Effect of storage and packaging conditions on physicochemical and bioactivity of matcha‐enriched muesli containing probiotic bacteria

Abstract

In the current study, the muesli samples fortified with matcha and probiotic bacteria were produced and the effect of storage time, temperature, and packaging condition on their physicochemical, microbial, and antioxidant properties was determined. A total of 12 treatments including the matcha‐enriched muesli samples containing encapsulated Lactobacillus plantarum or Lactobacillus reuteri and/or their combination, packed in aerobic and/or anaerobic conditions and stored at 4 and/or 25°C for 90 days were considered. The results showed that the water activity of all samples increased during storage at both temperatures, while the antioxidant activity decreased. The highest viability of probiotic bacteria was obtained at 4°C and anaerobic conditions. In addition, all samples had acceptable sensory properties. Generally, the findings of this study showed that the sample containing both bacteria packed in anaerobic condition and stored at 4°C had the best properties and can be considered as a bioactive and tasty product.

Full text

J Food Process Preserv. 2022;00:e16878. wileyonlinelibrary.com/journal/jfpp 
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https://doi.org/10.1111/jfpp.16878
© 2022 Wiley Periodicals LLC.
1 | INTRODUCTION
The ready- to- serve or ready- to- eat breakfast cereal products are
foods that are inherently stable and usually have a long shelf life
(Howarth, 1994). The most important benefits of this type of food
products are the elimination of all pre- consumption preparation and
also their richness in various nutrients and health- promoting com-
pounds. In addition, ready- to- eat product s are usually supplemented
by various attractive flavors increasing their popularity (Adeoye
et al., 2019). Today, in most countries and based on consumer tastes,
these ready- to- eat cereal products are offered in a wide variety of
rice krispies, corn flakes, cheerios, muesli, and so on.
Muesli, as a mixture of dried oats and other nuts or grains, seeds,
and fresh and/or dried fruits, is one of the most important ready-
to- eat breakfast cereal products consumed as breakfast or snack.
This product is a rich source of all basic nutrients such as carbohy-
drates, amino acids, fatty acids, minerals, vitamins, and dietary fibers
(Ebrahimi Monfared et al., 2021). Unlike granola, no oil or sweet-
ener is added because muesli contains a set of raw compounds and
where no baking process is performed and thereby is considered a
healthy product (Adeoye et al., 2019). In addition, the formulated
muesli samples had a remarkable difference in crude material such
as protein (9.93%), crude fat (14.67%), crude fiber (7.05%), ash con-
tent(6.13%),andenergy(394.03 kcal)withcommercialmuesli.Also,
Received:22January2022
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Revised:10M ay2022
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Accepted :22June20 22
DOI: 10.1111/jfpp.16878
ORIGINAL ARTICLE
Effect of storage and packaging conditions on physicochemical
and bioactivity of matcha- enriched muesli containing probiotic
bacteria
Kiamehr Ebrahimi Monfared1 | Maryam Gharachorloo1 | Afshin Jafarpour2 |
Javad Varvani3
1Department of Food Science and
Technology, Science and Research Branch,
Islamic A zad University, Tehran, Iran
2Depar tment of Food Science and
Technology, Garmsar Branch, Islamic Azad
University, Garmsar, Iran
3Department of Environment, Arak
Branch, Islamic Azad University, Arak, Iran
Correspondence
Maryam Gharachorloo, Department of
Food Science and Technology, Science and
Research Branch, Islamic Azad University,
Hesarak, Ashrafi Esfahani, Tehran, Iran.
Email: gharachorloo.m@gmail.com;
m_gharachorlo@srbiau.ac.ir
Abstract
In the current study, the muesli samples fortified with matcha and probiotic bacteria
were produced, and the effect of storage time, temperature, and packaging condi-
tion on their physicochemical, microbial, and antioxidant properties was determined.
A total of 12 treatments including the matcha- enriched muesli samples containing
encapsulated Lactobacillus plantarum or Lactobacillus reuteri and/or their combination,
packedinaerobicand/oranaerobicconditionsandstoredat4and/or25°Cfor90 days
were considered. The results showed that the water activity of all samples increased
during storage at both temperatures, while the antioxidant activity decreased. The
highest viability of probiotic bacteria was obtained at 4°C and under anaerobic con-
ditions. In addition, all samples had acceptable sensory properties. Generally, the
findings of this study showed that the sample containing both bacteria packed in an-
aerobic condition and stored at 4°C had the best properties and can be considered a
bioactive and tasty product.
Novelty impact statement: Matcha- enriched muesli containing encapsulated pro-
biotic bacteria was produced. Effect of storage time, temperature, and packaging
condition was determined. Product packed in anaerobic condition and stored at 4°C
had the best properties. Produced muesli showed remarkable bioactive and sensory
properties.

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the sensory quality of muesli samples was higher than commercial
muesli (Ebrahimi Monfared et al., 2021).
One of the most important constituents of muesli is oat. After
wheat, maize, rice, barley, and sorghum, oats are the sixth largest
grain produced in the world. This valuable cereal contains carbohy-
drate (66.3%), dietary f iber (10.6%), fat (6.9%), protein (16.9%), vitamin
(<1%), mineral (<1%), and β-glucan(solubleform≈ 4%)andthushasa
lot of nutritional and health benefits (Ahmad et al., 2014). β- glucan,
as a branched long- chain polysaccharide, is including the D- glucose
units connected by different glycosidic linkages based on its source.
