Propolis characterization and antimicrobial activities against Staphylococcus aureus and Candida albicans: A review

Propolis is a plant-based sticky substance that is produced by honeybees. It has been used traditionally by ancient civilizations as a folk medicine, and is known to have many pharmaceutical properties including antioxidant, antibacterial, antifungal, anti-inflammatory, antiviral, and antitumour effects. Worldwide, researchers are still studying the complex composition of propolis to unveil its biological potential, and especially its antimicrobial activity against a variety of multidrug-resistant microorganisms. This review explores scientific reports published during the last decade on the characterization of different types of propolis, and evaluates their antimicrobial activities against Staphylococcus aureus and Candida albicans. Propolis can be divided into different types depending on their chemical composition and physical properties associated with geographic origin and plant sources. Flavonoids, phenols, diterpenes, and aliphatic compounds are the main chemicals that characterize the different types of propolis (Poplar, Brazilian, and Mediterranean), and are responsible for their antimicrobial activity. The extracts of most types of propolis showed greater antibacterial activity against Gram-positive bacteria: particularly on S. aureus, as well as on C. albicans, as compared to Gram-negative pathogens. Propolis acts either by directly interacting with the microbial cells or by stimulating the immune system of the host cells. Some studies have suggested that structural damage to the microorganisms is a possible mechanism by which propolis exhibits its antimicrobial activity. However, the mechanism of action of propolis is still unclear, due to the synergistic interaction of the ingredients of propolis, and this natural substance has multi-target activity in the cell. The broad-spectrum biological potentials of propolis present it as an ideal candidate for the development of new, potent, and cost-effective antimicrobial agents.     

Natural products and their semi-synthetic derivatives against antimicrobial-resistant human pathogenic bacteria and fungi

Human infectious diseases caused by various microbial pathogens, in general, impact a large population of individuals every year. These microbial diseases that spread quickly remain to be a big issue in various health-related domains and to withstand the negative drug impacts, the antimicrobial-resistant pathogenic microbial organisms (pathogenic bacteria and pathogenic fungi) have developed a variety of resistance processes against many antimicrobial drug classes. During the COVID-19 outbreak, there seems to be an upsurge in drug and multidrug resistant-associated pathogenic microbial species. The preponderance of existing antimicrobials isn’t completely effective, which limits their application in clinical settings. Several naturally occurring chemicals produced from bacteria, plants, animals, marine species, and other sources are now being studied for antimicrobial characteristics. These natural antimicrobial compounds extracted from different sources have been demonstrated to be effective against a variety of diseases, although plants remain the most abundant source. These compounds have shown promise in reducing the microbial diseases linked to the development of drug tolerance and resistance. This paper offers a detailed review of some of the most vital and promising natural compounds and their derivatives against various human infectious microbial organisms. The inhibitory action of different natural antimicrobial compounds, and their possible mechanism of antimicrobial action against a range of pathogenic fungal and bacterial organisms, is provided. The review will be useful in refining current antimicrobial (antifungal and antibacterial) medicines as well as establishing new treatment strategies to tackle the rising number of human bacterial and fungal-associated infections.     

Propolis as a novel antibacterial agent

Propolis (bee glue) is a bee glue, sticky resinous material released from various plant sources such as bud exudates, flowers, and leaves modified by bee secretions and wax propolis is composed of resins, waxes, polyphenols, polysaccharides, volatile materials, and secondary metabolites that are responsible for various bioactivity such as antibacterial, anti-angiogenic, antiulcer, anti-inflammatory, antioxidant, and anti-viral activities. The physico-chemical characteristics and the natural properties of various kinds of propolis have been studied for the past decade. Novel active anti-microbial compounds have been identified in propolis. Those compounds positively modulated the antimicrobial resistance of multidrug resistant bacteria. Published research has indicated that propolis and its derivatives has many natural antimicrobial compounds with a broad spectrum against different types of bacteria and that it enhanced the efficacy of conventional antibiotics. Besides, the combination of propolis with other compounds such as honey has been studied whereby, such combinations have a synergistic effect against bacterial strains such as Escherichia coli and Staphylococcus aureus. The activity of propolis is very much dependent on seasonal and regional factors, and Middle Eastern propolis have shown best antibacterial efficacy. Propolis and its main flavonoids ingredients should not be overlooked and should be evaluated in clinical trials to better elucidate their potential application in various fields of medicine. Clinical antibacterial potential and its use in new drugs of biotechnological products should be conducted. This review aims at highlighting some of the recent scientific findings associated with the antibacterial properties of propolis and its components.     

