Characterization of Various Honey Samples from Different Regions of Morocco Using Physicochemical Parameters, Minerals Content, Antioxidant Properties, and Honey-Specific Protein Pattern

Lyoussi, Badiaa; Bakour, Meryem; El-Haskoury, Redouan; Imtara, Hamada; Hano, Christophe; Bíliková, Katarína

doi:https://doi.org/10.1155/2022/6045792

Journal of Food Quality

On this page

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

Special Issue

Biological Potential and Chemical Composition of Functional Food

View this Special Issue

Research Article | Open Access

Volume 2022 | Article ID 6045792 | https://doi.org/10.1155/2022/6045792

Characterization of Various Honey Samples from Different Regions of Morocco Using Physicochemical Parameters, Minerals Content, Antioxidant Properties, and Honey-Specific Protein Pattern

Badiaa Lyoussi,¹Meryem Bakour,¹Redouan El-Haskoury,¹Hamada Imtara,²Christophe Hano,³and Katarína Bíliková⁴

Academic Editor: Ali Akbar

Received15 Jul 2022

Accepted22 Aug 2022

Published20 Sept 2022

Abstract

Honey is a bee product relatively expensive; therefore, it has been a target of adulteration by many sweeteners. In this work, we evaluated the good quality, authenticity, and content in bioactive molecules of twenty-two Moroccan honey from different botanical origins and geographical areas. For that, the following analyses were determined: the content in total protein and especially the major royal jelly protein (apalbumin 1), the analysis of total acidity, free acidity, lactonic acidity, pH, ash, Pfund, electrical conductivity, and moisture. In addition, the content of sodium, potassium, calcium, and magnesium, the dosage of polyphenols, flavones, and flavonols, and the antioxidant activities were assessed. All analyzed samples had good antioxidant activities and present a source of antioxidant compounds, the predominant mineral in all honey samples was potassium, and the physicochemical parameters are in line with the standards’ recommended limits. The content of honey samples in total protein and apalbumin 1 ranged between 212 μg/g and 4121.2 μg/g and between 27.4 μg/g and 790.82 μg/g, respectively. Overall, the detection of apalbumin 1 in all honey samples and the results of physicochemical parameters, minerals, bioactive compounds, and antioxidant activities confirm the authenticity and no adulteration of Moroccan honey.

1. Introduction

Honey is a sweet product produced by bees from the nectar of plants. It is nutritious and has traditionally been consumed by humans since the oldest times [1]. Honey is a complex mixture that comprises carbohydrates (60–85%) mainly glucose and fructose, water (12–23%), and other minor constituents such as proteins, enzymes, free amino acids, lipids, vitamins, phenolic acids, flavonoids, and mineral salts [2]. The biochemical composition of honey mostly depends on its floral source, the honey bee species, weather conditions, and geographical origin [3].

There is a large volume of published studies describing the role of honey as functional food, it has been reported that honey has several pharmacological effects such as antioxidant, anticancer, antimicrobial, and inflammatory effects [4, 5]. It is widely used in wound healing and can counteract inflammation [6].

Honey is relatively expensive; thus, it has been a target of adulteration by many adulterants such as corn syrup, sugar, and cane [7]. To verify the authenticity of honey, many tools are recommended such as physicochemical parameters, sensory analysis, microscopical examination, and the analysis of chemical composition [1, 8]. In addition to that, apalbumin 1 is among the main protein that exists in royal jelly and also in honey; it has been suggested to use it as a marker of authenticity and quality of honey since this protein is specific to bees and cannot be replaced by other ingredients [9]. Therefore, the objective of this work was to determine the authenticity and quality of honey samples of different botanical and geographical origins in Morocco by the analysis of physicochemical parameters (pH, free acidity, lactone acidity, total acidity, moisture, electrical conductivity, ash, and Pfund), minerals content (sodium, potassium, calcium, magnesium), antioxidant content and activities (polyphenols, flavones/flavonols, DPPH, ABTS, RP), and the analysis of total protein and more specifically apalbumin 1.

2. Material and Methods

2.1. Honey Samples

Twenty-two honey samples were obtained from beekeepers, who installed their hives in seven different regions of Morocco. Three samples were multifloral, and nineteen were monofloral (the pollen grains of the predominant plant are higher than 45%). The honey samples S1, S4, S8, S11, S12, S18, S20, and S21 were obtained from the Fez-Meknes region. The honey samples S2, S6, S13, S14, S17, and S22 were obtained from the Rabat-Salé-Kénitra region. The honey sample S3 was obtained from the Souss-Massa region. The honey samples S5 and S7 were presented from the Oriental region. The sample S9 was presented from the Drâa-Tafilalet region. The honey samples S10, S15, and S16 were obtained from the Beni Mellal-Khenefra region, and honey sample S19 was obtained from the Tangier-Tetouan-Al Hoceïma. The honey samples were produced by three different bee species: Apis mellifera intermissa, Apis mellifera sahariensis, and Apis mellifera major (Table 1 and Figure 1).