For example, while water- insoluble β- glucan in yeast and mushroom
is including β1,3 and β1,6 linkages, the water- soluble grain β- glucan
contains β1,3 and β1,4 glycosidic linkages (Kurtuldu & Ozcan, 2018;
Maheshwari et al., 2017). The previous studies showed that this poly-
saccharide has tremendous health effects on low- density lipoprotein
(LDL) cholesterol reduction (De Araújo et al., 2017), weight control
(Slavin, 2005), diabetes control (De Munter et al., 2007), chronic dis-
ease reduction (Maheshwari et al., 2017), etc. In addition, this poly-
saccharide has been used for many years as a potential prebiotic in
various industries. A prebiotic improves consumer health as a non-
digestible food ingredient that selectively stimulates the growth and/
or activity of a limited number of colon bacteria (Roberfroid, 2007).
Also, these ingredients can stimulate the growth of probiotic bacteria
in prebiotic- fortified food products.
Probiotics are a group of live microbial presented in food supple-
ments that improve the maturation of the intestinal microflora (Nava
et al., 2005). Although probiotics may contain a variety of microor-
ganisms, the most common are bacteria belonging to Lactobacillus
and Bifidobacterium. Generally, three mechanisms have been pro-
posed for how probiotics work in the gastrointestinal tract: (a) pro-
duction of antimicrobial agents with the ability to inhibit pathogenic
microbes; (b) modulation of immune responses to suppress patho-
gens; and (c) specific competition with pathogens for adhesin recep-
tors in the large intestine (Nava et al., 2005). Also, it was reported
that probiotics can be positively effective on infantile diarrhea,
necrotizing enterocolitis, antibiotic- associated diarrhea, inflamma-
tory bowel disease, cancer, etc (Gupta & Garg, 2009). However, the
use of probiotics in food products such as muesli is associated with
limitations because the studies have shown that the formation of
probiotic colonies is significantly decreased by incubation (~5 min)
in gastric fluids. Therefore, they face stressful conditions to cross
the upper site of the gastrointestinal tract and reach the large in-
testine (Yao et al., 2020). In this regard, it seems that the entrap-
ment of probiotics in natural biopolymers through the encapsulation
processes can be very effective as reported previously (Rezvankhah
et al., 2020).
Nowadays, with increasing awareness and demand for nutraceuti-
cal products, natural bioactive ingredients are widely used to improve
the func tional proper ties of food produc ts. After water, tea is the most
consumed b everages in many count ries (Pastoriza et a l., 2017). Matcha
(Camellia sinensis) is a powdered type of Japanese green tea and so
far, many bioactive properties have been reported for it (Pastoriza
et al., 2017). Matcha is a rich source of health- promoting compounds
such as catechin, caffeine, phenolic acids, rutin, quercetin, Vitamin C,
chlorophyll, theanine, etc. (Dufresne & Farnworth, 2001). Different
studies showed that the most important antioxidant in matcha is cat-
echin which is a type of phenolic compound and has an antioxidant
capacity comparable to Vitamins C and E (Benzie & Szeto, 1999).
Caffeine is another important ingredient in matcha that, in addition to
creating a desirable taste, is also a potential antioxidant. Phenolic acids
presented in this kind of tea are known to have antioxidant properties
and anti- inflammatory, neuroprotective, and hypoglycemic effects
(Stefanello et al., 2019). Rutin, quercetin, Vitamin C, and chlorophyll
are also potential antioxidants (Carr & Maggini, 2017). Theanine, as
an amino acid found in matcha, is responsible for its unique non-
bitter taste and has a synergistic effect with caffeine (Ku et al., 2010).
Besides, the previous reports confirmed the anti- carcinogenic
(Andreasson et al., 2019), anti- inflammatory (Chu et al., 2017 ), cardio-
protective (Gokulakrisnan et al., 2011), and antiviral (Yang et al., 2020)
effects of matcha, and therefore, adding it to muesli will produce a
full- fledged nutraceutical product.
Due to the presence of probiotic bacteria and bioactive com-
pounds in some enriched products, the type of packaging (aerobic
or anaerobic) and storage conditions are two of the most important
factors in product durability. Therefore, the aim of this study was
to produce new muesli enriched with matcha and probiotic bacteria
of Lactobacillus plantarum and Lactobacillus reuteri and to study the
effect of packaging t ype (aerobic or anaerobic) and stor age tempera-
ture on the physicochemical, microbial, and sensory properties of
the produced ready- to- eat product.
2 | MATERIALS AND METHODS
2.1 | Materials
All muesli ingredients including oats, honey, nuts, milk powder, va-
nilla essential oil, cacao, matcha, and caramel were bought from a
local store in Tehran, Iran. Probiotic bacteria including Lactobacillus
plantarum ATCC 14917 and Lactobacillus reuteri ATCC 23272 were
supplied by the Iranian Biological Resource Center (IBRC), Tehran,
Iran. MRS culture medium was obtained from Merck Chemical Co.
(Darmstadt, Germany). 2,2- diphenyl- 1- picrylhydrazyl (DPPH) was
purchased from Sigma Chemical Co. (St. Louis, MO, USA). All the
other chemicals and reagents used in the present research were of
analytical grade.
2.2 | Preparation of probiotic bacteria
The probiotic bacteria including Lactobacillus plantarum ATCC 14917
and Lactobacillus reuteri ATCC 23272 were separately incubated
inMRSbroth(5 ml) for 24 hat 37°C and then weretransferredto
another MRS broth (95 ml)andincubated (Stuart OrbitalIncubator
S150, Staffordshire, UK) at same conditions. Afterward, the cells
were separated by centrifuging (Universal 320 centrifuge, Hettich,

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EBRAHIMI MON FARED Et al.
Germany) at 4000 g for 5 min and washed three times with sterile
peptone solution.
2.3 | Encapsulation of probiotic bacteria
Encapsulation was performed as reported by Mokarram
et al. (2009) with some modifications. For this purpose, sodium
alginate (0.04% w/w) and corn starch (0.02% w/w) were mixed
and sterilized and then, the probiotic bacteria (1.0 g washed bac-
teria suspension) were added separately and/or together and the
obtained mixture was agitated for 5 min. In the next step, a ho-
mogenous emulsion was prepared by mixing the prepared mix-
ture (10 ml) with cor n coil containing 0 .02% Tween 80 (100 ml)
for20 min.Afterward, 0.01 Mofcalciumchloridewas added and
thecapsuleswereformedandseparatedbycentrifuging(350 g for
10 min). Finally, the capsules were washed with 0.1% of peptone
water and stored at 4°C for next use.