Egyptian propolis: 1-antimicrobial activity and chemical composition of Upper Egypt propolis

The antimicrobial activity of four propolis samples collected from Upper Egypt against Staphylococcus aureus; Escherichia coli and Candida albicans was evaluated. There was a variation in the antimicrobial activity according to the propolis origin. Banisweif propolis showed the highest antimicrobial activity against Staphylococcus aureus, Escherichia coli and Candida albicans, but Fayoum propolis had moderate activity against all tested pathogens. Propolis collected from Assiut and Souhag gave lower antimicrobial activity. Propolis samples were investigated by GC/MS, 71 compounds were identified, 14 being new for propolis. Banisweif propolis is characterized by the presence of 7 caffeate esters and 4 triterpenoids. Fayoum propolis showed the highest amount of lactic acid and the presence of 3 chalcones. But Assiut propolis is characterized by the presence of 4 prenylated coumarates. Souhag propolis is characterized by the presence of 5 aliphatic dicarboxylic acids and some other new compounds to propolis.     

In vitro activity of propolis against Streptococcus pyogenes

Propolis, a multifunctional substance used by bees to maintain the safety of their hives, is popular for its therapeutic potential against some micro-organisms. Ethanolic extracts of two propolis specimens, collected from different areas within a region in the north-west of Italy, were examined to evaluate their antimicrobial activity against 46 Streptococcus pyogenes strains. By both agar dilution and agar diffusion methods, the minimal inhibitory concentration (MIC) and minimal bactericidal concentration (MBC) were 相似文献   

Egyptian propolis: 3. Antioxidant,antimicrobial activities and chemical composition of propolis from reclaimed lands

The free radical scavenging effect of two propolis samples collected from reclaimed land, Egypt as well as of vitamin C and caffeic acid in 1,1-diphenyl-2-picrylhydrazyl (DPPH) free radical system was determined. The antimicrobial (Staphylococcus aureus; Escherichia coli and Candida albicans) activity was also investigated. The results of the free radical scavenging effect of El-Saff and Ismailia propolis showed a concentration-dependent activity. The antioxidant activity was varied according to the examined material. It was obvious that caffeic acid and vitamin C showed the highest activity if compared with the propolis samples. El- Saff propolis had a higher antioxidant activity than Ismailia propolis, it showed a higher antibacterial activity against Staphylococcus aureus and a higher anti-fungal activity against Candida albicans. While the Ismailia propolis had a higher antibacterial activity against Escherichia coli, than El-Saff propolis. The chemical composition of propolis samples was investigated by GC/MS, where 75 compounds were identified, 22 being new for propolis. The Ismailia propolis was characterized by the presence of a highly significant amount of aromatic acid esters (47.3%) and triterpenoids (17.3%), while El-Saff propolis contained 3% and 1.9% respectively. The new esters belonged to 4-methoxyhydrocinnamic acid, hydroferulic acid and ferulic acid. El-Saff propolis had a very high significant amount (27%) of 2,6-bis-(pentanyloxy)-4-pentanylphenethanol, which is also a new compound for propolis.     

