Next Article in Journal
Adaptive Reproductive Strategies of an Ectoparasitoid Sclerodermus guani under the Stress of Its Entomopathogenic Fungus Beauveria bassiana
Next Article in Special Issue
Acceptance by Honey Bees of Wax Decontaminated through an Extraction Process with Methanol
Previous Article in Journal
Differential Susceptibility of Coleomegilla maculata and Scymnus creperus Larvae to Aggression by Solenopsis invicta Workers
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Insects
Volume 14
Issue 4
10.3390/insects14040319
insects-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

The Bioactive Value of Tamarix gallica Honey from Different Geographical Origins

by
Ahmed G. Hegazi
1,
Fayez M. Al Guthami
2,
Mohamed F. A. Ramadan
3,
Ahmed F. M. Al Gethami
4,
A. Morrie Craig
5,†,
Hesham R. El-Seedi
6,7,8,
Inmaculada Rodríguez
9 and
Salud Serrano
9,*
1
Department of Zoonotic Diseases, National Research Centre, Dokki, Giza 12622, Egypt
2
Al Guthami Company, Makkah 24211, Saudi Arabia
3
Pesticide Analysis Research Department, Central Agric. Pesticides Lab., Agric. Res. Center, Giza 12611, Egypt
4
Alnahalaljwal Foundation, Makkah 21926, Saudi Arabia
5
College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331, USA
6
International Research Center for Food Nutrition and Safety, Jiangsu University, Zhenjiang 212013, China
7
International Joint Research Laboratory of Intelligent Agriculture and Agri-Products Processing, Jiangsu Education Department, Jiangsu University, Nanjing 210024, China
8
Department of Chemistry, Faculty of Science, Menoufia University, Shebin El-Koom 32512, Egypt
9
Department of Food Science and Technology, Faculty of Veterinary Medicine, University of Córdoba, 14071 Córdoba, Spain
*
Author to whom correspondence should be addressed.
†
Retired.
Insects 2023, 14(4), 319; https://doi.org/10.3390/insects14040319
Submission received: 3 February 2023 / Revised: 20 March 2023 / Accepted: 24 March 2023 / Published: 27 March 2023
(This article belongs to the Special Issue Bee Products: Status, Properties, Opportunities, and Challenges)
Browse Figure
Review Reports Versions Notes

Abstract

:

Simple Summary

The current study was conducted to characterize Tamarix gallica honey in terms of its antimicrobial and antioxidant activities, melissopalynological analysis, physicochemical and biochemical properties, and total phenolic and flavonoid contents. For this purpose, Tamarix gallica honey samples from Saudi Arabia, Libya, and Egypt were collected and analyzed. Our results reveal the antimicrobial and antioxidant capacities of this type of honey. Tamarix gallica honey could be considered for therapeutical, food manufacturing, or nutraceutical purposes.

Abstract

This study was conducted to assess the bioactive value of Tamarix gallica honey samples collected from three countries. In total, 150 Tamarix gallica honey samples from Saudi Arabia (50), Libya (50), and Egypt (50) were collected and compared, based on the results of the melissopalynological analysis, their physicochemical attributes, antioxidant and antimicrobial activities, and biochemical properties, together with their total phenolic and total flavonoid contents. Depending on the geographical origin, we observed different levels of growth suppression for six resistant bacterial strains. The pathogenic microorganisms tested in this study were Staphylococcus aureus, Streptococcus mutans, Klebsiella pneumoniae, Escherichia coli, Proteus vulgaris, and Pseudomonas aeruginosa. There was a strong correlation between the polyphenol and flavonoid contents, as well as significant (p < 0.05) radical scavenging activities. The melissopalynological analysis and physicochemical properties complied with the recommendation of the Gulf and Egyptian Technical Regulations on honey, as well as the Codex Alimentarius of the World Health Organization and the European Union Normative related to honey quality. It was concluded that Tamarix gallica honey from the three countries has the capacity to suppress pathogenic bacterial growth and has significant radical scavenging activities. Moreover, these findings suggest that Tamarix gallica honey may be considered as an interesting source of antimicrobial compounds and antioxidants for therapeutical and nutraceutical industries or for food manufacturers.

1. Introduction

The drug resistance of some bacterial strains has provoked research into natural antimicrobial agents and plants, which could be the source of novel remedies [1]. Throughout history, natural products (particularly, honey) have been commonly used in nutrition, prevention, and as therapeutical agents. Apis mellifera worker honeybees collect nectar from different plants and produce honey with great diversity depending on the different botanical sources [2,3,4]. Thus, honey quality depends on different factors such as the botanical source, the plant chemical composition, the weather conditions, the soil mineral composition, and the geographical origin [5].
Honeybees produce important medicinal products, such as bee venom, royal jelly, honey, propolis, and beeswax. Honey is the most appreciated and widely used product [6,7]. Promising antimicrobial and antioxidant properties of honey can be applied in prophylaxis and therapeutical use for many diseases. Natural pure honey is well documented to contain novel antimicrobial compounds [8,9,10,11,12,13,14,15].
The antibiotic resistance of some bacterial strains has attracted research on natural honey as an antimicrobial agent [16]. The Tamarix gallica plant is indigenous to Saudi Arabia and the Sinai Peninsula, and it is common around the Mediterranean region. It is a tree or shrub halophyte from coastal regions and deserts, a relatively long-living plant that can tolerate a wide range of environmental conditions and resist abiotic stresses such as salt, high temperature, and drought stresses. Tamarix species are ornamental bushes or trees, known for their feathery foliage, mostly evergreen with pink or white blossoms [17]. Depending on the species, they may reach a large tree size, but most invasive species are multi-stemmed shrubs of less than 8 m that can grow 3 to 4 m in a growing season [18]. The leaves are alternate, sessile, small, punctate, and scalelike with salt-secreting glands and are self-pruning during drought periods [19]. The leaves of the plant are astringent and diuretic, used as an external compress for wounds to stop bleeding and as a laxative, an astringent, an antidiarrheal, and an antidysentery. The major chemical constituents of Tamarix are tamarixin, tamarixetin, troupin, 4-methylcoumarin, 3, 3′-di-0-methylellagic acid, and quercitol (methyl ester) [20]. Numerous polyphenols are also present, including anthocyanins, tannins, flavanones, isoflavones, resveratrol, and ellagic acid.
This genus is used in traditional medicine as a perspiration stimulant, an aperitif, a diuretic, and an astringent, for its antimicrobial activities and bioactive molecules [17]. It is also used in the treatment of various liver disorders due to its anti-inflammatory and antidiarrheic properties. Knowledge of the physical and chemical properties of Tamarix gallica honey is limited [21].
In general, honey authenticity is measured by different international standards, such as the Codex Alimentarius Standard, but this authenticity depends mainly on the geographical and botanical origins. As not much information about Tamarix gallica honey exists, the aim of this study was to assess the antimicrobial and antioxidant properties, as well as the total phenolic and total flavonoid contents, of Tamarix gallica honey from Saudi Arabia, Libya, and Egypt.

2. Materials and Methods

2.1. Materials

The reagents and chemicals used were of analytical grade and purchased from Sigma-Aldrich (St. Louis, MO, USA).