2.4 | Characterization of capsules
The encapsulation efficiency (EE) was determined by the method
reported by Ebrahimi Monfared et al. (2021). For this purpose, the
fresh microbeads (1.0 g) were mixed with 9.0 g of 0.1 M phosphate
buffer solution with a pH value of 7.2, and the resulting suspension
was stored for 1.0 h at room temperature under a mild condition of
stirring. This process was used to completely dissolve the microbe-
ads. Then, the viable cells were enumerated in the prepared sus-
pension and the EE was determined using the following equation:
The size and polydispersity index (PDI) of the prepared microbe-
ads were analyzed using a dynamic light scattering (DLS) appara-
tus (Mastersizer 2000, equipped with Hydro 2000S/G; Malvern
Instruments Ltd., Worcestershire, UK). The microbeads were diluted
with distilled water before the measurements to avoid multiple scat-
tering. Finally, the measurement was done at a laser wavelength of
659 nm,backscatteringangleof90°,andtemperatureof25°C.
Scanning electron microscopy (SEM, Cambridge Scientific
Instrument, S360, UK) was used to study the morphology of the mi-
crobeads loaded with probiotic bacteria. The microbeads were fixed
and coated with a thin gold/palladium layer before imaging. The SEM
micrographs were obtained at an accelerating voltage of 26.0 kV.
2.5 | Production of enriched muesli
In this step, the dried oats were first mixed with syrup (sucrose
syrup (50%), milk powder (3%), honey (40%), nut powder (1%),
vanilla essential oil (0.02%), and cacao and caramel (2%)), and then,
matcha (10% w/w based on the obtained results from pre- tests)
was added. This formulation has been optimized in our previous
study (Ebrahimi Monfared et al., 2021). In the next step, the en-
capsulated probiotic bacteria (108 log cfu/g of Lactobacillus plan-
tarum, Lactobacillus reuteri, and/or both bacteria) were added to
the obtained mixture. The resulting bioactive product was packed
with a two- layered package: an inside polypropylene layer and an
outside polyester cover layer. Finally, the packed products were
placed in aerobic and anaerobic (nitrogen gas as an anaerobic me-
dium)conditions and werestoredfor90 daysat temperaturesof
4 and 25°C, and their different properties were evaluated at in-
tervalsof 15 days. The treatment susedin the presentstudyare
indicated in Table 1.
2.6 | Determination of water activity (aw)
The aw of the homogenized muesli samples was determined using a
water activity meter (Aqua Lab, 4TE, United States of America).
2.7 | Viability of probiotic bacteria
The viability of probiotic bacteria was determined by the method de-
scribed by Mokarram et al. (2009) with some modifications. For this
purpose, the powdered sample (1 g) was mixed with sterile ringer so-
lution (0.85%), then the sterile citrate buffer (9 ml, 0.1 M, pH 6) was
added,andtheobtainedmixturewasagitatedfor15 min.Finally,the
samplespourplatedonMRSagarandincubated for48 hat37°C.
The formed colonies were counted by colony counter and the results
were reported as log cfu/g.
2.8 | Color
The parameters of L*, a*, and b* were determined by a HunterLab
colorimeter (Color Quest XE, HunterLab, Reston, VA, USA) at room
temperature.
2.9 | DPPH radical scavenging activity
The radical scavenging activity of the samples was evaluated by the
method described by Hosseini et al. (2020) with slight modifications.
In this stage, 0.5 mg of the powdered sample was mixed with 2 ml of
0.1 mMDPPHmethanolsolutionandstoredfor45 min indarkness.
Afterward,theabsorbance(A)wasreadat517 nmandDPPHradical
scavenging activity was calculated as follows:
(1)
EE
(%)=
total viable cells after encapsulation
total viable cells before encapsulation
×
100
(2)
DPPH radical scavenging activity
(%)=
A
Control
−A
Sample
A
Control
×
100

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2.10 | Sensory evaluation
The sensory proper ties (flavor, color, odor, texture, and total accept-
ability) of the samples were evaluated by 10 untrained panelists using
the 5- point hedoni c method. In this pa rt, number s 1, 2, 3, 4, and 5 show
poor, average, good, very good, and excellent scores, respectively.
2.11 | Statistical analysis
All the analyses were performed in triplicate and their results were
expressed as mean value ± SD (standard deviation of the mean).
The obtained data were subjected to one- way ANOVA using SPSS
software v. 20. For this purpose, a significance level of p = .05 was
applied.
3 | RESULTS AND DISCUSSION
3.1 | Characteristics of the capsules
The EE results showed that this parameter was found to be
52.81 ± 1.28%forthemicrobeadscontainingbothLactobacillus plan-
tarum and Lactobacillus reuteri. Also as shown in Figure 1, the evalu-
ation of particle size by DLS indicated that the diameter, PDI, and
Z-Averageofthesepreparedmicrobeadswerefoundtobe5850 nm,
0.185,and10,974 nm,respectively.Inaddition,SEMmicrographsof
the produced microbeads in two magnifications of 300 and 5000 are
shown in Figure 1. The SEM results showed that the produced mi-
crobeads had a spherical morphology which was in agreement with
the obser vations of Mokarram et al. (2009) who reported a globular
shape for calcium alginate beads loaded with Lactobacillus acidophi-
lus PTCC1643 and Lactobacillus rhamnosus PTCC1637. Similar results
were also reported by Sultana et al. (2000) who used alginate- starch
microbeads for the encapsulation of probiotic bacteria. Their SEM
results showed that the shape of microbeads was generally spherical
andtheirsizewas0.5–1 mm.
