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The review systematizes data about chemical composition of bark, leaves, inflorescences, and sprouts of different species of Salix L. The closest attention is payed to investigations of Salix, which has been recently carried out in our country and abroad. For every group of biologically active substances described in Salix there are data about suppressed types of pharmacological activity.

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Therapeutic value of medicinal plants is determined by biologically active substances (BAS) in their composition. At that, hundreds of BAS are simultaneously synthesized in every medicinal plant, which after entering human organism implement total pharmacological effect. Additional investigation of previously studied and long-term used medicinal plants sometimes allows revelation of new aspects of their biological activity. The purpose of this study is systematization of information about the composition of biologically active substances, revealed in the plants of Salix L. genus, which can serve as a prospective source for production of Russian medicinal drugs. The investigations for chemical composition of different species of Salix L. have started in xVIII century. History of application and chemical composition of some sorts of Salix are described in theses of studies for Salix alba and Salix acutifolia quite in details [1, 2]. In this paper, in order to avoid repetitions with above mentioned researches, we made a brief analytic review of presently known information about the chemical composition of some species of Salix, which have been lately carried out in our country and abroad. At present we know that phenolic glycosides, flavonoids, tannins as well as phenolic acids, ascorbic acid, amino acids, essential oils, and polysaccharides which can contribute in a total pharmacological effect, are the principal active substances of the studied species of Salix [3]. Quantitative composition of BAS in a bark and leaves is known to be changeable in different vegetation phases, and depends on growing conditions of the studied species of Salix [4, 5]. Ones of the principal representatives of biologically active substances of Salix family are phenolic glycosides with salicyl alcohol as an aglycone. The first phenolic glycoside, isolated from plants - salicin (salicoside), is a β-glycoside of salicyl alcohol. It was isolated from a willow bark by French scientist A. Leroux (1829). It is salicin which has principal types of Salix activity - anti-inflammatory, analgesic, and febrifuge actions [6]. Quantitative content of salicin in the studied Salix species varies rather broadly. This is connected not only with interspecies differences but with the quantitative determination method used at the first place. In our paper we will demonstrate data for the recent 10 years, obtained using contemporary method of high-performance liquid chromatography (HPLC), because currently this is the most widespread and rather convenient method to use. We have found that salycin content in Salix species widespread in the North Caucasus amounts to about 0.92% in a bark of Salix alba, about 0.2% in a bark of Salix triandra, about 0.81% in Salix purpurea bark [2]. In 2013 A.A. Petruk using HPLC method de- termined the content of salycin in leaves and inflorescences of some species of Salix genus, growing in Altay Krai and Novosibirsk Oblast. The content of salycin in leaves of the species under study amounted from 0.72% (S. albavar. vitellina) to 2.31% (S. alba (female)). The con- tent of salycin in inflorescences amounted from 1.31% (S. albavar. vitellina) to 1.78% (S. alba (female)) [7]. We should note, that European Pharmacopoeia considers only Salix species with at least 1.5% salycin (after alkaline hydro- lysis) to be pharmacopoeial [9]. Similar study was carried out on the example of bark of Salix acutifolia growing in Volga region. The general content of salicin after the alkaline hydrolysis fluctuated from 6.5 to 9.5% [8]. In 1926 another phenolic glycoside - salidroside - was isolated from the Salix bark, which had bifunctional properties, i.e. it is pronounced as an inhibitor or initiator of oxidation processes. The manifestation of one of the properties depends on concentration of salidroside in reaction environment, so if the concentration is low, salidroside will be an inhibitor of oxidation processes, at high concentrations it will be initiator [10]. The discovery of new analysis methods in xx century gave possibility to investigate BAS of different species of leading scientific centers of the world. With the help of chromatographic and spectral