2.2. Honey Samples

In total, 150 fresh Tamarix gallica honey samples (1 kg each) were collected from Saudi Arabia (50), Libya (50), and Egypt (50) during the 2021 harvest. Each honey sample was collected in a sterile universal glass container and kept at 2–8 °C until tested. The melissopalynological analysis corroborated its botanical authenticity as Tamarix gallica honey, which meant that the pollen content of this specific floral source was at least 55% [22,23,24].

2.3. Bacterial Strains

Six antibiotic-resistant bacterial strains (Gram-positive and Gram-negative) were used in this investigation to determine the antibacterial activities of the honey: Staphylococcus aureus (ATCC 25923), Streptococcus mutans (1815T), Proteus vulgaris (ATCC 13315), Pseudomonas aeruginosa (ATCC 27853), Klebsiella pneumoniae (ATCC 27736), and Escherichia coli (ATCC 35218). The identification and susceptibility patterns of all the clinical isolates were performed using the VITEK 2 compact system of the Department of Zoonotic Diseases, National Research Centre (Cairo, Egypt), which kindly provided and maintained these bacterial strains. Muller Hinton Agar (MHA) was used to subculture the bacterial strains. Then, the incubation was carried out at 37 °C overnight. A homogeneous suspension was obtained from a single colony of the tested microorganism using a sterile loop and inoculating it in 3 mL of Muller Hinton Broth (Sigma-Aldrich, St. Louis, MO, USA). To provide 0.5 McFarland  =  1 – 2 × CFU/mL, the suspension was standardized using a calibrated VITEK 2 DENSICHEK (BioMérieux, Inc., Marcy l′Etoile, France) [25,26].

2.4. Disc Diffusion Method

The measure of both the growth and the inhibition of the control bacterial strains mixed with honey was carried out using the disc diffusion method. This method was performed using prepared discs of approximately 6 mm diameter (Whatman filter paper no. 1). They were sterilized in a hot air oven according to the Clinical and Laboratory Standards Institute (CLSI) guidelines [27] and spotted with 0.2 mg of Tamarix gallica honey. The preparation for each bacterial strain suspension was carried out by inoculating the fresh stock culture into a tube containing 10 mL of Muller Hinton Broth (Sigma-Aldrich company) and then incubated aerobically at 37 °C for 24 h. A 0.5 McFarland turbidity standard (5 × 107 cells/mL) was used to adjust the bacterial suspension, followed by a further dilution to obtain 5 × 106 cells/mL. For all the dilution steps, physiological saline PBS pH 7.2 was used under aseptic conditions. These bacterial strains were enriched on selective broth for bacterial propagation. A separate tube containing 40 µL of 21.30% honey concentration was mixed with 0.20 µL/10 mL from the enriched broth of each propagated S. aureus, S. mutans, K. pneumoniae, E. coli, Proteus vulgaris, and P. aeruginosa, and further incubated at 37 °C for 24 h. The calculation of the mean values of inhibition was carried out from the triplicate readings in each test. The determination for the evaluations of the antibacterial activity of the different honey dilutions was performed according to Hegazi et al. [15].

2.5. Determination of the Minimum Inhibitory Concentration (MIC)

The MIC of different samples of Tamarix gallica honey was determined by a two-fold serial dilution method. Concentrations of 50, 25, 12.50, 6.25, 3.12, 1.56, and 0.78 mg/mL and 390, 195, and 97 µg/mL were performed from a serial dilution of 100 mg/mL. Briefly, 100 µL of the varying sample concentrations was added separately to the test tubes containing 9 mL of the standardized suspension of the tested bacteria (108 CFU/mL). Control tests with the studied organisms were performed using distilled water instead of honey. The test tubes were incubated at 37 °C for 24 h. The lowest concentration of these samples with no visible growth was taken as the MIC [28,29].

2.6. Detection of Total Phenolic Content (TPC)

The total phenolic content (TPC) was determined using Folin–Ciocalteu reagent, according to the method described by [30,31]. A honey solution of 0.5 mL was mixed with 2.5 mL Folin–Ciocalteu reagent (2N) and incubated for 5 min. Subsequently, 2 mL of sodium carbonate solution (75 g/L) was added and incubated for 2 h at 25 °C. After incubation, the absorbance was measured at a wavelength of 765 nm using a UV–Visible spectrophotometer (Perkin-Elmer Lambda 25, Waltham, MA, USA). For the calibration curve, a standard of gallic acid (0–1000 mg/L) was used. The mean value for the triplicate assays of the TPC was reported and expressed as milligrams of gallic acid equivalent (GAE) per gram of honey [32].

2.7. Determination of Total Flavonoid Content (TFC)

The total flavonoid content (TFC) was determined using a volume of 5 mL of diluted honey with a 0.1 g/mL concentration. This solution was mixed with 5 mL of 2% aluminum chloride (AlCl3). The mixture was then incubated for 10 min at 25 °C. The absorbance of the formed complex was measured at 415 nm using a UV–Visible spectrophotometer. The standard chemical for the calibration curve preparation was rutin with a concentration of 0–100 mg/L. The mean value of the triplicate assays of the TFC was reported and expressed as milligrams of rutin equivalent (RE) per gram of honey [32,33].

2.8. Antioxidant Assay to Determine the DPPH Scavenging Activity

The DPPH scavenging of the honey samples was determined by carrying out an antioxidant assay. This test is based on the reduction in the purple DPPH radical using an oxidizing antioxidant. The scavenging effects of vitamin C and caffeic acid corresponded to the quenching intensity of 1.1-diphenyl-2-picrylhydrazyl (DPPH), as carried out by [31,34]. A wavelength of 520 nm was set to measure the reduction in the purple DPPH radical.

2.9. Melissopalynological and Physicochemical Analysis

The quantitative and qualitative analyses of the pollen grains present in the honey were carried out by the detection of microscopic specimens [35] and based on the percentage of the pollen grain type that was the most dominant [36]. To classify honey as unifloral, this percentage of pollen type must show the highest counting of grains in the honey sediment, and the honey can be named after the plant these pollen grains come from [37,38].
The melissopalynological and physicochemical characterizations were determined. The sedimentation technique was used for the determination of pollen content as described by [24,36]. The water content [39], water-soluble solids [40], pH, total acidity, and electrical conductivity were also analyzed [41]. The analyses of sugar content, glucose, fructose, fructose/glucose ratio, fructose plus glucose %, and sucrose were performed by HPLC-DAD according to official methods [42]. The diastase activity was determined photometrically by the Phadebas method [43]. The results are expressed as a diastase number (DN) in Gothe or Schade units. One unit corresponds to the enzyme activity of 1 g of honey, which can hydrolyze 0.01 g of starch in 1 h at 40 °C and pH 5.2. The calculation modified by Bogdanov et al. [44], DN = 28.2 × ΔA620 + 2.64, was used. The determination of the hydroxymethylfurfural was made according to the Winkler method [45]. The results are expressed in HMF milligrams per kg of honey.

2.10. Statistical Analysis

SPSS Ver. 21 (IBM, New York, NY, USA) software for the statistical analysis was used on the triplicate results. The comparison between and within the tested groups was applied using one-way ANOVA. The mean ± standard error (SE) was used for all data, and a p-value less than 0.05 was considered significant.