3.2 | Water activity (aw)
Generally, the aw is defined as the free water present in the products
that is available for microbial activity (Senhofa et al., 2015). Based
on the product type, water activity usually ranges from 0.2 to 0.99;
for example, the dried fruit, biscuits, and some grain products have
aw higher than 0.4. It was also proved that bacteria such as probiot-
ics require aw higher than 0.8 for growth and activity (Vesterlund
et al., 2012). Table 2 shows the water activity of the different en-
riched muesli under different packaging conditions (aerobic and an-
aerobic), temperature, and storage time. This parameter was variable
from 0.7 to 0.82 and storage time has a positive ef fect on it. Senhofa
et al. (2015) reported a water activity of ~0.6 for muesli containing
chocolate and apricots. This difference can be related to the differ-
ence in the components of these two products.
Run Treatment type Abbreviation
1Muesli containing encapsulated Lactobacillus plantarum stored at
4°C under aerobic packaging
T1
2Muesli containing encapsulated Lactobacillus plantarum stored at
25°C under aerobic packaging
T2
3Muesli containing encapsulated Lactobacillus plantarum stored at
4°C under anaerobic packaging
T3
4Muesli containing encapsulated Lactobacillus plantarum stored at
25°C under anaerobic packaging
T4
5Muesli containing encapsulated Lactobacillus reuteri stored at 4°C
under aerobic packaging
T5
6Muesli containing encapsulated Lactobacillus reuteri stored at 25°C
under aerobic packaging
T6
7Muesli containing encapsulated Lactobacillus reuteri stored at 4°C
under anaerobic packaging
T7
8Muesli containing encapsulated Lactobacillus reuteri stored at 25°C
under anaerobic packaging
T8
9Muesli containing encapsulated Lactobacillus plantarum and
Lactobacillus reuteri stored at 4°C under aerobic packaging
T9
10 Muesli containing encapsulated Lactobacillus plantarum and
Lactobacillus reuteri stored at 25°C under aerobic packaging
T10
11 Muesli containing encapsulated Lactobacillus plantarum and
Lactobacillus reuteri stored at 4°C under anaerobic packaging
T11
12 Muesli containing encapsulated Lactobacillus plantarum and
Lactobacillus reuteri stored at 25°C under anaerobic packaging
T12
TABLE 1 Thetreatmentsappliedinthis
study

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3.3 | Viability evaluation of probiotic bacteria
Based on FAO and WHO reports, probiotics have beneficial ef-
fects on their host if consumed in sufficient quantity (Guergoletto
et al., 2010). Different strains of Lactobacillus such as L. plantarum
and L. reuteri can be considered probiotics in various products (Chu
et al., 2017). It was reported that these two bacteria are facultative
anaerobic bacteria and so the packaging type (aerobic or anaero-
bic) has an undeniable effect on their viability (Dadgar et al., 2014).
Table 3 shows the viability of the encapsulated probiotic bacteria in
the muesli fortified with matcha. The storage time had a negative ef-
fectontheprobioticviability,andafter90 days,thisparameterwas
FIGURE 1 DLSresult sandscanning
electron micrographs (magnifications
of 300 and 5000) of the microbeads
containing both Lactobacillus plantarum
and Lactobacillus reuteri

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significantly decreased. Therefore, the lowest probiotic viability for
all samples was observed on the 90th day of storage. In accordance
with our findings, Jouki et al. (2021) also reported that the viability
of probiotics encapsulated in quince seed gum- alginate beads used
for the fortification of a synbiotic drink was significantly decreased
during storage. Moreover, the results indicated that at all times of
storage, the highest viability was observed at samples T11 (muesli
containing encapsulated Lactobacillus plantarum and Lactobacillus
reuteri stored at 4°C under anaerobic packaging) and T12 (muesli
containing encapsulated Lactobacillus plantarum and Lactobacillus re-
uteri stored at 25°C under anaerobic packaging), whereas the lowest
viability was related to the sample T6 (muesli containing encapsu-
lated Lactobacillus reuteri stored at 25°C under aerobic packaging).
According to the results, it was found that the viability of bacteria at
4°C was higher than at 25°C. Yoha et al. (2020) studied the viability
of L. plantarumat4°Candroomtemperatureduring60 daysofstor-
age and reported that the bacterial viability was greater at a lower
temperature which can be due to the fact that at low temperatures,
the bacteria enter the death phase later. Moreover, it was reported
that at low temperatures close to above 0°C, the rate of detrimen-
tal chemical reactions is lower compared to the high temperatures
which these reactions could lead to cell damage (Xu et al., 2016).