2.2. Melissopalynological Analysis

The botanical origin of honey samples was determined using the method described by Louveaux et al. [10]. A minimum of 1000 pollen grains were counted for each honey sample under a microscope. If the percentage of any type of pollen grains found in honey exceeds 45% of the total pollen grains content, it is classified as the predominant and the honey is classified as monofloral.

2.3. Physicochemical Analysis

Total acidity, free acidity, lactonic acidity, pH, ash, electrical conductivity, and moisture, were analyzed using the methods recommended by the International Honey Commission [11]. Pfund was determined as described previously by Laaroussi et al. [12].

2.4. Minerals Content

The analysis of minerals elements (Na, K, Ca, and Mg) of honey samples was carried out using ICP- AES after the calcination method as described by Laaroussi et al. [12]. Briefly, the honey ashes were mixed with 5 ml of nitric acid 0.1 M and stirred on a heating plate until the total evaporation of nitric acid. Then, 10 ml of nitric acid was added and the mixture was made up to 25 ml with ultrapure water. All samples were analyzed in triplicate.

2.5. Polyphenols Content

The polyphenols content was assessed using the Folin-Ciocalteu method [13]. Briefly, 100 μL of aqueous extract of honey was mixed with 500 μl of Folin-Ciocalteau reagent solution (10 g of sodium tungstate and 2.5 g of sodium molybdate (2.5 g) were dissolved in 70 ml of distilled water; then, 5 ml of phosphoric acid (85%) and 10 ml of concentrated hydrochloric acid were added. After 10 hours, 15 g of lithium sulfate and 5 ml of distilled water were added and brought to 100 ml with distilled water) for 6 min, and then 400 μl of sodium carbonate (75 g/l) was added to the mixture. The absorbance was measured at 760 nm after 15 min of incubation. Gallic acid calibration was used as a standard for calibration. The results were expressed as milligrams of Gallic acid equivalents per gram (mg GAE/g).

2.6. Flavones and Flavonols Content

The content of flavones and flavonols was quantified by a colorimetric assay described previously by Bakour et al. [14]. Briefly, 500 μl of honey sample or standard was added to 500 μl of 20% AlCl₃. After 1 h at room temperature, the absorbance was measured at 420 nm. A quercetin calibration curve was prepared, and total content was expressed as mg of quercetin equivalents per 100 g of honey (mg QE/100 g).

2.7. Radical Scavenging Activity (DPPH Assay)

The radical scavenging activity of the honey solution against DPPH free radical was measured using the method described by Bakour et al. [15]. Briefly, 100 μl of the aqueous honey extract was mixed with 900 μl of a 100 μM solution of DPPH radical prepared in ethanol (96%). The absorbance of the solution was measured at 540 nm after 30 min of incubation in the dark. Several concentrations of samples were made, and the IC₅₀ (concentration of sample able to scavenge 50% of DPPH free radical) was determined graphically using the curve plotted by the percentage of DPPH inhibition as a function of the sample concentration:

2.8. Azino-Bis (3-Ethylbenzothiazoline-6-Sulphonic Acid (ABTS)

Azino-bis (3-ethylbenzothiazoline-6-sulphonic acid (ABTS) free radical scavenging activity was analyzed using the method described by Bakour et al. [15]. 75 μl of aqueous extract of honey or standard control (BHT) was mixed with 825 μl of ABTS solution, and the absorbance of the mixture was measured after 6 min at 734 nm. The tests were carried out in triplicate, and the IC₅₀ (concentration of sample able to scavenge 50% of ABTS free radical) was determined graphically using the curve plotted by the percentage of ABTS inhibition as a function of the sample concentration (equation (1)).

