Food Chemistry 313 (2020) 126129
Food Chemistry 313 (2020) 126129
Food Chemistry 313 (2020) 126129
Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem
A R T I C LE I N FO A B S T R A C T
Keywords: Thymoquinone is a chief phytochemical constituent of black cumin seed oil (BCSO) and shows strong bioactivity.
Black cumin seed oil It has a weak stability against environmental conditions like heat and light. Encapsulation process by
Yeast Saccharomyces cerevisiae is a popular technique to preserve the bioactivity and increase the stability of functional
Encapsulation bioactive compounds. In the current study, BCSO was encapsulated by both plasmolysed (PYC) and non-
Thymoquinone
plasmolysed yeast cell (NPYC) and stability of thymoquinone and bioactive properties of all samples were
Stability
Storage
evaluated. And also, some physicochemical, morphological and conformational characterizations were carried
out for the encapsules. The results showed that thymoquinone concentration and its bioactivity were preserved
better in PYC during storage compared to BCSO and NPYC. The highest degradation ratio of thymoquinone
during storage for the BCSO was 96.78% while the lowest one was for the PYC sample (52.63%).
https://doi.org/10.1016/j.foodchem.2019.126129
Received 18 September 2019; Received in revised form 17 December 2019; Accepted 25 December 2019
Available online 30 December 2019
0308-8146/ © 2019 Elsevier Ltd. All rights reserved.
K. Karaman Food Chemistry 313 (2020) 126129
2.1. Materials
In this study, the black cumin seed oil (BCSO) used in the en-
capsulation process was provided from Dr. Yılmaz Medicinal Plant and
Drug Raw Materials Co. (Kayseri, Turkey). BCSO was an oil sample
produced by the process of cold pressing of the black cumin seeds and
then filtration. Some quality parameters were informed by the producer
as: specific gravity: 0.919, iodine number: 119.5, total free fatty acid:
0.9 mg KOH/g oil, and major fatty acids were: oleic acid (22.05%),
linoleic acid (59.89%) and palmitic acid (12.05%). Thymoquinone level
was determined as 39.5 mg/g oil. The yeast of Saccharomyces cerevisiae
was purchased as Baker’s yeast (Pakmaya Co. Düzce, Turkey) from a
local market in Kayseri (Turkey).
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K. Karaman Food Chemistry 313 (2020) 126129
Fig. 2. Antiradical activities of black cumin seed oil (BCSO), plasmolysed loaded yeast encapsule (PYC) and nonplasmolysed loaded yeast encapsule (NPYC) (on the
left) and decrease levels of bioactivity performance during storage (on the right).
EE(%) = (WEO/WIO) × 100 (1) different concentration (25–175 mg/L). All measurements were per-
formed with three replications.
LC(g/kg) = (WTO − WSO)/WDMM (2)
where EE is the encapsulation efficiency, WEO is the weight of en- 2.4.2. Yeast encapsule performance to preserve the thymoquinone stability
capsulated oil, WIO is the weight of initial amount of oil, LC is the during storage
loading capacity, WTO is the weight of total oil, WSO is the weight of Thymoquinone is a sensitive bioactive component of BCSO against
surface oil and WDMM is the weight of dry mass of microcapsules. WEO is some environmental conditions like high heat and light and it under-
the calculated by subtracting the nonencapsulated oil from total goes to formation of radicals (Ghosheh et al., 1999). Due to sensitivity
amount of oil. All measurements were performed with two repetitions. of thymoquinone, a stability determination test was carried out. For this
purpose, Schaal oven test was followed (Przybylski et al., 1999). The
2.4. Bioactive properties of yeast encapsules black cumin seed oil, plasmolysed and nonplasmolysed loaded yeast
encapsules were placed in a test tubes and put into the desiccator in-
2.4.1. Thymoquinone concentrations and degradation ratios during storage cluding the NaCl solution to provide 75% relative humidity. The oven
by HPLC temperature was set 65 °C and the samples were stored for 8 days to
Thymoquinone, the main bioactive substance of BCSO was analyzed determine the stability performance of the yeast capsules in the pre-
by HPLC according to the methodology of Ghosheh, Houdi, and Crooks servation of the thymoquinone compared to native black cumin seed
(1999). For this purpose, thymoquinone extraction from the samples oil. In all storage intervals, thymoquinone extraction was performed
(both native oil and yeast capsules) was performed. A 100 mg of native and HPLC analysis of thymoquinone was carried out to determine its
oil or yeast capsule powder was weighed into a centrifuge tube and levels and decrease ratios. All analyses were replicated with two re-
4 mL of methanol (Merck, Germany) was added. Then all samples were petitions.