TABLE 2 Wateractivity(aw) of different treatments of the enriched muesli
Treatment
Water activity (aw)
Day
15 30 45 60 75 90
T10.72 ± 0.00Ae 0.76 ± 0.00Bd 0.77 ± 0.00Bc 0.79 ± 0.00Bb 0.80 ± 0.00Ba 0.80 ± 0.00Ca
T20.71 ± 0.00Be 0. 76 ± 0.01Bd 0.78 ± 0.02ABc 0.80 ± 0.02ABb 0.81 ± 0.02Aab 0.82 ± 0.02Aa
T30.70 ± 0.00Cd 0.74 ± 0.00Dc 0.75 ± 0.00Db 0.76 ± 0.00Eb 0.77 ± 0.00Ea 0.77 ± 0.00Fa
T40.70 ± 0.00Cf 0.74 ± 0.01De 0.76 ± 0.00Cd 0.77 ± 0.01CDc 0.78 ± 0.00Db 0.79 ± 0.00Da
T50.72 ± 0.00Ad 0.76 ± 0.00Bc 0.78 ± 0.00Ab 0.78 ± 0.00Cb 0.80 ± 0.01Ba 0.80 ± 0.00Ca
T60.71 ± 0.00Bf 0.75 ± 0.00Ce 0.77 ± 0.00Bd 0.78 ± 0.00Cc 0.79 ± 0.00Cb 0.81 ± 0.00Ba
T70.71 ± 0.00Be 0.74 ± 0.00Dd 0.76 ± 0.00Cc 0.77 ± 0.00Db 0.78 ± 0.00Da 0.78 ± 0.01Eab
T80.72 ± 0.00Ae 0.75 ± 0.01Cd 0.77 ± 0.01Bc 0.78 ± 0.00Cb 0.79 ± 0.00Ca 0.79 ± 0.00Da
T90.72 ± 0.00Af 0.76 ± 0.00Be 0.77 ± 0.00Bd 0.78 ± 0.00Cc 0.79 ± 0.01BCb 0.80 ± 0.01Cab
T10 0.72 ± 0.00Af 0.77 ± 0.00Ae 0.78 ± 0.00Ad 0.79 ± 0.00Bc 0.80 ± 0.00Bb 0.81 ± 0.00Ba
T11 0.72 ± 0.00Af 0.75 ± 0.00Ce 0.76 ± 0.00Cd 0.77 ± 0.00Dc 0.79 ± 0.00Ca 0.78 ± 0.00Eb
T12 0.72 ± 0.00Ad 0.76 ± 0.00Bc 0.78 ± 0.01Ab 0.79 ± 0.00Bb 0.79 ± 0.00Cb 0.80 ± 0.00Ca
Note: The different uppercase letters in each column and the different lowercase letters in each row are significantly different (p < .05).
TABLE 3 Viabilit yofprobioticbacteria(logcfu/g)ofdifferenttreatmentsoftheenrichedmuesli
Treatment
Viability of probiotic bacteria (log cfu/g)
Day
15 30 45 60 75 90
T17.05 ± 0.06CDa 6.69 ± 0.06CDb 6.44 ± 0.07BCc 6.18 ± 0.07Ed 6.02 ± 0.08Ede 5.87 ± 0.10EFe
T26.93 ± 0.07DEa 6.53 ± 0.07Bb 6.16 ± 0.1 2DBc 5.85 ± 0.05Fd 5.64 ± 0.09He 5. 41 ± 0.10 Hf
T37.18 ± 0.10BCa 6.90 ± 0.13ABb 6.52 ± 0.05Bcd 6.49 ± 0.09CDde 6.37 ± 0.09CDef 6.25 ± 0.10Cf
T47.07 ± 0.08CDa 6.76 ± 0.09BCb 6.54 ± 0.10Bc 6.35 ± 0.05Dde 6.22 ± 0.05De 6.05 ± 0.10Df
T56.85 ± 0.04DEa 6.44 ± 0.09Eb 6.17 ± 0.03Dc 5.88 ± 0.04Fd 5.65 ± 0.09Hef 5.48 ± 0.02Hf
T66.62 ± 0.04Fa 6.17 ± 0.03Fb 5.83 ± 0.05Ec 5.48 ± 0.05Gd 5.21 ± 0.08Ie 4.99 ± 0.05If
T76.86 ± 0.08DEa 6.54 ± 0.07DEb 6.31 ± 0.06CDc 6.09 ± 0.04Ed 5.94 ± 0.03EFe 5.78 ± 0.03Ff
T86.83 ± 0.05DEa 6.49 ± 0.12Eb 6.23 ± 0.05Dc 6.00 ± 0.05Ede 5.86 ± 0.06Fef 5.71 ± 0.07FGf
T97.14 ± 0.07BCa 6.79 ± 0.08BCb 6.53 ± 0.11Bc 6.30 ± 0.09Dde 6.24 ± 0.04Def 6.01 ± 0.10DEf
T10 6.99 ± 0.08Da 6.59 ± 0.10DEb 6.31 ± 0.08CDc 6.00 ± 0.09Ed 5.78 ± 0.04GHef 5 .61 ± 0.08Gf
T11 7.3 3 ± 0.07Aa 7.0 6 ± 0.08Ab 6.87 ± 0.10Acd 6.71 ± 0.07Ade 6.63 ± 0.06Aef 6.53 ± 0.05Af
T12 7.3 0 ± 0.06Aa 7. 03 ± 0.12Ab 6.77 ± 0.06Ac 6.56 ± 0.05BCd 6.45 ± 0.06BCef 6.35 ± 0.05BCf
Note: The different uppercase letters in each column and the different lowercase letters in each row are significantly different (p < .05).

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Besides, bacterial viability was better maintained under anaerobic
conditions than under aerobic which was due to the facultative an-
aerobic nature of these bacteria (Dadgar et al., 2014). In addition,
when the combination of these two bacteria was used, their viabil-
ity was higher than when used separately. Previous studies showed
that these two bacteria have a synergistic effect and can positively
affect each other's viability (Dell'Anno et al., 2021). Therefore, the
best sample regarding the probiotic viability was muesli containing
both probiotic bacteria packaged in anaerobic conditions and stored
at 4°C.