3. Results

The antibacterial activities of Tamarix gallica honey from the three countries were evaluated according to the zone of growth inhibition. The tested bacterial strains showed growth suppression in all the honey types (Table 1). Egyptian Tamarix gallica honey showed the highest zones of inhibition of 23.10 ± 0.38 mm, 29.33 ± 0.64 mm, 24.02 ± 0.34 mm, and 22.00 ± 0.58 mm against Staphylococcus aureus, Streptococcus mutans, Klebsiella pneumoniae, and Pseudomonas aeruginosa, respectively. Penicillin, Oxacillin, and Clindamycin showed effective antibacterial activity against the tested bacteria (Table 1).
The MIC tests are shown in Table 2. All the honey showed antibacterial potential against S. aureus, S. mutans, K. pneumoniae, and E. coli. However, the Libyan Tamarix gallica honey showed the strongest antibacterial potential against Pseudomonas aeruginosa and the Egyptian honey against Proteus vulgaris. The therapeutical antibiotics Penicillin, Oxacillin, and Clindamycin showed the highest MIC activity against all the tested bacteria (Table 2).
The total phenolic (mg GAE/100 g honey), total flavonoid (mg RE/100 g honey), and DPPH (mg AAE/100 g honey) contents are shown in Table 3. The highest level of total phenolics of the Tamarix gallica honey was observed in the honey from Egypt at 142.29 ± 15.32 (mg GAE/100 g honey), with the lowest level observed in the Saudi Arabian honey. The highest level of total flavonoids (mg RE/100 g honey) was detected in the honey from Saudi Arabia with a value of 83.1 ± 18.33 (mg RE/100 g honey). Moreover, the highest value of DPPH was detected in Egyptian honey.
The melissopalynological analysis of the Tamarix gallica honey from the different locations revealed that not only the specific botanical source giving the nectar but also other pollen grain types from different botanical sources were present in the pollen spectra. The pollen content and types obtained varied depending on the geographical origin of the sample (Figure 1 and Table 4).
The results of the physicochemical parameters (Table 5) revealed that the Tamarix gallica honey samples were comparable in water content, which ranged from 13.2 ± 0.58% (Libya) to 16.15 ± 0.11% (Egypt). The pH ranged from 4.20 ± 0.58 (Saudi Arabia) to 4.26 ± 0.53 (Egypt). The total acidity also varied from 13 ± 0.58 (Libya) to 21.5 ± 0.61 meq/l (Egypt). The electrical conductivity was 0.4 ± 0.003 (Libya) to 0.51 ± 0.004 mS/cm (Saudi Arabia). The insoluble solids ranged from 0.064 ± 0.006% (Saudi Arabia) to 0.075 ± 0.003% (Libya). The glucose, fructose, sucrose, and diastase activity levels in the different Tamarix gallica honey samples are shown in Table 5. The percentages of sugars were similar for the three geographical origins. The Egyptian honey had the highest value for diastase activity (28.15 ± 0.47 DN) and the lowest HMF (5.95 ± 0.55 mg/kg).

4. Discussion

The antibacterial activities of all the honey in this study were similar, which may be attributed to the narrow ranges of their total phenolic and flavonoid contents. There is a positive correlation between the TPC and the antibacterial activity of honey [46], which is suggested to be due to the inhibition in the virulence factors of the pathogen [47]. On the other hand, Makarewicz et al. [48] found a weak correlation between the antioxidant and antimicrobial activities of some Polish commercial honeys.
Honey has strong antibacterial activity due to the following factors: the phenolic compounds, the low pH, the high osmolarity, the hydrogen peroxide produced by glucose oxidase enzyme [13,14,49], and the presence of lysozyme, methylglyoxal, bee peptides, and high sugar contents [50]. The Tamarix gallica honey studied in this work showed different inhibition activities against the tested bacteria based on its origin, possibly due to its major phenolics and flavonoids: syringic acid, isoquercetin, gallic acid, ρ-coumaric, and catechin [51]. The presented results were in accordance with the research of several authors [50,52,53,54,55] stating that both Gram-positive and Gram-negative pathogenic bacteria are susceptible to honey. Other authors found the antimicrobial activity of honey to be directly related to its botanical origin and phenolic compounds, including mainly flavonoids and phenolic acids [16].
The total phenolic content ranged from 129.89 ± 10.66 to 142.29 ± 15.32 mg GAE/100 g honey, which was higher than the results found for honey from different countries, namely India [56] (47–98 mg GAE/100 g honey), Poland [57] (71.7 to 202.6 μg/g honey), Argentina [31] (18.730–107.213 mg GAE/100 g honey), Burkina Faso [58] (32.59–114.75 mg GAE/100 g honey), Portugal [55] (30.87 to 87.27 mg GAE/100 g), and Romania [59] (2–125 mg GAE/100 g honey). The total phenolic contents in different honey types have been reported [60,61,62,63]. The variability was associated with the floral origin of the honey, and multifloral honey was found to have higher phenolic contents than unifloral honey. The phenolic compounds, especially flavonoids in honey, have been reported to have antiviral, antimicrobial, antifungal, antioxidant, and anti-inflammatory activities [64].
Moreover, the flavonoid content depends mainly on the geographical and botanical origin. The total flavonoids in the Saudi Arabian and Egyptian Tamarix gallica honeys (83.1 ± 18.33 and 75.5 ± 13.47 mg RE/100 g honey, respectively) were greater than (p < 0.05) the Libyan ones (63.6 ± 11.13 mg RE/100 g honey). Similar results were obtained in the analysis of three unifloral honey types from Portugal, which showed that the darker the honey, the richer the phenolic content [65].
The antioxidant activity of the Tamarix gallica honey samples was determined by the DPPH radical scavenging method. The Tamarix gallica honey from Egypt (173.80 ± 10.51 mg AAE/100 g honey) and Saudi Arabia (153.30 ± 15.18 mg AAE/100 g honey) presented the highest levels of DPPH radical scavenging activities (p < 0.05), compared with the antioxidant activities of the Libyan honey samples. Similar results were reported in other studies [66,67,68]. Alves et al. [69] observed a positive correlation between the phenolic concentration, the antioxidant capacity, and the color of the honey. The volatile compounds came from the diverse floral sources [70,71] and were considered to be responsible for the most potent biological activity and of medical importance.
A long honey shelf life depends on its low water content, while high moisture in honey during storage promotes the process of fermentation. The water content of the investigated Tamarix gallica honey samples complied with the accepted range. According to the Codex Alimentarius, the water content of honey should not exceed 20%. The relative humidity and temperature affect the water content during honey production by honeybees [72].
With the aim of assessing the authenticity and the overall quality of the honey, the sugar content is determined [73]. The sugar analysis of honey is a good indicator of artificial (sugar solution) or natural (nectar) feeding of honeybees. The use of sugar solution to feed honeybees is showed when the glucose content in honey is much higher than its fructose content [74]. Our results revealed that the sum of the glucose and fructose, which measures the content of the reducing sugars in honey, was within the accepted range to prove the standardization and the authenticity of the honey, as observed by Aljohar et al. [7]. Fructose is the most dominant sugar in honey samples [75], and the ratio of fructose to glucose (F/G) indicates the natural feeding of honeybees [76]. The sucrose content in all honey samples did not exceed 5% in this study, which is the accepted level to prove the authenticity of honey, as observed by [77]. The diastase activity and hydroxymethylfurfural content are also important parameters used to prove the freshness of honey [78,79]. Diastase activity depends on many factors, such as the physiological period of the colony, the age of the bees, the nectar collection season, the amount of nectar, and its sugar content. The Codex Alimentarius of the World Health Organization, the European Union Quality Normative on honey, and the Gulf Technical Regulation on honey (GSO 147:2008-Standards Store-GCC Standardization Organization EOSC, 2005) recommend that the maximum level for the HMF content should not exceed 40 mg/kg; in countries with tropical temperatures, the HMF content should not exceed 80 mg/kg. In this study, all the examined Tamarix gallica honey samples complied with the accepted limit for the HMF content and diastase number, which are indicators of the authenticity and freshness of honey. All the Tamarix gallica honey samples were found to be within the accepted range of acidity. The honey acidity is related to the presence of organic acids, particularly gluconic acid, which was found to affect the honey flavor, texture, shelf life, and stability [80].