Composition and functional properties of propolis (bee glue): A review

Propolis is a natural substance collected by honey bees from various plants such as, poplar, palm, pine, conifer secretions, gums, resins, mucilage and leaf buds. It is collected and brought very painstakingly by honey bees to be used for sealing cracks and crevices occurring in their hives. Originally, it as an antiseptic meant for preventing bee-hive from microbial infections along with preventing decomposition of intruders. Additionally, propolis has been used in folk medicine for centuries. The biological characteristics of propolis depend upon its chemical composition, plant sources, geographical zone and seasons. More than 300 compounds have been identified in propolis such as, phenolic compounds, aromatic acids, essential oils, waxes and amino acids. Many scientific articles are published every year in different international journals, and several groups of researchers have focused their attention on the chemical compounds and biological activity of propolis.     

In vitro antimicrobial activity of propolis samples from different geographical origins against certain oral pathogens

Propolis is an agent having antimicrobial properties, however, its composition can vary depending on the area where it is collected. In the present study, the antimicrobial activity of five propolis samples, collected from four different regions in Turkey and from Brazil, against nine anaerobic strains was evaluated. Ethanol extracts of propolis (EEP) were prepared from propolis samples and we determined minimum inhibitory concentrations (MIC) and minimum bactericidal concentrations (MBC) of EEP on the growth of test microorganisms by using agar dilution method. All strains were susceptible and MIC values ranged from 4 to 512 microg/ml for propolis activity. Propolis from Kazan-Ankara showed most effective MIC values to the studied microorganisms. MBC values of Kazan-Ankara EEP samples were ranged from 8 to 512 microg/ml. Death was observed within 4 h of incubation for Peptostreptococcus anaerobius and micros and Lactobacillus acidophilus and Actinomyces naeslundii, while 8 h for Prevotella oralis and Prevotella melaninogenica and Porphyromonas gingivalis, 12 h for Fusobacterium nucleatum, 16 h for Veillonella parvula. It was shown that propolis samples were more effective against Gram positive anaerobic bacteria than Gram negative ones. The organic chemical compositions of EEPs were determined by high-resolution gas chromatography coupled to mass spectrometry (GC-MS). The main compounds of EEPs were flavonoids such as pinobanksin, quercetin, naringenin, galangine, chrysin and aromatic acids such as cafeic acid. Because of increased antimicrobial resistance, propolis may be kept in mind in the treatment of oral cavity diseases.     

Chemical compositions and antimicrobial activities of four different Anatolian propolis samples

Propolis means a gum that is gathered by bees from various plants. It is known for its biological properties, having antibacterial, antifungal and healing properties. The aims of this study were to evaluate the antimicrobial activity of four different Anatolian propolis samples on different groups of microorganisms including some oral pathogens and comparison between their chemical compositions. Ethanol extracts of propolis (EEP) were prepared from four different Anatolian propolis samples and examined whether EEP inhibit the growth of the test microorganisms or not. For the antimicrobial activity assays, minimum inhibitory concentrations (MIC) were determined by using macrodilution method. The MIC values of the most effective propolis (TB) were 2 microg/ml for Streptococcus sobrinus and Enterococcus faecalis, 4 microg/ml for Micrococcus luteus, Candida albicans and C. krusei, 8 microg/ml for Streptococcus mutans, Staphylococcus aureus, Staphylococcus epidermidis and Enterobacter aerogenes, 16 microg/ml for Escherichia coli and C. tropicalis and 32 microg/ml for Salmonella typhimurium and Pseudomonas aeruginosa. The chemical compositions of EEP's were determined by high-temperature high-resolution gas chromatography coupled to mass spectrometry. The main compounds of four Anatolian propolis samples were flavonoids such as pinocembrin, pinostropin, isalpinin, pinobanksin, quercetin, naringenin, galangine and chrysin. Although propolis samples were collected from different regions of Anatolia all showed significant antimicrobial activity against the Gram positive bacteria and yeasts. Propolis can prevent dental caries since it demonstrated significant antimicrobial activity against the microorganisms such as Streptococcus mutans, Streptococcus sobrinus and C. albicans, which involves in oral diseases.     