TABLE 4 Colorparameters(L*, a*, and b*) of different treatments of the enriched muesli
Treatment
Color parameters
Day
15 30 45 60 75 90
T1L* 10.26 ± 0.23BCa 9.10 ± 0.21Db 8.66 ± 0.19Dc 8.21 ± 0.19Dd 7.76 ± 0.19Ee 7.3 2 ± 0 .19Ef
a* 5.71 ± 0.07Bd 6.16 ± 0.51BCbcd 6.39 ± 0.05Bc 6.68 ± 0.12Bb 6.92 ± 0.11Ba 7.19 ± 0.09Ba
b* 3.14 ± 0.19ABe 3.79 ± 0.25ABd 4.04 ± 0.07ABcd 4.06 ± 0.15BCbcd 4.15 ± 0.09Bb 4. 51 ± 0 .11Ba
T2L* 9.35 ± 0.45Ca 8.05 ± 0.47Eb 7. 42 ± 0.48Ec 6.77 ± 0.49Ed 6.14 ± 0.49Fe 5.51 ± 0.52 Ff
a* 6.04 ± 0.27Ad 6.73 ± 0.17ABc 7. 09 ± 0.33ABbc 7.4 2 ± 0 .24Ab 7. 79 ± 0.23Aab 8.16 ± 0.29Aa
b* 3.27 ± 0 .12Ac 3.95 ± 0.31Ab 4.19 ± 0.19ABb 4.33 ± 0.18Ab 4.81 ± 0.11 Aa 4.95 ± 0.37ABa
T3L* 11.40 ± 0.46Aa 10.93 ± 0.41ABb 10.46 ± 0.22Bc 10.47 ± 0.36Ac 10.19 ± 0.36Ace 9.90 ± 0.39ABd
a* 5.01 ± 0.28DEc 5.17 ± 0.18Dc 5.46 ± 0.19Dbc 5.47 ± 0.12Eab 5.61 ± 0 .14Fa 5. 74 ± 0.23Fa
b* 2.86 ± 0 .12Bb 3.06 ± 0.23Cab 3.39 ± 0.19Ca 3.36 ± 0.07Da 3.37 ± 0.17 Da 3.52 ± 0. 35Ba
T4L* 10.86 ± 0.39ABa 10.19 ± 0.36Bb 9.73 ± 0.22Cbc 9.49 ± 0.32Cc 9.13 ± 0.32Ccd 8.79 ± 0.32Cd
a* 5.25 ± 0.27CDc 5.53 ± 0.32Cbc 5.85 ± 0. 20Cb 6.00 ± 0.19Dab 6.16 ± 0.19Da 6.38 ± 0.22Da
b* 2.84 ± 0.24Bb 3.34 ± 0.38BCa 3.54 ± 0.15BCa 3.74 ± 0.34BCa 3.97 ± 0.16 Ca 3.96 ± 0.27Ba
T5L* 9.68 ± 0.45Ca 8.78 ± 0.42Db 8.33 ± 0.41D bc 7.87 ± 0.39Dcd 7.42 ± 0.39Ede 6 .96 ± 0.35Ee
a* 5.83 ± 0 .24Bd 6.30 ± 0.36Bbcd 6.64 ± 0.23Bbc 6.81 ± 0.18Bb 7.0 8 ± 0.18Bab 7. 39 ± 0.18Ba
b* 3.13 ± 0. 27ABc 3.74 ± 0.30ABb 4.11 ± 0.12ABb 4.20 ± 0.18ABab 4.22 ± 0.24 Bab 4.49 ± 0.16Ba
T6L* 9.25 ± 0.19Ca 7.91 ± 0.20Eb 7.25 ± 0.23Ec 6.6 4 ± 0.29Ed 6.05 ± 0.29Fe 5.30 ± 0.30Ff
a* 6.16 ± 0 .11Af 6.91 ± 0.19Ae 7.19 ± 0 .16Ad 7.52 ± 0.14Ac 7. 87 ± 0.13Ab 8.21 ± 0.10Aa
b* 3.30 ± 0.07Ad 4.04 ± 0.16Ac 4.28 ± 0.26ABbc 4.49 ± 0.13Ab 4.40 ± 0.10 Bb 4.91 ± 0.06Aa
T7L* 11.03 ± 0.12Aa 10.49 ± 0.1 2Bb 10.25 ± 0.09Bb 9.99 ± 0.09Bc 9.76 ± 0.09Bcd 9. 50 ± 0.09Bd
a* 5.13 ± 0.08Df 5.40 ± 0.07Ce 5.56 ± 0.07Dd 5.76 ± 0.05Dc 5.82 ± 0.04Eb 5.99 ± 0.09Ea
b* 2.85 ± 0.18Bc 3.17 ± 0.21Cc 3.57 ± 0.17BCb 3.70 ± 0.21Cab 3 .74 ± 0.17Cab 3.83 ± 0.06Da
T8L* 10.36 ± 0.32Ba 9.69 ± 0.33Cb 9.34 ± 0.34Cbc 9.01 ± 0.35Ccd 8.68 ± 0.35Dde 8.35 ± 0.33CDe
a* 5.49 ± 0 .19Cc 5.87 ± 0 .12Cb 6.07 ± 0.27BCb 6.27 ± 0.19CDab 6.45 ± 0.22CDab 6.55 ± 0.18CDa
b* 3.08 ± 0 .15ABd 3.53 ± 0.22Bdc 3.79 ± 0.37ABabc 3.78 ± 0.08Cbc 3.94 ± 0.18C ab 4.06 ± 0.20CDa
T9L* 9.85 ± 0.33Ca 8.95 ± 0.33Db 8.50 ± 0.31Dbc 8.04 ± 0.30Dcd 7.61 ± 0.30Ede 7.16 ± 0.31Ee
a* 5.85 ± 0.17Bd 6.31 ± 0.18Bc 6.47 ± 0.20Bc 6.78 ± 0.14Bbc 6.99 ± 0.12Bab 7.2 8 ± 0.21Ba
b* 3.06 ± 0.05Bd 3.82 ± 0.26ABc 3.98 ± 0.08ABbc 4.21 ± 0.09Abc 4.28 ± 0.28Babc 4.35 ± 0.03Ba
T10 L* 9.35 ± 0.23Ca 8.08 ± 0.17Eb 7. 43 ± 0.13Ec 6.79 ± 0.15Ed 6.11 ± 0.15Fe 5.48 ± 0.19Ff
a* 6.07 ± 0 .15Af 6.77 ± 0.09Ae 7.14 ± 0.09Ad 7.3 9 ± 0.09Ac 7.81 ± 0.10ABb 8.19 ± 0.14Aa
b* 3.23 ± 0 .14Ae 4.08 ± 0.29Ad 4.32 ± 0.15Acd 4.47 ± 0.14Ac 4.75 ± 0.11Ab 5.05 ± 0.06Aa
T11 L* 11.52 ± 0.34Aa 11.0 4 ± 0.32Aab 10.81 ± 0.32Abc 10.56 ± 0. 31Acd 10.31 ± 0.31Ade 10.08 ± 0.34Ae
a* 4.87 ± 0.25Ec 5.16 ± 0.19Dc 5.24 ± 0.24Dbc 5.45 ± 0.18Eb 5.51 ± 0.20Fa b 5.84 ± 0. 24EFa
b* 2.66 ± 0. 27Bd 3.11 ± 0.06Cc 3.31 ± 0.22Cbc 3.45 ± 0.14CDa 3.36 ± 0.03Dab 3.58 ± 0.23Ba
T12 L* 10.45 ± 0.05Ba 9.75 ± 0.09Cb 9.41 ± 0.17Cc 9.01 ± 0.11Cd 8.66 ± 0.11De 8.28 ± 0.11Df
a* 5.46 ± 0.06Ce 5.83 ± 0.13Cd 6.03 ± 0.08Cd 6.23 ± 0.05CDc 6.44 ± 0.05Cb 6.64 ± 0.02Ca
b* 2.92 ± 0 .16Bc 3.46 ± 0.11Bb 3.89 ± 0 .12ABa 3.89 ± 0.19BCa 3.87 ± 0.10 Ca 4.06 ± 0.17CDa
Note: The different uppercase letters in each column (for each color parameter) and the different lowercase letters in each row are significantly
different (p < .05).