5. Conclusions

We have concluded that Tamarix gallica honey from Egypt, Saudi Arabia, and Libya has the capacity to suppress pathogenic bacterial growth and has significant free radical scavenging activities. Moreover, these findings suggest that Tamarix gallica honey may be considered as an interesting source of antimicrobial compounds and antioxidants for therapeutical or nutraceutical industries and for food manufacturers. The physicochemical and melissopalynological characterization was carried out, describing this type of unifloral honey for the first time.

Author Contributions

Conceptualization, A.G.H.; methodology, M.F.A.R. and H.R.E.-S.; validation, M.F.A.R. and S.S.; formal analysis, M.F.A.R.; investigation, A.G.H., M.F.A.R., H.R.E.-S. and A.F.M.A.G.; resources, F.M.A.G.; data curation, A.F.M.A.G. and A.M.C.; writing—original draft preparation, A.G.H., S.S., I.R., H.R.E.-S. and A.M.C.; writing—review and editing, A.G.H., A.M.C., I.R., A.F.M.A.G. and S.S.; visualization, H.R.E.-S., A.G.H. and A.M.C.; supervision, A.G.H. and S.S.; project administration, F.M.A.G.; funding acquisition, F.M.A.G. and A.F.M.A.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Research Center of Egypt under registration number 12/5/1 and the Alnahalaljwal Foundation (Makkah, Saudi Arabia).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The data supporting reported results can be found in the manuscript.

Acknowledgments

The authors are grateful for the financial support from the National Research Center of Egypt under registration number 12070104 and the Al Guthami Foundation, Saudi Arabia.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

