmolysis by NaCl
EE 60.27%
EE 88.33%
Max EE 76.10 ± 6.92%
Plasmolysis by NaCl
Physical destruction through milling
Plasmolysis by NaCl
Enzymatic hydrolysis
EY 101.90 ± 5.5%,
In addition of yeast cell coating, there is an
external coating of hydroxypropyl
methylcellulose (HPMC)
Carboxy methyl cellulose (CMC) was used as
second coating.
Probiotics was coated by two layer of calcium
chloride, the third coating was cell wall and
another calcium chloride layer.
Adding maltodextrin in some emulsion
samples
Diffusion coefficient (Deff) assessment
Deff homogenized cells > autolyzed > pulsed
electric field treatment
Autolysis, pulsed electric fields and highpressure homogenization
Using The concentrated powder form (CPF)
technology
Max EE 86.4 ± 5.0
—
Notes
Adding maltodextrin in some emulsion
samples
Max EE 55.1 ± 7.4
Encapsulation efficiency (EE) & loading
capacity (LC)
Enzymatic hydrolysis
Pretreatments before encapsulation
Selected publications regarding application of S. cerevisiae cells in microencapsulation of food ingredients
Core materials
TABLE 1
38
75
40
6
42
10
15
39
52
25
60
67
85
62
References
DADKHODAZADE ET AL.
5 of 12
6 of 12
FIGURE 3
DADKHODAZADE ET AL.
A schematic structure of yeast cell
S. cerevisiae cell wall is composed of 10 nm layer of mannoproteins
digestion and encapsulated curcumin released in intestinal compart-
which are highly glycosylated and a network of 1, 3-β glucans, and
ment without any changes in the cell walls.53
1,6-β glucans are connected to a thin layer of chitin under them. The
The amphiphilic nature of cell wall due to the presence of man-
thickness of the cell wall is about 70–100 nm, it consists approxi-
noproteins made it a bio-emulsifier. Manos and polypeptide chain
mately 15–25% of cell's dry mass.41,44 β-glucans and chitin stand for
showed hydrophilic and hydrophobic properties, respectively.54 Dif-
41
cell rigidity and mannoproteins provide cell porosity.
Cell permeabil-
ferent strains of baker's yeasts have been used to extract man-
ity can be increased by implying chemical treatments. Any modifica-
noproteins to be applied in food products.55-57 Dikit et al. used
tions that affect mannoproteins and disrupt disulfide bonds and
S. cerevisiae KA01 isolated from palm wine and the emulsifier obtained
hydrophobic linkages can change porosity.48
from this strain had potential application in salad dressing. The
As Zelotnik et al. reported, in aqueous solution, small polar mole-
extracted mannoproteins could be used at pH 5–8 and extreme condi-
cules or nonpolar ones can pass through the cell wall easily, but the
tions of temperature and salinity in food industry.55 Also, there are
restrictive factors are the size of molecule and also polarity properties
studies which used Yarrowia lipolytica (Y. Lipolitica) to extract emulsi-
of the cell. Only molecules with molecular weight of less than 620 Da
fier.58,59 Amaral et al. named the extracted bio-emulsifier “Yansan”
with a limited molecular radius of 0.81 nm dimensions can freely pass
which had high emulsification activity and formed a stable water in oil
through the cell wall.49 It has been proved that yeast cell wall has anti-
emulsion in pH range of 3–9.59 Yeast cell by-products have been used
mutagenic and antigenotoxic activity associated with free radical scav-
in microencapsulation process. According to Marson et al, Maillard
enging properties of the yeast cell wall. Also, β-D-glucan can
conjugates of hydrolyzed yeast cell debris of Saccharomyces pas-
potentially prevent lipid peroxidation and inhibit the oxidative dam-
torianus were a good choice of encapsulation carrier for ascorbic acid
ages of DNA.50 In a survey, the preventive effect of yeast cell wall on
by spray drying process. Enzymatic hydrolysis led to degradation of
cancer cells in a mice was confirmed.51
proteins and enhanced cell wall porosity and promoted rupture of
Besides using whole yeast cell in microencapsulation, cell wall can
yeast cells. β-glucans as main functional ingredients of cell wall in
be used as a carrier by itself. Mokhtari et al. used alginate micro-beads
encapsulation process were remained after hydrolysis.60 Hamza et al.
