[Retracted] HS-GC-IMS and ATR-FT-MIR Analysis Reveal the Differences in Volatile Compounds, Proteins, and Polyphenols of Royal Jelly

Chen, Di; Lu, Wenjing; Ye, Qin; Zhang, Cen; Ge, Xiao; Xiao, Chaogeng

doi:https://doi.org/10.1155/2022/3223558

Advances in Materials Science and Engineering

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusions Data Availability Conflicts of Interest Acknowledgments Supplementary Materials References Copyright Related Articles

Research Article Retraction

!

This article has been Retracted. To view the article details, please click the ‘Retraction’ tab above.

Special Issue

Application of Materials in Agricultural Engineering

View this Special Issue

Research Article | Open Access

Volume 2022 | Article ID 3223558 | https://doi.org/10.1155/2022/3223558

[Retracted] HS-GC-IMS and ATR-FT-MIR Analysis Reveal the Differences in Volatile Compounds, Proteins, and Polyphenols of Royal Jelly

Di Chen,¹Wenjing Lu,¹Qin Ye,¹Cen Zhang,¹Xiao Ge,²and Chaogeng Xiao¹

Academic Editor: Palanivel Velmurugan

Received11 Feb 2022

Revised15 Mar 2022

Accepted23 Mar 2022

Published15 Apr 2022

Abstract

Royal jelly (RJ) produced by honeybees (Apis mellifera) is a traditional functional food and usually suffers adverse impacts from heat exposure during collection and transportation. Based on the gas chromatography, the change to volatile compounds in RJ was screened by ion mobility spectrometry. Chemical characteristics were analyzed by infrared spectroscopy combined with a diamond ATR. The results showed that the flavor can be distinguished using HS-GC-IMS based on principal component analysis and 26 compounds, including esters, aldehydes, and ketone, were identified as the differential volatile compounds in RJ. Spectroscopy results suggested that the specific bands were related to the proteins and polyphenols, which were verified by electrophoresis and the Folin–Ciocalteu method. Water-soluble proteins were decreased by 13.11%, and polyphenols contents were decreased by 25.72% compared with the control. Thus, the combination of ATR-FT-MIR and volatile compound analysis can help to identify the quality of RJ quickly and sensitively from the aspect of flavor and chemical characteristics. Our study gives a meaningful suggestion for the analytic strategy of RJ quality.

1. Introduction

Royal jelly (RJ) represented a traditional food with broad bioactivity. This white-yellowish gelatinous-viscous substance was the main food of bee larvae and queen bees with a special flavor [1–3]. Nearly 100 tons of royal jelly were exported to Europe and Japan every year. RJ was secreted by the salivary glands of a specific honeybee [4]. It has numerous functional properties, including antioxidative activity, immune regulation, antibacterial activity, and antitumor activity, as well as insulin-like activity [5, 6]. These bioactive of RJ were largely dependent on its freshness and chemical composition characteristics. However, improper storage will lead to the degradation of the RJ flavor and have a great impact on its chemical composition [7–10]. So, analyzing the changes of favor and chemical characteristics is important to detect the RJ freshness and ensure its quality.

The flavor is a useful index in determining whether the quality of RJ is acceptable on the spot. The variation of flavor composition is essential for the freshness evaluation of RJ, as well as its quality. It was reported that RJ harvested at 48 h contained more unique volatile compositions compared to the samples harvested at 72 h [11]. In addition, the flavor was also related to the quality of RJ commercial products. With the increasing emphasis on rapid detection of RJ quality, flavor characteristics analysis becomes critically important. Therefore, clarifying the flavor characteristics change is the key to the detection of RJ quality and ultimately satisfies collection preferences. Headspace extraction has been broadly applied in the analysis of volatile constituents. Moreover, volatile compounds of RJ have been evaluated under low temperature and room temperature storage, and 25 different compounds were found [12, 13]. However, some flavor compounds can only be detected by a certain method, and different flavor compounds may be extracted by different detection method as the complexity of foodstuffs. Up to now, less information is available on the characteristic of the RJ flavor by using ion mobility spectrometry.