The inhibitory activity of typified propolis against Enterococcus species

Propolis, a natural bee product widely used for its antimicrobial activity, was tested against isolates of Enterococcus from humans, pig-tailed macaques, isolates of refractory endodontic treatment cases, and isolates from Lactobacillus-containing food supplements. Typification of the propolis was performed by high-performance liquid chromatography (HPLC) by which prenylated compounds, cinnamic acid derivatives, and flavonoids were detected as the main constituents. Minimum inhibitory concentrations (MIC) were determined using the agar dilution method. All human and animal Enterococcus isolates demonstrated MIC values of 1600 microg/mL. Enterococcal species of human and animal origin were inhibited by propolis. Particularly, human isolates of E. faecium and E. faecalis of refractory endodontic treatment cases were susceptible to propolis of Brazilian origin.     

Chemical composition and antimicrobial activity of European propolis

Three propolis samples from Austria, Germany and France were investigated by GC/MS, where eleven compounds were being new for propolis. The samples showed some similarities in their qualitative composition. Phenylethyl-trans-caffeate, benzyl ferulate and galangin were predominant in German propolis. Benzyl caffeate was predominant in French sample. Pinocembrin was predominant in French and Austrian propolis and trans-p-coumaric acid was predominant in all samples. The antimicrobial activity against Staphylococcus aureus; Escherichia coli, and Candida albicans was evaluated. German propolis showed the highest antimicrobial activity against Staphylococcus aureus and Escherichia coli. While Austrian propolis has the highest activity against Candida albicans. French propolis was effective against all pathogens but less than German and Austrian propolis.     

HPTLC-MS as an efficient hyphenated technique for the rapid identification of antimicrobial compounds from propolis

The well-known anti-infective properties of propolis are determined by its chemical composition, which in turn is influenced by geographical factors and reflects the botanical diversity in the vicinity of the beehive. Although there are several reports on the anti-infective properties of crude propolis, few are aimed at identifying specific compound(s) responsible for the observed activities. Using South African propolis as an example, the application of high performance thin layer chromatography-bioautography in tandem with mass spectrometry was investigated for the rapid identification of antimicrobial and anti-quorum sensing (anti-QS) compounds. Pinocembrin was found to be responsible for the observed antifungal activity of the propolis against Candida albicans. Three compounds were found to be active against all of the evaluated Gram-positive and Gram-negative bacteria. The identity of the first was confirmed as pinobanksin, one remains unidentified, while the third corresponds to either pinobanksin 3-O-pentanoate or 2-methylbutyrate. The identification of caffeic acid as the anti-QS component was confirmed quantitatively using the violacein inhibitory assay.     

Antiparasitic Properties of Propolis Extracts and Their Compounds

Propolis is a bee product that has been used in medicine since ancient times. Although its anti-inflammatory, antioxidant, antimicrobial, antitumor, and immunomodulatory activities have been investigated, its anti-parasitic properties remain poorly explored, especially regarding helminths. This review surveys the results obtained with propolis around the world against human parasites. Regarding protozoa, studies carried out with the protozoa Trypanosoma spp. and Leishmania spp. have demonstrated promising results in vitro and in vivo. However, there are fewer studies for Plasmodium spp., the etiological agent of malaria and less so for helminths, particularly for Fasciola spp. and Schistosoma spp. Despite the favorable in vitro results with propolis, helminth assays need to be further investigated. However, propolis has shown itself to be an excellent natural product for parasitology, thus opening new paths and approaches in its activity against protozoa and helminths.     