for encapsulation of probiotic bacteria (L. acidophilus and B. bifidum)
used glucan mannan lipid particles of S. cerevisiae cell wall for encap-
followed by coating by cell wall of S. cerevisiae. Then, they were added
sulation of humic acid. As yeast cell component could show biological
to grape juice and the juice properties was assessed during storage
degradation of mycotoxins effects, these microparticles help detoxifi-
time. Results demonstrated that coating of bacteria with yeast cell
cation of aflatoxin B1 in SGF.61 Vélez-Erazo et al. encapsulated sun-
had a positive effect on survival of L. acidophilus, but had no effect on
flower oil in spent brewer's yeast (as by product) and also evaluated
B. bifidum. Also, it caused some changes in color of juice and its tur-
emulsifying ability of these yeast cells. They used enzymatic protein
bidity.52 Young et al. (2020) evaluated bio-accessibility of curcumin
hydrolysis of yeast cells and applied the concentrated hydrolyzed pro-
encapsulated in native cells (S. cerevisiae) and yeast cell wall particles
tein as emulsifying agent. Their findings showed that higher protein
during simulated gastrointestinal digestion. They mentioned that yeast
concentration led to more stable emulsion. Also, spent brewer's yeast
cell wall particles indicated faster intestinal release after gastric
could enhance oxidative stability of the loaded oil.62
7 of 12
DADKHODAZADE ET AL.
4.2
Plasma membrane
|
from the cell and more space is provided for loading of core material.68 Many compounds have been used for plasmolysis such as some
There is an inner layer surrounded by cell wall (<10 μm), called plasma
enzymes (as adenylate kinase and pyruvate kinase), sucrose, NaCl,
membrane. This bilayer membrane consists of two phospholipid
glycerol, and some organic solvents like acetone and ethyl acetate.69
44
chains with excess amount of strolls and also neutral lipids.
It has a
Shi et al. reported that EE of water soluble chlorogenic acid increased
similar structure as liposome and it makes yeast cell suitable for being
from 6.2% for untreated samples to 12.6% in the case of plasmolysed
used as a coating in encapsulation. Plasma membrane has been men-
yeast strains. Plasmolysis was applied by 5% NaCl solution at 54 C
tioned as the main obstacle of cell permeability owing to controlling
and agitation rate of 150 rpm for 24 hr. It is in line with the patent of
all material which pass in or out of cell.6,11 Sultana et al. studied the
Serozym Laboratories (1973) who announced that when yeast cells
release and stability of encapsulated flavors (D-limonene and ethyl
are pretreated by plasmolysis, the absorption of flavors is
hexanoate) in S. cerevisiae cells. They used the lipid bilayer membrane
enhanced.36,40 Similarly, plasmolysed yeast cells were employed in
of yeast cells as natural encapsulant. The results showed that temper-
encapsulation of purslane seed oil and an increscent of EE (from
ature affected the rate of flavor release and the oxidative stability of
52.96 to 60.27%) and loading capacity (from 186.87 to 211.68 g kg−1)
D-limonene was high in yeast powder.18 Martinelli et al. used mimetic
was reported compared to nonplasmolyzed cells. The procedure they
plasma membrane-derived nanovesicles for the aim of encapsulating
used to obtain plasmolyzed yeast cells was 10% NaCl solution, 55 C,
drugs. They said these coatings are efficient transporters and can be
150 rpm for 48 h.39 Takallo et al. in a comparative study of three pre-
used in different therapeutic procedures.
63
treatment on S. cerevisiae (autolysis, plasmolysis, and enzymatic
hydrolysis) indicated that plasmolysis was more efficient since it provided higher yeast extract content.70
5 | PRETREATMENTS PRIOR TO YEAST
ENCAPSULATION
On the contrary, in a study by Paramera et al., it was revealed that
plasmolysis with NaCl made no difference in the amount of curcumin
that was finally encapsulated in yeast cells. This disclosed that cur-
According to previous research, performing a chemical pretreatment
cumin was entrapped in yeast cells through forming interactions and
on yeast cells in order to empty the content of cell could increase the
specific bonds with yeast membrane and its cell wall. Therefore,
loading of core materials and as a result, improved encapsulation yield.
depleting cell was not much effective to increase loading and effi-
The most applied techniques are autolysis, plasmolysis, and hydrolysis
ciency of the process.69 Similarly, Young et al. encapsulated curcumin
64
by enzymes.
and fisetin in yeast cells and also yeast cell wall by vacuum infusion.
Using vacuum infusion could improve the limitations of encapsulation
process. After optimizing the encapsulation process and using vacuum
5.1
Autolysis
|
infusion, results showed that curcumin was loaded three-time more,
and fisetin two times more than the usual method. They stated that
Autolysis is the act of native hydrolytic enzymes of the cell that release
performing plasmolysis caused loading decrease and the presence of
cytoplasmic compound.65 In food industry, autolysis is used abundantly
cytoplasmic organelles of yeast cell could increase core loading by
and the process and the process is usually preformed at around pH 5.5
increasing core-organelle binding.71
66
and 50 C.
