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J. Dairy Sci.

104:1484–1493
https://doi.org/10.3168/jds.2020-18842
© 2021 American Dairy Science Association®. Published by Elsevier Inc. and Fass Inc. All rights reserved.

Physicochemical and microbiological characteristics of camel


milk yogurt as influenced by monk fruit sweetener
Alina Buchilina and Kayanush Aryana*
School of Nutrition and Food Sciences, Louisiana State University Agricultural Center, Baton Rouge 70803

ABSTRACT L. acidophilus was not affected by the incorporation


of monk fruit sweetener. Monk fruit sweetener can
Camel milk, similar to cow milk, contains all of the es- be added in camel milk yogurts as a health-beneficial
sential nutrients as well as potentially health-beneficial 0-calorie sweetener.
compounds with anticarcinogenic, antihypertensive, Key words: camel milk, fermented, culture bacteria,
and antioxidant properties. Camel milk has been used probiotic bacteria, monk fruit sweetener
for the treatment of allergies to cow milk, diabetes, and
autism. Camel milk helps decrease cholesterol levels in
INTRODUCTION
blood and improves metabolism. One of the most desir-
able food tastes is sweetness. However, the excessive in- Camel milk is a good source of health-beneficial
gestion of sugar negatively affects human health. Monk compounds in the human diet (Kaskous, 2016). The
fruit sweetener is a natural, 0-calorie sweetener with presence of bioactive peptides, lactoferrin, l-lactate,
many health-beneficial functions. Monk fruit sweetener bifidobacteria, insulin, and mono- and polyunsaturated
helps decrease symptoms of asthma and diabetes, pre- fatty acids in camel milk help treat human diseases
vents oxidation and cancer, protects the liver, regulates such as tuberculosis, asthma, diabetes, and food aller-
immune function, and lowers glucose levels. Monk fruit gies. Camel milk also contains substances with anti-
sweetener is 100 to 250 times sweeter than sucrose. The carcinogenic, antihypertensive, and healing properties
objective of this study was to examine the influence of as well as bacteriostatic activity against gram-positive
different concentrations of monk fruit sweetener on the and gram-negative microorganisms (Devendra et al.,
physicochemical properties and microbiological counts 2016; Kaskous, 2016).
of drinking yogurt made from camel milk. Camel milk The main difference between the composition of cow
drinking yogurt was produced with 0, 0.42, 1.27, and and camel milk is the protein content. The camel milk
2.54 g/L of monk fruit sweetener and stored for 42 d. ratio of casein to whey protein is lower than in cow milk,
The physicochemical characteristics and microbiologi- affecting the firmness of coagulum, which results in the
cal counts of yogurts were measured at d 1, 7, 14, 21, formation of soft gel during camel milk fermentation
28, 35, and 42. For the physicochemical characteristics, (Devendra et al., 2016). Camel milk has more β-casein
pH, titratable acidity, viscosity, and color [lightness- than cow milk, with about 65 and 36%, respectively, of
darkness (L*), red-green axis (a*), yellow-blue axis total casein (Devendra et al., 2016). β-Casein is more
(b*), chroma (C*), and hue angle (h*)] values were digestible and hypoallergenic. The higher percentage of
evaluated. The counts of Streptococcus thermophilus, β-casein, along with the decreased amount of α-casein
Lactobacillus bulgaricus, Lactobacillus acidophilus, co- and the absence of β-lactoglobulin, in camel milk low-
liforms, and yeast and mold were determined. Three ers its allergenicity and makes camel milk beneficial
replications were conducted. The sweetener addition for human health. Fermented camel milk, due to the
significantly influenced pH, viscosity, and color (a*, increased content of β-casein, has more antioxidant
b*, C*, and h*) values. Control samples had signifi- peptides (Izadi et al., 2019). The main whey protein
cantly higher pH values, lower viscosity, lower b* and of camel milk is α-lactalbumin. The α-lactalbumin
C* values, and higher h* values than the samples with of camel milk is more susceptible to a break-down by
1.27 and 2.54 g/L of monk fruit sweetener. Growth of pancreatic proteases and has higher antioxidant activ-
S. thermophilus, L. bulgaricus, and probiotic culture ity than cow α-lactalbumin (Park and Haenlein, 2013).
β-Lactoglobulin is lacking in camel milk, but other
Received May 4, 2020.
whey proteins such as lactoferrin and immunoglobulins
Accepted September 12, 2020. are present in concentrations higher than in cow milk
*Corresponding author: karyana@​agcenter​.lsu​.edu (Devendra et al., 2016).