analysis methods the knowledge about glycoside composition of different Salix species was broadened. Foreign [11, 12] and Russian [13, 14, 15, 16] scientists discovered the representatives of these compounds group like salikortin, tremuloidin (tremulatsin) fragilin, grandidentatin, purpurein, salireposide, triandrin, vimalin and other compounds. Later triandrin and vimalin were included with phenilpropanoids group. Triandrin was established to have neurotropic activity, manifesting actoprotective, antihypnogenic, cerebroprotective action [17]. In 2014 a study for branches of S. glandulosa Seemen was carried out in Korea; 12 new phenolic glycosides out of 13 previously described glycosides were discovered. The rang of compounds showed signified inhibiting effect on the synthesis of nitrogen oxide in experimental model of microglia activation with liposaccharides [18]. The next important group of BAS, discovered in the Salix species under study was flavonoids. Chemical structure and pharmacological properties of these compound group has been under study since early xIx century, when in 1814 crystalline substance of quercetin was isolated from an oak bark. In 1864 rutin was isolated from Ruta graveolens, which was discovered later in some species of Salix. Interest in flavonoids rose significantly when in 1936 famous American scientists of Hungarian origin, Noble prize awardee A. Szent-Györgyi (1893-1986) discovered that flavonoids from a lemon bark have P-vitamin activity i.e. ability to lessen the permeability and capillary fragility [19]. The first investigations on the flavonoids determination in Salix date back to 1931-1933 when French phytochemists C.Charaux and J.Rabate discovered naringenin-5-glycoside in a bark of Salix purpurea [3]. At this point the range of flavonoids was identified in bark and leaves of different Salix species, and their chemical structure was established. Representatives of the classification subgroups of flavonoids are encountered in many species of Salix [3, 12, 14, 15, 16]. Luteolin is representative of flavones in Salix, which is encountered in S. purpurea, leaves of S.acutifolia, S.caprea, S.acutifolia, S.alba, S.triandra, S.vestita, S.berberifolia, S. myrtilloides, S.saxatilis, S.pyrolifolia [14, 20, 21]. One more representative of flavones is apigenin, discovered and quantitatively determined in leaves of S.saxatilis and S.recervigemmis [21]. Flavonoids, represented by quercetin, discovered in S.triandra (leaves and inflorescences) and leaves of S.acutifolia, S.alba, S.caprea, S.vestita, S.berberifolia, S.myrtilloides, S.nummularia, S. recervigemmis, S.krylovii, S.sphenophylla have more signified biligenic action [13, 14, 21] as well as rutin in leaves and inflorescences of S.triandra, Salixalba и Salix alba var. vitellina, and leaves of S.acutifolia и S. songarica Anderss [14, 16, 21]. Flavonoids are known to have biligenic action, which grows in the raw of flavones, chalcones, flavanones, flavanoles. G.V. Obolentseva established in her work an antiulcer action of flavonoids, which development mechanism is in some degree connected with anti-inflammatory and spasmolytic properties. The experiments showed that glycosides of flavonoles and chalcones were the most active [19]. Flavonoles representatives are described above, and the representative of chalcones in Salix family is isosalipurposide, flavonoid discovered in a bark of S. purpurea, S.elburensis, S. daphnoides, and S. acutifolia [1, 14]. Flavonoids were proved to be exogenous low-molecular antioxidants, which neutralize an action of active oxygen molecules. We established that plant tissues, as well as animals organisms flavonoids together with ascorbic acid participate in enzymatic processes of oxidation and repairing. Such fla- vones as diosemetin and its glycosides (capreoside and salicapreoside), discovered in Salix caprea, have venotonic activity and are applied in varicose veins, phlebitis, and hemorrhoid, and in gynecology [22]. Flavonoids have signified anti-allergic effect, which is conditioned by the damage of allergy mediators release. They restore functions of cell membranes with direct biochemical confunction, simultaneously suppressing phosphodiesterase activity, which promotes the accumulation of cAMP in a cell. At that the most efficient inhibitors of phosphodiesterase are flavones and flavonoles, which are parts of the above mentioned Salix species. Flavonoids, as specific inhibitors of phosphodiesterases are powerful nucleotide metabolism regulators and in this connection are of potential pharmacological interest [23, 24]. Recent investigations of flavonoids from different Salix species are worth a special attention. So, in 2012 V.B. Braslavskiy defended his thesis of Doctor of Pharmaceutical Sciences on Complex Pharmacognostic and Physical and Chemical Investigation of Flavonoids and Phenylpropanoids of Salicaceae Family. In this paper the author pays more attention to the study of representatives of Populus genus, and chemical composition of two Salix species was studied as well: S. viminalis L. and S. acutifolia Willd. As the result, using UV, NMR spectroscopy and mass spectrometria, as well as chemical transformation, 7 substances were identified. They belonged to flavonoids, 5 substances belonged to phenylpropanoids and 5 substances belonged to simple phenols. For the first time the following substances were isolated from a bark of S. acutifolia Willd.: naringenin, prunin, catechin, isosalipurpol, syringin, triandrin, sa- likortin, tremulatsin, acyl saligenin. As the re- sult of the pharmacological studies conducted, they showed that Salix genus plants with flavonoids and phenylpropanoids are prospective source of antimicrobial, anti-inflammatory, and adaptogenic medicinal drugs [25]. Besides, flavonoids prunin and cynaroside, isolated from S. S. acutifolia Willd. at dose 5 mg/kg showed diuretic and saluretic effects, which are based on the mechanisms of combined influence on glomerular filtration and canalicular ions transfer [26]. In 2012 A.A. Petruk, using HPLC method studied flavonoid composition of some species of Salix, which grow in Asian Russia. She discovered quercetin, kaempferol, apigenin, luteolin, and rutin, with dominance of quercetin and luteolin [20, 21, 27]. The investigations of flavonoids from some Salix species have been carried out in Belarus. In 2015 Belarus authors published the article about the study for dependence of content of flavonoids in Salix viminalis leaves on the size and position of a leaf on a sprout. The content of flavonoids in certain leaves hover from 1.2% to 11%, i.e. it is rather significant, while average values in leaves of one sprout change significantly less from 4.08% to 5.76%. The dependence of the flavonoids on the leaf position on a sprout is completely the opposite to the dependence described for a length and weight of a lead, it means that the smallest leaves accumulate maximum quantity of flavonoids [28]. The same authors determined the content of flavonoids in inflorescences, leaves, and bark of S. caprea. As the results of the study, a bark of S. caprea is recommended as prospective medicinal plant raw materials, which contain proanthocyanidins, providing anti-inflammatory and antioxidant action. Leaves and inflorescences, especially male, which accumulate significant quantity of flavone and flavonoles derivatives, can be the source for obtainment of medicinal drugs with cardiotonic and venotonic action [22]. Salix species also have tannins. A bark of some species may contain up to 20% of tannins [29]. Nature of tannins from different Salix species was studied; these were tannins of pyrogallic and pyrocatechin groups. Salix species with tannins of only pyrogallic group were determined: S.triandra, S.caprea, S.viminalis. Species like S.alba, S. рurpurea, S.pentandra, S. fragilis contatin tannins of pyrocatechin group [14]. The content of tannins in some Salix species may reach 20%, and bark of S.aurita L. had the highest quantity of tannins [29]. Some pharmacological properties of tannins are known. Astringent action is conditioned by the capability of tannins to connect with proteins, creating complexes, which conduces the wound and burn healing processes, diarrhea treatment. Antioxidant action is conditioned by the inhibition of active forms of oxygen. Anti-inflammation action of tannins was implemented with several mechanisms (inhibition of the production and accumulation of prostaglandins, inflammation markers, nitrogen oxide in microphages [30]. A.A. Petruk in her papers, published in 2009, studied tannins of some Salix species (Salicaceae), which grow in Asian Russia. The study for tannins content using permanganatometric method showed that leaves of S. phylicifolia have the bigger amount of tannins (7.1%), three Salix species had more than 5% of tannins: S. gracilistyla, S. pentandra, S.pyrolifolia [31]. The same author determined a seasonal dynamics of tannins accumulation on the example of Salix species, introduced in Central Siberian Botanic Garden. The leaves samples of all studied species the amount of tannins were higher than in inflorescences (in leaves from 3.3 to 7.1%, and from 0.8 to 1.2% in inflorescences). The higher amount of tannins in leaves was observed in the period of growth of laminas, or in period of their maximum size [27]. A.A. Petruk also carried out the study for a seasonal dynamics of flavonoid and tannin content in leaves and inflorescences of S. alba. It showed that leaves of the studied plants had the biggest amount of flavonoids and tannins, among them S. albavar. vitellina stood out by the amount of flavonoids - 4.60%, and S. alba × S. blanda by the content of tannins - 4.57%. Maximums of flavonoids and tannins content in inflorescences is observed in full bloom period, and in leaves it is observed in a period of their active growth, and at the end of vegetation period, before the leaf shedding. This time is considered by A.A. Petruk to be an optimal period for raw materials gathering. Digeneous inflorescences have the biggest amount of flavonoids and tannins comparing with male and female inflorescences. The results obtained made an author to prove the impossibility of an index of quantitative content of phenolic com- pounds mentioned, as chemotaxonomic marker for Salix genus, because of the broad spectrum of their changeability [20]. Some studied Salix species are also known to have phenolcarbonic acids, such as salicylic, chlorogenic, p-hydroxycinnamic, caffeic, and ferulic acids [4, 14, 32]. Free salicylic acid is encountered in S.laponum, S.purpurea, S.planifolia и S. аlba [33]. Salicylic acid and its derivatives are known as anti-inflammatory, febrifuge, and anesthetic agents [3, 6]. Many phenolcarbonic acids are efficiently neutralize free radicals implementing antioxidant action. The derivatives of hydroxycinnamic acids implement biligenic and anti-inflammatory effect, as well as fungistatic activity. Chlorogenic acid possesses a signified physiological activity and is a natural antioxidant. Chlorogenic acid is found in leaves of S. purpurea, S. elbursensis, S. triandra и S.аlba [4, 14, 32]. Ferulic acid implements anti-inflammatory, anti-allergic, anti- tumor, antitoxic, hepatoprotectory, antibacterial, anti-virus and other pharmacological effects [34]. It was discovered in S.alba, which grows in the North Caucasus [2, 14]. Caffeic and ferulic acids were revealed to have anti-hypoxic action, implement protective action for cardiacmuscle while modelling lethal tachyarrhythmia, increase lifetime of experimental animals, and significantly increase a level of cerebral blood flow with course application, without significant influence on the indexes of systematic hemodynamics. Caffeic acid and ferulic acid implement cardio-protective action [34, 35]. Caffeic acid is found in S. alba, S. еlbursensis и S.рurpurea, which grow in the North Caucasus [14]. The leaves of some Salix species growing in Finland are known to have chlorogenic and p-hydroxycinnamic acids [4, 32]. Some Salix species, for example S.caprea contain ascorbic acid. This compounds is a powerful antioxidant, and is also necessary for restoration of other antioxidants like tocopherols and carotinoids. Ascorbic acid conduces the formation of connective tissue in human’s organism, exhibits fermentative activity, conduces iron adsorption, and has an antisclerotic action [3]. Carbohydrates are natural compounds, widespread in vegetable kingdom. Polysaccharides possess a whole range of pharmacological properties; including a signified anti-inflammatory, wound healing, antioxidant action, activate functions of immune system [36]. German scientists were occupied with studies for polysaccharides in cortex of Salix alba. They isolated xylan and glucomannan from the hemicellulose of Salix alba cortex. Pectin substances of the Salix alba cortex consist of galacturonic acid, arabinose, and arabinogalactan. In Czechoslovakia scientists S. Karacsonyi and M.Pasteka were occupied with investigations for structural forms of neutral polysaccharides from the Salix alba. They determined the structure of glucomannan, which consisted of β-D-glycose and β-D-mannose [37]. Biologically active substances like essential oils, lipids, resinous substances, ferments were revealed in Salix [3]. Amino acid composition of leaves of S.acutifolia, S.caprea, S. alba was studied as well [38]. Chemical elements are known to be the most important catalyzers of various biochemical processes, metabolism, play a significant role in adaptation of organism in its normal and pathological state [39]. Elemental composition of Salix pentandra cortex was studied. As the result, important micro- and macro-elements like nitrogen, phosphorus, calcium, magnesium, sodium, potassium were discovered [40]. The date mentioned above concerns primarily the Cortex of different Salix species, rarely of leaves. At the same time, the whole range of researches has been carried out lately to prove the prospects of Salix sprouts use as medicinal plant raw materials. So, O.O. Khiteva (2012) studied chemical composition of Salix alba sprouts, and showed a rich BAS complex (high content of condensed tannins was established (epigallocatechin, catechin, epicatechin, epicatechingallate, catechingallate) in total from 3.5 to 9.0% in different periods of gathering; flavonoids (rutin, quercetin, and 2 unidentified substances) in total 0.5-1.5% in terms of rutin; phenolic acids (ferulic, salicylic, cinnamic) amounted to 0.8% in terms of ferulic acid; triterpene saponins (0.53%). The salicin content amounted to 0.05-0.19%)). Pharmacological investigations showed a signified antiexuda- tive and antiproliferative activity of Salix alba sprouts decoction, compared with acetylsalicylic acid [2]. Chemical composition and pharmacological activity of Salix purpurea [41] and Salix triandra sprouts were studied further [42, 43, 44]. The results of these studies also proved the prospects of Salix sprouts as plant raw materials with anti-inflammatory activity. Since 2013-2014 the investigations for Salix sprouts have been carried out in Ukraine. The comparative analysis of phenolic compounds of sprouts of S. caprea, S. purpurea, S. viminalis of Ukrainian flora was done. Rather high level of accumulation of fenolic nature biologically active substances was revealed using HPLC method. The sprouts of the species under study showed a high level of catechin, epicatechin, chlorogenic acid, some flavonoids. Sprouts of S.purpurea had especially high content of flavonoids; also some derivatives of naringenin were revealed, as well as luteolin-6-C-glycoside, isosalipurposide, luteolin-7-glycoside. This allowed authors to make conclusions about the prospects of further investigations of the sprouts of these Salix species [45]. Apart from this, amino acid composition of S.alba, S.triandra, S.viminalis, S.purpurea. S.fragilis was investigated. The sprouts were discovered to have more than 20 amino acids, 9 of which were essential. The results of the studies for amino acid composition give evidence about the prospects of implementation of studied Salix species [46, 47]. A group of Ukrainian authors published the results of elemental analysis of S.caprea sprouts. Potassium (1120), calcium (895), and silicium (450) were dominant macroelemens (mg/100g). And phosphorus (195), iron (56) and aluminum (28) were dominant microelements (mg/100g) [48]. The use of Salix sprouts is economically attractive, because it allows a significant broadening of raw material base. Besides, the harmful effect for a plant while raw materials gathering is getting less, in comparison with traditional raw materials (cortex) [49]. Big amount of Russian Salix species are worth noting, because of their belonging to dominating landscape types in high humidity areas, especially along the reservoirs banks and river valleys, and also their successful cultivation in industry. One of the distinguishing features of Salix genus is their capability to fast growth, substrate colonization, and reproduction [50]. All this conditions a theoretic possibility of a large scale gathering of Salix raw materials in our country to produce Russian medicinal drugs. Conclusions Currently we know that phenolic glycosides, flavonoids, tannins, and phenolic acids are principal active substances of the studied Salix species. Each of these compound groups exhibits its certain pharmacological effect. Rich chemical composition is characteristic not only for a cortex of Salix (traditionally used raw materials) but also for leaves, inflorescences, and sprouts. Recent years, active investigations for Salix sprouts have been carried out not only abroad, but in Russia and Ukraine as well. The use of these raw materials is economically attractive, because it allows significant broadening of raw materials base. And the harmful effect for a plant while gathering is less comparing with traditional raw materials (cortex). A great diversity of Salix species, which grow in Russia, and possibility of their industrial scale cultivation conduces the necessity for further comprehensive investigations for chemical composition and pharmacological activity of well-studied and understudied Salix species, which grow in different regions of Russia.

About the authors

O. O Frolova

Pyatigorsk Medical and Pharmaceutical Institute - branch of Volgograd State Medical University

Pyatigorsk, Russian Federation

E. V Kompantseva

Pyatigorsk Medical and Pharmaceutical Institute - branch of Volgograd State Medical University

Pyatigorsk, Russian Federation

T. M Dementieva

Far-Eastern State Medical University

Khabarovsk, Russian Federation


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