References

  1. Vaou, N.; Stavropoulou, E.; Voidarou, C.; Tsigalou, C.; Bezirtzoglou, E. Towards Advances in Medicinal Plant Antimicrobial Activity: A Review Study on Challenges and Future Perspectives. Microorganisms 2021, 9, 2041. [Google Scholar] [CrossRef] [PubMed]
  2. Silva, L.R.; Videira, R.; Monteiro, A.P.; Valentão, P.; Andrade, P.B. Honey from Luso region (Portugal): Physicochemical characteristics and mineral contents. Microchem. J. 2009, 93, 73–77. [Google Scholar] [CrossRef]
  3. Habib, H.M.; al Meqbali, F.T.; Kamal, H.; Souka, U.D.; Ibrahim, W.H. Physicochemical and biochemical properties of honeys from arid regions. Food Chem. 2014, 153, 35–43. [Google Scholar] [CrossRef]
  4. Mustafa, G.; Iqbal, A.; Javid, A.; Hussain, A.; Bukhari, S.M.; Ali, W.; Saleem, M.; Azam, S.M.; Sughra, F.; Ali, A.; et al. Variations in nutritional profile of honey produced by various species of genus Apis. Braz. J. Biol. 2021, 83, e246651. [Google Scholar] [CrossRef]
  5. Machado De-Melo, A.A.; de Almeida-Muradian, L.B.; Sancho, M.T.; Pascual-Maté, A. Composition and properties of Apis mellifera honey: A review. J. Apic. Res. 2017, 57, 5–37. [Google Scholar] [CrossRef]
  6. Fyfe, L.; Okoro, P.; Paterson, E.; Coyle, S.; McDougall, G.J. Compositional analysis of Scottish honeys with antimicrobial activity against antibiotic-resistant bacteria reveals novel antimicrobial components. LWT-Food Sci. Technol. 2017, 79, 52–59. [Google Scholar] [CrossRef]
  7. Aljohar, H.I.; Maher, H.M.; Albaqami, J.; Al-Mehaizie, M.; Orfali, R.; Alrubia, S. Physical and chemical screening of honey samples available in the Saudi market: An important aspect in the authentication process and quality assessment. Saudi Pharm. J. 2018, 26, 932–942. [Google Scholar] [CrossRef]
  8. Cornara, L.; Biagi, M.; Xiao, J.; Burlando, B. Therapeutic properties of bioactive compounds from different honeybee products. Front. Pharm. 2017, 8, 412. [Google Scholar] [CrossRef] [Green Version]
  9. Hegazi, A. Antimicrobial Activity of Different Egyptian Honeys as Comparison of Saudi Arabia Honey. Res. J. Microbiol. 2011, 6, 488–495. [Google Scholar] [CrossRef] [Green Version]
  10. Hegazi, A.G.; Al-Menabbawy, K.; Abd, E.H.; Rahman, E.; Helal, S.I.; Hegazi, A. Novel Therapeutic Modality Employing Apitherapy for Controlling of Multiple Sclerosis. J. Clin. Cell. Immunol. 2015, 6, 2. [Google Scholar] [CrossRef] [Green Version]
  11. Hegazi, A.G.; Abd Allah, F.M. Antimicrobial Activity of Different Saudi Arabia Honeys. Glob. Vet. 2012, 9, 53–59. [Google Scholar]
  12. Hegazi, A.G. Medical importance of bee products. Glob. Vet. 2012, 12, 136–146. [Google Scholar]
  13. Hegazi, A.G.; Guthami, F.M.A.; Gethami, A.F.M.A.; Fouad, E.A. Antibacterial and Antioxidant Activities of Some Saudi Arabia Honey Products. Iran. J. Med. Microbiol. 2020, 14, 490–500. [Google Scholar] [CrossRef]
  14. Hegazi, A.G.; al Guthami, F.M.; Al Gethami, A.F.M.; Fouad, E.A.; Abdou, A.M. Antibacterial activity and characterisation of some Egyptian honey of different floral origin. Bulg. J. Vet. Med. 2021, 24, 278–290. [Google Scholar] [CrossRef]
  15. Hegazi, A.G.; Al Guthami, F.M.; Al Gethami, A.F.M.; Abd Allah, F.M.; Saleh, A.A.; Fouad, E.A. Potential antibacterial activity of some Saudi Arabia honey. Vet. World 2017, 10, 233–237. [Google Scholar] [CrossRef] [Green Version]
  16. Mandal, M.D.; Mandal, S. Honey: Its medicinal property and antibacterial activity. Asian Pac. J. Trop. Biomed. 2011, 1, 154–160. [Google Scholar] [CrossRef] [Green Version]
  17. Saïdana, D.; Mahjoub, M.A.; Boussaada, O.; Chriaa, J.; Chéraif, I.; Daami, M.; Mighri, Z.; Helal, A.N. Chemical composition and antimicrobial activity of volatile compounds of Tamarix boveana (Tamaricaceae). Microbiol. Res. 2008, 163, 445–455. [Google Scholar] [CrossRef] [PubMed]
  18. Sisneros, D. Herbicide Analysis: Lower Colorado River Saltcedar Vegetation Management Study; Bureau of Reclamation: Denver, CO, USA, 1991; p. 165.
  19. Diggs, G.M., Jr.; Lipscomb, B.L.; O’Kennon, R.J. Shinner’s and Mahler’s Illustrated Flora of North Central Texas; Botanical Research Institute of Texas: Fort Worth, TX, USA, 1999. [Google Scholar]
  20. KalamUrfi, M.; Mujahid, M.; Badruddeen; Akhtar, J.; Khalid, M.; Irfan Khan, M.; Usmani, A. Tamarix gallica: For traditional uses, phytochemical and pharmacological potentials. J. Chem. Pharm. Res. 2016, 8, 809–814. [Google Scholar]
  21. Boulaaba, M.; Snoussi, M.; Saada, M.; Mkadmini, K.; Smaoui, A.; Abdelly, C.; Ksouri, R. Antimicrobial activities and phytochemical analysis of Tamarix gallica extracts. Ind. Crop. Prod. 2015, 76, 1114–1122. [Google Scholar] [CrossRef] [Green Version]
  22. Von Der Ohe, W.; Oddo, L.P.; Piana, M.L.; Morlot, M.; Martin, P. Harmonized methods of melissopalynology. Apidologie 2004, 35, S18–S25. [Google Scholar] [CrossRef]
  23. Adamchuk, L.; Sukhenko, V.; Akulonok, O.; Bilotserkivets, T.; Vyshniak, V.; Lisohurska, D.; Lisohurska, O.; Slobodyanyuk, N.; Shanina, O.; Galyasnyj, I. Methods for determining the botanical origin of honey. Potravin. Slovak J. Food Sci. 2020, 14, 483–493. [Google Scholar] [CrossRef] [PubMed]
  24. Louveaux, J.; Maurizio, A.; Vorwohl, G. Methods of Melissopalynology. Bee World 1978, 59, 139–157. [Google Scholar] [CrossRef]
  25. Joyanes, P.; Conejo, M.D.C.; Martínez-Martínez, L.; Perea, E.J. Evaluation of the VITEK 2 System for the Identification and Susceptibility Testing of Three Species of Nonfermenting Gram-Negative Rods Frequently Isolated from Clinical Samples. J. Clin. Microbiol. 2001, 39, 3247. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Idelevich, E.A.; Schüle, I.; Grünastel, B.; Wüllenweber, J.; Peters, G.; Becker, K. Acceleration of Antimicrobial Susceptibility Testing of Positive Blood Cultures by Inoculation of Vitek 2 Cards with Briefly Incubated Solid Medium Cultures. J. Clin. Microbiol. 2014, 52, 4058. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Matuschek, E.; Brown, D.F.J.; Kahlmeter, G. Development of the EUCAST disk diffusion antimicrobial susceptibility testing method and its implementation in routine microbiology laboratories. Clin. Microbiol. Infect. 2014, 20, O255–O266. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Dahiya, P.; Purkayastha, S. Phytochemical Screening and Antimicrobial Activity of Some Medicinal Plants Against Multi-Drug Resistant Bacteria from Clinical Isolates. Indian J. Pharm. Sci. 2012, 74, 443. [Google Scholar] [CrossRef] [Green Version]
  29. Parvekar, P.; Palaskar, J.; Metgud, S.; Maria, R.; Dutta, S. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) of silver nanoparticles against Staphylococcus aureus. Biomater. Investig. Dent. 2020, 7, 105–109. [Google Scholar] [CrossRef]
  30. Beretta, G.; Granata, P.; Ferrero, M.; Orioli, M.; Facino, R.M. Standardization of antioxidant properties of honey by a combination of spectrophotometric/fluorimetric assays and chemometrics. Anal. Chim. Acta 2005, 533, 185–191. [Google Scholar] [CrossRef]
  31. Bertoncelj, J.; Doberšek, U.; Jamnik, M.; Golob, T. Evaluation of the phenolic content, antioxidant activity and colour of Slovenian honey. Food Chem. 2007, 105, 822–828. [Google Scholar] [CrossRef]
  32. Chua, L.S.; Rahaman, N.L.A.; Adnan, N.A.; Eddie Tan, T.T. Antioxidant activity of three honey samples in relation with their biochemical components. J. Anal. Methods Chem. 2013, 2013, 313798. [Google Scholar] [CrossRef]
  33. Isla, M.I.; Craig, A.; Ordoñez, R.; Zampini, C.; Sayago, J.; Bedascarrasbure, E.; Alvarez, A.; Salomón, V.; Maldonado, L. Physico chemical and bioactive properties of honeys from Northwestern Argentina. LWT-Food Sci. Technol. 2011, 44, 1922–1930. [Google Scholar] [CrossRef]
  34. Ruiz-Ciau, D.; Cuevas-Glory, L.; Quijano, L.; Sauri-Duch, E. Chemical Composition and Antioxidant DPPH Activity of the Floral and Leaves Essential Oils of Montanoa speciosa DC. Am. J. Plant Sci. 2017, 8, 745–753. [Google Scholar] [CrossRef] [Green Version]
  35. Kirs, E.; Pall, R.; Martverk, K.; Laos, K. Physicochemical and melissopalynological characterization of Estonian summer honeys. Procedia Food Sci. 2011, 1, 616–624. [Google Scholar] [CrossRef] [Green Version]
  36. Chukwuemeka, R.; Simeonov, V. Evaluation of Pollen and Chemical Composition of Honey Samples Sourced from Open Markets in Anambra State, Nigeria to Ascertain their Authenticity. J. Appl. Life Sci. Int. 2019, 22, 1–12. [Google Scholar] [CrossRef] [Green Version]
  37. Wrońska-Pilarek, D.; Danielewicz, W.; Bocianowski, J.; Maliński, T.; Janyszek, M. Comparative pollen morphological analysis and its systematic implications on three European oak (Quercus L., Fagaceae) species and their spontaneous hybrids. PLoS ONE 2016, 11, e0161762. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Tsigouri, A.; Passaloglou-Katrali, M.; Sabatakou, O. Palynological characteristics of different unifloral honeys from Greece. Grana 2022, 43, 122–128. [Google Scholar] [CrossRef]
  39. Chataway, H.D. The determination of moisture in honey. Can. J. Res. 1932, 6, 532–547. [Google Scholar] [CrossRef]
  40. Nyau, V.; Mwanza, E.; Moonga, H. Physico- chemical qualities of honey harvested from different beehive types in Zambia. Afr. J. Food Agric. Nutr. Dev. 2013, 13, 7415–7427. [Google Scholar] [CrossRef]
  41. Yadata, D. Detection of the Electrical Conductivity and Acidity of Honey from Different Areas of Tepi. Food Sci. Technol. 2014, 2, 59–63. [Google Scholar] [CrossRef]
  42. Zhou, J.; Yao, L.; Li, Y.; Chen, L.; Wu, L.; Zhao, J. Floral classification of honey using liquid chromatography–diode array detection–tandem mass spectrometry and chemometric analysis. Food Chem. 2014, 145, 941–949. [Google Scholar] [CrossRef]
  43. Schade, J.E.; Marsh, G.L.; Eckert, J.E. Diastase activity and hydroxymethylfurfural in honey and their usefulness in detecting heat adulteration. Food Res. 1958, 23, 446–463. [Google Scholar] [CrossRef]
  44. Bogdanov, S.; Martin, P.; Lullmann, C. Harmonized methods of the European Honey Commission. Apidologie Suppl. 1997, 28, 1–59. [Google Scholar]
  45. Winkler, O. Beitrag zum Nachweis und zur Bestimmung von Oxymethylfurfural in Honig und Kunsthonig. Z. Lebensm. Unters. 1955, 102, 160–167. [Google Scholar] [CrossRef]
  46. Nayaka, N.M.D.; Fidrianny, I.; Sukrasno; Hartati, R.; Singgih, M. Antioxidant and antibacterial activities of multiflora honey extracts from the Indonesian Apis cerana bee. J. Taibah Univ. Med. Sci. 2020, 15, 211–217. [Google Scholar] [CrossRef]
  47. Stagos, D.; Soulitsiotis, N.; Tsadila, C.; Papaeconomou, S.; Arvanitis, C.; Ntontos, A.; Karkanta, F.; Adamou-Androulaki, S.; Petrotos, K.; Spandidos, D.A.; et al. Antibacterial and antioxidant activity of different types of honey derived from Mount Olympus in Greece. Int. J. Mol. Med. 2018, 42, 726. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  48. Makarewicz, M.; Kowalski, S.; Lukasiewicz, M.; Małysa-Paśko, M. Antimicrobial and Antioxidant Properties of Some Commercial Honeys Available on the Polish Market. Czech J. Food Sci. 2017, 35, 401–406. [Google Scholar] [CrossRef] [Green Version]
  49. Libonatti, C.; Varela, S.; Basualdo, M. Antibacterial activity of honey: A review of honey around the world. J. Microbiol. Antimicrob. 2014, 6, 51–56. Available online: https://academicjournals.org/journal/JMA/article-full-text-pdf/FA9B2D144111 (accessed on 3 November 2022). [CrossRef] [Green Version]
  50. Almasaudi, S. The antibacterial activities of honey. Saudi J. Biol. Sci. 2021, 28, 2188–2196. [Google Scholar] [CrossRef] [PubMed]
  51. Ksouri, R.; Falleh, H.; Megdiche, W.; Trabelsi, N.; Mhamdi, B.; Chaieb, K.; Bakrouf, A.; Magné, C.; Abdelly, C. Antioxidant and antimicrobial activities of the edible medicinal halophyte Tamarix gallica L. and related polyphenolic constituents. Food Chem. Toxicol. 2009, 47, 2083–2091. [Google Scholar] [CrossRef]
  52. Szweda, P. Antimicrobial Activity of Honey. In Honey Analysis; Vagner De Alencar Arnaut De Toledo; IntechOpen: Rijeka, Croatia, 2017. [Google Scholar]
  53. Morroni, G.; Alvarez-Suarez, J.M.; Brenciani, A.; Simoni, S.; Fioriti, S.; Pugnaloni, A.; Giampieri, F.; Mazzoni, L.; Gasparrini, M.; Marini, E.; et al. Comparison of the antimicrobial activities of four honeys from three countries (New Zealand, Cuba, and Kenya). Front. Microbiol. 2018, 9, 1378. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Matzen, R.D.; Leth-Espensen, J.Z.; Jansson, T.; Nielsen, D.S.; Lund, M.N.; Matzen, S. The Antibacterial Effect in Vitro of Honey Derived from Various Danish Flora. Derm. Res. Pr. 2018, 2018, 7021713. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  55. Gonçalves, J.; Ribeiro, I.; Marçalo, J.; Rijo, P.; Faustino, C.; Pinheiro, L. Physicochemical, Antioxidant and Antimicrobial Properties of selected Portuguese Commercial Monofloral Honeys. J. Food Nutr. Res. 2018, 6, 645–654. [Google Scholar] [CrossRef] [Green Version]