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Camel milk has a higher concentration of l-lactate, yogurts significantly decreased during storage for 28 d
and cow milk is rich in d-lactate. l-Lactate decreases (Torrico et al., 2019).
milk allergenicity, which makes camel milk beneficial Monk fruit is also known as Luo Han Guo or Sir-
for the individuals with lactose intolerance. (Kaskous, aitia grosvenorii. Monk fruit sweetener helps prevent
2016). Camel milk has a potential positive effect on asthma, diabetes, and cancers. Monk fruit sweetener
people with autism. In the intestines of autistic indi- has liver protection properties, regulates immune func-
viduals, the break-down of caseins in cow milk leads tion, and lowers the level of glucose in blood (Li et
to the formation of casomorphin, which is a strong al., 2014). Also, monk fruit sweetener is a 0-calorie
opioid responsible for brain damage. The absence of sweetener, and its sweetness ranges from 100 to 250
β-lactoglobulin in camel milk may solve this problem times that of sucrose (Baotang, 2018). Mogrosides are
(Al-Ayadhi and Elamin, 2013). Moreover, camel milk the main substances responsible for the sweet taste of
has protective proteins (lactoferrin, lysozyme, and im- S. grosvenorii fruit. Mogroside V is the main compo-
munoglobulins) that may improve the development nent, with a content of 0.5 to 1.4% in the dried fruit of
of the brain (Devendra et al., 2016). Consumption of S. grosvenorii (Li et al., 2014). Mogrosides present in
camel milk also helps increase the number of genera monk fruit sweetener have antioxidant effects, making
Allobaculum, Akkermansia, and Bifidobacterium in a the sweetener health-beneficial (Zhang et al., 2011).
human intestine. These genera have a positive effect Microorganisms may convert mogrosides to other mole-
on the physiological functions of the organism, help cules during fermentation. Wang et al. (2019) and Chiu
prevent obesity, and decrease inflammation (Wang et et al. (2020) showed that fungal cultures and yeast
al., 2018). strains can metabolize mogroside. Saccharomyces cere-
In the human diet, sweetness is one of the most de- visiae and Dekkera bruxellensis converted mogroside V
sirable tastes (McCain et al., 2018). The main source into mogroside III E and siamenoside I, respectively,
of sweetness is table sugar or sucrose (Carocho et al., during the 4-d fermentation. Also, mogroside IV was
2017). However, the excessive consumption of sugar detected as a byproduct of mogroside fermentation by
has a negative effect on human well-being, possibly other yeast strains (Wang et al., 2019). Consumption
resulting in obesity, glycemic spike and diabetes, dental of mogroside V from water extracts of S. grosvenorii by
decay, cardiovascular diseases, hypertriglyceridemia, Ganoderma lucidum mycelium led to the formation of
cancer, and kidney diseases (O’Donnell and Kearsley, mogroside III E as well as mogroside IV, mogroside II
2012; Carocho et al., 2017). With the growth of ill- A, and siamenoside I through deglycosylation reaction
nesses related to sugar intake, alternative sweeteners (Chiu et al., 2020).
are becoming increasingly used in food products. However, the incorporation of monk fruit sweetener
Sugar is an important component of dairy products. in camel milk drinking yogurt has not been studied yet.
Sugar acts as a bulking agent, affects texture and vis- The objective of this paper was to study the influence
cosity, improves taste and color, and can be used as of different concentrations of monk fruit sweetener on
a preservative (McCain et al., 2018). Therefore, when the microbiological and physicochemical properties of
sugar is replaced with sweeteners, properties of yogurt drinking yogurt made with camel milk.
may change. According to Yang et al. (2014), addition of
rebaudioside A decreased the hardness and consistency
MATERIALS AND METHODS
of yogurt with an increasing dosage of the sweetener,
but the increasing dosages of erythritol and isomalto- Yogurt Preparation
oligosaccharide improved these yogurt characteristics.
Viscosity was also affected by these 3 sweeteners. Vanilla-flavored drinking yogurt made from camel
Addition of rebaudioside A, erythritol, and isomalto- milk was manufactured at the Louisiana State Univer-
oligosaccharide increased yogurt viscosity; however, sity Dairy Processing Plant (Baton Rouge, LA). Camel
concentrations of the sweeteners played an important milk was reconstituted from powder (Drome Dairy,
role (Yang et al., 2014). On the other hand, addition Centennial, CO) by dispensing 500 g of camel milk
of sweeteners may not have a considerable effect on the powder in 3.785 L of distilled water. Each sample had
rheological properties of yogurt. Miele et al. (2017) con- 7.57 L of camel milk for each of the 4 treatments. The
cluded that addition of aspartame and monellin did not first sample was the control with 0 g/L of monk fruit
affect the storage modulus (G′) value of yogurt because sweetener (Julian Bakery Pure Monk, Oceanside, CA),
these sweeteners were incorporated in a small amount. the second sample contained 0.42 g/L of monk fruit
Some sweeteners are not significantly different from sweetener, the third contained 1.27 g/L, and the forth
sucrose. Yogurts with d-tagatose had similar viscosity contained 2.54 g/L. Reconstituted camel milk with
values to yogurts with sucrose, and viscosity in both monk fruit sweetener was pasteurized at 82.2°C for 30
Journal of Dairy Science Vol. 104 No. 2, 2021
Buchilina and Aryana: CAMEL MILK YOGURT WITH MONK FRUIT SWEETENER 1486

