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Biological Activities of Honeybee Products

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A special issue of Molecules (ISSN 1420-3049). This special issue belongs to the section "Natural Products Chemistry".

Deadline for manuscript submissions: closed (30 June 2019) | Viewed by 78456

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Dr. Juraj Majtan

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Laboratory of Apidology and Apitherapy, Department of Microbial Genetics, Institute of Molecular Biology, Slovak Academy of Sciences, Dubravska Cesta 21, 845 51 Bratislava, Slovakia
Interests: honeybee products; wound healing; antibacterial activity; immunomodulation
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Special Issue Information

Dear colleague,

Honeybee products are well established in modern medicine and their use in clinical practice is increasing because of their biological and therapeutic properties. Honey, the most frequently used bee product in medicine (wound care), is touted to the public as less toxic and more effective than conventional drugs for various ailments, because it is “natural” and its efficacy is based on knowledge gained over thousands of years. Honey, as a potent antimicrobial product can inhibit the growth of a wide range of bacteria, including multi-drug resistant pathogens, yeast, and fungi. Natural honey represents an ideal agent that meets all criteria needed for it to be therapeutically useful in treating bacterial infections. In light of recent advances in api-medical research, honey and other bee products also exhibit immunomodulatory activities and are able to stimulate various different responses in immune and cutaneous cells. However, the mechanisms underlying the biological activities of honeybee products, including honey, have not been fully elucidated, often because of the synergistic interactions of several active molecules. The aim of this Special Issue is to highlight the most recent results in the field of the biological properties of honeybee products, and it is dedicated to the identification and characterisation of new biological active compounds. Studies dealing with the processing of honeybee products (e.g. sterilisation) in order to standardise bee products for medical usage are also welcome.

Dr. Juraj Majtan
Guest Editor

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Keywords

honeybee products
bioactive compounds
drug discovery
mechanisms of biological action
antimicrobial action
immunomodulatory action

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Published Papers (9 papers)

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Research

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19 pages, 6242 KiB

Open AccessArticle

Identification of Resveratrol as Bioactive Compound of Propolis from Western Romania and Characterization of Phenolic Profile and Antioxidant Activity of Ethanolic Extracts

by Alexandra Duca, Adrian Sturza, Elena-Alina Moacă, Monica Negrea, Virgil-Dacian Lalescu, Diana Lungeanu, Cristina-Adriana Dehelean, Danina-Mirela Muntean and Ersilia Alexa

Molecules 2019, 24(18), 3368; https://doi.org/10.3390/molecules24183368 - 16 Sep 2019

Cited by 38 | Viewed by 4863

Abstract

The present study aimed to assess the phenolic content of eight ethanolic propolis samples (P1–P8) harvested from different regions of Western Romania and their antioxidant activity. The mean value of total phenolic content was 214 ± 48 mg gallic acid equivalents (GAE)/g propolis. All extracts contained kaempferol (514.02 ± 114.80 μg/mL), quercetin (124.64 ± 95.86 μg/mL), rosmarinic acid (58.03 ± 20.08 μg/mL), and resveratrol (48.59 ± 59.52 μg/mL) assessed by LC-MS. The antioxidant activity was evaluated using 2 methods: (i) DPPH (2,2-diphenyl-1-picrylhydrazyl) assay using ascorbic acid as standard antioxidant and (ii) FOX (Ferrous iron xylenol orange OXidation) assay using catalase as hydrogen peroxide (H₂O₂) scavenger. The DPPH radical scavenging activity was determined for all samples applied in 6 concentrations (10, 5, 3, 1.5, 0.5 and 0.3 mg/mL). IC₅₀ varied from 0.0700 to 0.9320 mg/mL (IC₅₀ of ascorbic acid = 0.0757 mg/mL). The % of H₂O₂ inhibition in FOX assay was assessed for P1, P2, P3, P4 and P8 applied in 2 concentrations (5 and 0.5 mg/mL). A significant H₂O₂% inhibition was obtained for these samples for the lowest concentration. We firstly report the presence of resveratrol as bioactive compound in Western Romanian propolis. The principal component analysis revealed clustering of the propolis samples according to the polyphenolic profile similarity. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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17 pages, 1063 KiB