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3.4 | Color parameter evaluation
The color of a product has a strong effect on its acceptance by con-
sumers. In this part, three color parameters including L*, a*, and b* of
the fortified muesli were evaluated. L* parameter was ranged from
0 (black) to 100 (white) and a* parameter is due to green- red colors
with negative values toward green and positive values toward red,
whereas b* parameter is related to blue- yellow colors with negative
values toward blue and positive toward yellow (Hosseini et al., 2021).
Table 4 indicates the color parameters of fortified muesli packed
in aerobic and/or anaerobic conditions during 90 days of storage
at 4 and 25°C. As observed, storage time had a negative effect on
L* so that with an increase in storage time, this factor was signifi-
cantly decreased. The decrease in L* parameter may be related to
the production of exopolysaccharides by probiotic bacteria because
the previous studies showed that the polysaccharides can reduce
L* by absorbing water (García- Pérez et al., 2005). Moreover, it was
reported that the development of proteolysis by probiotic bacteria
can reduce the L* of food products resulting in a product with lower
lightness (Costa et al., 2017). Also, Table 4 shows that the fortified
muesli had a red and yellow color which can be related to the color of
its components. Also, the increase in red color during storage can be
related to the activity of probiotic bacteria and thereby, a decrease
in pH, leading to an increase in the red color of some antioxidants
present in the muesli samples originating from matcha which was
used to enrich the samples (Hosseini et al., 2021).
3.5 | DPPH radical scavenging activity
Electron transfer assays such as DPPH radical scavenging activ-
ity are colorimetric methods used for the study of an antioxidant's
capacity for the reduction of an oxidant. In this experiment, the ni-
trogen atom in the DPPH molecule is reduced by a hydrogen atom
from antioxidants which this donating ability of hydrogen determines
the scavenging activity of the samples (Kedare & Singh, 2011). Table 5
shows the DPPH radical scavenging activity of different samples of
fortified muesli. The results showed that all of the prepared muesli
samples with different formulations which were stored under various
conditions had the ability to scavenge the free DPPH radicals. This
antioxidant activity is related to their ingredients, especially matcha
which is a rich source of natural antioxidant agents including polyphe-
nols and other phytonutrients (Shi et al., 2020). In addition, probiotic
bacteria such as L. plantarum and L. reuteri are able to produce free
amino acids and various biologically active peptides that increase an-
tioxidant activity (Sah et al., 2014). Accordingly, the highest radical
scavenging activity was related to the T11 sample (muesli containing
encapsulated Lactobacillus plantarum and Lactobacillus reuteri stored
at 4°C under anaerobic packaging), and the lowest antioxidant activ-
ity was observed for the T2 sample (muesli containing encapsulated
Lactobacillus plantarum stored at 25°C under aerobic packaging). As
can be seen, the antioxidant activity in samples containing both pro-
biotic bacteria was significantly higher than those containing one of
the bacteria which was possibly due to the synergistic effects of these
two bacteria as stated earlier (Dell'Anno et al., 2021). Also, the study
of the antioxidant capacity of samples during storage showed that the
samples stored at 4°C (especially T11) retained more antioxidant prop-
erties than the samples stored at 25°C due to the higher viability of
probiotic bacteria at this temperature. Comparison with other studies
showed that the fortified muesli produced in this study has a higher
antioxidant capacity than the muesli containing the dried fruits/nuts
of cranberries, apples, apricots, and almonds reported by Sumczynski
et al. (2015), which could be related to the presence of matcha and
probiotic bacteria in the obtained muesli in the present study.