2.9. Ferric Reducing Power

The reducing power of the aqueous honey extract was determined using the method described by Bakour et al. [15]. 50 μl of aqueous honey extract (50% W/V) was mixed with 200 μl of 0.2 M sodium phosphate buffer (pH 6.6) and 200 μl of 1% potassium ferricyanide. The mixture was incubated at 50°C for 20 min. Then, 200 μl of 10% trichloroacetic acid (TCA) was added, and the mixture was centrifuged at 3000 rpm for 10 min. 500 μl of the above solution from each reaction was diluted with 500 μl of distilled water, and 100 μl of 0.1% ferric chloride (FeCl₃) was added. The absorbance was measured at 700 nm, and ascorbic acid was used as a reference standard. The results were represented in EC₅₀ values, corresponding to the concentration providing 50% of the antioxidant activity or 0.5 of absorbance in the reducing power assay measured at 700 nm.

2.10. Determination of Protein Concentration

The total protein content of the honey samples was determined by microplate assay according to Bradford [16]. To 100 μl of the sample or its dilution in physiological solution was added 100 μl of QuickStart Bradford reagent (BioRad, Laboratories, Inc., USA). The absorbance was measured at 595 nm. Bovine serum albumin (BSA, Sigma, USA) was used as standard. Each sample was analyzed at three dilutions and each dilution in three parallel analyses.

2.11. Determination of Apalbumin 1 in Honey by ELISA

Honey samples were analyzed using enzyme-linked immunosorbent assay (ELISA) for apalbumin 1 quantification as described previously in detail [17]. The 96 well/flat-bottom microtiter plates (Brand, Germany) were coated with antigen-diluted honey samples at dilution of 0.05% and/or 0.001% in Milli-Q water and/or standard solution of apalbumin 1 and incubated overnight at 4°C. After washing with TBS buffer (100 mmol/L Tris and 150 mmol/L NaCl, pH 7.5), the plates were incubated with polyclonal rabbit anti-apa1 antibody in milk buffer (2% nonfat milk in TBS) and then with peroxidase-conjugated anti-rabbit IgG in milk buffer for 1 h. Detection was done by adding 3% ABTS (2,2′-azino-bis-(3-benzthiazoline-6-sulfonic acid, Southern Biotech, USA), in 50 mmol/L citrate buffer pH 4.3; supplemented by hydrogen peroxide. The absorbance at 405 nm was read in a Microplate Spectrophotometer Power Wave TM XS (BioTek Instruments, INC, Winooski, Vermont, USA).

2.12. Statistical Analysis

All data are presented as mean ± SD (standard deviation). Graphpad prism (version 5.0; GraphPad Software, Inc., San Diego, USA) was used to compare honey samples using a one-way analysis of variance (ANOVA) followed by Tukey’s test, and was considered significant. Correlations between the parameters studied were achieved by the Pearson correlation coefficient (r). The principal component analysis (PCA) was accomplished using Past: paleontological statistics software package for education and data analysis, version 3.20.

3. Results and Discussion

3.1. Physicochemical Parameters

Twenty-two honey samples of different botanical and geographical origins of Morocco were analyzed for physicochemical parameters. The results presented in Table 2 showed that the pH values ranged between 3.59 ± 0.10 in Euphorbia resinifera honey from Tiznit and 4.30 ± 0.20 in Ziziphus lotus honey from Marmoucha; these values are within the range recommended by Council Directive 2001/110/EC [18]. Free acidity ranged between 11.45 ± 0.12 mEq/kg in Salvia rosmarinus honey and 30.81 ± 1.20 mEq/kg in Thymus vulgaris from Timhdit, lactone acidity ranged between 5.09 ± 0.96 mEq/kg in Ziziphus lotus honey and 17.50 ± 0.22 mEq/kg in Bupleurum spinosum honey, and total acidity ranged between 18.30 ± 0.30 mEq/kg in Citrus sinensis honey and 42.28 ± 0.30 mEq/kg in Ceratonia siliqua honey. These values are in line with those recommended by Codex Alimentarius Commission [19]. For moisture values, all honey samples are below the maximum limit (20%) except the Arbutus unedo honey sample from Tetouan which was slightly higher (20.90 ± 0.15%). The recommended value of moisture in honey indicates its maturity and reflects the desirable density [20]. For electrical conductivity, all honey samples are bellowing the maximum limit allowed (800 μS/cm) except Ceratonia siliqua honey from Taounate (948.33 ± 1.63 μS/cm) and Arbutus unedo honey from Tetouan (913.51 ± 6.21 μS/cm). Similarly, the ash contents in all honey samples are below the limits (0.6%) except for the multifloral honey sample from Skoura (0.92 ± 0.02%). The ash content reflects the mineral composition in honey. It is influenced by soil and botanical origins [12]. On the other hand, Pfund is a parameter that reflects honey color, the analysis of Pfund showed values ranging between 19.67 ± 0.64 mm in Citrus limon honey and 128.74 ± 1.20 mm in Ceratonia siliqua honey. According to the Pfund scale, the color of our honey samples ranged between white color and dark amber [21].