min, tempered to 40°C, and then 50 mL of colorless rpm. The readings were collected with the Wingather
vanilla flavor (Watkins, Winona, MN) was added to software (Brookfield Engineering Laboratories). The
each pail of 7.57 L of camel milk. Then, each sample viscosity was determined in a 946.3-mL container at 6
pail of 7.57 L of camel milk was inoculated with 2.4 mL ± 2°C. Yogurt samples were not stirred before analysis.
of each of the following freshly thawed cultures: Strep- Average of 100 data points were recorded per sample.
tococcus thermophilus STI-06 (Chr. Hansen’s Labora- Three replications were conducted.
tory, Copenhagen, Denmark), Lactobacillus bulgaricus Color. Color of yogurt samples was measured at d
LB-12 (Chr. Hansen’s Laboratory), and Lactobacil- 1, 7, 14, 21, 28, 35, and 42 using a calibrated Mini
lus acidophilus LYO 50 (Danisco, Dairy Connection, Scan XE Plus colorimeter (Hunter Lab, Reston, VA).
Madison, WI). Obtained mixtures were poured into the The following characteristics of yogurt were analyzed:
cups of 946.3 mL and 147.9 mL volume capacity until L* (lightness-darkness), a* (red-green axis), b* (yellow-
filled. These cups were transferred to an incubator and blue axis), C* (chroma), and h* (hue angle). Readings
fermented at 40°C until the pH dropped to 4.7 ± 0.1, were taken under D 65 illumination, 10° observer, and
measured with a calibrated pH meter (Thermo Scien- in the reflected mode. Before readings, each sample was
tific, Orion Star A111, Dawsonville, GA). Change of stirred 5 times clockwise and counterclockwise to incor-
yogurt pH during fermentation is presented in Table 1. porate the separated whey. Each sample was measured
Cups were then placed into a cooler at 4 ± 1°C until 5 times, and 3 replications were conducted.
needed. The experiment was carried out in 3 replica-
tions. Each replication was stored in the cooler for 42 d Microbial Analyses
and analyzed for microbiological and physicochemical
characteristics at d 1, 7, 14, 21, 28, 35, and 42. Control The pour plate technique was used to analyze culture
and treatments were randomized to minimize any pos- growth. Streptococcus thermophilus agar for Strep. ther-
sible biases during the experiment. mophilus enumeration was prepared according to Dave
and Shah (1996). Difco Lactobacillus de Man, Rogosa,
Physicochemical Characteristics and Sharpe (MRS) agar for L. bulgaricus enumeration
was prepared according to the manufacturer’s direc-
pH and Titratable Acidity. The pH and titratable tions (Difco, Becton, Dickinson and Company, Sparks,
acidity (TA) of the vanilla-flavored drinking yogurts MD), and the procedure was carried out according to
made with camel milk were measured at d 1, 7, 14, Tharmaraj and Shah (2003). The MRS-sorbitol agar
21, 28, 35, and 42. The pH meter (The Lab Depot, for L. acidophilus counts was prepared according to
Dawsonville, GA) was calibrated with pH buffers 7.00 Dave and Shah (1996) and Tharmaraj and Shah (2003).
and 4.00 (Fisher Chemical, Pittsburgh. PA). Titratable Serial yogurt dilutions in peptone water from 10−1 to
acidity, expressed as percent of lactic acid, was deter- 10−6 were prepared. Dilutions from 10−2 to 10−6 were
mined by titration of 9 mL of yogurt sample with 0.1 plated on Strep. thermophilus agar, MRS-sorbitol agar,
N sodium hydroxide solution with phenolphthalein as and Lactobacillus MRS agar in duplicate. Pour plates
an indicator. with MRS-sorbitol agar were incubated anaerobically
Viscosity. Viscosity was measured at d 1, 7, 14, 21, at 37°C for 48 h in an anaerobic jar for L. acidophi-
28, 35, and 42. Measurements were carried out using lus enumeration. Pour plates with Strep. thermophilus
a Brookfield DV-II viscometer (Brookfield Engineering agar were incubated aerobically at 37°C for 24 h for
Laboratories, Stoughton, MA) and a helipath stand Strep. thermophilus enumeration. The growth of L. bul-
set in downward motion with an RV-1 spindle at 5 garicus was determined using Lactobacilli MRS agar;