TABLE 5 DPPHradicalscavengingactivity(%)ofdifferenttreatmentsoftheenrichedmuesli
Treatment
DPPH radical scavenging activit y (%)
Day
15 30 45 60 75 90
T147.27 ± 0.66Ea 42.69 ± 0.64Ea 38.07 ± 0.76Ea 36.40 ± 0.88Ea 34.40 ± 0. 82Fa 33.16 ± 0 .97Ea
T244.05 ± 0.58Ga 38.45 ± 0.77Ga 33.28 ± 0 .74Ga 30.40 ± 0.84Ha 27.97 ± 0.97Ia 25.44 ± 0.77Ha
T350.77 ± 0 .61Ca 47. 89 ± 0.70Ca 44.40 ± 0.52Ca 42.65 ± 0.17Ca 41 .86 ± 0.74Ba 40.54 ± 1.01Ba
T449.73 ± 0.17Da 45.27 ± 0.17 Da 40.46 ± 0.02Da 38.79 ± 0.55Da 3 7.4 8 ± 0.56Da 36.07 ± 0.82Da
T549.3 7 ± 0.48Da 44.65 ± 0.68Da 39. 65 ± 0.57Da 37. 82 ± 0.70Ea 35.58 ± 0. 22Ea 33.91 ± 0.12Ea
T646.68 ± 0.47Fa 41. 24 ± 0.54Fa 35.89 ± 0.38Fa 32.36 ± 0.53Ga 29.97 ± 0.18 Ha 27. 66 ± 0.48Ga
T751.8 4 ± 0.45Ba 48.45 ± 0.61Ba 44.93 ± 0.84Ba 43.63 ± 0. 55Ba 42.45 ± 0.58Ba 41.07 ± 0.73Ba
T851.0 0 ± 0.48BCa 46.33 ± 0.60Ca 41.4 6 ± 0.99Ca 39. 58 ± 0.99CDa 3 7.4 0 ± 0.49Da 35.88 ± 0.56Da
T950.83 ± 0.64BCa 45.95 ± 0.86CDa 40.86 ± 1 .15CDa 38.07 ± 0.68Da 36.11 ± 0 .61Ea 35.57 ± 0.92Da
T10 48.37 ± 0.33Ea 42.76 ± 0.66Ea 37.19 ± 0.50Ea 34.20 ± 0.59Fa 31.85 ± 0.82Ga 30.14 ± 0.39Fa
T11 54.82 ± 0.52 Aa 51.12 ± 0.66Aa 47.12 ± 0.72Aa 45.79 ± 0.59Aa 44.49 ± 0.55Aa 43.07 ± 0.38Aa
T12 51.71 ± 0.44Ba 47.16 ± 0.58Ca 42.51 ± 0.64Ca 39.87 ± 0.83CDa 3 9.0 1 ± 0.18Ca 38.09 ± 0.53Ca
Note: The different uppercase letters in each column and the different lowercase letters in each row are significantly different (p < .05).

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3.6 | Sensory properties
Sensory properties are one of the most important factors that
make a customer- friendly product. In this study, various sensory
properties of the fortified muesli including flavor, color, odor,
texture, and total acceptability were evaluated and the obtained
results are shown in Figure 2. As observed, all treatments espe-
cially sample T11 (muesli containing encapsulated Lactobacillus
plantarum and Lactobacillus reuteri stored at 4°C under anaerobic
packaging), had very good sensory properties which can be attrib-
uted to the ingredients (especially matcha) as well as present pro-
biotic bacteria in it. In a similar study, Phongnarisorn et al. (2018)
reported that the enrichment of biscuits with matcha can posi-
tively affect the sensory properties of this product. In another
study, Ahmad et al. (2015) reported that the addition of green
tea powder to wheat flour can improve the sensory properties of
the produced cookies. In our previous study (Ebrahimi Monfared
et al., 2021) also, we observed that the encapsulation process of
muesli with probiotic bacteria had a positive effect on its sensory
attributes and acceptability by the panelists. In a study conducted
by Senhofa et al. (2015) also, it was reported that the packaging
type (paper tube, paper bag, and Doypack) had a significant effect
on the sensory properties (texture, aroma, taste, and overall ac-
ceptance) of cereal muesli during storage. Moreover, the sensory
FIGURE 2 Sensorypropertiesincluding(a)flavor,(b)color,(c)odor,(d)texture,and(e)totalacceptabilityoftheproducedmuesliunder
90 daysstorageat4and25°C

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EBRAHIMI MONFAR ED Et al .
evaluation results showed that the scores for sensory properties
of different muesli samples were decreased during the storage and
the lowest scores were observed on the final day (i.e., 90) of the
storage. This observation is in line with the results of probiotic
bacteria viability and color parameters results which were de-
creased with increasing the storage time having a negative effect
on the acceptability of the final products by the sensory panelists.
4 | CONCLUSION
The aim of this study was to investigate the physicochemical, mi-
crobial, and antioxidant properties of matcha- enriched muesli sam-
ples containing encapsulated probiotic bacteria packed in aerobic
and anaerobic conditions and stored at 4 and 25°C for 90 days.
The obtained results showed that the combination of both bacte-
ria (Lactobacillus plantarum and Lactobacillus reuteri), temperature of
4°C, and anaerobic packaging lead to a product with the best micro-
bial, bioactivity, and sensory attributes. Therefore, it can be used
as a functional product with high durability and excellent health-
giving/promoting properties.
AUTHOR CONTRIBUTIONS
Kiamehr Ebrahimi Monfared: Methodology. Maryam Gharachorloo:
Investigation; supervision. Afshin Jafarpour: Investigation; supervi-
sion. Javad Varvani: Software; validation.
ACKNOWLEDGEMENT
The authors would like to thankful from Razi Laboratory Complex
Experts in Science and Research Branch, Islamic Azad University.
DATA AVAIL ABILI TY STATEMENT
The data that support the findings of this study are available on re-
quest from the corresponding author.
ORCID
Maryam Gharachorloo https://orcid.org/0000-0002-7062-026X
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How to cite this article: Ebrahimi Monfared, K.,
Gharachorloo, M., Jafarpour, A., & Varvani, J. (2022). Effect
of storage and packaging conditions on physicochemical and
bioactivity of matcha- enriched muesli containing probiotic
bacteria. Journal of Food Processing and Preservation, 00,
e16878. https://doi.org/10.1111/jfpp.16878