3.2. Minerals Content

The mineral contents in honey samples were summarized in Table 2; the predominant metal in the majority of honey samples was potassium followed by sodium, calcium, and then magnesium. The same results were obtained by Bouhlali et al. [22] for eleven Moroccan honey from various floral origins.

The Arbutus unedo honey sample presented the highest potassium content of 1299.56 ± 3.25 mg/kg, and Salvia rosmarinus honey presented the lowest content (270.57 ± 0.85 mg/kg). The contents in sodium ranged between 41.64 ± 0.54 mg/kg in Salvia rosmarinus honey and 264.56 ± 0.45 mg/kg in Arbutus unedo honey, and the contents in calcium ranged between 22.12 ± 0.21 in multifloral honey sample from Skoura and 283.13 ± 2.36 mg/kg in Arbutus unedo honey, and the contents in magnesium ranged between 13.55 ± 0.56 mg/kg in Ziziphus lotus honey from Marmoucha and 218.72 ± 1.54 mg/kg in multifloral from Elmers. The mineral content in honey is influenced by soil composition, botanical origin, climatic conditions, and seasonal variations [23].

Honey is a good source of trace elements that are essential for the proper functioning of the body [24]. Many studies have shown the pharmacological effect of dietary minerals; for instance, it was proven that potassium plays a crucial role in endothelial and cardiovascular function and can reduce blood pressure [25]. Similarly, calcium dietary intake is very important for the good health of the skeleton, the function of skeletal muscles, and nerve conduction [26, 27]. In addition, it was proven in a study conducted by Kh et al. [28] that magnesium supplementation can prevent blood pressure elevation and significantly reduce platelet aggregation.

3.3. Polyphenols, Flavones, Flavonols, and Antioxidant Activities

Polyphenols are secondary metabolites widely present in the plant kingdom and known for their pharmacological properties, such as antioxidant, anti-inflammatory, immunomodulatory, and antidiabetic effects [29, 30]. The analysis of polyphenols in honey samples revealed a range between 13.70 ± 0.30 mg GAE/100 g found in the Citrus sinensis honey sample (S5) and 246.20 ± 10.40 mg GAE/100 g in Ceratonia siliqua honey (S12). Flavones and flavonols ranged between 0.70 ± 0.10 mg QE/100 g in Citrus sinensis honey sample (S5) and 31.70 ± 1.70 mg QE/100 g Ceratonia siliqua honey (S12) (Table 3). Our results are higher than those obtained by Petretto et al. [31] for seven commercial Moroccan honey samples from different floral origins and lower than those found in monofloral honey (Bupleurum spinosum) collected from Moroccan Middle Atlas [12]. Moreover, the antioxidant compounds’ rate in honey is affected by several factors such as its floral source, geographical origin, honey maturation processing, handling, and storage [32]. In addition, we observed that honey samples from the same botanical origin (S2 and S17: Ammi visnaga), (S4 and S15: Ziziphus lotus), (S10, S11, S12: Ceratonia siliqua) have different content in antioxidant compounds; the same results were found by Laaroussi et al. [12]. This is explained by the presence of secondary pollen and nectar from other floral sources [33].

Concerning the antioxidant activity, the DPPH method is largely used to test the free radical scavenging ability of various samples [20, 34]. The DPPH IC₅₀ values (the concentration with scavenging activity of 50%) of Moroccan honey samples showed significant differences among analyzed samples and ranged between 9.3 ± 1.0 mg/ml in Ziziphus lotus honey sample and 93.40 ± 6.10 mg/ml in Citrus sinensis honey sample.

The second method used to evaluate the antioxidant activity of honey samples was the ABTS cation radical assay (ABTS^•+). It is based on the interaction between the nitrogen atom of ABTS and hydrogen donating antioxidant; this reaction produces the decolorization of the solution [34]. The IC₅₀ of the ABTS test ranged between 58.96 ± 0.92 mg/ml in the Citrus limon honey sample and 2.30 ± 0.10 mg/ml in the Ziziphus lotus honey sample (Table 3). Furthermore, the reducing power on the ferric ion of honey samples was analyzed; this method is based on the reduction of ferric ion Fe (III) to ferrous ion Fe (II) by the antioxidant compound. The reaction was visualized by the formation of Perl’s Prussian blue complex with maximum absorption at 700 nm [35]. The results of reducing power showed a range of EC₅₀ between 1.60 ± 0.01 mg/ml obtained by Ziziphus lotus honey from Marmoucha and 17.58 ± 0.34 mg/ml obtained by Citrus limon honey from Khnichat.