Table 1. The pH during the camel yogurt manufacturing process as influenced by various concentrations of
monk fruit sweetener

pH

0 g/L 0.42 g/L 1.27 g/L 2.54 g/L


Hours of fermentation monk fruit monk fruit monk fruit monk fruit
0 (initial) 5.90 ± 0.06A,a 5.91 ± 0.06A,a 5.82 ± 0.16A,a 5.88 ± 0.16A,a
1 5.71 ± 0.08A,a 5.69 ± 0.05A,a 5.59 ± 0.14A,a 5.61 ± 0.18A,a
2 5.35 ± 0.26B,a 5.32 ± 0.06B,a 5.17 ± 0.30B,a 5.19 ± 0.30B,a
3 4.88 ± 0.08C,a 4.83 ± 0.18C,a 4.76 ± 0.17C,a 4.75 ± 0.15C,a
A–C
Means with different uppercase letters within a column are significantly different (P < 0.05).
a
Means with same lowercase letter within a row are not significantly different.

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plates were incubated anaerobically at 43°C for 72 h


in anaerobic jars. Quebec Darkfield colony (Leica Inc.,
Buffalo, NY) counter was used to count the colonies
grown. The counts of cultures in each of the 4 samples
were enumerated in duplicate. Also, samples of yogurt
were plated on coliforms Petrifilms (3M, St. Paul, MN)
with violet red bile agar and Petrifilms (3M) for rapid
yeast and mold count.

Statistical Analysis

Data were analyzed using Proc Mixed of the SAS 9.3


program (SAS Institute, Cary, NC). The Strep. ther-
mophilus, L. bulgaricus, and L. acidophilus counts were
converted to a log10 scale before analysis in SAS. Bon-
Figure 1. The pH of yogurt as affected by monk fruit sweetener
ferroni (Dunn) t-test was used to determine significant over 42 d of storage. Concentrations of monk fruit sweetener in the
differences at P < 0.05 for main effects (treatment and yogurt were 0 (control), 0.42, 1.27, or 2.54 g/L. Error bars indicate SD.
day) and interaction effect (treatment × day).

yogurt samples with 1% and 2% S. grosvenorii fruit


RESULTS AND DISCUSSION
extract, while samples with 0.5% extract were similar
Physicochemical Characteristics of Yogurt to control samples without the extract (Abdel-Hamid
et al., 2020). The authors suggested that incorporation
pH. The pH during camel yogurt manufacture as of S. grosvenorii fruit extract could enhance the bacte-
influenced by various concentrations of monk fruit rial growth, and the increased fermentation could be
sweetener is shown in Table 1. At any given time point attributed to the addition of fruit byproducts (Abdel-
(0, 1, 2, 3 h) the pH values of the control and yogurts Hamid et al., 2020). As it was mentioned above, mo-
with all amounts of monk fruit sweetener were not sig- grosides may undergo conversions to other components
nificantly different from each other. Over the yogurt during fermentation, but the mechanism of mogroside
manufacture time of 3 h, the yogurts with all studied bioconversion by lactic acid bacteria is not known yet.
concentrations of monk fruit sweetener were similar to Thus, more data is needed on how these components
the control, significantly (P < 0.05) dropping in pH affect yogurt fermentation. Continued growth of starter
at h 2 and 3 of manufacture. The pH values of yogurt cultures was the reason for the decrease of pH during
samples over 42 d of storage are shown in Figure 1. the storage (Kailasapathy et al., 2008).
The amount of added monk fruit sweetener influenced Titratable Acidity. The TA values of yogurt sam-
the pH of yogurt during storage (P < 0.05). The con- ples are shown in Figure 2. The dosage of monk fruit
trol had a significantly (P < 0.05) higher pH than the sweetener and the storage period did not significantly
yogurts with 1.27 and 2.54 g/L of monk fruit sweet- affect TA of yogurts (P > 0.05). A similar pattern was
ener. Storage time was a significant factor (P < 0.05). found for the nutritive sweetener erythritol (Costa et
Overall pH decreased during the storage period of 42 al., 2019). Erythritol, similar to monk fruit sweetener,
d. The pH values noticeably decreased by the seventh lowered the pH of yogurts without changing the TA. In
day compared with the first day and remained stable yogurt, TA measures lactic acid as a result of lactose
for the rest period of storage. According to Kalicka et fermentation by lactic acid bacteria (Bouteille et al.,
al. (2017) and Kim et al. (2016), addition of stevia (a 2013). As the pathway of mogroside metabolization by
natural nonnutritive sweetener, similar to monk fruit bacteria is still unknown, it is possible that end prod-
sweetener) decreased the value of yogurt pH, especially ucts other than lactic acid were produced in yogurt
with the increasing dosage of stevia. According to our samples, and TA did not change.
data, incorporation of monk fruit sweetener enhanced
yogurt fermentation and significantly (P < 0.05) de- Viscosity
creased pH values. Abdel-Hamid et al. (2020) reported
that the addition of water extract of S. grosvenorii fruits Changes of viscosity in yogurt are shown in Figure
in buffalo milk yogurt accelerated fermentation and 3. The treatment effect was an important factor (P <
decreased yogurt pH after cold storage for 24 h. Signifi- 0.05) influencing the viscosity of yogurts. The viscosity
cant (P < 0.05) reduction of pH was reported in buffalo of yogurts increased with the increased amount of monk

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viscosity occurred at d 21, 28, 35, and 42 compared


with d 1. Also, in the second week, a slight whey
separation occurred in all yogurt samples, which slowly
continued throughout the rest of the storage period.
Therefore, the increase in viscosity during storage could
occur because of the postacidification in yogurts, which
resulted in whey separation and an increase in protein
cross-linking. (Hernández-Rodríguez et al., 2017).

Color

The L* Value (Lightness–Darkness). The L*


characteristic of color of yogurt is shown in Figure 4.
The incorporation of the sweetener did not affect the L*
values (P > 0.05), and the control samples and samples
with any amount of the sweetener were not different
from each other. According to Costa et al. (2019), ad-
dition of sweeteners such as sucralose, xylitol, stevia,
Figure 2. The titratable acidity of yogurt as affected by monk erythritol, erythritol with oligofructose, and erythritol
fruit sweetener over 42 d of storage. Concentrations of monk fruit
sweetener in the yogurt were 0 (control), 0.42, 1.27, or 2.54 g/L. Error with polydextrose did not affect the L* value.
bars indicate SD. The increase of storage days was significant (P <
0.05), and the L* values of yogurt samples at d 14
were lower than the L* values at d 21, 28, 35, and 42.
fruit sweetener. Viscosity values of the samples with Because the samples were stirred to incorporate slightly
1.27 and 2.54 g/L of the sweetener were significantly (P separated whey before color measurements, the curd
< 0.05) higher than the viscosity of the control sample. concentration or whey separation did not influence
Mogrosides and steviosides belong to the same type of the L* values. The noticeable decrease of lightness in
sweetener; they are terpenoids. Hernández-Rodríguez samples on d 14 of storage may be explained by the
et al. (2017) studied the microstructures of full-fat and increased number of L. acidophilus in all treatments
reduced-fat yogurts with stevia. The authors observed (Olson and Aryana, 2008).
that yogurts with stevia formed larger casein micelle The a* Value (Red–Green Axis). The a* charac-
clusters, and the porosity of the gel was decreased teristic of color of yogurt is shown in Figure 5. Addition
compared with yogurt samples with sucrose. Such a
structure could be formed through the interaction of
stevioside present in stevia with milk proteins that are
bound by hydrophobic interactions (Hernández-Rodrí-
guez et al., 2017). Rheology of yogurts with stevia was
improved, as the storage (G') and the loss parameters
(G'') were higher than that of yogurts with sucrose
(Hernández-Rodríguez et al., 2017). Aryana and Olson
(2017) reported that the formation of hydrophobic in-
teractions between sweeteners and milk proteins may
enhance yogurt viscosity. Therefore, we hypothesized
that a similar reaction may occur between mogrosides
present in monk fruit sweetener and proteins of camel
milk. Also, increased dosage of monk fruit sweetener
could increase initial total solids of the yogurt mixtures
that improved initial viscosity and strengthened the gel
network (Lee and Lucey, 2010). Therefore, samples with
higher dosage of the sweetener had increased values of
viscosity throughout the storage period.
The day effect was significant (P < 0.05), and viscos-
Figure 3. Viscosity of yogurt as affected by monk fruit sweetener
ity of all yogurt samples increased with the increased over 42 d of storage. Concentrations of monk fruit sweetener in the
storage time. Significant (P < 0.05) difference in yogurt yogurt were 0 (control), 0.42, 1.27, or 2.54 g/L. Error bars indicate SD.

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of monk fruit sweetener significantly increased (P <


0.05) the a* value of yogurts. Control yogurt and yo-
gurt with 0.42 g/L of the sweetener had significantly (P
< 0.05) lower a* values than the sample with 2.54 g/L.
The increase of the a* value can be explained by the
addition of monk fruit sweetener, which was added as
powder of light-brown color. Consequently, the addition
of monk fruit sweetener could result in color change to
red in yogurt samples. Only samples at d 14 and 28 of
storage were significantly different from each other (P
< 0.05). Over 42 d of storage, the greenness in yogurts
decreased. The increase of the a* value occurred be-
cause of the alteration of yogurt structure caused by
gel stirring and the decrease in pH. Changes in yogurt
structure resulted in the possible leakage of natural pig-
ments to the yogurt matrix (Costa et al., 2015). Figure 5. The red-green axis (a*) characteristic of color of yogurt as
The b* Value (Yellow–Blue Axis). The b* char- affected by monk fruit sweetener over 42 d of storage. Concentrations
acteristic of color of yogurt is shown in Figure 6. The of monk fruit sweetener in the yogurt were 0 (control), 0.42, 1.27, or
2.54 g/L. Error bars indicate SD.
treatment effect was significant (P < 0.05); therefore,
the control and 0.42 g/L had the lowest b* values, and
yogurts with 2.54 g/L of sweetener had the highest b* milk, which had a yellowish color (Popov-Raljić et al.,
values. Also, samples with 1.27 g/L of the sweetener 2008).
had values higher than the control and 0.42 g/L of The C* Value (Chroma). Changes of the C* pa-
sweetener, but lower than 2.54 g/L of sweetener. The rameter in yogurt are shown in Figure 7. Monk fruit
increase of the b* value and the color change toward sweetener affected the C* value (P < 0.05). The control
yellowness is also associated with the light-brown color and 0.42 g/L of sweetener samples had similar values
of the sweetener (Costa et al., 2015). Storage time af- that were significantly (P < 0.05) higher than of sam-
fected the b* values of yogurts (P < 0.05). Samples at ples with 1.27 g/L of the sweetener, but the 2.54 g/L of
the first day had higher b* values than the samples at sweetener samples had the highest C* values. Increase
d 42 of storage. A continuous decrease of the b* value of chroma values occurred with the increased amount
during storage was explained by the deterioration of of sweetener. The changes of the C* value could happen
the riboflavin, β-carotene, and vitamin A present in because of the different solubilities of the sweetener and
light scattering effect (Rad et al., 2019). At d 42 of
storage, the C* values significantly decreased compared

Figure 4. The lightness-darkness (L*) characteristic of color Figure 6. The yellow-blue axis (b*) characteristic of color of
of yogurt as affected by monk fruit sweetener over 42 d of storage. yogurt as affected by monk fruit sweetener over 42 d of storage.
Concentrations of monk fruit sweetener in the yogurt were 0 (control), Concentrations of monk fruit sweetener in the yogurt were 0 (control),
0.42, 1.27, or 2.54 g/L. Error bars indicate SD. 0.42, 1.27, or 2.54 g/L. Error bars indicate SD.