Czerniak et al. mentioned that EE increased from 32.6% for
There are other pretreatments such as ultrasound, pulsed electric
control sample (without autolysis) to 45.3% for samples autolysed by
fields and high-pressure homogenization67 which have been used in
addition of ethyl acetate and hydrolysis with Glucanex R200 (yeast lytic
yeast microencapsulation process. Pham-Hoang et al loaded yeast cells
enzyme). Ethyl acetate increased cell membrane permeability and
(Y. lipolytica) with β-carotene and used two strategies (using solvent and
6
Glucanex R200 did a relative hydrolysis on cell wall. These results are
using ultrasounds) to facilitate carotene loading. It has been reported that
consistent with the results of Shi et al. who observed about 50%
ultrasonication resulted in four times better EE than the other strategy.
increase in EE by performing plasmolysis before encapsulation.40 Dim-
They also declared that by increasing the concentration of β-carotene in
opoulos et al. which encapsulated oregano essential oil in S. cerevisiae
chloroform, carotene adhesion to yeast wall increased and no more caro-
yeast cells announced that yeast cells pretreated by autolysis showed
tene got inside the cells. Therefore, the ultrasounds procedure (6 min at
significant increase in effective diffusion and also the permeability of cell
50%) improved the encapsulation of β-carotene in yeast cells.72
67
walls was significantly improved.
5.2
|
Plasmolysis
Plasmolysis in microencapsulation is defined as a pretreatment tech-
6 | QUALITY ASPECTS OF YEAST CELL
MICROCAPSULES
6.1
|
Photochemical and oxidative stability
nique performed in order to pull out the internal water from the cell.
Meanwhile, some water soluble ingredients such as water soluble pro-
Most bioactive compounds have weak stability against environmental
teins, nucleic acid, saccharides, and some enzymes are also extracted
conditions such as light. Encapsulation processes can protect them
8 of 12
DADKHODAZADE ET AL.
from photo-degradation.73 Guorong Shi et al demonstrated that sta-
Therefore, the rate of release is slow in dry yeasts.69 Studies carried
bility of resveratrol to light increased via microencapsulation in yeast
out by atomic force microscopy showed that, when yeast cells get in
cells. It has been mentioned that the mannoprotein layer and 1, 3
touch with water and swell, some holes appear on the external layer
β-glucans in the yeast cell wall contributed to protection against
of proteins (mannoproteins) which causes an increase of permeability
photo-degradation.10,74
in wet yeasts.42,75
Paramera et al carried out a research on encapsulation of cur-
It has been mentioned that when microcapsules are placed in a
cumin in yeast cells (S. cerevisiae) and demonstrated that retention of
solution, they may release their content by two processes called disin-
curcumin after 30 days exposure to sunlight was almost 62.8% for
tegration and dissolution. Dissolution is a relatively slow stage which
nonencapsulated samples compared to 87.2% for yeast-encapsulated
occurs after the disintegration process. Disintegration starts with
curcumin. They stated that the protection of curcumin against light
decomposition of microcapsules that results in production of disso-
73
was due to its interaction with cell wall or lipid bilayer membrane.
In
lute. The higher the solubility of the core material, the faster the dis-
another research, Kavosi et al applied yeast cells for microencapsula-
solution in water environment. Core particle size, its affinity to
tion of purslane seed oil. Besides the nutritional ingredients such as
environment matrix, and its hydrophobic-hydrophilic properties affect
omega-3 fatty acids, this oil contains high amount of iron and copper
dissolution rate. These two processes occur concurrently.76 These are
ions which make it susceptible to oxidative agents as light and oxygen.