3.4. Proteins and Apalbumin 1 Content

Proteins are one of the minor compounds found in honey. Their percentages vary according to the honeybee origin. The honey produced by Apis mellifera contains a range between 0.6% and 1.6% of proteins while the honey produced by Apis cerana contains a range between 0.1% and 3.3% of proteins [36]. It was reported that the amount of protein from bee secretions in honey is higher than that of protein from plants [37]. Among these proteins, there are enzymes responsible for the transformation of nectar components into honey such as glucose-6-oxidase, invertase, and diastase [9]. Furthermore, the major royal jelly protein “apalbumin 1” is one of the most abundant proteins in honey originating from bee secretions, it is an important criterion for honey quality examination, and its detection in honey samples is an indicator of the authenticity and no adulteration [9]. In addition, this protein of 55 kDa had a wide range of biological properties and health-promoting functions such as the immunostimulation effect, the increase of TNF-α release by macrophages, and the antihypertensive activity [38–40].

The results of total protein and apalbumin-1 content in honey are summarized in Table 4 and Figure 2. According to the results obtained, the range of protein content in honey samples was between 0.021% found in Salvia rosmarinus honey and 0.412% found in Bupleurum spinosum honey. These results are in line with those obtained in other studies [17, 36].

For apalbumin 1 analysis, the highest content was shown in Origanum vulgare honey (790.82 μg/g), it represents 58.24% of total protein presented in this honey, followed by Bupleurum spinosum honey (787.73 μg/g), and it represents 19.11% of total protein. Whereas the lowest content of apalbumin 1 was found in Salvia rosmarinus honey (212 μg/g), it represents 12.92% of total protein. As shown in Table 4, the percentage of apalbumin 1 in honey samples ranged between 0.011% and 0.079%; these results are higher than those obtained for honey samples from Italia and Slovakia ranging between 0.08% and 0.03% [17].

Overall, the obtained results showed that all analyzed samples contain an important amount of apalbumin 1, the detection of this protein in honey is a criterion of honey’s good quality, and it is an indicator of authenticity and no adulteration [9].

3.5. Correlation and Multivariate Analysis

The correlation test between the studied parameters is presented in Table 5. The results revealed significant Pearson correlations () among the different parameters. The antioxidant compounds (polyphenols, flavones, and flavonols) correlate positively with total acidity, ash, Pfund, and the content of sodium and potassium. Polyphenols content correlates negatively with ABTS, DPPH, and RP tests (r = −0.420, r = −0.595, and r = −0.746, respectively). On the other hand, flavones and flavonols correlate negatively with DPPH (r = −0.578) and RP (r = −0.737). RP test correlates positively with DPPH and ABTS (r = 0.553 and r = 0.799, respectively). Total acidity correlates positively with free acidity (r = 0.917) and lactonic acidity (r = 0.614). Electrical conductivity correlates positively with total acidity (r = 0.459), ash (r = 0.765), Pfund (r = 0.611), sodium (r = 0.738), potassium (r = 0.738), calcium (r = 0.562), polyphenols (r = 0.678), and flavones and flavonols (r = 0.685). The content in apalbumin 1 correlates positively with total acidity (r = 0.431), Pfund (r = 0.471), and the content in protein (r = 0.554) while the protein content correlates negatively with pH (r = −0.480) and positively with free acidity (r = 0.554), lactone acidity (r = 0.629), total acidity (r = 0.710), and Pfund (r = 0.570). Furthermore, a principal component analysis (PCA) was applied to the obtained results (Figure 3). PCA is one of the techniques most used for performing multivariate analysis; it is characterized by low difficulty and rapid analysis [41]. Figure 3(a) represents the PCA for physicochemical analysis of the studied honey samples; the PC1 and PC2 explained a variance of 56%. The first component (PC1) explained 39.274% and represents in its positive part all parameters studied except pH that exists in the negative part. The second component (PC2) explained 16.726% and represents in its positive part pH, moisture, Mg, Ca, K, Na, ash, and electrical conductivity, while in the negative part we found Pfund, free acidity, total acidity, and lactonic acidity. The honey samples S8, S9, S7, S4, and S15 shared characteristics regarding pH, moisture, Mg, Ca, K, Na, ash, and electrical conductivity, whereas the honey samples S21 and S18 shared the characteristics for Pfund, free acidity, total acidity, and lactonic acidity.