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Buchilina and Aryana: CAMEL MILK YOGURT WITH MONK FRUIT SWEETENER 1490

Figure 7. The chroma (C*) characteristic of color of yogurt as af-


Figure 8. The hue angle (h*) characteristic of color of yogurt as
fected by monk fruit sweetener over 42 d of storage. Concentrations of
affected by monk fruit sweetener over 42 d of storage. Concentrations
monk fruit sweetener in the yogurt were 0 (control), 0.42, 1.27, or 2.54
of monk fruit sweetener in the yogurt were 0 (control), 0.42, 1.27, or
g/L. Error bars indicate SD.
2.54 g/L. Error bars indicate SD.

with the first day of storage (P < 0.05). The decrease in counts of Strep. thermophilus at d 28. Lactobacillus bul-
the C* value could be attributed to the different levels garicus species are more proteolytic and produce essen-
of gel opacity (Vargas et al., 2008). tial compounds for the growth of Strep. thermophilus
The h* Value (Hue Angle). Changes of the h* (Shihata and Shah, 2002). Also, the incorporation of
parameter in yogurt are shown in Figure 8. The incor- the dominant Strep. thermophilus culture could result
poration of monk fruit sweetener affected the h* value in the increase of the log10 counts at the end of storage
of yogurts (P < 0.05). Control yogurts had significantly (Birollo et al., 2000).
(P < 0.05) higher h* values than 1.27 and 2.54 g/L Lactobacillus bulgaricus. The growth of L. bul-
of sweetener. Yogurt with 2.54 g/L of sweetener had garicus is shown in Figure 10. The addition of monk
significantly (P < 0.05) lower h* values. To obtain the fruit sweetener did not influence the growth of L. bul-
h* value, the ratio of the b* value to the a* value needs garicus (P > 0.05). The presence of sweeteners in foods
to be calculated; therefore, with the decrease of the b* can decrease L. bulgaricus counts by the increasing of
value and the increase of the a* value, the overall h* osmotic pressure (Birollo et al., 2000). Apparently, it
value of the samples decreased. Sample values at d 14 was not the case for monk fruit sweetener.
were significantly higher than values at d 28 (P < 05).
Whey separation of yogurts could cause these results.

Bacterial Growth

Streptococcus thermophilus. The log10 counts of


Strep. thermophilus are shown in Figure 9. The addition
of monk fruit sweetener in any concentration did not
have an influence on the growth of Strep. thermophilus
(P > 0.05). Cultures of Strep. thermophilus can survive
in the presence of various concentrations of different
sugars (Vinderola et al., 2002). Also, Abdel-Hamid et
al. (2020) did not observe the influence of water extract
of monk fruit on the growth of Strep. thermophilus in
buffalo yogurt.
Storage time had important influence on log10 counts
(P < 0.05) of Strep. thermophilus. Log10 counts signifi-
cantly (P < 0.05) increased at d 28 and remained stable Figure 9. Growth of Streptococcus thermophilus in yogurt as af-
fected by monk fruit sweetener over 42 of d storage. Concentrations of
until d 42. Symbiotic growth of Strep. thermophilus monk fruit sweetener in the yogurt were 0 (control), 0.42, 1.27, or 2.54
with L. bulgaricus could lead to the increase in the g/L. Error bars indicate SD.

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Buchilina and Aryana: CAMEL MILK YOGURT WITH MONK FRUIT SWEETENER 1491

may have had a synergistic effect with the inhibitory


factors. Also, L. acidophilus counts could decrease be-
cause of the formation of hydrogen peroxide by L. bul-
garicus that caused disruption of the bacterial cell walls
(Mani-López et al., 2014).
Coliform, Yeast, and Mold. During the storage
for 42 d, coliforms, yeast, and mold were not observed
in any of the yogurt samples. This suggested that the
heat treatment and storage conditions were carried
out properly and that there was no postpasteurization
contamination.

CONCLUSIONS

Incorporation of monk fruit sweetener into camel milk


yogurts significantly decreased the pH and increased
Figure 10. Growth of Lactobacillus bulgaricus in yogurt as affected
by monk fruit sweetener over 42 d of storage. Concentrations of monk the viscosity of yogurts. The color characteristics a*,
fruit sweetener in the yogurt were 0 (control), 0.42, 1.27, or 2.54 g/L. b*, C*, and h* were also significantly affected by the
Error bars indicate SD. addition of the sweetener. Titratable acidity and the
L* value of camel milk yogurts were not affected by
the addition of monk fruit sweetener. Increase in the
The day effect was significant (P < 0.05), and the amount of the sweetener did not significantly influence
log10 of L. bulgaricus decreased by the end of storage counts of Strep. thermophilus, L. bulgaricus, and L. aci-
compared with the first day. Because of the presence dophilus; however, increase in storage days significantly
of lactoferrin, IgG, and lysozyme in the concentrations affected log10 counts of the added cultures. The counts
higher than in cow milk, camel milk can be a less suit- of Strep. thermophilus had the highest number at d 28 of
able medium for the growth of the Lactobacillus species storage, but were not significantly different. The counts
(Attia et al., 2001). Lactoferrin, IgG, and lysozyme of L. bulgaricus and L. acidophilus lowered significantly
could perform as growth inhibitors, causing noticeable over the storage period. Monk fruit sweetener can be
decline in the bacterial growth during fermentation. used as a zero caloric health-beneficial sweetener in the
Lactobacillus acidophilus. The growth of L. aci- production of yogurt made with camel milk.
dophilus is shown in Figure 11. The addition of monk
fruit sweetener did not affect the growth of L. acidophi-
lus (P > 0.05). The presence of different sugars in dif-
ferent concentrations is not critical for the growth of
probiotic bacteria (Vinderola et al., 2002). Davoodi et
al. (2016) studied the growth of probiotic species from
the Lactobacillus genera influenced by the addition
of glucose, sucrose, stevia leaf, and stevioside in vari-
ous concentrations. Probiotics grew in the presence of
these sweeteners and metabolized natural zero caloric
sweeteners such as stevia and stevioside (Davoodi et
al., 2016).
The increase in days in storage was significant (P <
0.05), and the counts increased at d 14 compared with
d 1, and then significantly (P < 0.05) decreased at d 35
and 42. Initial log counts of L. acidophilus were lower
than expected based on culture growth in cow milk.
The dramatic decrease in growth of L. acidophilus in
camel milk was attributed to the inhibitory factors such
as lysozyme, lactoferrin, lactoperoxidase, IgG, and IgA Figure 11. Growth of Lactobacillus acidophilus in yogurt as af-
fected by monk fruit sweetener over 42 d of storage. Concentrations of
that affected bacterial growth during the storage period monk fruit sweetener in the yogurt were 0 (control), 0.42, 1.27, or 2.54
(Attia et al., 2001). The pH drop over storage period g/L. Error bars indicate SD.

Journal of Dairy Science Vol. 104 No. 2, 2021


Buchilina and Aryana: CAMEL MILK YOGURT WITH MONK FRUIT SWEETENER 1492

ACKNOWLEDGMENTS Hernández-Rodríguez, L., C. Lobato-Calleros, C. Ramírez-Santiago,


M. Rodríguez-Huezo, and M. Meraz. 2017. Microstructure and
rheology of yogurt added with protein-L. plantarum-polysaccha-
This study was supported by USDA Hatch funds ride coacervate and stevia in substitution of milk-fat and sucrose.
and Fulbright Scholarship (US Department of State, Rev. Mex. Ing. Quim. 16:77–89.
Washington, DC) for first author. The authors have not Izadi, A., L. Khedmat, and S. Y. Mojtahedi. 2019. Nutritional and
therapeutic perspectives of camel milk and its protein hydroly-
stated any conflicts of interest. sates: A review on versatile biofunctional properties. J. Funct.
Foods 60:103441. https:​/​/​doi​.org/​10​.1016/​j​.jff​.2019​.103441.
Kailasapathy, K., I. Harmstorf, and M. Phillips. 2008. Survival of
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