mixed by vortex for 2 min and centrifuged at 7500 g and 10 °C for
5 min. Finally, the supernatant was filtered using 0.45 μm filter and the 2.4.3. DPPH radical scavenging activity
filtrates were injected into the HPLC (Shimadzu LC 2030C, Japan). Antiradical activity of the samples exposed to Schaal oven test was
Isocratic mobile phase consisting of methanol:2-propanol (Merck, determined using the DPPH radical (2,2-diphenyl-1-picrylhydrazyl-
Germany) and ultrapurified water (45:5:50%) was used. The flow rate Merck, Germany) according to the method of He et al. (2011). For this
was 1 mL/min and the column (Inertsil ODS 4 column, 5μ, 46 × 250 purpose, 100 μL of supernatant obtained for the thymoquinone analysis
mm) temperature was set at 40 °C. PDA detector was used, and the was mixed with 3900 μL of DPPH solution (0.1 mM in methanol) and
absorbance was recorded at 254 nm. Thymoquinone levels of the the samples were mixed by vortex. Then the samples were incubated for
samples were determined using a calibration curve prepared by a high 30 min at dark conditions and room temperature. Finally, the absor-
purity thymoquinone standard (Sigma Chemical Co. (St. Louis, MO) at bances of the samples were recorded at 517 nm using a
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K. Karaman Food Chemistry 313 (2020) 126129
Fig. 3. Comparison of FTIR spectrum for a) Plasmolysed loaded yeast, b) Nonplasmolysed loaded yeast, c) Plasmolysed unloaded yeast and d) Nonplasmolysed
unloaded yeast and e) Black cumin seed oil.
spectrophotometer (UV-vis 1800 Shimadzu spectrophotometer, Shi- mixture was exposed to incubation for 6 min at room temperature.
madzu Corp., Japan). The results were expressed as % inhibition which Finally, the absorbance values of the samples were measured at 734 nm
was calculated using the following formula (Eq.3). by a spectrophotometer (UV-vis 1800 Shimadzu spectrophotometer,
Shimadzu Corp., Japan). The ABTS.+ radical scavenging activity of the
% Inhibition = ((A control − A sample)/A control) × 100 (3)
samples as % inhibition was calculated using the following equation
where Asample is the absorbance of sample; Acontrol is the absorbance of (Eq.4).
DPPH solution. All measurements were performed with four replica- % Inhibition = ((A control − A sample)/A control) × 100 (4)
tions.
.+
where Asample is the absorbance of ABTS with sample; Acontrol refers to
2.4.4. ABTS.+ radical scavenging activity the absorbance of ABTS.+ without sample. The % inhibition values
In addition to the DPPH radical scavenging activity, ABTS.+ radical were converted into the Trolox values and all results were expressed as
scavenging activity test was also performed according to the method of Trolox equivalent antiradical capacity (microgram Trolox/g sample).
Gong et al. (2012). For this aim, an ABTS.+ stock solution was prepared
by dissolving the ABTS.+ radical (Sigma, St. Louis, MO, USA) in 2.5. Morphological and conformational characterization of microcapsules
2.45 mmol/L potassium persulfate to create the radical substance
during the storage for 16 h at dark conditions and room temperature. At 2.5.1. Scanning electron microscopy imaging (SEM)
the end, the ABTS.+ radical solution was diluted by using a phosphate To monitor the surface and microstructure of both freeze dried
buffer solution (pH 7.4) until the absorbance value of 0.7 ± 0.05 at microcapsules and unloaded yeast cells, Scanning Electron Microscopy
734 nm was recorded. Then 30 μL of undiluted supernatant obtained for system (LEO 440 Computer-Controlled Digital Scanning Electron
the thymoquinone analysis was mixed by ABTS.+ solution and the Microscope, Zeiss, Oberkochen, Germany) was used. The samples were
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K. Karaman Food Chemistry 313 (2020) 126129
Fig. 4. Comparison of DSC spectrum for plasmolysed and nonplasmolysed loaded and unloaded yeast microcapsules. a) Plasmolysed loaded yeast, b)
Nonplasmolysed loaded yeast, c) Plasmolysed unloaded yeast and d) Nonplasmolysed unloaded yeast.
analyzed while operating at an accelerating voltage of 5 kV with dif- 2.5.2. Fourier transform infrared spectroscopy (FT-IR)
ferent magnifications of 5KX, 10KX, 20KX, and 30KX. IR spectrum and the state of the bonds in the structure, binding sites
of both unloaded and loaded yeast cell structures and black cumin seed
oil were monitored by using Perkin Elmer 400 FT-IR Spectrometer
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K. Karaman Food Chemistry 313 (2020) 126129
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K. Karaman Food Chemistry 313 (2020) 126129
Fig. 6. Comparison of SEM images of plasmolysed loaded (a and b), nonplasmolysed loaded (c and d), plasmolysed unloaded (e and f) and nonplasmolysed unloaded
(g and h) yeast encapsules. Magnification for a, c, e and g was 5KX and for b, d, f and h was 10 KX.