in line with the study of Pham-Hoang et al that investigated encapsu-
They encapsulated the oil in baker's yeast with an excess coating of
lation of amphiphilic flavor compounds in yeast cells (Y. lipolytica) and
carboxy methyl cellulose (CMC). Measuring the peroxide value of
the effects of structural factors on encapsulation. Amphiphilic mole-
encapsulated oil showed an improved oxidative stability of oil after
cules have similarities to plasma membrane of yeast cells so that they
30 days of storage in comparison with nonencapsulated samples. Also,
enter the yeast cells easily. The other parameters that affect the
they revealed that using plasmolysed yeast cells had positive effect on
encapsulation process are polarity of active molecule and its side
oil oxidative stability because by removing water-soluble compounds
chains, general hydrophobicity, parameters related to shape, and vol-
from yeast cells through plasmolysis, more space was available and
ume of the molecule. Better encapsulation is accomplished for mole-
more oil was located in the inner space of cell instead of being near
cules with strongest polar part.77
the surface. This could help to protect oil from oxidant factors such as
oxygen.39
Sultana and Yoshii analyzed the release profile of flavor compounds (D-limonene and ethyl hexanoate) from spray-dried encapsulated yeast (S. cerevisiae) powder by a dynamic vapor sorption system
coupled with gas chromatography. They found that the maximum
6.2
|
release flux was obtained at incubation temperature of 60 C and 80%
Thermal stability
relative humidity (RH). Also, the release mechanism parameters
Yeast microcapsules are known as stable carriers against elevated
showed a controlled release for both types of flavor. Ethyl hexanoate
temperatures due to their cell wall that cover the plasma membrane
had higher affinity to migrate toward the water phase at 80% RH due
as an extra coating to protect the core material. Micro-capsulation of
to its lower activation energy (6 kJ/mol) than D-limonene (41 kJ/
curcumin in yeast cells had an efficient role in its protection from
mol).78
heating stress at high temperatures (above 200 C).73 Also, microen-
Paramera et al. worked on encapsulated curcumin in modified
capsulation of flavors can keep them safe in harsh processes in food
starch, β-cyclodextrin, and baker's yeast and their observation con-
industry. Limonene as a flavoring was encapsulated in a thermo-stable
firmed that yeast microcapsules had a slow release in simulated gas-
particle by means of yeast cells. Limonene was released from yeast
tric fluid (SGF). They pointed out that the concentration of curcumin
microcapsules when the temperature was above 265 C. This hap-
in SGF increased after its encapsulation in yeast cells probably due to
75
It was in accordance with the
the interactions of curcumin with coating that increased its solubil-
results reported by Paramera et al which indicated that yeast
ity.73 Also, other researchers noted that in yeast microcapsules, inter-
(S. cerevisiae) structure was stable almost up to 265 C and it was des-
action of curcumin with mannoproteins, glucans of cell wall or
troyed above this temperature.69
phospholipid of plasma membrane could significantly increase the sol-
pened due to cell wall break down.
ubility.73,79 Guorong Shi et al. reported that encapsulation of resveratrol in yeast cells (S. cerevisiae) can improve its low bioavailability
6.3
|
In vitro release and target delivery of the core
caused by its rapid metabolism in the body. The sustained release of
resveratrol from yeast cells considered as potential target delivery of
It has been mentioned that microcapsules prepared by yeast cells can
the core and solved the problem. Ninety percent of resveratrol encap-
control the release of core material and provide sustained release of
sulated in yeast cells released in SGF in about 90 min. This is because
the core and target delivery. Normand et al. used limonene-containing
of the structure of plasma membrane and also the protein layer of cell
yeast microcapsules as a model to observe its release properties con-
wall that were responsible for permeability. These structures repre-
sidering different water activities and temperatures. They noted that
sent a selectivity roll for bioactive compounds passing through
temperatures above 260 C and water activity above 0.7 were neces-
them.10,47 Guorong Shi et al. compared the release profile of chlo-
sary for release of limonene from these yeast microcapsules.
rogenic acid encapsulated in yeast cells in stimulated gastric fluid
9 of 12
DADKHODAZADE ET AL.
(pH 1.2), phosphate buffer (pH 7.4) and distilled water. The highest
during storage time. However, mouth feel was not desirable and got a
release of chlorogenic acid was observed in stimulated gastric fluid. In
low score compared to control sample (juice without microcapsules).
the first 2 hr, about 95% of chlorogenic acid was released in SGF and
Samples received a low score on total acceptance, as many panelists
after passing 5 hr, a complete release was observed. They mentioned
felt the yeast flavor and considered it as undesirable properties.52 It
these results are consistent with cell wall structure that is formed
seems fruit juices are not suitable matrix for incorporation of yeast
from mannoproteins with different chains of glucans and chitin.40,80,81
microcapsules. Possibly applying multi-coating or using other acid
Plasma membrane and the outer layer of protein are the main factors
resistance coatings like alginate can help to cover yeast flavor in food
of permeability and acid or base can destroy them partially. That is the
or drinks in which yeast flavor is undesirable, but for foods in which
reason of faster release in SGF followed by phosphate buffer (PH 7.4)
yeast flavor is in conformity with other ingredients such as bakery or
than distilled water. It is remarkable that profile of release in phos-
meat products, yeast capsules will be a good choice.