  56. Saxena, S.; Gautam, S.; Sharma, A. Physical, biochemical and antioxidant properties of some Indian honeys. Food Chem. 2010, 118, 391–397. [Google Scholar] [CrossRef]
  57. Kaškonienė, V.; Maruska, A.; Kornysova, O.; Charczun, N.; Ligor, M.; Buszewski, B. Quantitative and qualitative determination of phenolic compounds in honey. Cheminė Technol. 2009, 52, 74–80. [Google Scholar]
  58. Meda, A.; Lamien, C.E.; Romito, M.; Millogo, J.; Nacoulma, O.G. Determination of the total phenolic, flavonoid and proline contents in Burkina Fasan honey, as well as their radical scavenging activity. Food Chem. 2005, 91, 571–577. [Google Scholar] [CrossRef]
  59. Al, M.L.; Daniel, D.; Moise, A.; Bobis, O.; Laslo, L.; Bogdanov, S. Physico-chemical and bioactive properties of different floral origin honeys from Romania. Food Chem. 2009, 112, 863–867. [Google Scholar] [CrossRef]
  60. Srećković, N.Z.; Mihailović, V.B.; Katanić Stanković, J.S. Physico-chemical, antioxidant and antimicrobial properties of three different types of honey from central Serbia. Kragujev. J. Sci. 2019, 41, 53–68. [Google Scholar] [CrossRef]
  61. Roby, M.H.H.; Abdelaliem, Y.F.; Esmail, A.H.M.; Mohdaly, A.A.A.; Ramadan, M.F. Evaluation of Egyptian honeys and their floral origins: Phenolic compounds, antioxidant activities, and antimicrobial characteristics. Environ. Sci. Pollut. Res. 2020, 27, 20748–20756. [Google Scholar] [CrossRef]
  62. Perna, A.; Intaglietta, I.; Simonetti, A.; Gambacorta, E. A comparative study on phenolic profile, vitamin C content and antioxidant activity of Italian honeys of different botanical origin. Int. J. Food Sci. Technol. 2013, 48, 1899–1908. [Google Scholar] [CrossRef]
  63. Alvarez-Suarez, J.; Gasparrini, M.; Forbes-Hernández, T.; Mazzoni, L.; Giampieri, F. The Composition and Biological Activity of Honey: A Focus on Manuka Honey. Foods 2014, 3, 420–432. [Google Scholar] [CrossRef] [Green Version]
  64. Silici, S.; Sagdic, O.; Ekici, L. Total phenolic content, antiradical, antioxidant and antimicrobial activities of Rhododendron honeys. Food Chem. 2010, 121, 238–243. [Google Scholar] [CrossRef]
  65. Ferreira, I.C.F.R.; Aires, E.; Barreira, J.C.M.; Estevinho, L.M. Antioxidant activity of Portuguese honey samples: Different contributions of the entire honey and phenolic extract. Food Chem. 2009, 114, 1438–1443. [Google Scholar] [CrossRef]
  66. van den Berg, A.J.; van den Worm, E.; van Ufford, H.C.Q.; Halkes, S.B.; Hoekstra, M.J.; Beukelman, C.J. An in vitro examination of the antioxidant and anti-inflammatory properties of buckwheat honey. J. Wound Care 2008, 17, 172–178. [Google Scholar] [CrossRef] [Green Version]
  67. Bueno-Costa, F.M.; Zambiazi, R.C.; Bohmer, B.W.; Chaves, F.C.; da Silva, W.P.; Zanusso, J.T.; Dutra, I. Antibacterial and antioxidant activity of honeys from the state of Rio Grande do Sul, Brazil. LWT-Food Sci. Technol. 2016, 65, 333–340. [Google Scholar] [CrossRef] [Green Version]
  68. Boussaid, A.; Chouaibi, M.; Rezig, L.; Hellal, R.; Donsì, F.; Ferrari, G.; Hamdi, S. Physicochemical and bioactive properties of six honey samples from various floral origins from Tunisia. Arab. J. Chem. 2018, 11, 265–274. [Google Scholar] [CrossRef] [Green Version]
  69. Alves, J.; Antonio, L.; Da Costa, M.A.; Da Silva, S.J.R.; Flach, A. Color, phenolic and flavonoid content, and antioxidant activity of honey from Roraima, Brazil. Food Sci. Technol. Camp. 2014, 34, 69–73. [Google Scholar]
  70. Manyi-Loh, C.E.; Ndip, R.N.; Clarke, A.M. Volatile Compounds in Honey: A Review on Their Involvement in Aroma, Botanical Origin Determination and Potential Biomedical Activities. Int. J. Mol. Sci. 2011, 12, 9514. [Google Scholar] [CrossRef] [Green Version]
  71. Devi, A.; Jangir, J. Chemical characterization complemented with chemometrics for the botanical origin identification of unifloral and multifloral honeys from India. Food Res. Int. 2018, 107, 216–226. [Google Scholar] [CrossRef]
  72. Abou-Shaara, H.F.; Owayss, A.A.; Ibrahim, Y.Y.; Basuny, N.K. A review of impacts of temperature and relative humidity on various activities of honey bees. Insect Soc. 2017, 64, 455–463. [Google Scholar] [CrossRef]
  73. Geană, E.I.; Ciucure, C.T.; Costinel, D.; Ionete, R.E. Evaluation of honey in terms of quality and authenticity based on the general physicochemical pattern, major sugar composition and δ13C signature. Food Control 2020, 109, 106919. [Google Scholar] [CrossRef]
  74. Moumeh, B.; Garrido, M.D.; Diaz, P.; Peñaranda, I.; Linares, M.B. Chemical analysis and sensory evaluation of honey produced by honeybee colonies fed with different sugar pastes. Food Sci. Nutr. 2020, 8, 5823–5831. [Google Scholar] [CrossRef] [PubMed]
  75. el Sohaimy, S.A.; Masry, S.H.D.; Shehata, M.G. Physicochemical characteristics of honey from different origins. Ann. Agric. Sci. 2015, 60, 279–287. [Google Scholar] [CrossRef] [Green Version]
  76. Szczesna, T.; Waś, E.; Semkiw, P.; Skubida, P.; Jaśkiewicz, K.; Witek, M. Changes in the Physicochemical Properties of Starch Syrups after Processing by Honeybees. Agriculture 2021, 11, 335. [Google Scholar] [CrossRef]
  77. Kazeminia, M.; Mahmoudi, R.; Aali, E.; Ghajarbygi, P. Evaluation of Authenticity in Honey Samples from Qazvin, Iran. J. Chem. Health Risks 2023, 13, 73–83. [Google Scholar] [CrossRef]
  78. Bentabol Manzanares, A.; Hernández García, Z.; Rodríguez Galdón, B.; Rodríguez Rodríguez, E.; Díaz Romero, C. Physicochemical characteristics of minor monofloral honeys from Tenerife, Spain. LWT-Food Sci. Technol. 2014, 55, 572–578. [Google Scholar] [CrossRef]
  79. Pasias, I.N.; Kiriakou, I.K.; Proestos, C. HMF and diastase activity in honeys: A fully validated approach and a chemometric analysis for identification of honey freshness and adulteration. Food Chem. 2017, 229, 425–431. [Google Scholar] [CrossRef]
  80. Warui, M.W.; Hansted, L.; Gikungu, M.; Mburu, J.; Kironchi, G.; Bosselmann, A.S. Characterization of Kenyan Honeys Based on Their Physicochemical Properties, Botanical and Geographical Origin. Int. J. Food Sci. 2019, 2019, 2932509. [Google Scholar] [CrossRef]
Insects 14 00319 g001 550