properties. Shi et al. (2007) used yeast cells-based microencapsulation 3.3. Evaluation of bioactive performance of the yeast encapsules by
process for the preserving of chlorogenic acid against to the unsuitable antiradical scavenging tests
conditions and they observed no significant chemical changes during
the encapsulation, and a good stability for the yeast-encapsulated After the determination of thymoquinone level and stability of the
chlorogenic acid was also monitored. In a similar study, Young and active substance in microcapsules during storage, change in radical
Nitin (2019) compared to plasmolysed and nonplasmolysed yeast cells scavenging activity of the yeast microcapsule samples was also in-
on the thermal stability of curcumin encapsulated by S.cerevisiae cell vestigated. The ABTS.+ and DPPH radical scavenging activities of BCSO
and they reported that the results presented in this study showed that at the beginning of the storage were calculated as 9.75 μg Trolox/g
plasmolysed yeast microcarriers performed better barrier against sample and 20.2%, respectively. For the PYC and NPYC samples, the
thermal degradation compared to native yeast microcarriers. radical scavenging activity was also lower compared to native oil be-
cause of the lower bioactive constituents like thymoquinone. After
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K. Karaman Food Chemistry 313 (2020) 126129
8 days storage, the ABTS.+ and DPPH radical scavenging activities of monitored in Fig. 3a, b and e indicated that C]O ester functional
the samples decreased dramatically for BCSO and recorded as 1.81 μg groups entered into the main ingredient structure. That situation can be
Trolox/g sample and 2.77%, respectively (p < 0.05, Fig. 2). Similarly, considered as proof of encapsule formation given that black cumin seed
both radicals were also tested to determine the antiradical performance oil is the source of ester bonds. Dadkhodazade, Mohammadi, and
of the samples and it was observed that the ABTS.+ and DPPH radical Shojaee-Aliabadi (2018) stated that they observed bands at 2925 cm−1
scavenging activities of PYC and NPYC were determined as 5.61 μg for CeH groups of lipids, stretching vibrations of amide Ι, amide ΙΙ and
Trolox/g sample and 5.45% and 16.5 μg Trolox/g sample and 55.9%, mannans absorption band at 1647, 1547 and 1057 cm−1, respectively.
respectively. As is seen, the highest radical scavenging activity was These results were generally in accordance to the current research re-
measured for the sample encapsulated by nonplasmolysed yeast cell sults while bands obtained around 1547 cm−1 did not observed at
(NPYC) compared to BCSO and PYC although it had the lowest thy- processed yeasts for encapsulation (Fig. 3a and b). Galichet,
moquinone concentration. Similar to the change in BCSO, increase of Sockalingum, Belarbi, and Manfait (2001) and Burattini et al. (2008)
the storage period caused a significant decrement in the radical informed that component bands at around 1026 cm−1 were related to
scavenging activity of both PYC and NPYC samples but the decrease mainly β-glucans (β(1 → 4)) and in the current study, those bands could
percentage was of course significantly lower than that of the BCSO be observed for plasmolysed and nonplasmolysed loaded yeast cells
during storage (p < 0.05, Fig. 2). The main reason behind the higher while the band obtained from nonplasmolysed one (Fig. 3b) was more
antiradical performance of NPYC compared to others is the yeast cell intense. Regarding to Fig. 3c and d, it could be said that plasmolysis
content. The antiradical activities of plasmolysed and nonplasmolysed process shifted to left the bands.
unloaded yeast cells by ABTS.+ and DPPH test were also determined. It
was determined that ABTS.+ and DPPH radical scavenging activities of 3.4.2. DSC characteristics of the samples
plasmolysed and nonplasmolysed unloaded yeast capsules were DSC spectrum of loaded and unloaded microcapsule cells were il-
0.613 μg Trolox/g sample and 2.56% and 2.13 μg Trolox/g sample and lustrated in Fig. 4. When plasmolysed loaded encapsules (a) and plas-
5.39%, respectively. It is clear from the results that the unloaded molysed unloaded yeast cells (c) were compared with each other and it
(empty) yeast capsule bioactivity was affected by the plasmolysis pro- is clear that the loading caused a decrement in Tg and melting peak.
cess and it was resulted that the plasmolysis caused a decrease in the And opposite behavior was observed in crystallization peak and as a
bioactivity of the yeast cells. Plasmolysis which means the loss of cy- result of oil loading, crystallization temperature decreased. When
toplasmic material because of water loss due to osmosis caused re- compared with Fig. 4c and d, due to plasmolysis treatment, Tg, Tm and
moving of the yeast cell components. It is usually performed by im- Tc showed a decrement in yeast cells. While Tg of nonplasmolysed yeast
mersing cells in strong saline or sugar solutions (Pham-Hoang et al., was 77.19 °C and after plasmolysis that value decreased to 56.29 °C. Tm
2013). It was reported that the yeasts (Baker’s or dry yeast) have strong and Tc also decreased from 120.12 °C and 309.07 °C to 108.48 °C and
antioxidant and antiradical activity and could be evaluated as novel and 278.92 °C, respectively. Salari, Bazzaz, Rajabi, and Khashyarmanesh
natural antioxidant ingredient (Hassan, 2011). It was also reported that (2013) informed that exothermic peak was observed at 352 °C by
the antioxidant and antiradical activity of yeast were related to glu- maxium occurrence for freeze-dried nonplasmolysed yeast and also
tathione, Maillard reaction products and sulfur containing amino acids stated that Tc decreased after plasmolysis with 20% (w/v) NaCl solu-
present in the yeast cell (Soomer & Jamieson, 1996). In a study about tion, similar to the current results. Paramera et al. (2011) stated that
the antioxidant performance of the yeasts, the beef patties were added plasmolysis altered the lipid form of the membrane and caused to form
with yeast extract and it was observed that the yeast extracts prevented mobility and, thus, fluidity that’s why plasmolysed yeast cells had lower
the thiobarbituric acid reactive substances formation in the sample Tm compared to nonplasmolysed ones. Regarding to Fig. 4a and b,
(Wang & Xiong, 2005). In the light of this knowledge, it could be in- there were significant differences between the DSC thermograms due to
ferred from that the plasmolysis process increased the oil absorption plasmolysis treatment for encapsulation. In Fig. 4b, it was observed two
capacity and encapsulation efficiency and also increased the stability of endothermic peaks that the first one at 98.10 °C and the second one at
active ingredient but caused a decrease in the bioactivity of the material 208.51 °C while that situation was not detected completely in plas-
due to the removal of the some antioxidant components in the cell of molysed loaded yeast cell (Fig. 4a). It was concluded that the first en-
the yeasts. In another similar study, oxidative and thermal stability of dothermic peak was due to yeast phospholipid bilayer and the second
curcumin encapsulated with yeast cell were investigated and plasmo- one was due to black cumin seed oil (Fig. 4b) and besides not performed
lysed yeast capsule showed weaker antioxidant performance compared of plasmolysis treatment on the yeast cell limited the interaction of
to nonplasmolysed yeast capsule and they expected lower antioxidant yeast cell and oil. These results were in accordance with the report of
activity for the nonplasmolysed yeast capsule because they stated that Paramera et al. (2011).
caustic conditions and high heat would oxidize and degrade any innate
antioxidant systems within the cytoplasm. But the high level of glu- 3.4.3. XRD spectrum of the samples
tathione up to 10 mM (Penninckx, 2002) which is an essential in- XRD results of plasmolysed loaded, nonplasmolysed loaded yeast
tracellular oxidative stress regulator had a strong antioxidant activity. encapsules and also plasmolysed unloaded, nonplasmolysed unloaded
Based on the plasmolysis of the yeast cell, a desiccation process results a yeast cells and the black cumin seed oil were shown in Fig. 5. de Barros
decrement in the ratio of the reduced form of glutathione to the oxi- Fernandes et al. (2016) informed that a crystalline material exhibits
dized form (GSH:GSSG) and this result causes a decrease in the Trolox sharp peaks while amorphous materials provide a broader peak pattern.
equivalent antioxidant performance (Espindola Ade, Gomes, Panek, & In the present study, samples behaved as an amorphous material with
Eleutherio, 2003). poor crystallinity generally. Guler and Sarioglu (2014) also informed
that raw S.cerevisiae cells had amorphous phase similar to the results of
3.4. Morphological and conformational characterization of the yeast the present research. It was observed that black cumin seed oil showed
encapsules peaks at 2θ = 19.74°. Nonplasmolysed loaded and unloaded yeast cells
showed two peaks at 2θ = 8.21°, 19.41° and 2θ = 9.18°, 19.16° re-
3.4.1. FT-IR spectrum of the samples spectively. When plasmolysis process occurred, two peaks were mon-
Fig. 3 shows FT-IR spectrum of plasmolysed loaded yeast encapsules itored at 2θ = 6.71°, 19.00° for loaded cells and at 2θ = 5.79°, 18.90°
(a), nonplasmolysed loaded yeast encapsules (b), plasmolysed unloaded for unloaded cells. XRD pattern of black cumin seed oil had the highest
yeast cells (c), nonplasmolysed unloaded yeast cells (d) and black intensity and loaded yeast cells followed it. That situation could be
cumin seed oil (e) samples. According to FT–IR spectra (Fig. 3) the explained by black cumin seed oil incorporated the yeast cell and in-
absorption bands were observed at approximately 1741 cm−1 and only tensity values were observed as to be higher than those of the unloaded
8
K. Karaman Food Chemistry 313 (2020) 126129
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