phate buffer is slightly different from two other environments as chlorogenic acid is unstable in base condition.40
7
6.4 | Commercial scope and influence of yeast
microcapsules on the sensory properties of foods
|
CONC LU SION
Yeast-loaded microcapsules are a good choice for use in food products,
as the process of encapsulation is simple and it is recognized as safe
material in food industry. Moreover, these capsules provide controlled
Yeast cells and yeast extracts are known as flavor-improver agents
release of active core in GIT leading to increased bio-accessibility of
that highly contain nonvolatile compounds such as amino acids,
core materials. The plasma membrane keeps core materials safe and
B-group vitamins, peptides, and nucleotides. Yeast extracts have been
protects them from leakage. The structure of yeast cells increases the
used to increase consumers' acceptance of sensory properties in bak-
thermal stability of microcapsules up to 260 C. Yeast cells have intracel-
ery and meat products, sauce, soap, and cheese.82 As Alim et al. study
lular space for loading of the core material and this space would
revealed, most of aroma-active compounds of yeast extract generated
increase by applying some pretreatments and emptying cell before the
during heating.83 It is worthy to know that yeast cell microcarriers
microencapsulation process. Studies have demonstrated that the utiliza-
could have controlled release of flavor without breaking their cells in
tion of yeast cells for encapsulation of bioactive compounds can have
contact with mucus membrane of the nose and tongue in the mouth
potential applications in the food industry, especially in encapsulation of
and also external adhesive protein of yeasts help them to remain in
bioactive compounds with strong aroma such as some essential oils.
mouth longer and long lasting release happen for yeast encapsulated
Because yeast-cell-based carriers can mask their flavor and extend their
component.42 Yeast cells are suitable carriers for encapsulation of
bioactivity without worrying about changing the organoleptic character-
components with strong flavor such as essential oils that change the
istics of foods. However, they cannot release flavor in a pure fat matrix
sensory attributes of foods. In addition, adding high dosage of essen-
and the presence of some water is required to open the outside mem-
tial oils in food components decrease the sensory acceptability, but
brane of yeast cells that is a challenge to utilize them in foods with high
using encapsulated essential oil can improve the organoleptic proper-
fat content. Further investigations should be performed for encapsula-
ties.84 Nakhaee Moghadam et al. used yeast microcapsules containing
tion of more than a bioactive compound and their synergistic effect in
Zataria multiflora Bioss (essential oil) as an antimicrobial component in
yeast cells. Also, it can be expected that, yeast-cell-based encapsulation
commercial chicken soup. They expressed that minimum inhibitory
as an effective approach will be used in large-scale for development of
concentration and minimum bactericidal concentration decreased sig-
functional foods with high efficiency over the next decade.
nificantly after encapsulation. Fortunately, encapsulation could
improve sensory properties and decrease the consumer rejection.33 In
ACKNOWLEDG MENT
another study, Beikzadeh et al. assessed the effect of incorporation of
Supporting for this study provided by Food Safety Research Center of
encapsulated flaxseed oil (source of omega-3 fatty acids) in
Shahid Beheshti University of Medical Sciences is gratefully
S. cerevisiae cells on the flavor of breads. Their investigations indicated
acknowledged.
the lowest flavor and overall sensory scores for the samples containing free flaxseed oil that was due to the oily nature created in
CONFLIC T OF INT ER E ST
these products. There is sensory evaluation about garlic flavor encap-
The authors declare that there is no conflict of interests.
sulated in yeast cells used in instant noodle, which indicated better
taste, smell and authenticity than spray-dried powder of flavor at the
PE ER RE VIEW
same amount. Yeast-encapsulated beef flavor used in battered prod-
The peer review history for this article is available at https://publons.
ucts was superior to its conventional spray-dried powder in smell, the
com/publon/10.1002/btpr.3138.
lasting of flavor after swelling and also the impact after the first
chew.14,42 On the contrary, in a study regarding sensory evaluation of
DATA AVAILABILITY STAT EMEN T
grape juice containing encapsulated probiotic bacteria in alginate and
The data that support the findings of this study are available from the
yeast cell wall, no significant difference was reported in color of juice
corresponding author upon reasonable request.
10 of 12
DADKHODAZADE ET AL.
ORCID
Nasim Khorshidian
https://orcid.org/0000-0002-7898-130X
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How to cite this article: Dadkhodazade E, Khanniri E,
Khorshidian N, Hosseini SM, Mortazavian AM, Moghaddas
Kia E. Yeast cells for encapsulation of bioactive compounds in
food products: A review. Biotechnol Progress. 2021;e3138.
https://doi.org/10.1002/btpr.3138