Figure 1. Images of pollen grains from microscopic preparations of the Tamarix gallica honey from different geographical origins.
Figure 1. Images of pollen grains from microscopic preparations of the Tamarix gallica honey from different geographical origins.
Insects 14 00319 g001
Table
Table 1. The inhibition zone (in mm) of Tamarix gallica honey against various pathogenic microorganisms by the disc diffusion method (mean values ± SE). Each test was run in triplicate.
Table 1. The inhibition zone (in mm) of Tamarix gallica honey against various pathogenic microorganisms by the disc diffusion method (mean values ± SE). Each test was run in triplicate.
Antibacterial ActivityGram-PositiveGram-Negative
Honey OriginStaphylococcus aureusStreptococcus mutansKlebsiella pneumoniaeEscherichia coliProteus vulgarisPseudomonas aeruginosa
Saudi Arabia21.33 ± 0.8818.33 ± 0.8822.05 ± 0.68 15.33 ± 0.3321.50 ± 0.3021.00 ± 1.15
Libya16.01 ± 0.5816.33 ± 0.8811.03 ± 0.5618.05 ± 0.5816.06 ± 0.3119.67 ± 0.33
Egypt23.10 ± 0.3829.33 ± 0.6424.02 ± 0.3419.16 ± 0.6020.01 ± 0.3422.00 ± 0.58
Penicillin53.02 ± 0.6437.00 ± 0.6433.12 ± 0.3832.35 ± 0.1241.14 ± 0.2137.21 ± 0.28
Oxacillin46. 21 ± 0.3333.02 ± 0.3650.01 ± 0.1326.29 ± 0.1838.22 ± 0.2939.33 ± 0.16
Clindamycin50. 55 ± 0.3134.01 ± 0.2244.41 ± 0.2329.11 ± 0.4145.14 ± 0.3042.17 ± 0.19
Table
Table 2. The minimal inhibitory concentration (MIC *), in mg/mL, of Tamarix gallica honey from Saudi Arabia (n = 50), Egypt (n = 50), and Libya (n = 50) against the antibiotic-resistant bacterial strains.
Table 2. The minimal inhibitory concentration (MIC *), in mg/mL, of Tamarix gallica honey from Saudi Arabia (n = 50), Egypt (n = 50), and Libya (n = 50) against the antibiotic-resistant bacterial strains.
Gram-positive
50 mg/mL25 mg/mL12.5 mg/mL6.25 mg/mL3.12 mg/mL1.56 mg/mL0.78 mg/mL390 µg/mL195 µg/mL97 µg/mL
Staphylococcus aureus
Saudi Arabia0.080.150.20.250.30.40.40.40.40.4
Libya0.070.20.250.30.30.40.40.40.40.4
Egypt0.050.150.1750.20.30.40.40.40.40.4
Streptococcus mutans
Saudi Arabia0.090.150.20.250.270.40.40.40.40.4
Libya0.090.150.250.30.30.40.40.40.40.4
Egypt0.080.10.1750.20.30.40.40.40.40.4
Gram-negative
50 mg/mL25 mg/mL12.5 mg/mL6.25 mg/mL3.12 mg/mL1.56 mg/mL0.78 mg/mL390 µg/mL195 µg/mL97 µg/mL
Klebsiella pneumoniae
Saudi Arabia0.10.120.20.250.270.40.40.40.40.4
Libya0.10.20.250.30.350.40.40.40.40.4
Egypt0.10.10.1750.20.30.40.40.40.40.4
Escherichia coli
Saudi Arabia0.090.150.20.250.270.40.40.40.40.4
Libya0.090.150.250.30.30.40.40.40.40.4
Egypt0.080.10.1750.20.30.40.40.40.40.4
Proteus vulgaris
Saudi Arabia0.090.10.170.250.250.20.20.20.20.2
Libya0.090.150.250.30.30.40.40.40.40.4
Egypt0.080.10.170.20.30.10.10.10.10.1
Pseudomonas aeruginosa
Saudi Arabia0.080.10.150.20.250.40.40.40.40.4
Libya0.090.10.150.120.30.10.10.10.10.1
Egypt0.080.10.120.20.30.40.40.40.40.4
Drugs for positive control for growth inhibition
Staphylococcus aureusStreptococcus mutansKlebsiella pneumoniaeEscherichia coliProteus vulgarisPseudomonas aeruginosa
Penicillin8 × 10−61.6 × 10−66.4 × 10−78 × 10−61.28 × 10−51.6 × 10−7
Oxacillin1.6 × 10−83.2 × 10−81.28 × 10−71.6 × 10−78 × 10−66.4 × 10−8
Clindamycin8 × 10−71.28 × 10−66.4 × 10−88 × 10−71.6 × 10−61.6 × 10−7
* MIC, concentration required for 99% bacteriostatic effect.
Table
Table 3. The total phenolics, total flavonoids, and DPPH of the Tamarix gallica honey (mean values ± SE).
Table 3. The total phenolics, total flavonoids, and DPPH of the Tamarix gallica honey (mean values ± SE).
HoneySamples (n)Total Phenolics (mg GAE/100 g Honey)Total Flavonoids (mg RE/100 g Honey)DPPH
(mg AAE/100 g Honey)
Saudi Arabia50129.89 ± 10.6683.1 ± 18.33153.30 ± 15.18
Libya50134.11 ± 13.3063.6 ± 11.13101.00 ± 11.82
Egypt50142.29 ± 15.3275.5 ± 13.47173.80 ± 10.51
Table
Table 4. Pollen analysis of the Tamarix gallica honey from different origins.
Table 4. Pollen analysis of the Tamarix gallica honey from different origins.
Honey OriginBotanical FamilyBotanical SpeciesFrequency of Occurrence *
Saudi ArabiaRhamnaceae
Mimosaceae
Tamaricaceae		Ziziphus jujuba
Acacia asak
Tamarix gallica		++
+
++++
LibyaRhamnaceae
Tamaricaceae
Tamaricaceae		Ziziphus jujuba
Tamarix atlantis
Tamarix gallica		++
++
++++
EgyptRhamnaceae
Poaceae
Tamaricaceae
Tamaricaceae
Brassicaceae		Ziziphus lotus
Oryza meyeriana
Tamarix nilotica
Tamarix gallica
Brassica tournefortii Gouan		++
++
++
++++
+
* ++++: more than 70%; ++: 60%; +: 50%.
Table
Table 5. The physicochemical parameters of the Tamarix gallica honey from Saudi Arabia (n = 50), Egypt (n = 50), and Libya (n = 50) (mean values ± SE).
Table 5. The physicochemical parameters of the Tamarix gallica honey from Saudi Arabia (n = 50), Egypt (n = 50), and Libya (n = 50) (mean values ± SE).
Physicochemical ParametersHoney Origin
SaudiLibyaEgypt
Moisture (%)14.94 ± 0.8813.2 ± 0.5816.15 ± 0.11
Fructose (%)40.94 ± 0.6839.33 ± 0.4839.74 ± 0.33
Glucose (%)35.64 ± 0.4435.13 ± 1.4835.64 ± 0.58
Fructose/glucose ratio1.141.111.11
Fructose + Glucose (%)76.57 ± 1.8574.46 ± 3.0575.38 ± 2.66
Sucrose (%)1.28 ± 0.301.75 ± 0.221.75 ± 0.32
HMF (mg/kg)22.36 ± 0.1020.25 ± 0.455.95 ± 0.55
Acidity (meq/l)19.6 ± 1.6113 ± 0.5821.5 ± 0.61
Diastase (DN)18.9 ± 0.3810.25 ± 0.6428.15 ± 0.47
Electrical conductivity (mS/cm)0.51 ± 0.0040.4 ± 0.0030.47 ± 0.0022
Water-insoluble solids content (%)0.064 ± 0.0060.075 ± 0.0030.065 ± 0.004
pH4.20 ± 0.584.25 ± 0.274.26 ± 0.53
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Hegazi, A.G.; Guthami, F.M.A.; Ramadan, M.F.A.; Gethami, A.F.M.A.; Craig, A.M.; El-Seedi, H.R.; Rodríguez, I.; Serrano, S. The Bioactive Value of Tamarix gallica Honey from Different Geographical Origins. Insects 2023, 14, 319. https://doi.org/10.3390/insects14040319

AMA Style

Hegazi AG, Guthami FMA, Ramadan MFA, Gethami AFMA, Craig AM, El-Seedi HR, Rodríguez I, Serrano S. The Bioactive Value of Tamarix gallica Honey from Different Geographical Origins. Insects. 2023; 14(4):319. https://doi.org/10.3390/insects14040319

Chicago/Turabian Style

Hegazi, Ahmed G., Fayez M. Al Guthami, Mohamed F. A. Ramadan, Ahmed F. M. Al Gethami, A. Morrie Craig, Hesham R. El-Seedi, Inmaculada Rodríguez, and Salud Serrano. 2023. "The Bioactive Value of Tamarix gallica Honey from Different Geographical Origins" Insects 14, no. 4: 319. https://doi.org/10.3390/insects14040319

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop