Poplar-Type Propolis: Comparison
Please note this is a comparison between Version 2 by Lily Guo and Version 4 by Lily Guo.

Propolis is a resinous mixture, made by the honeybees from substances collected from tree or other plant buds, plant exudates, or resins found in the stem, branches, or leaves of different plants. 

  • Poplar-Type Propolis

1. Introduction

1. Introduction

Propolis is a bee product, made by the honeybees (Apis mellifera) from different resins, collected from plant leaves, buds, or exudates, mixed with bee saliva and wax[1]. This mixture is taken into the hive and used to protect the bee family from outside enemies, to bond the frames between them, to seal any hole in the hive, and to maintain a stable indoor temperature[2]. The color of propolis varies greatly with the botanical source and geographical origin. Poplar-type propolis color can vary from yellow orangish, to reddish and brown, or dark brown. Plant bud resins from Poplar species are primary sources for propolis from temperate zones (Europe, North America, and Asia), but also other species contribute to the chemistry of propolis from these areas (Betula sp., Acacia sp., Pinus sp., Salix, or Aesculus hippocastanum[3]. To the best of our knowledge, poplar type propolis have the widest spread along the globe, and its composition and properties are the most studied from all bee products, apart from honey.

Having such a large distribution over the temperate zones of the globe, poplar-type propolis is also very different in chemical compounds, although volatiles from the class of terpenoids and polyphenolic substances (phenolic acids and flavonoids) are the major compounds. A recent study by[4], identified a new type of propolis rich in flavonoids which exhibit also a very powerful antibacterial activity.

Different studies on the chemical composition of propolis have made possible the classification of propolis from different countries, knowing the fact that European propolis have as the main vegetal source, the exudates from different Populus species. It is generally accepted that propolis from temperate zones are rich in pinocembrin, pinobanksin, galangin, chrysin, caffeic, and ferulic acids; these are all phenolics reported in Poplar exudates. Miguel (2013) [5] reviewed the propolis type of countries from the Mediterranean basin. Italian propolis samples analysis revealed the presence of phenolic acids and flavonoids as the main components and concluded that poplar-type propolis was characteristic to Italy[6][7]. Other studies[8][9] have reported also phenolic acids and their esters and flavonoids in propolis samples from France. Hydroalcoholic extracts of propolis from Spain, revealed the presence of flavonoids as predominant components, demonstrating the poplar appurtenance[10][11]. Portuguese propolis characterization revealed methylated and/or esterified or hydroxylated derivatives of poplar flavonoids [5][12].

1.1. Chemical Composition and Analysis Methods

Propolis is known to be a very important natural antibiotic. Its properties were observed before its chemical composition was really analyzed. Before the development of separation and purification techniques to reveal chemical components of propolis, the existing studies focused mostly on bioactive properties and mainly attributed its entire composition to these properties. After the mentioned techniques were used more and more, the chemical composition of propolis was established, and its properties were attributed to different classes of compounds originating from different geographical areas [13][5][14][12][15][16][17].

Generally speaking, poplar-type propolis have about 50% resins, 30% beeswax, 10% aromatic oils, 5% pollen, and 5% other substances (minerals, vitamins, and amino acids)[18], and, so far, more than 350 compounds have been identified and quantified[19][20].

Different scientific studies have classified these components as phenolic acids and their esters, all classes of flavonoids (aglycones and glycosides), chalcones and dihydrochalcones, terpenes and hydrocarbons, alcohols and their esters, aldehydes, amino acids, fatty acids, sterols, sugars, and sugar alcohols[19]. The majority of these substances came from resins, plant exudates, but also from bee metabolism. Sugars and pollen came from cross contamination with nectar and the fatty component of propolis (fatty acids, esters, and glycerol) came from beeswax[19]. The major compounds of poplar-type propolis all over the world are presented in Table 1. As can be seen in the table, the majority of compounds belong to polyphenolic substances.

Table 1. Chemical composition of poplar-type propolis of the major producing poplar-type propolis of the world.

Plant Material

Separated Compounds

Adsorbent/Mobile Phases

Reference

Brazilian poplar buds

Flavonoid profiles

HPTLC RP-18 F254Merck/Ethanol-water (55:54, v/v)

[21]

Brazilian poplar buds

Gallic, ferulic, caffeic p-coumaric acids, quercetin, kaempferol, chrysin, pinocembrin, pinostrobin

TLC Silica gel 60 Merck/Hexane-ethyl acetate (3:2, v/v)

[22]

Populus balsamifera

Neutral substances (acylglycerides and sterols)

TLC Silica gel L40/100/petroleum ether-diethyl ether-acetic acid (80:20:1, v/v/v or 70:30:1, v/v/v); heptanes-benzene (9:1, v/v)

[23]

Populus nigra, P.nigra “Italica”. P.x can.”Robusta”, P.x canescens, P. berolinensis, P. maximowiczii, P. balsamifera, P. tremula

Apigenin, quercetin, kaempferol, chrysin, naringenin, caffeic acid phenethylester (CAPE), galangin, pinocembrin, caffeic acid

TLC Silica gel 60 Merck/hexane-ethylacetate-glacial acetic acid (5:3:1, v/v/v)

[24]

Populus alba, P. tremula, P. nigra “Italica”, P. x canadensis “Robusta”, P. canadensis “Marilandica”, P. balsamifera, P. candicans, P. simonii

Apigenin, luteolin, genkwanin, chrysin, tectochrysin, galangin, isorhamnetin, kaempferol, quercetin, myricetin, eriodictyol, naringenin, pinocembrin, pinostrobin, pinobanksin, chrysin 5, 7-dimethylether, pinocembrin 5, 7-dimethylether

TLC Silica gel 60 Merck/hexane-ethyl acetate-formic acid (60:40:1.3, v/v/v)

[25]

 

Over time, the methods used for propolis analysis have evolved significantly. Due to the nature of the main components of propolis, spectrophotometric and chromatographic (liquid and gas) methods have been used. Two different types of extraction are used in propolis analysis, i.e., extraction for the nonvolatile metabolites and the extraction for volatiles analysis. The first class of compounds are obtained by simple extraction with ethanol or methanol of different concentrations, extraction time, and temperatures[26] . Because no international regulations are available for propolis analysis, different conditions are used for these extractions. Generally, phenolic compounds are determined by liquid chromatography with different detections. A study on Portuguese propolis[27] used liquid chromatography with diode-array detection coupled to electrospray ionization tandem mass spectrometry (LC-DAD-ESI-MS) and characterized the phenolic compounds by comparing UV spectra, retention time, and MS information (m/z values) with reference compounds.

The most recent study on propolis phenolics and volatiles[28] used ultrahigh-performance liquid chromatography with diode array detector and quadrupole time-of-flight mass spectrometry (UHPLC-DAD-QqTOF-MS), and identified a high number of compounds (118 phenolics), suggesting that equipment and methods that are more elaborate and up-to-date can identify and quantify more compounds.

Propolis volatiles are responsible for the aroma and smells of the product, although they are found in small concentrations. Volatiles may give important information regarding plant sources, and thus the origin of propolis. Volatiles that present as the most abundant compounds in poplar-type propolis, include monoterpenes, sesquiterpenes, and organic compounds[29][30][31][32].

The most important criteria in gas chromatography mass spectrometry analysis is the computed match factor of the spectrum and the respective one in the existing library[33]. The identification of the compounds is generally done by computer searches in available libraries. In GC analysis, in some cases, unidentified compounds remain, because their spectra are not found in the respective libraries. In these cases, only the structural type of the compound is proposed, based on the fragmentation spectrum of the query compound.

Another method of propolis composition analysis is fourier transform infrared attenuated total reflectance (FTIR-ATR)[28]. The complexity of the propolis spectrum measured by FTIR, give its’ overall chemical composition, and the identification of every signal represents a demanding task. Trained specialists can distinguish different signals corresponding to particular organic compounds, based on the literature data of propolis composition and different spectral data of FTIR libraries. The mentioned study is among the few studies existing on propolis analysis.

Over the last decades, the old method of TLC has been improved, and coupled with high-performance liquid chromatography, for direct identification of the antioxidant compounds of poplar propolis and other natural matrices, using also antioxidant radical 2, 2-diphenyl-1-picrylhidrazyl (DPPH) [34][35]. The method is based on the separation of bioactive constituents from the polyphenolic class using high-performance thin layer chromatography, visualization of the compounds being made using DPPH as the derivatizing reagent. Overall, the most used analysis methods for chemical composition of propolis extracts remains liquid and gas chromatography.

1.2. Main Bioactive Properties of Propolis

Regarding the bioactive properties of propolis, there are many demonstrated activities such as antioxidant [36][37][38][39], anti-inflammatory[40], antibacterial[41][42][43][44], antifungal[45][46][47], anticancer[48][49][50][51], immunosuppressant[40], and antiviral activity[52][53][54][55][56][57]. Antioxidant activity of propolis extracts have been evaluated over time using different spectrophotometric methods in vitro. The simplest method used for antioxidant activity determination for different natural extracts, including plants and in our case propolis, is radical scavenging activity (RSA) using 2, 2-diphenyl-1-picrylhidrazyl (DPPH) assay. DPPH is a stable radical which reacts with bioactive compounds present in the extract and is expressed as a % of inhibition[58][59]. Combining HPTLC and DPPH, a new method has been developed that is simple and accurate, which facilitates explorative work by testing different natural matrices with complex chemical composition[35]. The method is regarded as a novel analytical quality control tool that can be applied to different complex natural matrices. Ferric reducing ability power (FRAP) assay is based on the redox reaction between the bioactive compounds contained in the extract and the Fe3+-TPTZ complex (FRAP reagent) and is expressed as the potential of the antioxidants to reduce Fe3+ to Fe2+, which is spectrophotometrically measured at 593 nm[60].

Miguel et al.[37] demonstrated that there were no statistical difference between the antioxidant activities of brown propolis harvested in different seasons of the year. According to their results, the ABTS (2, 2’-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) value was between 0.019 mg/mL in spring collected propolis and 0.020 mg/mL in those harvested during the winter period. The DPPH values ranged between 0.027 mg/mL and 0.031 mg/mL, respectively.

A more recent study by Seibert et al., 2019[39] reported that the concentration required to obtain a 50% antioxidant effect of propolis (EC50) using the DPPH method was 25.04 for ethanolic extracts and 3.14% when the ABTS method was applied. For hexanic extracts and etyl acetate extracts, with both methods, the values were superior.

Svečnjak et al. (2020)[28] analyzed seven raw propolis coming from the Croatian Islands and stated that the highest activity was observed for the samples of Populus spp. origin. The antioxidant potential of these samples, determined by DPPH ranging from 2.6 to 81.6 mg GAE/g and by FRAP assay values ranging from 0.1 to 0.8 mmol Fe2+/g were registered.

Generally, in propolis research observations, the antimicrobial activity of the extracts has been higher in Gram-positive as compared with Gram-negative bacteria, where limited effects have been observed [61][62][63]. Gram-negative bacteria have a species-specific structure of the outer membrane and produce a hydrolytic enzyme which breaks down the active ingredients of propolis[64]. The antibacterial activity of propolis is due to its bioactive compounds (aromatic compounds and polyphenols). Interactions among different classes of chemical compounds have an important role, which has also been demonstrated against Paenibacillus larvae (a honeybee pathogen) [65]. Flavone/flavonols and flavanone/dihydroflavonols are the two main classes of phenolics in propolis. The mentioned study developed a statistical model to detect a potential interaction between the two classes of flavonoids and the inhibition activity of different propolis extracts (10 mg/mL) originating in different geographical origins from Romania on Paenibacillus larvae. The inhibitory effect of different propolis extracts was statistically significant. The content of these compounds influences the strength of antibacterial effects, and the significant interaction effect between flavonoids should also be taken into consideration. How does propolis acts as bactericidal agent? It has a direct action on the microorganism and another indirect activity by stimulating the immune system of the bees for activating natural defense of the organism against different bacterial diseases. The process stops the division of bacterial cells, destroying the cell wall and bacterial cytoplasm, and thus stopping the bacterial protein synthesis, as described in different scientific studies[66][67][68][69].

A comprehensive review was published recently [70] that characterized the latest studies on the antibacterial activity of propolis on Gram-positive (Staphylococcus aureus, S. epidermidis, Streptococcus mutans, S. viridians, S. pyogenes, S. pneumoniae, S. oralis, S. agalactiae, S. sobrinus, Enterococcus spp. Micrococcus luteus, Bacillus subtilis, and Clostridium dificile) and Gram-negative bacteria (Escherichia coli, Salmonella spp., Klebsiella spp., Yersinia enterocolitica, Proteus mirabilis, Shigella flexneri, Enterobacter cloacae, Enterobacter aerogenes, Pseudomonas aeruginosa, Acinetobacter baumannii, Haemophilus influenza, Campylobacter jejuni, Bacteroides fragilis, and Burkholderia cepacia). Propolis antibacterial activity was most often tested on E. coli, S. aureus, Salmonella spp, and P. aeruginosa[70]. More than 600 bacterial strains were tested, according to literature studies, and the efficacy of propolis on Gram-positive over Gram-negative bacteria was confirmed, the first class presenting lower minimum inhibitory concentrations (MIC) over the second class[70].

Cancer is one of the most severe and often deadly diseases in our times. Treatment methods include surgery, but also chemotherapy, radiotherapy, or immunotherapy according to individual characteristics of the patient. Chemotherapy and radiotherapy have different toxic effects and, nowadays, different antioxidant substances are used as enhancers of the immune system and reduce the toxic effects on patients. Propolis is a very powerful antioxidant and its antiproliferative activity has been tested either in vitro on different cancer cells or in vivo on animal models, where reduction of the tumor was observed. In 2003, Orsolic and Basic[71] observed an anti-metastatic activity of a water-soluble propolis derivative upon a CBA mouse mammary carcinoma tumor. The propolis derivative reduced the metastases in mice lung and also changed several immunological parameters of mice. Other different malignant cells (ME45 malignant melanoma, HTC 116, Caco-2, DLD-1, HT-29 human colorectal carcinoma, A549 and H23 lung cancer cells, MCF-7 hormone dependent and MDA-MB-468 human breast cell lines, LN18, and U87 glioblastoma cell lines), were treated in vitro with propolis extracts and an antitumor activity was observed, dependent on the cell lines. At the same time, L-929 normal fibroblast cells were not affected by propolis at a concentration of 1 μg/mL [72]. A recently published study[73] used propolis and a new designed product (chitosan-coated nano-propolis NP) to reduce the side effects of cisplatin, a drug widely used in cancer treatment. The in vivo study used Wistar rats divided into seven groups with different treatment schemes. The experimental groups treated with propolis and NP ameliorated the cisplatin effect and protected liver and kidney tissue from the toxicity induced by the drug.

Another important property of propolis extracts is exerted in oral cavity diseases[61]. Dental caries can be caused by different bacteria (Streptococcus mutans, S. sobrinus, different Actinomyces, and Lactobacillus). Propolis extract have antimicrobial activity against L. fermentum isolated from cavities of patients diagnosed with dental caries[42]. A comprehensive review on the potential uses of propolis in oral health was published in 2010 by Parolia et al.[66]. Different beneficial properties of propolis were mentioned, which included dental surgical wound healing, new storage media following avulsion[74][75][76], pulp capping agent[77], as an intracanal irrigant [78], as a mouth rinse [75][79], for dentinal hypersensitivity [80][81], for treatment of perodontitis [82], for treatment of denture stomatitis[83], as an intra-canal medicament [84], an effect on recurrent aphthous stomatitis[85], and an effect on Candida albicans[86]. A conclusion of the review was that propolis can be used in all these pathologies, but cautions must be taken due to some allergic reactions in some patients. Propolis extracts can also be used in the composition of mouthwashes and toothpastes, to enhance the prevention of microbial infection and treatment of gums inflammation.

2. Plant Sources for Poplar-Type Propolis

2. Plant Sources for Poplar-Type Propolis

Propolis is a resinous mixture, made by the honeybees from substances collected from tree or other plant buds, plant exudates, or resins found in the stem, branches, or leaves of different plants. These materials are generally lipophilic, such as mucilage, gums, and resins [9]. The list presented in this monograph includes numerous plant sources for propolis in different parts of the world. Two different approaches are used to determine the plant origin of propolis, i.e., observations of bee behavior or the chemical analysis of propolis and also plant materials[29]. Definitively, the second approach is more appropriate and correct, because it is scientifically proven. In early 1980s (40 years ago), scientific papers were published to evidence the similarity of plant species and propolis in different geographical regions[87][88][89][90][91][92][93].

In temperate zones, exudates from buds of the Populus species are the main source of resins for bees. In Europe, North America, and even New Zealand and the continental part of Australia, it has been reported that Populus was the main plant sources[88][89][92][93][18], although other plant resins are reported as precursors of propolis in the temperate zones of Europe and North America, including pine (Pinus sp.), alder (Alnus glutinosa), horse chestnut (Aesculus hippocastanum), elm (Ulmus sp.), ash (Fraxinus sp.), oak (Quercus sp.), and beech (Fagus sp.) [94][89][95][96][2]. In northern parts of Russia, aspen and silver birch buds (Betula veruucosa) supply bees with resins for propolis production[97][98][26][99].

Poplars (Populus spp., Salicaceae) include about 100 species and a lot of hybrids. These plants are the fastest growing species with very deep root systems (up to 20 m) and five-year-old trees are capable of uptaking up to 200 L of water per day[100]. Poplar hybrids, growing up to 3 m per year, are free of competition with weeds, even during the beginning of plantation.

Birches (Betula L.) are an essential ecological component in northern temperate and boreal forests [101]. In Europe, two important trees occur naturally, i.e., silver birch (Betula pendula Roth) and downy birch (Betula pubescens Ehrh.). These trees differ regarding the morphology of their leaves, twigs, branches, bark, seeds, and catkin scales, as well as cell size and wood anatomy, and they can reach a height of 20–30 m[102].

Generally, the genus Salix is very diverse, representing over 300 species [103] growing in the form of trees, shrubs, or dwarf shrubs with procumbent stems. Among the flavonoids most characteristic for poplars are flavanones, especially pinocembrin and pinostrobin. These compounds have shown antioxidant and anti-inflammatory effects in many in vitro tests and may play an important role in the pharmacological activity of Populus[104][105] [106].

Furthermore, propolis has been used by humans as a traditional folk medicine to maintain good health since ancient times, due to many beneficial properties[107] including antioxidant, anti-inflammatory, immunomodulatory, antimicrobial, antitumor, anticancer, cardioprotective, neuroprotective, and many more[108].

Chemical determinations of propolis composition have led to the conclusion that more than one plant resin has been found in propolis[109][110][111][112] and the question raised has been if the bees show selectivity when collecting the resins in areas where multiple plant sources are found and what is the reason for this. Different studies have been published[113][114][115] that have shown that bees collect resins discriminately, due to proximity, availability, or even toxicity.

Differences in the chemical composition of poplar buds may be from different phenolic compounds such as terpenoids, flavonoid aglycones, and their chalcones, as well as phenolic acids and their esters[116], and therefore it is important to control the quality of plant material in terms of qualitative and quantitative profiles. A study conducted by de Marco et al. (2017)[117] compared the bioactive compounds of poplar buds and Italian propolis. The authors quantified the total flavonoids, chrysin, galangin, pinocembrine, and caffeic acid phenethyl ester (CAPE) that were responsible for the antioxidant activity of these matrices. The results obtained were in the range of 1.40% and 24.18% for poplar buds freeze-dried extract and 1.52% to 28.78% for Italian propolis freeze-dried extract.

Therefore, plants are the main source of bioactive compounds of propolis and bees intervene only with different enzymes to finalize the chemical composition of propolis.

References

  1. Ristivojević, P.; Trifković, J.; Andrić, F.; Milojković-Opsenica, D. Poplar-type Propolis: Chemical Composition, Botanical Origin and Biological Activity. Nat. Prod. Commun. 2015, 10, 1869–1876, doi:10.1177/1934578x1501001117.
  2. Bankova, V.; Popova, M.; Trusheva, B. Plant Sources of Propolis: An Update from a Chemist’s Point of View. Nat. Prod. Commun. 2006, 1, 1023–1028, doi:10.1177/1934578x0600101118.
  3. De Groot, A.C.; Popova, M.P.; Bankova, V.S. An Update on the Constituents of Poplar-Type Propolis; Acdegroot Publishing: Wapserveen, The Netherlands, 2014; ISBN 978-90-813233-0-7.
  4. Fernández-Calderón, M.C.; Navarro-Pérez, M.L.; Blanco-Roca, M.T.; Gómez-Navia, C.; Pérez-Giraldo, C.; Vadillo-Rodríguez, V. Chemical Profile and Antibacterial Activity of a Novel Spanish Propolis with New Polyphenols also Found in Olive Oil and High Amounts of Flavonoids. Molecules 2020, 25, 3318, doi:10.3390/molecules25153318.
  5. Miguel, M.G. Chemical and biological properties of propolis from the western countries of the Mediteraneean basin and Portugal. Int. J. Pharm. Pharmaceut. Sci. 2013, 5, 403–409.
  6. Aliboni, A.; D’Andrea, A.; Massanisso, P. Propolis Specimens from Different Locations of Central Italy: Chemical Profiling and Gas Chromatography–Mass Spectrometry (GC−MS) Quantitative Analysis of the Allergenic Esters Benzyl Cinnamate and Benzyl Salicylate. J. Agric. Food Chem. 2011, 59, 282–288, doi:10.1021/jf1034866.
  7. Papotti, G.; Bertelli, D.; Bortolotti, L.; Plessi, M. Chemical and Functional Characterization of Italian Propolis Obtained by Different Harvesting Methods. J. Agric. Food Chem. 2012, 60, 2852–2862, doi:10.1021/jf205179d.
  8. Hegazi, A.G.; El-Hady, F.K.A.; Allah, F.A.M.A. Chemical Composition and Antimicrobial Activity of European Propolis. Z. Nat. C 2000, 55, 70–75, doi:10.1515/znc-2000-1-214.
  9. Boisard, S.; Shahali, Y.; Aumond, M.; Derbré, S.; Blanchard, P.; Dadar, M.; Le Ray, A.; Richomme, P. Anti‐AGE activity of poplar‐type propolis: Mechanism of action of main phenolic compounds. Int. J. Food Sci. Technol. 2019, 55, 453–460, doi:10.1111/ijfs.14284.
  10. Volpi, N.; Bergonzini, G. Analysis of flavonoids from propolis by on-line HPLC–electrospray mass spectrometry. J. Pharm. Biomed. Anal. 2006, 42, 354–361, doi:10.1016/j.jpba.2006.04.017.
  11. El‐Guendouz, S.; Lyoussi, B.; Miguel, M.G. Insight on Propolis from Mediterranean Countries: Chemical Composition, Biological Activities and Application Fields. Chem. Biodivers. 2019, 16, e1900094, doi:10.1002/cbdv.201900094.
  12. Falcão, S.I.; Vilas-Boas, M.; Estevinho, L.M.; Barros, C.; Domingues, M.D.R.; Cardoso, S.M. Phenolic characterization of Northeast Portuguese propolis: Usual and unusual compounds. Anal. Bioanal. Chem. 2009, 396, 887–897, doi:10.1007/s00216-009-3232-8.
  13. Marcucci, M.C. Propolis: Chemical composition, biological properties and therapeutic activity. Apidologie 1995, 26, 83–99, doi:10.1051/apido:19950202.
  14. Gardini, S.; Bertelli, D.; Marchetti, L.; Graziosi, R.; Pinetti, D.; Plessi, M.; Marcazzan, G.L. Chemical composition of Italian propolis of different ecoregional origin. J. Apic. Res. 2018, 57, 639–647, doi:10.1080/00218839.2018.1494911.
  15. Christov, R.; Trusheva, B.; Popova, M.; Bankova, V.; Bertrand, M. Chemical composition of propolis from Canada, its antiradical activity and plant origin. Nat. Prod. Res. 2006, 20, 531–536, doi:10.1080/14786410500056918.
  16. Popova, M.P.; Bankova, V.; Bogdanov, S.; Tsvetkova, I.; Naydenski, C.; Marcazzan, G.L.; Sabatini, A.-G. Chemical characteristics of poplar type propolis of different geographic origin. Apidologie 2007, 38, 306, doi:10.1051/apido:2007013.
  17. Toreti, V.C.; Sato, H.H.; Pastore, G.M.; Park, Y.K. Recent Progress of Propolis for Its Biological and Chemical Compositions and Its Botanical Origin. Evid. Based Complement. Altern. Med. 2013, 2013, 1–13, doi:10.1155/2013/697390.
  18. Huang, S.; Zhang, C.; Wang, K.; Li, G.Q.; Hu, F.-L. Recent Advances in the Chemical Composition of Propolis. Molecules 2014, 19, 19610–19632, doi:10.3390/molecules191219610.
  19. De Groot, A.C. Propolis. Dermatitis 2013, 24, 263–282, doi:10.1097/der.0000000000000011.
  20. Saleh, K.; Zhang, T.; Fearnley, J.; Watson, D.G. A Comparison of the Constituents of Propolis from Different Regions of the United Kingdom by Liquid Chromatography-High Resolution Mass Spectrometry using a Metabolomics Approach. Curr. Metab. 2015, 3, 42–53, doi:10.2174/2213235x03666150328000505.
  21. Park, Y.K.; Alencar, S.M.; Aguiar, C.L. Botanical Origin and Chemical Composition of Brazilian Propolis. J. Agric. Food Chem. 2002, 50, 2502–2506, doi:10.1021/jf011432b.
  22. Adelmann, J.; Passos, M.; Breyer, D.H.; Dos Santos, M.H.R.; Lenz, C.; Leite, N.F.; Lancas, F.M.; Fontana, J.D. Exotic flora dependence of an unusual Brazilian propolis: The pinocembrin biomarker by capillary techniques. J. Pharm. Biomed. Anal. 2007, 43, 174–178, doi:10.1016/j.jpba.2006.07.014.
  23. Isaeva, E.V.; Lozhkina, G.A.; Ryazanova, T.V. A study of the alcohol extract from balsam poplar buds. Russ. J. Bioorg. Chem. 2010, 36, 929–933, doi:10.1134/s1068162010070228.
  24. Bertrams, J.; Müller, M.B.; Kunz, N.; Kammerer, D.R.; Stintzing, F.C. Phenolic compounds as marker compounds for botanical origin determination of German propolis samples based on TLC and TLC-MS. J. Appl. Bot. Food Qual. 2013, 86, 143–153, doi:10.5073/JABFQ.2013.086.020.
  25. Pobłocka-Olech, L.; Migas, P.; Krauze-Baranowska, M. TLC determination of some flavanones in the buds of different genus Populus species and hybrids. Acta Pharm. 2018, 68, 199–210, doi:10.2478/acph-2018-0018.
  26. Popravko, S.A.; Sokolov, I.V.; Torgov, I.V. New natural phenolic triglycerides. Chem. Nat. Compd. 1982, 18, 153–157, doi:10.1007/bf00577181.
  27. Falcão, S.I.; Vale, N.; Gomes, P.; Domingues, M.R.M.; Freire, C.; Cardoso, S.M.; Vilas-Boas, M. Phenolic Profiling of Portuguese Propolis by LC-MS Spectrometry: Uncommon Propolis Rich in Flavonoid Glycosides. Phytochem. Anal. 2013, 24, 309–318, doi:10.1002/pca.2412.
  28. Svečnjak, L.; Marijanović, Z.; Okińczyc, P.; Kuś, P.M.; Jerković, I. Mediterranean Propolis from the Adriatic Sea Islands as a Source of Natural Antioxidants: Comprehensive Chemical Biodiversity Determined by GC-MS, FTIR-ATR, UHPLC-DAD-QqTOF-MS, DPPH and FRAP Assay. Antioxidants 2020, 9, 337, doi:10.3390/antiox9040337.
  29. Bankova, V.; De Castro, S.L.; Marcucci, M.C. Propolis: Recent advances in chemistry and plant origin. Apidologie 2000, 31, 3–15, doi:10.1051/apido:2000102.
  30. Isidorov, V.A.; Vinogorova, V.T. GC-MS Analysis of Compounds Extracted from Buds of Populus balsamifera and Populus nigra. Z. Nat. C 2003, 58, 355–360, doi:10.1515/znc-2003-5-612.
  31. Miguel, M.G.; Nunes, S.; Cruz, C.; Duarte, J.; Antunes, M.D.C.; Cavaco, A.M.; Mendes, M.D.D.S.; Lima, A.S.; Pedro, L.G.; Barroso, J.G.; et al. Propolis volatiles characterisation from acaricide-treated and -untreated beehives maintained at Algarve (Portugal). Nat. Prod. Res. 2013, 27, 743–749, doi:10.1080/14786419.2012.696261.
  32. Melliou, E.; Stratis, E.; Chinou, I. Volatile constituents of propolis from various regions of Greece—Antimicrobial activity. Food Chem. 2007, 103, 375–380, doi:10.1016/j.foodchem.2006.07.033.
  33. Kasiotis, K.M.; Anastasiadou, P.; Papadopoulos, A.; Machera, K. Revisiting Greek Propolis: Chromatographic Analysis and Antioxidant Activity Study. PLoS ONE 2017, 12, e0170077, doi:10.1371/journal.pone.0170077.
  34. Morlock, G.E.; Ristivojevic, P.; Chernetsova, E.S. Combined multivariate data analysis of high-performance thin-layer chromatography fingerprints and direct analysis in real time mass spectra for profiling of natural products like propolis. J. Chromatogr. A 2014, 1328, 104–112, doi:10.1016/j.chroma.2013.12.053.
  35. Islam, K.; Sostaric, T.; Lim, L.Y.; Hammer, K.; Locher, C. Development and validation of an HPTLC–DPPH assay and its application to the analysis of honey. J. Planar Chromatogr. Mod. TLC 2020, 33, 301–311, doi:10.1007/s00764-020-00033-0.
  36. Russo, A.; Cardile, V.; Sánchez, F.; Troncoso, N.; Vanella, A.; Garbarino, J. Chilean propolis: Antioxidant activity and antiproliferative action in human tumor cell lines. Life Sci. 2004, 76, 545–558, doi:10.1016/j.lfs.2004.07.019.
  37. Miguel, M.G.; Nunes, S.; Dandlen, S.A.; Cavaco, A.M.; Antunes, M.D. Phenols and antioxidant activity of hydro-alcoholic extracts of propolis from Algarve, South of Portugal. Food Chem. Toxicol. 2010, 48, 3418–3423, doi:10.1016/j.fct.2010.09.014.
  38. Torres, A.; Sandjo, L.; Friedemann, M.; Tomazzoli, M.; Maraschin, M.; Mello, C.; Dos Santos, A.R.S. Chemical characterization, antioxidant and antimicrobial activity of propolis obtained from Melipona quadrifasciata quadrifasciata and Tetragonisca angustula stingless bees. Braz. J. Med Biol. Res. 2018, 51, e7118, doi:10.1590/1414-431x20187118.
  39. Seibert, J.B.; Bautista-Silva, J.P.; Amparo, T.R.; Petit, A.; Pervier, P.; Almeida, J.C.D.S.; Azevedo, M.C.; Silveira, B.M.; Brandão, G.C.; De Souza, G.H.B.; et al. Development of propolis nanoemulsion with antioxidant and antimicrobial activity for use as a potential natural preservative. Food Chem. 2019, 287, 61–67, doi:10.1016/j.foodchem.2019.02.078.
  40. Araujo, M.A.R.; Libério, S.A.; Guerra, R.N.M.; Ribeiro, M.N.S.; Nascimento, F.R.F. Mechanisms of action underlying the anti-inflammatory and immunomodulatory effects of propolis: A brief review. Rev. Bras. Farm. 2012, 22, 208–219, doi:10.1590/s0102-695x2011005000167.
  41. Boyanova, L.; Kolarov, R.; Gergova, G.; Mitov, I. In vitro activity of Bulgarian propolis against 94 clinical isolates of anaerobic bacteria. Anaerobe 2006, 12, 173–177, doi:10.1016/j.anaerobe.2006.06.001.
  42. Koru, O.; Toksoy, F.; Acikel, C.H.; Tunca, Y.M.; Baysallar, M.; Guclu, A.U.; Akca, E.; Tuylu, A.O.; Sorkun, K.; Tanyuksel, M.; et al. In vitro antimicrobial activity of propolis samples from different geographical origins against certain oral pathogens. Anaerobe 2007, 13, 140–145, doi:10.1016/j.anaerobe.2007.02.001.
  43. Kharsany, K.; Viljoen, A.; Leonard, C.; Van Vuuren, S. The new buzz: Investigating the antimicrobial interactions between bioactive compounds found in South African propolis. J. Ethnopharmacol. 2019, 238, 111867, doi:10.1016/j.jep.2019.111867.
  44. Veloz, J.J.; Alvear, M.; Salazar, L.A. Antimicrobial and Antibiofilm Activity against Streptococcus mutans of Individual and Mixtures of the Main Polyphenolic Compounds Found in Chilean Propolis. BioMed Res. Int. 2019, 2019, 1–7, doi:10.1155/2019/7602343.
  45. Kujumgiev, A.; Tsvetkova, I.; Serkedjieva, Y.; Bankova, V.; Christov, R.; Popov, S. Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. J. Ethnopharmacol. 1999, 64, 235–240, doi:10.1016/s0378-8741(98)00131-7.
  46. Banskota, A.; Tezuka, Y.; Adnyana, I.K.; Ishii, E.; Midorikawa, K.; Matsushige, K.; Kadota, S. Hepatoprotective and anti-Helicobacter pylori activities of constituents from Brazilian propolis. Phytomedicine 2001, 8, 16–23, doi:10.1078/0944-7113-00004.
  47. Ota, C.; Unterkircher, C.; Fantinato, V.; Shimizu, M. Antifungal activity of propolis on different species of Candida. Mycoses 2001, 44, 375–378, doi:10.1046/j.1439-0507.2001.00671.x.
  48. Akao, Y.; Maruyama, H.; Matsumoto, K.; Ohguchi, K.; Nishizawa, K.; Sakamoto, T.; Araki, Y.; Mishima, S.; Nozawa, Y. Cell Growth Inhibitory Effect of Cinnamic Acid Derivatives from Propolis on Human Tumor Cell Lines. Biol. Pharm. Bull. 2003, 26, 1057–1059, doi:10.1248/bpb.26.1057.
  49. Valente, M.J.; Baltazar, A.F.; Henrique, R.; Estevinho, L.; Carvalho, M.; Estevinho, L.M. Biological activities of Portuguese propolis: Protection against free radical-induced erythrocyte damage and inhibition of human renal cancer cell growth in vitro. Food Chem. Toxicol. 2011, 49, 86–92, doi:10.1016/j.fct.2010.10.001.
  50. Da Cunha, M.G.; Franchin, M.; Galvão, L.; Ruiz, A.L.; Carvalho, J.E.; Ikegaki, M.; De Alencar, S.M.; Koo, H.; Rosalen, P. Antimicrobial and antiproliferative activities of stingless bee Melipona scutellaris geopropolis. BMC Complement. Altern. Med. 2013, 13, 23, doi:10.1186/1472-6882-13-23.
  51. Dos Santos, T.L.; Queiroz, R.F.; Sawaya, A.C.H.F.; Lopez, B.G.-C.; Soares, M.B.; Bezerra, D.P.; Rodrigues, A.C.B.; De Paula, V.F.; Waldschmidt, A.M. Melipona mondury produces a geopropolis with antioxidant, antibacterial and antiproliferative activities. Anais da Academia Brasileira de Ciências 2017, 89, 2247–2259, doi:10.1590/0001-3765201720160725.
  52. Schnitzler, P.; Neuner, A.; Nolkemper, S.; Zundel, C.; Nowack, H.; Sensch, K.H.; Reichling, J. Antiviral Activity and Mode of Action of Propolis Extracts and Selected Compounds. Phytother. Res. 2010, 24 (Suppl. 1), S20–S28, doi:10.1002/ptr.2868.
  53. Ma, X.; Guo, Z.; Shen, Z.; Wang, J.; Hu, Y.; Wang, D. The immune enhancement of propolis adjuvant on inactivated porcine parvovirus vaccine in guinea pig. Cell. Immunol. 2011, 270, 13–18, doi:10.1016/j.cellimm.2011.03.020.
  54. Shimizu, T.; Takeshita, Y.; Takamori, Y.; Kai, H.; Sawamura, R.; Yoshida, H.; Watanabe, W.; Tsutsumi, A.; Park, Y.K.; Yasukawa, K.; et al. Efficacy of Brazilian Propolis against Herpes Simplex Virus Type 1 Infection in Mice and Their Modes of Antiherpetic Efficacies. Evid. Based Complement. Altern. Med. 2011, 2011, 1–9, doi:10.1155/2011/976196.
  55. Fernandes, M.H.V.; Ferreira, L.D.N.; Vargas, G.D.; Fischer, G.; Hübner, S.D.O. Efeito do extrato aquoso de própolis marrom sobre a produção de ifn-γ após imunização contra parvovírus canino (cpv) e coronavírus canino (ccov). Ciên. Anim. Bras. 2015, 16, 235–242, doi:10.1590/1089-6891v16i223458.
  56. Hazem, A.; Pitică-Aldea, I.M.; Popescu, C.; Matei, L.; Dragu, D.; Economescu, M.; Alexiu, I.; Crişan, I.; Diaconu, C.C.; Bleotu, C.; et al. The antiviral/virucidal effects of alcoholic and aqueous extracts with propolis. Farmacia 2017, 65, 868–876.
  57. Braakhuis, A.J. Evidence on the Health Benefits of Supplemental Propolis. Nutrients 2019, 11, 2705, doi:10.3390/nu11112705.
  58. Mihai, C.M.; Mărghitaş, L.A. Antioxidant capacity of Transylvanian propolis. Bull. Anim. Sci. Biotechnol. 2010, 67, 266–270.
  59. Galeotti, F.; Maccari, F.; Fachini, A.; Volpi, N. Chemical Composition and Antioxidant Activity of Propolis Prepared in Different Forms and in Different Solvents Useful for Finished Products. Foods 2018, 7, 41, doi:10.3390/foods7030041.
  60. Cottica, S.M.; Sawaya, A.C.H.F.; Eberlin, M.N.; Franco, S.L.; Zeoula, L.M.; Visentainer, J.V. Antioxidant activity and composition of propolis obtained by different methods of extraction. J. Braz. Chem. Soc. 2011, 22, 929–935, doi:10.1590/s0103-50532011000500016.
  61. Wagh, V.D. Propolis: A Wonder Bees Product and Its Pharmacological Potentials. Adv. Pharmacol. Sci. 2013, 2013, 1–11, doi:10.1155/2013/308249.
  62. Martinotti, S.; Ranzato, E. Propolis: A new frontier for wound healing? Burn. Trauma 2015, 3, 1–7, doi:10.1186/s41038-015-0010-z.
  63. Dezmirean, D.S.; Mărghitaş, L.A.; Chirila, F.; Copaciu, F.; Simonca, V.; Bobiş, O.; Erler, S. Influence of geographic origin, plant source and polyphenolic substances on antimicrobial properties of propolis against human and honey bee pathogens. J. Apic. Res. 2017, 56, 588–597, doi:10.1080/00218839.2017.1356205.
  64. Sforcin, J.M. Biological Properties and Therapeutic Applications of Propolis. Phytother. Res. 2016, 30, 894–905, doi:10.1002/ptr.5605.
  65. Mihai, C.M.; Mărghitaş, L.A.; Dezmirean, D.S.; Chirilă, F.; Moritz, R.F.; Schlüns, H. Interactions among flavonoids of propolis affect antibacterial activity against the honeybee pathogen Paenibacillus larvae. J. Invertebr. Pathol. 2012, 110, 68–72, doi:10.1016/j.jip.2012.02.009.
  66. Parolia, A.; Thomas, M.S.; Kundabala, M.; Mohan, M. Propolis and its potential used in oral health. Int. J. Med. Med. Sci. 2010, 2, 210–215.
  67. Sforcin, J.M.; Bankova, V. Propolis: Is there a potential for the development of new drugs? J. Ethnopharmacol. 2011, 133, 253–260, doi:10.1016/j.jep.2010.10.032.
  68. Machado, B.; Pulcino, T.; Silva, A.; Melo, D.; Silva, R.; Mendonca, I. Propolis as an alternative in prevention and control of dental cavity. J. Apither. 2016, 1, doi:10.5455/ja.20160726115117.
  69. Anjum, S.I.; Ullah, A.; Khan, K.A.; Attaullah, M.; Khan, H.; Ali, H.; Bashir, M.A.; Tahir, M.; Ansari, M.J.; Ghramh, H.A.; et al. Composition and functional properties of propolis (bee glue): A review. Saudi J. Biol. Sci. 2019, 26, 1695–1703, doi:10.1016/j.sjbs.2018.08.013.
  70. Przybyłek, I.; Karpiński, T.M. Antibacterial properties of propolis. Molecules 2019, 24, 2047, doi:10.3390/moleculas24112047.
  71. Orsolic, N.; Basic, I. Immunomodulatory by water-soluble derivative of propolis: A factor of antitumor reactivity. J. Ethnopharm. 2003, 84, 265–273, doi:10.1016/s0378-8741902000329-x.
  72. Popova, M.; Giannopoulou, E.; Skalicka‐Woźniak, K.; Graikou, K.; Widelski, J.; Bankova, V.; Kalofonos, H.P.; Sivolapenko, G.B.; Gaweł-Bęben, K.; Antosiewicz, B.; et al. Characterization and Biological Evaluation of Propolis from Poland. Molecules 2017, 22, 1159, doi:10.3390/molecules22071159.
  73. Seven, P.T.; Seven, I.; Karakus, S.; Mutlu, S.I.; Arkali, G.; Sahin, Y.M.; Kilislioglu, A. Turkish Propolis and Its Nano Form Can Ameliorate the Side Effects of Cisplatin, Which Is a Widely Used Drug in the Treatment of Cancer. Plants 2020, 9, 1075, doi:10.3390/plants9091075.
  74. Martin, M.P.; Pileggi, R. A quantitative analysis of Propolis: A promising new storage media following avulsion. Dent. Traumatol. 2004, 20, 85–89, doi:10.1111/j.1600-4469.2004.00233.x.
  75. Özan, F.; Sümer, Z.; Polat, Z.A.; Er, K.; Özan, U.; Değer, O. Effect of mouth rinse containing propolis on oral microorganisms and human gingival fibroblast. Eur. J. Dent. 2007, 11, 195–200.
  76. Sabir, A.; Tabbu, C.R.; Agustiono, P.; Sosroseno, W. Histological analysis of rat dental pulp tissue capped with propolis. J. Oral Sci. 2005, 47, 135–138, doi:10.2334/josnusd.47.135.
  77. Al-Qathami, H.; Al-Madi, E. Comparison of sodium hypochlorite, propolis and salineas root canal irrigants: A pilot study. Saudi Dent. J. 2003, 5, 100–102.
  78. Koo, H.; Cury, J.A.; Rosalen, P.L.; Ambrosano, G.M.; Ikegaki, M.; Park, Y.K. Effect of a Mouthrinse Containing Selected Propolis on 3-Day Dental Plaque Accumulation and Polysaccharide Formation. Caries Res. 2002, 36, 445–448, doi:10.1159/000066535.
  79. Mahmoud, A.S.; Almas, K.; Dahlan, A.A. The effect of propolis on dentinal hypersensitivity and level of satisfaction among patients from a university hospital Riyadh, Saudi Arabia. Indian J. Dent. Res. 2000, 10, 130–137.
  80. Almas, K.; Mahmoud, A.; Dahlan, A. A comparative study of propolis and saline application on human dentin. A SEM study. Indian J. Dent. Res. 2001, 12, 21–27.
  81. Toker, H.; Ozan, F.; Ozer, H.; Ozdemir, H.; Eren, K.; Yeler, H. A Morphometric and Histopathologic Evaluation of the Effects of Propolis on Alveolar Bone Loss in Experimental Periodontitis in Rats. J. Periodontol. 2008, 79, 1089–1094, doi:10.1902/jop.2008.070462.
  82. Santos, V.R.; Gomes, R.T.; De Mesquita, R.A.; De Moura, M.D.G.; França, E.C.; De Aguiar, E.G.; Naves, M.D.; Abreu, J.A.S.; Abreu, S.R.L. Efficacy of Brazilian propolis gel for the management of denture stomatitis: A pilot study. Phytother. Res. 2008, 22, 1544–1547, doi:10.1002/ptr.2541.
  83. Oncag, O.; Cogulu, D.; Uzel, A.; Sorkun, K. Efficacy of propolis as an intracanal medicament against Enterococcus faecalis. Gen. Dent. 2006, 54, 319–322.
  84. Samet, N.; Laurent, C.; Susarla, S.M.; Samet-Rubinsteen, N. The effect of bee propolis on recurrent aphthous stomatitis: A pilot study. Clin. Oral Investig. 2007, 11, 143–147, doi:10.1007/s00784-006-0090-z.
  85. Martins, R.S.; Péreira, E.S.J.; Lima, S.M.; Senna, M.I.B.; Mesquita, R.A.; Santos, V.R. Effect of commercial ethanol propolis extract on the in vitro growth of Candida albicans collected from HIV-seropositive and HIV-seronegative Brazilian patients with oral candidiasis. J. Oral Sci. 2002, 44, 41–48, doi:10.2334/josnusd.44.41.
  86. Bachevski, D.; Damevska, K.; Simeonovski, V.; Dimova, M. Back to the basics: Propolis and COVID ‐19. Dermatol. Ther. 2020, 33, e13780, doi:10.1111/dth.13780.
  87. Popravko, S.A.; Kononenko, G.P.; Tikhomirova, V.I.; Vulfson, N.S. Secondary metabolites of birch. IV. Identification of group of flavonoid aglycones in silver birch buds (Betula verucosa). Bioorg. Chem. 1979, 5, 1662–1667.
  88. Tămaş, M.; Marinescu, I.; Ionescu, F. Flavonoidele din muguri de plop. Stud. Cercet. Biochim. 1979, 22, 207–213.
  89. Nagy, E.; Papay, V.; Litkei, G.; Dinya, Z. Investigation of the chemical constituents, particularly the flavonoid components, of propolis and Populi gemma by GC/MS method. Stud. Org. Chem. 1986, 23, 223–232.
  90. Greenaway, W.; Scaysbrook, T.; Whatley, F.R. The analysis of bud exudates of Populus x euramericana and of propolis, by gas chromatography-mass spectrometry. Proc. R. Soc. Lond. 1987, 232, 249–272.
  91. Bankova, V.; Dyulgerov, A.; Popov, S.; Evstatieva, L.; Kuleva, L.; Pureb, O.; Zamjansan, Z. Propolis produced in Bulgaria and Mongolia: Phenolic composition and plant origin. Apidologie 1992, 23, 79–85.
  92. Garciaviguera, C.; Ferreres, F.; Tomasbarberan, F.A. Study of Canadian Propolis by GC-MS and HPLC. Z. Nat. C 1993, 48, 731–735, doi:10.1515/znc-1993-9-1009.
  93. Markham, K.R.; Mitchell, K.A.; Wilkins, A.L.; Daldy, J.A.; Lu, Y. HPLC and GC-MS identification of the major organic constituents in New Zeland propolis. Phytochemistry 1996, 42, 205–211, doi:10.1016/0031-9422(96)83286-9.
  94. Simone-Finstrom, M.D.; Spivak, M. Propolis and bee health: The natural history and significance of resin use by honey bees. Apidologie 2010, 41, 295–311, doi:10.1051/apido/2010016.
  95. Greenaway, W.; Scaysbrook, T.; Whatley, F.R. Composition of Propolis in Oxfordshire, U.K. and its Relation to Poplar Bud Exudate. Z. Nat. C 1988, 43, 301–304, doi:10.1515/znc-1988-3-423.
  96. Taber, S. Bees and Beekeeping. Bull. Èntomol. Soc. Am. 1976, 22, 30, doi:10.1093/besa/22.1.30.
  97. Popravko, S.A. Chemical Composition of Propolis, its Origin and Standardization. In A Remarcable Hive Product: PROPOLIS; Harnaj, V., Ed.; Apimondia Publishing House: Bucharest, Romania, 1978; pp. 15–18.
  98. Popravko, S.A.; Kononenko, G.P.; Tikhomirova, V.I.; Vulfson, N.S. Secondary metabolites of birch. IV. Identification of group of flavonoid aglycones in silver birch buds (Betula verucosa). Bioorg. Chem. 1979, 5, 1662–1667
  99. Popravko, S.A.; Tikhomirova, V.I.; Vulfson, N.S. Comparative Study of the Chemical Composition and Biological Activity of Propolis and Its Sources. In Propolis; Apimondia Pub. Housem: Bucharest, Romania, 1985; pp. 35–37.
  100. Gawroński, S.W.; Greger, M.; Gawrońska, H. Plant Taxonomy and Metal Phytoremediation. Soil Biol. 2011, 30, 91–109, doi:10.1007/978-3-642-21408-0_5.
  101. Fischer, A.; Lindner, M.; Abs, C.; Lasch, P. Vegetation dynamics in central european forest ecosystems (near-natural as well as managed) after storm events. Folia Geobot. Phytotaxon. 2002, 37, 17–32, doi:10.1007/bf02803188.
  102. Hynynen, J.; Niemisto, P.; Vihera-Aarnio, A.; Brunner, A.; Hein, S.; Velling, P. Silviculture of birch (Betula pendula Roth and Betula pubescens Ehrh.) in northern Europe. Forestry 2010, 83, 103–119, doi:10.1093/forestry/cpp035.
  103. Smart, L.B.; Cameron, K.D. Genetic Improvement of Willow (Salix spp.) as a Dedicated Bioenergy Crop. In Genetic Improvement of Bioenergy Crops; Springer: Berlin/Heidelberg, Germany, 2008.
  104. Rasul, A.; Millimouno, F.M.; Eltayb, W.A.; Ali, M.; Li, J.; Li, X. Pinocembrin: A Novel Natural Compound with Versatile Pharmacological and Biological Activities. BioMed Res. Int. 2013, 2013, 1–9, doi:10.1155/2013/379850.
  105. Patel, N.K.; Jaiswal, G.; Bhutani, K.K. A review on biological sources, chemistry and pharmacological activities of pinostrobin. Nat. Prod. Res. 2016, 30, 2017–2027, doi:10.1080/14786419.2015.1107556.
  106. Pobłocka-Olech, L.; Inkielewicz-Stepniak, I.; Krauze-Baranowska, M. Anti-inflammatory and antioxidative effects of the buds from different species of Populus in human gingival fibroblast cells: Role of bioflavanones. Phytomedicine 2019, 56, 1–9, doi:10.1016/j.phymed.2018.08.015.
  107. Daugsch, A.; Moraes, C.S.; Fort, P.; Park, Y.K. Brazilian Red Propolis—Chemical Composition and Botanical Origin. Evid. Based Complement. Altern. Med. 2008, 5, 435–441, doi:10.1093/ecam/nem057.
  108. Farooqui, T. Beneficial effects of propolis on human health and neurological diseases. Front. Biosci. 2012, E4, 779, doi:10.2741/418.
  109. Bankova, V.; Popova, M.; Bogdanov, S.; Sabatini, A.-G. Chemical composition of European propolis: Expected and unexpected results. Z. Nat. C 2002, 57, 530–533, doi:10.1515/znc-2002-5-622.
  110. Popova, M.; Trusheva, B.; Khismatullin, R.; Gavrilova, N.; Legotkina, G.; Lyapunov, J.; Bankova, V. The Triple Botanical Origin of Russian Propolis from the Perm Region, Its Phenolic Content and Antimicrobial Activity. Nat. Prod. Commun. 2013, 8, 617–621, doi:10.1177/1934578x1300800519.
  111. Isidorov, V.A.; Szczepaniak, L.; Bakier, S. Rapid GC/MS determination of botanical precursors of Eurasian propolis. Food Chem. 2014, 142, 101–106, doi:10.1016/j.foodchem.2013.07.032.
  112. Isidorov, V.A.; Bagan, R.; Szczepaniak, L.; Swiecicka, I. Chemical profile and antimicrobial activity of extractable compounds of Betula litwinowii (Betulaceae) buds. Open Chem. 2015, 13, 125–137, doi:10.1515/chem-2015-0019.
  113. Leonhardt, S.D.; Blüthgen, N. A Sticky Affair: Resin Collection by Bornean Stingless Bees. Biotropica 2009, 41, 730–736, doi:10.1111/j.1744-7429.2009.00535.x.
  114. Wilson, M.B.; Spivak, M.; Hegeman, A.D.; Rendahl, A.; Cohen, J.D. Metabolomics Reveals the Origins of Antimicrobial Plant Resins Collected by Honey Bees. PLoS ONE 2013, 8, e77512, doi:10.1371/journal.pone.0077512.
  115. Wilson, M.B.; Brinkman, D.; Spivak, M.; Gardner, G.; Cohen, J.D. Regional variation in composition and antimicrobial activity of US propolis against Paenibacillus larvae and Ascosphaera apis. J. Invertebr. Pathol. 2015, 124, 44–50, doi:10.1016/j.jip.2014.10.005.
  116. Dudonné, S.; Poupard, P.; Coutière, P.; Woillez, M.; Richard, T.; Mérillon, J.-M.; Vitrac, X. Phenolic Composition and Antioxidant Properties of Poplar Bud (Populus nigra) Extract: Individual Antioxidant Contribution of Phenolics and Transcriptional Effect on Skin Aging. J. Agric. Food Chem. 2011, 59, 4527–4536, doi:10.1021/jf104791t.
  117. De Marco, S.; Piccioni, M.; Pagiotti, R.; Pietrella, D. Antibiofilm and Antioxidant Activity of Propolis and Bud Poplar Resins versusPseudomonas aeruginosa. Evid. Based Complement. Altern. Med. 2017, 2017, 1–11, doi:10.1155/2017/5163575.
More