(a)

(b)

Figure 3(b) represents the PCA for polyphenols, flavones/flavonols, the antioxidant activities (DPPH, ABTS, and RP) and the content in total protein and apalbumin 1. The two principal components (PC1 and PC2) explained a variance of 76.973%. The first component explained 55.936% and represents in its positive part apalbumin 1, proteins, polyphenols, and flavones/flavonols, and in its negative part, we found the antioxidant test (DPPH, ABTS, and RP), whereas the second component explained 21.037% and represents in its positive part proteins, apalbumin 1, DPPH, and ABTS and in its negative part polyphenols, flavones/flavonols, and ABTS. S4, S11, and S7 honey samples shared the characteristics for polyphenols and flavones/flavonols content while S15, S17, S18, S19, S20, S21, and S22 honey samples shared the characteristics for apalbumin 1 and proteins. It was suggested that the difference in the physicochemical parameters, minerals content, and bioactive molecules of honey is related to the soil composition, botanical origin, and climatic conditions [32]. In sum, this study supplied new information about the antioxidant activity, protein, and apalbumin contents in Moroccan honey obtained from different botanical origins.

4. Conclusions

Our results assert that Moroccan honey samples are rich in bioactive compounds such as polyphenols, flavones/flavonols, and proteins and are endowed with great antioxidant activities. Nevertheless, the detection of the major royal jelly protein apalbumin 1 in all analyzed samples confirms the quality and no adulteration of Moroccan honey.

Data Availability

The data used to support the findings of this study are included within the article.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This work was supported by funds from the Conseil Régional Centre-Val de Loire and Conseil Départementald’Eure et Loir.