Antimicrobial activity of the extract and isolated compounds from Baccharis dracunculifolia D. C. (Asteraceae)

Baccharis dracunculifolia D.C. (Asteraceae) is the most important plant source of the Brazilian green propolis. Since propolis is known for its antimicrobial activity, the aim of this work was to evaluate the antimicrobial activities of B. dracunculifolia and some of its isolated compounds. The results showed that the leaves extract of B. dracunculifolia (BdE) presents antifungal and antibacterial activities, especially against Candida krusei and Cryptococcus neoformans, for which the BdE showed IC50 values of 65 microg mL(-1) and 40 microg mL(-1), respectively. In comparison to the BdE, it was observed that the green propolis extract (GPE) showed better antimicrobial activity, displaying an IC50 value of 9 microg mL(-1) against C. krusei. Also, a phytochemical study of the BdE was carried out, affording the isolation of ursolic acid (1), 2a-hydroxy-ursolic acid (2), isosakuranetin (3), aromadendrin-4'-methylether (4), baccharin (5), viscidone (6), hautriwaic acid lactone (7), and the clerodane diterpene 8. This is the first time that the presence of compounds 1, 2, and 8 in B. dracunculifolia has been reported. Among the isolated compounds, 1 and 2 showed antibacterial activity against methicillin-resistant Staphylococcus aureus, displaying IC50 values of 5 microg mL(-1) and 3 microg mL(-1), respectively. 3 was active against C. neoformans, showing an IC50 value of 15 microg mL(-1) and a MIC value of 40 microg mL(-1), while compounds 4-8 were inactive against all tested microorganisms. The results showed that the BdE, similar to the GPE, displays antimicrobial activity, which may be related to the effect of several compounds present in the crude extract.     

Chemical properties and antioxidant and antimicrobial activities of slovenian propolis

The chemical composition as well as the antioxidant and antimicrobial activities of two EtOH extracts of propolis (PEEs) from Slovenia were determined. EtOH was used as extracting solvent at 70 and 96%, providing the extracts PEE70 and PEE96, respectively. The extraction with 70% EtOH was more efficient than that with 96% EtOH, as the PEE70 was richer in total phenolic compounds than the PEE96. The Slovenian propolis was characterized by different phenolic acids and flavonoids. The PEE96 was slightly richer in three specific compounds, i.e., caffeic acid, ferulic acid, and luteolin, while all other substances detected showed higher contents in the PEE70. The PEE70 showed a stronger reducing power and ability to scavenge free radicals and metal ions than the PEE96. Both PEEs were in the main more effective against Gram-positive bacteria than against fungi and Gram-negative bacteria like Salmonella and Escherichia coli, with the exception of Campylobacter. The PEE96 decreased the intracellular oxidation in Saccharomyces cerevisiae in a dose-dependent manner. The antimicrobial activities and antioxidant properties were related to the total phenolic contents. The two PEEs have the potential for use as natural antimicrobial and antioxidant additives in foods.     

Egyptian propolis: 2. Chemical composition,antiviral and antimicrobial activities of East Nile Delta propolis

Three propolis samples from East Nile Delta, Egypt were collected. Propolis samples were investigated by GC/MS,103 compounds were identified, 20 being new for propolis. Dakahlia propolis was a typical poplar propolis but it contained two new caffeate esters and two new triterpenoids. Ismailia propolis was characterized by the presence of new triterpenic acid methyl esters and it did not contain any aromatic acids, esters and flavonoids. Sharkia propolis was characterized by the presence of caffeate esters only, some di- and triterpenoids. The antiviral (Infectious Bursal Disease Virus and Reo-Virus) and antimicrobial (Staphylococcus aureus; Escherichia coli and Candida albicans) activities of propolis samples were investigated. Dakahlia propolis showed the highest antiviral activity against Infectious Bursal Disease Virus (IBDV) and the highest antibacterial activity against Escherichia coli and the highest antifungal activity against Candida albicans. While Ismailia propolis had the highest antiviral activity against Reo-virus. Sharkia propolis showed the highest antibacterial activity against Staphylococcus aureus and moderate antiviral activity against infectious bursal disease virus and reovirus.     

Interactions among flavonoids of propolis affect antibacterial activity against the honeybee pathogen Paenibacillus larvae

Propolis is derived from plant resins, collected by honeybees (Apis mellifera) and renown for its antibacterial properties. Here we test the antibacterial effects of ethanolic extracts of propolis from different origins on Paenibacillus larvae, the bacterial pathogen that causes American Foulbrood, a larval disease that can kill the honeybee colony. All tested propolis samples inhibited significantly the growth of P. larvae tested in vitro. The extracts showed major differences in the content of total flavonoids (ranging from 2.4% to 16.4%) and the total polyphenols (ranging between 23.3% and 63.2%). We found that it is not only the content of compounds in propolis, which influences the strength of antimicrobial effects but there is also a significant interaction effect among flavonoids of the propolis extracts. We propose that interaction effects among the various chemical compounds in propolis should be taken into account when considering the antibacterial effects against honeybee pathogens.     

In vitro study of the antimicrobial activity of Brazilian propolis against Paenibacillus larvae

The honey bee disease American foulbrood (AFB) is a serious problem since its causative agent (Paenibacillus larvae) has become increasingly resistant to conventional antibiotics. The objective of this study was to investigate the in vitro activity of propolis collected from various states of Brazil against P. larvae. Propolis is derived from plant resins collected by honey bees (Apis mellifera) and is globally known for its antimicrobial properties and particularly valued in tropical regions. Tests on the activity of propolis against P. larvae were conducted both in Brazil and Minnesota, USA using two resistance assay methods that measured zones of growth inhibition due to treatment exposure. The propolis extracts from the various states of Brazil showed significant inhibition of P. larvae. Clear dose responses were found for individual propolis extracts, particularly between the concentrations of 1.7 and 0.12 mg propolis/treatment disk, but the source of the propolis, rather than the concentration, may be more influential in determining overall activity. Two of the three tested antibiotics (tylosin and terramycin) exhibited a greater level of inhibition compared to most of the Brazilian samples, which could be due to the low concentrations of active compounds present in the propolis extracts. Additionally, the majority of the Brazilian propolis samples were more effective than the few collected in MN, USA. Due to the evolution of resistance of P. larvae to conventional antibiotic treatments, this research is an important first step in identifying possible new active compounds to treat AFB in honey bee colonies.     

Composition and in vitro antimicrobial activity of Populus buds and poplar-type propolis

The antibacterial activity of propolis has been widely investigated. Since reports dealing with antimicrobial activity of the origin of propolis are not available, this study was carried out aiming to analyse the in vitro antimicrobial activity of the methanol extracts of poplar type propolis and Populus (Populus nigra, P. alba, P. tremuloides) buds as its sources against standard strains of a panel of microorganisms by determining the minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC). The concentrations of the “poplar” phenolics were relatively high (4.5%) and some compounds typical for P. nigra such as pinobanksin and 4,3 acetyloxycaffeate were found in the propolis sample by GC-MS. The poplar type propolis and Populus bud exudates were found to inhibit most clinically important microorganisms in a wide spectrum including pathogenic yeasts but not Gram-negative bacteria.     

Terpenes with antimicrobial activity from Cretan propolis

Five terpenes, the diterpenes: 14,15-dinor-13-oxo-8(17)-labden-19-oic acid and a mixture of labda-8(17),13E-dien-19-carboxy-15-yl oleate and palmitate as well as the triterpenes, 3,4-seco-cycloart-12-hydroxy-4(28),24-dien-3-oic acid and cycloart-3,7-dihydroxy-24-en-28-oic acid were isolated from Cretan propolis. Moreover, 18 known compounds were also isolated, seven of them for the first time as propolis components. All structures were established on the basis of spectroscopic analysis and chemical evidence. All isolated compounds were tested for antimicrobial activity against some Gram-positive and Gram-negative bacteria as well as against some human pathogenic fungi showing a broad spectrum of antimicrobial activity.