Open AccessArticle

Comparison of Physicochemical, Microbiological Properties and Bioactive Compounds Content of Grassland Honey and other Floral Origin Honeys

by Laura Agripina Scripcă, Liliana Norocel and Sonia Amariei

Molecules 2019, 24(16), 2932; https://doi.org/10.3390/molecules24162932 - 13 Aug 2019

Cited by 23 | Viewed by 4870

Abstract

The aim of this study was to compare the physicochemical, the microbiological, and the antioxidant characteristics of unifloral honey, polyfloral honey, honeydew, and hay meadows honey. Hay meadow is type of semi-natural grassland with a great floral diversity, an important resource for pollinators. Grasslands are the source of the spring nectar honey obtained in May and June. Water content, sugars (fructose, glucose, sucrose, trehalose, melezitose, maltose, erlose, turanose, and raffinose), electrical conductivity, phenolic content (gallic acid, protocatechuic acid, 4-hydrxybenzoic acid, vanilic acid, chlorogenic acid, caffeic acid, p-coumaric acid, rosmarinic acid, myricetin, quercitin, luteolin, kaempferol), color, viscosity, and microbiological characteristics were performed for all samples of honey. The total polyphenols content was significant for grassland honey (21.50 mg/100 g) and honeydew (30.49 mg/100 g) and less significant for acacia (0.08 mg/100 g) and rape honey (0.14 mg/100 g). All samples were microbiologically safe, and standard plate count (SPC) values were <10 cfu/g for all the samples, but the grassland honey had the highest microbiological quality: 33.3% of samples without microorganisms, 50.0% with the presence of yeast under limit, and 16.7% with yeast and mold under limit, a situation that does not meet other types of honey. The results of statistical analysis obtained with principal component analysis (PCA) showed a major difference between the grassland honey and the other types of honey. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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14 pages, 786 KiB

Open AccessArticle

Pyrrolizidine Alkaloids: The Botanical Origin of Pollen Collected during the Flowering Period of Echium vulgare and the Stability of Pyrrolizidine Alkaloids in Bee Bread

by Christina Kast, Verena Kilchenmann, Hans Reinhard, Katharina Bieri and Otmar Zoller

Molecules 2019, 24(12), 2214; https://doi.org/10.3390/molecules24122214 - 13 Jun 2019

Cited by 27 | Viewed by 4244

Abstract

Previous studies have shown that pollen products sold as nutritional supplements and used in apitherapy may contain toxic pyrrolizidine alkaloids (PAs) if bees collect pollen from PA-containing plants, such as Echium vulgare. In this study, the botanical origin of pollen from two observation sites was studied. Despite a high PA content in pollen samples that bees collected during E. vulgare’s flowering period, bees were found to collect relatively few Echium pollen loads. Thus, the monitoring of pollen loads collected at the apiaries is unviable to estimate the risk of PA contamination in pollen or bee bread. In a second step, the stability of PAs in bee bread samples containing PAs at concentrations of 2538 ng/g and 98 ng/g was assessed over a period of five or six months, respectively. No significant PA reduction was observed in bee bread stored at 15 °C, but there were overall PA reductions of 39% and 33% in bee bread stored at 30 °C, reflecting hive conditions. While PA N-oxides decreased over time, other types of PAs remained relatively stable. Monitoring PAs in pollen products remains important to ensure consumer safety and should include echivulgarine (and its N-oxide), the major PA type found in pollen from E. vulgare. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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24 pages, 1692 KiB

Open AccessArticle

The Anti-Staphylococcal Potential of Ethanolic Polish Propolis Extracts

by Katarzyna Grecka, Piotr M. Kuś, Piotr Okińczyc, Randy W. Worobo, Justyna Walkusz and Piotr Szweda

Molecules 2019, 24(9), 1732; https://doi.org/10.3390/molecules24091732 - 3 May 2019

Cited by 60 | Viewed by 6771

Abstract

The principal objective of this study was to determine the anti-staphylococcal potential of ethanol extracts of propolis (EEPs). A total of 20 samples of propolis collected from apiaries located in different regions of Poland were used in the study. The two-fold broth microdilution method revealed some important differences in the antimicrobial activity of investigated EEPs. Up to the concentration of 4096 µg/mL no activity was observed against Gram-negative bacteria (E. coli and P. aeruginosa). Staphylococci exhibited much higher susceptibility. The highest efficiency observed for EEP12 and EEP20 (MIC values ranged between 32 and 256 µg/mL). However, the achievement of bactericidal effect usually required higher concentrations. In the case of clinical isolates of S. aureus MBC values for EEP12 and EEP20 ranged from 512 to 1024 µg/mL. The HPLC analysis revealed that these two products contained a higher concentration of flavonoids (flavonols, flavones, and flavanones) compared to other investigated EEPs. In checkerboard test, a synergistic anti-staphylococcal effect was observed for the action of EEP20 in combination with amikacin, kanamycin, gentamycin, tetracycline, and fusidic acid (all these antibiotics inhibit protein synthesis). Moreover, the investigated EEPs effectively eradicated staphylococcal biofilm. The obtained results clearly confirm the high anti-staphylococcal potential of propolis harvested in Polish apiaries. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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20 pages, 3981 KiB

Open AccessArticle

Antibacterial Activity of Different Blossom Honeys: New Findings

by Marcela Bucekova, Lucia Jardekova, Valeria Juricova, Veronika Bugarova, Gabriele Di Marco, Angelo Gismondi, Donatella Leonardi, Jarmila Farkasovska, Jana Godocikova, Maros Laho, Jaroslav Klaudiny, Viktor Majtan, Antonella Canini and Juraj Majtan

Molecules 2019, 24(8), 1573; https://doi.org/10.3390/molecules24081573 - 21 Apr 2019

Cited by 137 | Viewed by 8374

Abstract

Antibacterial activity is the most investigated biological property of honey. The goal of this study was to evaluate the antibacterial activity of 57 Slovak blossom honeys against Staphylococcus aureus and Pseudomonas aeruginosa and investigate the role of several bioactive substances in antibacterial action of honeys. Inhibitory and bactericidal activities of honeys were studied to determine the minimum inhibitory and bactericidal concentrations. The contents of glucose oxidase (GOX) enzyme, hydrogen peroxide (H₂O₂), and total polyphenols (TP) were determined in honeys. We found that honey samples showed different antibacterial efficacy against the tested bacteria as follows: wildflower honeys > acacia honeys > rapeseed honeys. Overall antibacterial activity of the honeys was statistically-significantly correlated with the contents of H₂O₂ and TP in honeys. A strong correlation was found between the H₂O₂ and TP content. On the other hand, no correlation was found between the content of GOX and level of H₂O₂. Antibacterial activity of 12 selected honeys was markedly reduced by treatment with catalase, but it remained relatively stable after inactivation of GOX with proteinase-K digestion. Obtained results suggest that the antibacterial activity of blossom honeys is mainly mediated by H₂O₂ levels present in honeys which are affected mainly by polyphenolic substances and not directly by GOX content. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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12 pages, 1697 KiB

Open AccessArticle

Propolis Induces AQP3 Expression: A Possible Way of Action in Wound Healing

by Simona Martinotti, Giorgia Pellavio, Umberto Laforenza and Elia Ranzato

Molecules 2019, 24(8), 1544; https://doi.org/10.3390/molecules24081544 - 19 Apr 2019

Cited by 35 | Viewed by 4778

Abstract

Propolis is the generic name of a complex of resinous compound collected by honeybees and it has been utilized for many years in folk medicine. As other products generated by honeybees (such as royal jelly, pollen, honey), propolis has great therapeutic properties, but very little scientific information is available. Therefore, this study was aimed at exploring the potential wound healing properties of propolis. To that end, we utilized an in vitro scratch wound healing model consisting of human immortalized keratinocytes. Our scratch wound data clearly demonstrated that propolis induced a pronounced increase in the wound repair abilities of keratinocytes. A cell migration assay showed that propolis stimulated keratinocytes to close the wound. We revealed the role of H₂O₂ as the main mediator of propolis regenerative properties. We showed that this extracellularly released H₂O₂ could pass across the plasma membrane through a specific aquaporin (i.e., AQP3) modulating intracellular responses. The data offer a biological characterization of propolis positive effects suggesting that propolis could also be utilized in wound treatment within clinical settings. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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14 pages, 1475 KiB

Open AccessArticle

10-HDA, A Major Fatty Acid of Royal Jelly, Exhibits pH Dependent Growth-Inhibitory Activity Against Different Strains of Paenibacillus larvae

by Mária Šedivá, Maroš Laho, Lenka Kohútová, Andrea Mojžišová, Juraj Majtán and Jaroslav Klaudiny

Molecules 2018, 23(12), 3236; https://doi.org/10.3390/molecules23123236 - 7 Dec 2018

Cited by 35 | Viewed by 6771

Abstract

Paenibacillus larvae (P. larvae) is a bacterial pathogen causing American foulbrood (AFB), the most serious disease of honeybee larvae. The food of young larvae could play an important role in the resistance of larvae against AFB. It contains antibacterial substances produced by honeybees that may inhibit the propagation of the pathogen in larval midguts. In this study, we identified and investigated the antibacterial effects of one of these substances, trans-10-hydroxy-2-decenoic acid (10-HDA), against P. larvae strains including all Enterobacterial Repetitive Intergenic Consensus (ERIC) genotypes. Its inhibitory activities were studied by determining the minimum inhibitory concentrations (MICs). It was found that 10-HDA efficacy increases substantially with decreasing pH; up to 12-fold differences in efficacy were observed between pH = 5.5 and pH = 7.2. P. larvae strains showed different susceptibility to 10-HDA; up to 2.97-fold differences existed among various strains with environmentally important ERIC I and ERIC II genotypes. Germinating spores of the pathogen were generally more susceptible to 10-HDA than vegetative cells. Our findings suggest that 10-HDA could play significant role in conferring antipathogenic activity to larval food in the midguts of young larvae and contribute to the resistance of individual larvae to P. larvae. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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11 pages, 1756 KiB

Open AccessArticle

Identification of Ubiquinones in Honey: A New View on Their Potential Contribution to Honey’s Antioxidant State

by Katrina Brudzynski and Liset Maldonado-Alvarez

Molecules 2018, 23(12), 3067; https://doi.org/10.3390/molecules23123067 - 23 Nov 2018

Cited by 8 | Viewed by 3650

Abstract

Honey is composed of macromolecules arranged into multicomponent colloidal particles dispersed in a supersaturated sugar solution. The core part of colloidal particles in honey is made up of high-molecular weight protein-polyphenol complexes. We designed a multi-step extraction process to gain better insight into the phenolic compounds strongly bound to proteins in honey. Honeys were sequentially extracted by solvents of reduced polarities and the extraction process was monitored by LC-ESI-MS/MS. Unexpectedly, the results revealed ubiquinone-like compounds that partitioned to both, soluble supernatants and protein-bound insoluble residues from which they were released after the pronase-digestion of proteins. The accurate mass measurement and MS/MS fragmentation patterns using UPHLC-MS/MS coupled to quadrupole orbitrap confirmed their identification as ubiquinones. Distribution of ubiquinone-bound proteins was further investigated by the fractionation of honey protein-polyphenol complexes by size-exclusion chromatography followed by LC-ESI-MS analysis. Mass spectra revealed the presence of ubiquinones (UQs) in fractions of high polyphenol to protein ratio. The dominant mass peaks observed in these fractions were identified as UQ-3, UQ-5, and UQ-7. Since the quinone group of UQs is involved in redox reaction, we discuss the possibility that UQs may contribute to the antioxidant/proxidant activity of these complexes. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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Review

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17 pages, 1898 KiB

Open AccessReview

Antibacterial Properties of Propolis

by Izabela Przybyłek and Tomasz M. Karpiński

Molecules 2019, 24(11), 2047; https://doi.org/10.3390/molecules24112047 - 29 May 2019

Cited by 410 | Viewed by 31772

Abstract

Researchers are continuing to discover all the properties of propolis due to its complex composition and associated broad spectrum of activities. This review aims to characterize the latest scientific reports in the field of antibacterial activity of this substance. The results of studies on the influence of propolis on more than 600 bacterial strains were analyzed. The greater activity of propolis against Gram-positive bacteria than Gram-negative was confirmed. Moreover, the antimicrobial activity of propolis from different regions of the world was compared. As a result, high activity of propolis from the Middle East was found in relation to both, Gram-positive (Staphylococcus aureus) and Gram-negative (Escherichia coli) strains. Simultaneously, the lowest activity was demonstrated for propolis samples from Germany, Ireland and Korea. Full article

(This article belongs to the Special Issue Biological Activities of Honeybee Products)

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