References

M. Sahlan, S. Karwita, M. Gozan et al., “Identification and classification of honey’s authenticity by attenuated total reflectance Fourier-transform infrared spectroscopy and chemometric method,” Veterinary World, vol. 12, no. 8, pp. 1304–1310, 2019.
View at: Publisher Site | Google Scholar
A. A. Machado De-Melo, L. B. Almeida-Muradian, M. T. Sancho, and A. Pascual-Maté, “Composition and properties of Apis mellifera honey: a review,” Journal of Apicultural Research, vol. 57, no. 1, pp. 5–37, 2018.
View at: Publisher Site | Google Scholar
S. M. Kadri, R. Zaluski, and R. O. Orsi, “Nutritional and mineral contents of honey extracted by centrifugation and pressed processes,” Food Chemistry, vol. 218, pp. 237–241, 2017.
View at: Publisher Site | Google Scholar
R. El-Haskoury, N. Al-Waili, J. El-Hilaly, W. Al-Waili, and B. Lyoussi, “Antioxidant, hypoglycemic, and hepatoprotective effect of aqueous and ethyl acetate extract of carob honey in streptozotocin-induced diabetic rats,” Veterinary World, vol. 12, pp. 1916–1923, 2019.
View at: Publisher Site | Google Scholar
B. Kaya and A. Yıldırım, “Determination of the antioxidant, antimicrobial and anticancer properties of the honey phenolic extract of five different regions of Bingöl province,” Journal of Food Science & Technology, vol. 58, no. 6, pp. 2420–2430, 2021.
View at: Publisher Site | Google Scholar
H. Imtara, N. Al-Waili, M. Bakour, W. Al-Waili, and B. Lyoussi, “Evaluation of antioxidant, diuretic, and wound healing effect of Tulkarm honey and its effect on kidney function in rats,” Veterinary World, vol. 11, no. 10, pp. 1491–1499, 2018.
View at: Publisher Site | Google Scholar
R. Fakhlaei, J. Selamat, A. Khatib et al., “The toxic impact of honey adulteration: a review,” Foods, vol. 9, no. 11, p. 1538, 2020.
View at: Publisher Site | Google Scholar
S. Bogdanov, “Authenticity of honey and other bee products: state of the art,” Bulletin of University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca. Animal Science and Biotechnologies, vol. 63, p. 64, 2007.
View at: Google Scholar
K. Bilikova, T. Kristof Krakova, K. Yamaguchi, and Y. Yamaguchi, “Major royal jelly proteins as markers of authenticity and quality of honey,” Archives of Industrial Hygiene and Toxicology, vol. 66, no. 4, pp. 259–267, 2015.
View at: Publisher Site | Google Scholar
J. Louveaux, A. Maurizio, and G. Vorwohl, “Methods of melissopalynology,” Bee World, vol. 59, no. 4, pp. 139–157, 1978.
View at: Publisher Site | Google Scholar
S. Bogdanov, Harmonised Methods of the International Honey Commission, Swiss Bee Research Centre FAM, Bern, Switzerland, vol. 5, pp. 1–62, 2002.
H. Laaroussi, T. Bouddine, M. Bakour, D. Ousaaid, and B. Lyoussi, “Physicochemical properties, mineral content, antioxidant activities, and microbiological quality of Bupleurum spinosum gouan honey from the middle atlas in Morocco,” Journal of Food Quality, vol. 2020, Article ID 7609454, 12 pages, 2020.
View at: Publisher Site | Google Scholar
H. Laaroussi, M. Bakour, D. Ousaaid et al., “Protective effect of honey and propolis against gentamicin-induced oxidative stress and hepatorenal damages,” Oxidative Medicine and Cellular Longevity, vol. 2021, Article ID 9719906, 19 pages, 2021.
View at: Publisher Site | Google Scholar
M. Bakour, M. D. G. Campos, H. Imtara, and B. Lyoussi, “Antioxidant content and identification of phenolic/flavonoid compounds in the pollen of fourteen plants using HPLC-DAD,” Journal of Apicultural Research, vol. 59, pp. 35–41, 2019.
View at: Publisher Site | Google Scholar
M. Bakour, Â. Fernandes, L. Barros, M. Sokovic, I. C. F. R. Ferreira, and B. Lyoussi, “Bee bread as a functional product: chemical composition and bioactive properties,” LWT—Food Science and Technology, vol. 109, pp. 276–282, 2019.
View at: Publisher Site | Google Scholar
M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, no. 1-2, pp. 248–254, 1976.
View at: Publisher Site | Google Scholar
K. Bilikova and J. Simuth, “New criterion for evaluation of honey: quantification of royal jelly protein apalbumin 1 in honey by ELISA,” Journal of Agricultural and Food Chemistry, vol. 58, no. 15, pp. 8776–8781, 2010.
View at: Publisher Site | Google Scholar
Council of the European Union, “Council directive 2001/110/EC of 20 december 2001 relating to honey,” Official Journal of the European Communities, vol. 10, pp. 47–52, 2002.
View at: Google Scholar
Codex Alimentarius Commission, Revised Codex Standard for Honey, Codex Alimentarius Commission, Rome, Italy, vol. 12, 1981.
S. Singh and R. P. Singh, “In vitro methods of assay of antioxidants: an overview,” Food Reviews International, vol. 24, no. 4, pp. 392–415, 2008.
View at: Publisher Site | Google Scholar
A. Belay, W. Solomon, G. Bultossa, N. Adgaba, and S. Melaku, “Botanical origin, colour, granulation, and sensory properties of the Harenna forest honey, Bale, Ethiopia,” Food Chemistry, vol. 167, pp. 213–219, 2015.
View at: Publisher Site | Google Scholar
E. T. Bouhlali, M. Bammou, K. Sellam et al., “Physicochemical properties of eleven monofloral honey samples produced in Morocco,” Arab Journal of Basic and Applied Sciences, vol. 26, no. 1, pp. 476–487, 2019.
View at: Publisher Site | Google Scholar
M. A. Morgano, M. C. T. Martins, L. C. Rabonato, R. F. Milani, K. Yotsuyanagi, and D. B. Rodriguez-Amaya, “A comprehensive investigation of the mineral composition of Brazilian bee pollen: geographic and seasonal variations and contribution to human diet,” Journal of the Brazilian Chemical Society, vol. 23, pp. 727–736, 2012.
View at: Publisher Site | Google Scholar
M. Solayman, M. A. Islam, S. Paul et al., “Physicochemical properties, minerals, trace elements, and heavy metals in honey of different origins: a comprehensive review,” Comprehensive Reviews in Food Science and Food Safety, vol. 15, no. 1, pp. 219–233, 2016.
View at: Publisher Site | Google Scholar
K. J. Aaron and P. W. Sanders, “Role of dietary salt and potassium intake in cardiovascular health and disease: a review of the evidence,” Mayo Clinic Proceedings, vol. 88, no. 9, pp. 987–995, 2013.
View at: Publisher Site | Google Scholar
R. Heaney, “The importance of calcium intake for lifelong skeletal health,” Calcified Tissue International, vol. 70, no. 2, pp. 70–73, 2002.
View at: Publisher Site | Google Scholar
B. Tandoğan and N. N. Ulusu, “Importance of calcium,” Turkish Journal of Medical Sciences, vol. 35, pp. 197–201, 2005.
View at: Google Scholar
R. Kh, M. Khullar, M. Kashyap, P. Pandhi, and R. Uppal, “Effect of oral magnesium supplementation on blood pressure, platelet aggregation and calcium handling in deoxycorticosterone acetate induced hypertension in rats,” Journal of Hypertension, vol. 18, no. 7, pp. 919–925, 2000.
View at: Publisher Site | Google Scholar
H. Laaroussi, M. Bakour, D. Ousaaid et al., “Effect of antioxidant-rich propolis and bee pollen extracts against D-glucose induced type 2 diabetes in rats,” Food Research International, vol. 138, Article ID 109802, 2020.
View at: Publisher Site | Google Scholar
N. Yahfoufi, N. Alsadi, M. Jambi, and C. Matar, “The immunomodulatory and anti-inflammatory role of polyphenols,” Nutrients, vol. 10, no. 11, p. 1618, 2018.
View at: Publisher Site | Google Scholar
G. L. Petretto, C. I. G. Tuberoso, G. Vlahopoulou et al., “Volatiles, color characteristics and other physico-chemical parameters of commercial Moroccan honeys,” Natural Product Research, vol. 30, no. 3, pp. 286–292, 2016.
View at: Publisher Site | Google Scholar
M. E. A. Mohammed, “Factors affecting the physicochemical properties and chemical composition of bee’s honey,” Food Reviews International, vol. 38, no. 6, pp. 1330–1341, 2020.
View at: Publisher Site | Google Scholar
S. Aazza, B. Lyoussi, D. Antunes, and M. G. Miguel, “Physicochemical characterization and antioxidant activity of 17 commercial Moroccan honeys,” International Journal of Food Sciences & Nutrition, vol. 65, no. 4, pp. 449–457, 2014.
View at: Publisher Site | Google Scholar
A. M. Pisoschi and G. P. Negulescu, “Methods for total antioxidant activity determination: a review,” Biochemistry & Analytical Biochemistry, vol. 1, p. 106, 2011.
View at: Google Scholar
M. N. Alam, N. J. Bristi, and M. Rafiquzzaman, “Review on in vivo and in vitro methods evaluation of antioxidant activity,” Saudi Pharmaceutical Journal, vol. 21, no. 2, pp. 143–152, 2013.
View at: Publisher Site | Google Scholar
S.-R. Won, C.-Y. Li, J.-W. Kim, and H.-I. Rhee, “Immunological characterization of honey major protein and its application,” Food Chemistry, vol. 113, no. 4, pp. 1334–1338, 2009.
View at: Publisher Site | Google Scholar
G. Cebrero, O. Sanhueza, M. Pezoa et al., “Relationship among the minor constituents, antibacterial activity and geographical origin of honey: a multifactor perspective,” Food Chemistry, vol. 315, Article ID 126296, 2020.
View at: Publisher Site | Google Scholar
J. Majtán, E. Kovácová, K. Bíliková, and J. Simúth, “The immunostimulatory effect of the recombinant apalbumin 1-major honeybee royal jelly protein-on TNFα release,” International Immunopharmacology, vol. 6, no. 2, pp. 269–278, 2006.
View at: Publisher Site | Google Scholar
T. Matsui, A. Yukiyoshi, S. Doi, H. Sugimoto, H. Yamada, and K. Matsumoto, “Gastrointestinal enzyme production of bioactive peptides from royal jelly protein and their antihypertensive ability in SHR,” The Journal of Nutritional Biochemistry, vol. 13, no. 2, pp. 80–86, 2002.
View at: Publisher Site | Google Scholar
J. Šimúth, K. Bíliková, E. Kováčová, Z. Kuzmová, and W. Schroder, “Immunochemical approach to detection of adulteration in honey: physiologically active royal jelly protein stimulating TNF-α release is a regular component of honey,” Journal of Agricultural and Food Chemistry, vol. 52, no. 8, pp. 2154–2158, 2004.
View at: Publisher Site | Google Scholar
C. I. Mureșan, M. Cornea-Cipcigan, R. Suharoschi, S. Erler, and R. Mărgăoan, “Honey botanical origin and honey-specific protein pattern: characterization of some European honeys,” Lebensmittel-Wissenschaft & Technologie, vol. 154, Article ID 112883, 2022.
View at: Publisher Site | Google Scholar

Copyright

Copyright © 2022 Badiaa Lyoussi 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

Views

514

Downloads

716

Citations