Ion mobility spectrometry combined with GC is feasible and useful in analyzing flavor and figuring out specific volatile compounds in recent years, which is rapid, sensitive, and simple. It can establish fingerprints at the ppb level in real time for detected samples according to the characterization of drift time and GC retention [14, 15]. It also investigates unbiased information and screens specific makers through nontarget analysis from a large amount of data. Therefore, ion mobility spectrometry combined with GC has been broadly applied in flavor analysis, drug study, and security detection [16]. As a new food resource, rapid detection of high quality RJ has drawn more and more attention. ATR-FT-MIR was another technique for rapid detection. Our study aimed to analyse the variation of flavor and chemical characteristics of RJ during the process of storage. Principal component analysis was performed on the flavor data which was acquired by the ion mobility spectrometry combined with GC. Verification of chemical characteristics changes was carried out based on the ATR-FT-MIR data. Integration of the two techniques may provide a new supplementary analytical strategy for the quality control of RJ.

2. Materials and Methods

2.1. Materials

RJ was obtained from the same colony of Apis mellifera. L at the Hangzhou Kangli Food, Co., Ltd, Zhejiang, China. The latitude and longitude are 120.2 E and 30.3 N. The same colony of Apis mellifera RJ was acute frozen and then placed at −80°C until analysis. Afterward, the RJ samples obtained from the same batch were prepared at different storage conditions based on the experiment. BSA was received from Beyotime Co. Ltd (Hangzhou, China). Last but not least, Folin–Ciocalteu was received from Zeheng Biological Technology Co. Ltd. (Hangzhou, China).

2.2. Ion Mobility Spectrometry Combined with GC Analysis

Flavor analysis was conducted with a FlavourSpec® flavor analyzer (GAS, Dortmund, Germany). The capillary column (ID: 0.53 mm) was applied in the GC. Ion mobility spectrometry combined with GC analysis was performed according to the literature with minor modifications [17]. RJ was placed in a plastic tube and adjusted for 15 min at 50°C. The incubation speed is set at 500 rpm. Headspace samples of 500 µL were automatically injected at 85°C. Carrier gas N₂ flows for 2 min at a rate of 0.002 L/m, and then, the flow of carrier gas changed to 0.01 L/m in the following 8 min, then changed to 0.1 L/m (10–20 min), and finally reached 0.15 L/m (20–30 min). Volatile constituents were departed by the column at 60°C, and the temperature of IMS was set at 45°C. RI and drift time were used to identify volatile constituents.

2.3. ATR-FT-MIR Spectroscopy

RJ samples were analyzed by a VERTEX70 attenuated total reflection midinfrared spectrometer (Bruker, USA) coupled with a diamond ATR accessory. Spectra data were acquired with scans of 24 and a resolution level of 4 cm⁻¹. The medium infrared spectra signal of the sample was detected in the region of 400–4000 cm⁻¹ for five replicates. Approximately 0.05 g of RJ was transferred to the ATR diamond that was cleaned with ethanol (75%). Background air spectrum was applied to each RJ sample spectra. Spectral data were analyzed by the OPUS version 6.5 (Agilent, USA) and the origin version 8.5.

2.4. Detection of Water-Soluble Protein and Total Polyphenol Content (TPC)

2.4.1. Determinations of Major Royal Jelly Proteins

Major royal jelly proteins (MRJPs) were extracted with PBS solution for 24 h at 4°C as previously described by Chen [18]. The extract of MRJPs was obtained by centrifuging (Eppendorf, Germany) at 12,000 rpm for 30 min under 4°C. SDS-PAGE was used to separate proteins that were present in MRJPs, and concentrations of MRJP (major royal jelly protein) 1 and MRJP3 were determined by Image J.

2.4.2. Determinations of Water-Soluble Proteins

The water-soluble proteins’ content in RJ was determined using BSA as a standard. 50 μL of RJ diluted in distilled water was mixed with 250 μL of Coomassie light blue solution. After being cultured in the little light circumstances for 30 min, the light absorption value was taken at 595 nm. A standard curve was acquired by detecting the absorbance gradient of the BSA solution [19].

2.4.3. Determinations of Total Polyphenol Content (TPC)

Total polyphenol content was detected using the literature method with some minor revisions [20]. Undiluted Folin–Ciocalteu reagent (1 mL) was added to an equal volume 10 mg/mLRJ solution, and then, 1 minute later, 5 mL of 1 M aqueous Na₂CO₃ was added. Finally, about 3 mL of purified water was added to the reaction system, making the volume up to 10 mL. The control contained all the reaction reagents except RJ. After being cultured at 25°C for 1 h, the light absorption value was determined at 760 nm. Polyphenol content was presented as protocatechuic acid (PCA) equivalents (mg PCA/g) based on the PCA calibration curve, and the values were presented as means of triplicate analyzes.

2.5. Statistical Analysis

IMS data were processed with vocal processing software, including an ion mobility spectrometry combined with a GC analysis library, a dynamic PCA plug-in, gallery plug-in, and reporter plug-in, which were used to analyze samples from different perspectives. Analysis of variance was performed in SPSS 18.0 (SPSS, USA), and a value of <0.05 was regarded as a statistically significant difference between groups. The results were presented as the mean ± sd.

3. Results

3.1. Chemical Characterization by HS-GC-IMS

The 3D topographic of RJ sample is shown in Figure 1 according to the normalized reaction ion peak position and the ion drift time. Our study demonstrated that the volatile substances of 28°C stored RJ were well separated from the samples at frozen conditions (−20°C), as shown in the top three-dimension plot graphic. Most flavor components signal peaks were found in the RIP relative of 1.0–2.0 and the measurement run time of 1000–100 s. Many peaks were decreased at 28°C storage while some peaks were enhanced. In particular, many small peaks appeared during the measurement run time of 200–400 s and RIP relative of 1.0–1.5, indicating the formation of little other substances in 28°C stored RJ. The qualitative and quantitative results are shown in Figure 2. HS-GS-IMS have detected 45 signal peaks and 31 compounds were identified (Table 1). Volatile compounds of RJ samples were ketones, esters, aldehydes, alcohols, and others according to the identified components.

(a)

(b)

Fingerprint showed the effects of storage conditions on the variation of volatile compounds (Figure 3). A great deal of flavor contents of ethyl acetate, heptanal, 2-pentanone, 2-nonanone (D), ethyl octanoate (D), ethyl octanoate (M), 2-nonanone (M), ethyl hexanoate (M), 3-methyl-1-butanol, 2-heptanone (D), ethyl hexanoate (D), 2-heptanone (M), 2-propanol, butyl acetate (D), butyl acetate (M), n-Nonanal, ethanol, 6-methyl-5-heptene-2-one, benzaldehyde (D), and benzaldehyde (M) were relatively low in RJ at 28°C for 30 days (R2), indicating the loss of these volatile compounds were affected by the temperature, which might be the result of the action of enzymes or thermal decomposition during ambient temperature storage. On the contrary, 3-methylbutanol, 2-methylbutanal, furfural (D), furfural (M), 2-butanone, and 2-methylpropanoic acid were obviously enhanced in RJ at 28°C for 30 days compared to the frozen samples (R1). Volatile organic compounds in the differential model exhibited an obvious difference, and total volatile organic matter content was decreased in the process of ambient temperature storage (Figure S1).

As illustrated in Figure 4, the principal component analysis showed that RJ at the different storage conditions could be well separated. Ninety six percent of PC-1 and 2% of PC-2 explained 98% of the total variance, indicating that they could explain the main flavor characteristic. The PC-1 value decreased in the following order: R1 < R2. The close distance between samples means small differences, while the far distance means significant differences. Thus, the samples have great differences in flavor, and the regions of each group of RJ samples can be clearly separated.

3.2. Spectroscopy Characterization by ATR-FT-MIR

The average ATR-FT-MIR spectrum of the RJ samples gives molecular vibrations affected by ambient temperature storage (Figure 5). Stretching vibration of O-H of protein-glycoconjugate covalent bond could raise a strong band at 3268 cm⁻¹. Spectral features related to stretching vibrations interaction of protein-glycoconjugate covalent bond for both O-H and C-O are also characterized in spectral of 3700–3200 cm⁻¹ and 1260–1000 cm⁻¹(with max absorption at 1059 cm⁻¹).

(a)

(b)

The most prominent absorption with broadband at 1636 cm⁻¹ that refer to the vibration of H-O-H deformation and carbonyl group stretching of proteins was shown in the fingerprint region. Protein’s thalidomide I band characteristic absorption peak was located at 1600–1700 cm⁻¹. Thus, signal at 1636 cm⁻¹ is arising from the stretching vibrations of the carbonyl group of backbone conformation of the proteins in RJ. As shown in Figure 5(a), the band at 1546 cm⁻¹ (thalidomide II bands 1500–1600 cm⁻¹) occurs because of the C-N stretching vibrations and N-H deformation vibration. The reduced interaction between protein molecules causes the band to move. Absorption occurring at 1238 cm⁻¹ and 1059 cm⁻¹ is arising from stretching vibrations of a carbonyl group in the carbohydrates.

In Figure 5, differences of band positions and intensities represent unique spectral patterns of the samples, indicating significant differences of the composition. Variations in protein content (at 3268, 1636, 1546, and 1059 cm⁻¹) present in RJ were distinguished significantly between analyzed samples, and the differences were mainly related to the protein, polyphenols, and flavonoid, as their corresponding spectral in the fingerprint (1800–800 cm⁻¹) are the prominent variation. RJ under 28°C storage reflect unique spectral features in the fingerprint region represented by the protein-glycoconjugate band at 1059 cm⁻¹ due to the relatively low protein content, while frozen samples showed higher protein content (absorption maximum at 3268 and 1059 cm⁻¹).

3.3. Verification of Chemical Changes

Content of MRJP1with 57 kDa in RJ stored at 28°C was significantly lower than those stored at −20°C, as shown in Figure 6(a) (). In addition, a similar phenomenon also was observed on MRJP3 (Figure 6(b) and Figure S2). Major royal jelly proteins were significantly decreased once the storage time was beyond 20 days of whatever stored at 28°C or 4°C. Figures 6(c) and 6(d) show that the content of water-soluble proteins and phenolic was significantly reduced by 13.11% and 25.72% at 28°C compared to −20°C for 30 days (). However, no significant difference was observed within 20 days (), indicating these bioactive constituents were also affected by the storage time except temperature.

(a)

(b)

(c)

(d)

4. Discussion

It is not a simple task to analyze all the flavor compounds with one simple method as the complexity of foodstuffs and the techniques are not sensitive enough [21–23]. So, as a rapid, simple, and sensitive analytical technique, HS-GC-IMS with high resolution was used in this study to assess the flavor changes and provide a supplementary analytical method for distinguishing RJ [24]. In the present study, RJ stored at −20°C contained a large number of acid, ester, aldehyde, and ketone compounds, and flavor compounds were gradually decomposed during the 28°C storage. Thus, the overall content of flavor compounds in frozen RJ was much higher than those stored at 28°C, similar to the reported literature that RJ of low temperature, and keeps the composition of volatile compounds unchanged [12]. The HS-GC-IMS results showed that the ambient temperature storage led to the decrease and formation of some flavor substances in RJ, exhibiting great effects on the composition of volatile constituents. However, special attention should be paid to discrepancies of the volatile compound between literature and the obtained data in this study, as previous studies using GS-MS have shown that 28°C storage make d-ethyl acetate increase twice. The differential methods for RJ collection and preparation can cause these discrepancies, as described above, as the analysis of volatile organic compounds is influenced by both extraction and detection techniques [12, 25]. In addition, as different plants also affect the flavor composition of benzoic acid methyl ester, acetic acid, octanoic acid, and hexanoic acid [13], RJ samples harvested from different plants should be studied in the future.

FTIR spectroscopy with ATR is able to accurately reflect the secondary structure information of the protein by the spectral absorption band of Amide-I and Amide-II at 1547 cm⁻¹ with highly specific signals [26]. The relative spectra intensity of the typical bands of RJ stored at 28°C was decreased compared to the frozen samples. Moreover, temperature caused the amide-I band to move, which was similar with the reports of [27]. Furthermore, analysis of phenolic compounds of RJ is also important to the quality evaluation [28]. ATR-FT-MIR used in the present study can reflect the variation of polyphenol, which was verified by the total polyphenol analysis. These results were similar with the result of Zhao et al. that RJ phenol contents are decreased obviously at room temperature [12, 13]. So, FTIR with ATR in the present study can reflect the variation of proteins and polyphenols and is suitable to monitor chemical changes of RJ during the process of storage [29].

Based on the ATR-FT-MIR results, verification analysis of water-soluble proteins and the total polyphenol content was then carried out. Ambient temperature caused the significantly reduction of the content of water-soluble proteins. MRJPs were important bioactivity constituents of RJ [30–32]; it can affect the biological function in bee larvae and determine the freshness and quality of RJ. So, it was usually used as a freshness marker for RJ [33]. Interestingly, the SDS-PAGE result showed that MRJP1, which consists about half of water-soluble proteins, was decreased significantly after ambient storage, indicating this protein makes an important attribution to this vibration in the ATR-FT-MIR spectrum (Figure 5 and Figure S2). However, the decrease of MRJP1 may be caused by molecules aggregation rather than degradation, as reported by Qao et al. [34].

Notably, China produces more than 4,000 tons of RJ annually and is the largest producer of RJ globally [34, 35]. In order to analyze the quality and freshness, there is a strong desire to develop sensitive and rapid methods to investigate the chemical composition variation of RJ [36]. Flavor and characteristic of the ATR-FT-MIR spectrum were important indicators to make sure the high quality of produced RJ [28]. Integration of the two techniques presented in this study could effectively distinguish the samples and was a potential new analytical strategy for the quality control of RJ.

5. Conclusions

In this study, HS-GC-IMS combined with ATR-FT-MIR were performed to assess the variation to volatile and heat sensitive compounds in RJ. The volatile compound fingerprints were constructed and a total of 31 differential compounds affected by the temperature were identified. The main flavor compounds in RJ were attributed to esters, aldehydes, and ketones based on HS-GC-IMS. PCA results indicate that the samples at different temperatures can be well separated. Verification of the ATR-FT-MIR results indicated that the temperature had more impact on the change of proteins and polyphenols compared to storage time. As a reliable analytical tool, HS-GC-IMS combined with ATR-FT-MIR is able to screen the quality of RJ quickly and sensitively from the aspects of flavor and chemical characteristics. Our study can give a meaningful suggestion for the analytic strategy of RJ quality.

Data Availability

No data were used to support this study.

Conflicts of Interest

All authors of this article declare that they have no conflicts of interest.

Acknowledgments

We would like to thank the laboratory colleagues for their advice and the financial support from the Zhejiang Province Key Research and Development Project, (Grant no. 2018C02051).

Supplementary Materials

Figure S1: GS-IMS Spectra of Volatile Organic Compounds Difference comparison in different RJ samples. Figure S2: SDS-PAGE analysis of MRJPs (A). M refers to Marker and 1–9 represent RJ stored at −20°C (day 10, 20, 30), 4°C (day 10, 20, 30), and 28°C (day 10, 20, 30), respectively. (Supplementary Materials)

References

M. Martinello and F. Mutinelli, “Antioxidant activity in bee products: a review,” Antioxidants, vol. 10, no. 1, p. 71, 2021.
View at: Publisher Site | Google Scholar
A. Buttstedt, R. F. A. Moritz, and S. Erler, “Origin and function of the major royal jelly proteins of the honeybee (Apis mellifera) as members of theyellowgene family,” Biological Reviews, vol. 89, no. 2, pp. 255–269, 2014.
View at: Publisher Site | Google Scholar
L. Shen, W. Zhang, F. Jin et al., “Expression of recombinant AccMRJP1 protein from royal jelly of Chinese honeybee in pichia pastoris and its proliferation activity in an insect cell line,” Journal of Agricultural and Food Chemistry, vol. 58, no. 16, pp. 9190–9197, 2010.
View at: Publisher Site | Google Scholar
A. Ramanathan, A. J. Nair, and V. S. Sugunan, “A review on royal jelly proteins and peptides,” Journal of Functional Foods, vol. 44, pp. 255–264, 2018.
View at: Publisher Site | Google Scholar
N. Ab Hamid, A. B. Abu Bakar, A. A. Mat Zain et al., “Composition of royal jelly (RJ) and its anti-androgenic effect on reproductive parameters in a polycystic ovarian syndrome (PCOS) animal model,” Antioxidants, vol. 9, no. 6, p. 499, 2020.
View at: Publisher Site | Google Scholar
A. Hadi, A. Najafgholizadeh, E. Aydenlu et al., “Royal jelly is an effective and relatively safe alternative approach to bloodlipid modulation: a meta-analysis,” Journal of. Functiaonal. Food., vol. 41, pp. pp202–209, 2018.
View at: Publisher Site | Google Scholar
M. Kamakura, T. Fukuda, M. Fukushima, and M Yonekura, “Storage-dependent degradation of 57-kDa protein in royal jelly: a possible marker for freshness,” Bioscience Biotechnology and Biochemistry, vol. 65, pp. 277–284, 2001.
View at: Publisher Site | Google Scholar
L.-r. Shen, Y.-r. Wang, L. Zhai et al., “Determination of royal jelly freshness by ELISA with a highly specific anti-apalbumin 1, major royal jelly protein 1 antibody,” Journal of Zhejiang University - Science B, vol. 16, no. 2, pp. 155–166, 2015.
View at: Publisher Site | Google Scholar
S. Tamura, S. Amano, T. Kono et al., “Molecular characteristics and physiological functions of major royal jelly protein 1 oligomer,” Proteomics, vol. 9, no. 24, pp. 5534–5543, 2009.
View at: Publisher Site | Google Scholar
A. Maghsoudlou, A. S. Mahoonak, H. Mohebodini, and F. Toldra, “Royal jelly: chemistry, storage and bioactivities,” Journal of Apicultural Science, vol. 63, no. 1, pp. 17–40, 2019.
View at: Publisher Site | Google Scholar
Y. H. Guo, L. B. Zhou, Q. Z. Pan, and L. Z. Zhang, “Effect of different harvesting times on the yield and composition of royal jelly,” ActaAgriculturaeUniversitatis, vol. 37, pp. 120–125, 2015.
View at: Google Scholar
V. A. Isidorov, S. Bakier, and I. Grzech, “Gas chromatographic-mass spectrometric investigation of volatile and extractable compounds of crude royal jelly,” Journal of Chromatography B, vol. 885-886, pp. 109–116, 2012.
View at: Publisher Site | Google Scholar
Y.-z. Zhao, Z.-g. Li, W.-l. Tian, X.-m. Fang, S.-k. Su, and W.-j. Peng, “Differential volatile organic compounds in royal jelly associated with different nectar plants,” Journal of Integrative Agriculture, vol. 15, no. 5, pp. 1157–1165, 2016.
View at: Publisher Site | Google Scholar
M. Li, H. Du, and S. Lin, “Flavor changes of tricholoma matsutake singer under different processing conditions by using HS-GC-IMS,” Foods, vol. 10, no. 3, p. 531, 2021.
View at: Publisher Site | Google Scholar
N. Gerhardt, M. Birkenmeier, S. Schwolow, S. Rohn, and P. Weller, “Volatile-compound fingerprinting by headspace-gas-chromatography ion-mobility spectrometry (HS-GC-IMS) as a benchtop alternative to 1H NMR profiling for assessment of the authenticity of honey,” Analytical Chemistry, vol. 90, no. 3, pp. 1777–1785, 2018.
View at: Publisher Site | Google Scholar
D. Cavanna, S. Zanardi, C. Dall'Asta, and M. Suman, “Ion mobility spectrometry coupled to gas chromatography: a rapid tool to assess eggs freshness,” Food Chemistry, vol. 271, pp. 691–696, 2019.
View at: Publisher Site | Google Scholar
X. A. Chen, “Variations of volatile flav-our compounds in fingercitron(Citrus medica L. var. sarcodactylis) pickling process revealed by E-nose, HS-SPME-GC-MS and HS-GC-IMS,” Food res int1, vol. 38, Article ID 109717, 2020.
View at: Publisher Site | Google Scholar
D. Chen, X.-x. Xin, H.-c. Qian, Z.-y. Yu, and L.-r. Shen, “Evaluation of the major royal jelly proteins as an alternative to fetal bovine serum in culturing human cell lines,” Journal of Zhejiang University - Science B, vol. 17, no. 6, pp. 476–483, 2016.
View at: Publisher Site | Google Scholar
O. Lowry, N. Rosebrough, A. L. Farr, and R. Randall, “Protein measurement with the Folin phenol reagent,” Journal of Biological Chemistry, vol. 193, no. 1, pp. 265–275, 1951.
View at: Publisher Site | Google Scholar
Q. Ma, J. Bi, J. Yi, X. Wu, X. Li, and Y. Zhao, “Stability of phenolic compounds and drying characteristics of apple peel as affected by three drying treatments,” Food Science and Human Wellness, vol. 10, no. 2, pp. 174–182, 2021.
View at: Publisher Site | Google Scholar
P. R. Pandeya, R. Lamichhane, K. H. Lee et al., “Bioassay-guided isolation of active anti-adipogenic compound from royal jelly and the study of possible mechanisms,” BMC Complementary and Alternative Medicine, vol. 19, no. 33, p. 33, 2019.
View at: Publisher Site | Google Scholar
W. Wardencki and J. Curyo, “A review of theoretical and practical aspects of solid-phase microextraction in food analysis,” Inter j food sci tech, vol. 39, pp. 703–717, 2010.
View at: Google Scholar
J. Wang and Y. Li, “Optimization of HS-SPME/GC-MSmethod for determination ofvolatile components in royal jelly,” Fish Farming International, vol. 46, pp. 239–245, 2020.
View at: Google Scholar
M. Li, R. Yang, H. Zhang, S. Wang, D. Chen, and S. Lin, “Development of a flavor fingerprint by HS-GC-IMS with PCA for volatile compounds of Tricholoma matsutake Singer,” Food Chemistry, vol. 290, pp. 32–39, 2019.
View at: Publisher Site | Google Scholar
E. Boselli, M. F. Caboni, A. G. Sabatini, G. L. Marcazzan, and G. Lercker, “Determination and changes of free amino acids in royal jelly during storage,” Apidologie, vol. 34, no. 2, pp. 129–137, 2003.
View at: Publisher Site | Google Scholar
N. Cebi, F. Bozkurt, M. T. Yilmaz, and O. Sagdic, “An evaluation of FTIR spectroscopy for prediction of royal jelly content in hive products,” Journal of Apicultural Research, vol. 59, no. 2, pp. 146–155, 2020.
View at: Publisher Site | Google Scholar
L. M. Wu et al., “Research on overall assessment of royaljelly freshness by FTIR spectroscopy,” Spectroscopy and Spectral Analysis, vol. 29, pp. 3236–3240, 2009.
View at: Google Scholar
N. López-Gutiérrezet, “Fast analysis of polyphenols in royal jelly products using automatedTurboFlow™-liquidchromatography-Orbitrap high resolution mass spectrometry,” J chromatogra. B, vol. 973, pp. 17–28, 2014.
View at: Google Scholar
P. A. Tarantilis, C. S. Pappas, E. Alissandrakis, P. C. Harizanis, and M. G. Polissiou, “Monitoring of royal jelly protein degradation during storage using Fourier-transform infrared (FTIR) spectroscopy,” Journal of Apicultural Research, vol. 51, no. 2, pp. 185–192, 2012.
View at: Publisher Site | Google Scholar
X.-x. Xin, Y. Chen, D. Chen et al., “Supplementation with major royal-jelly proteins increases lifespan, feeding, and fecundity in Drosophila,” Journal of Agricultural and Food Chemistry, vol. 64, no. 29, pp. 5803–5812, 2016.
View at: Publisher Site | Google Scholar
X. Liu, C. Jiang, Y. Chen, F. Shi, C. Lai, and L. Shen, “Major royal jelly proteins accelerate onset of puberty and promote ovarian follicular development in immature female mice,” Food Science and Human Wellness, vol. 9, no. 4, pp. 338–345, 2020.
View at: Publisher Site | Google Scholar
A. Buttstedt, C. H. Ihling, M. Pietzsch, and R. F. A. Moritz, “Royalactin is not a royal making of a queen,” Nature, vol. 537, no. 7621, pp. E10–E12, 2016.
View at: Publisher Site | Google Scholar
H. O. Mokaya, L. K. Njeru, and H. M. G. Lattorff, “African honeybee royal jelly: p,” Food Bioscience, vol. 37, Article ID 100733, 2020.
View at: Publisher Site | Google Scholar
J. T. Qao et al., “Nonenzymaticbrowning and proteinaggregation in royal jelly during roomtemperature storage,” Journal of Agricultural and Food Chemistry, vol. 66, pp. 1881–1888, 2018.
View at: Google Scholar
S. Ahmad, M. G. Campos, F. Fratini, S. Z. Altaye, and J. Li, “New insights into the biological and pharmaceutical properties of royal jelly,” International Journal of Molecular Sciences, vol. 21, pp. 1–26, 2020.
View at: Publisher Site | Google Scholar
A. Pina, O. Begou, D. Kanelis, H. Gika, and A. Zotou, “Targeted profiling of hydrophilic-constituents of royal-jelly by hydrophilic interaction liquid chromatographytandem mass spectrometry,” Journal of Chromatography, vol. 1531, pp. 53–63, 2017.
View at: Google Scholar

Copyright

Copyright © 2022 Di Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies