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Article

Analysis of Essential Oil of Salix babylonica Collected in Vietnam: Phytochemical Components and Antibacterial and Anticancer Activity

by
Phu Hiep Hoang
1,
Thien Hien Tran
2,* and
Van Khang Pham
3,*
1
Faculty of Biology, Thai Nguyen University of Education, Thai Nguyen City 250000, Vietnam
2
Institute of Applied Technology and Sustainable Development, Nguyen Tat Thanh University, Ho Chi Minh City 700000, Vietnam
3
Faculty of Chemistry, Thai Nguyen University of Education, Thai Nguyen City 250000, Vietnam
*
Authors to whom correspondence should be addressed.
Processes 2024, 12(1), 33; https://doi.org/10.3390/pr12010033
Submission received: 24 July 2023 / Revised: 6 October 2023 / Accepted: 9 October 2023 / Published: 22 December 2023
(This article belongs to the Topic New Trends on Separation and Extraction of Bioactive Compounds and Respective Applications)
Review Reports Versions Notes

Abstract

:
This study investigated the chemical compositions and inhibitory activities of essential oils (EOs) of Salix babylonica from Vietnam. The gas chromatography–mass spectrometry (GC/MS) system was used to analyze the chemical compositions of Salix babylonica essential oils. A total of twenty-eight and thirty-one compounds were identified in essential oils of the leaves and bark, among which many chemical compositions were identified for the first time in this plant. Salix babylonica essential oils demonstrated antibacterial activities against Gram-negative strains such as Pseudomonas aeruginosa (PA) and Escherichia coli and Gram-positive strains such as Staphylococcus aureus (SA), and demonstrated anti-cancer activities against three cancer cell lines (HepG2, MCF-7 cell, and A549). The evaluation of the ability to inhibit three strains of microorganisms and inhibit the growth of three cancer cell lines was first conducted using essential oils extracted from the plant species S. babylonica collected in Asia, which will be the basis for using essential oils of this plant in medicine.

1. Introduction

The Salix genus (Salicaceae family, Salix genus), commonly known as weeping willow, is a perennial shrub plant widely growth in Africa, Asia, Europe, and North America [1]. Salix plants are used as an ornamental plant and also as herbs in folk medicine for the treatment of thorn pain, gingivitis, antipyretic, delirium, blindness, loess, and hemoptysis [1]. Its flowers and fruits are used to treat overturning and radiation, and Salix plants are also used for rheumatism, neuralgia, deworming, as an antiseptic, and as an anthelmintic drug [1,2].
Many works have reported the biological and chemical compositions of Salix plants such as flavonoids, organic acids groups, phenolics groups and their derivatives, terpenes, sterols, lignans, and volatiles [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19]. Flavonoids of the Salix plant constitute typical chemical compositions such as flavones, flavan-3-ols, chalcones, dihydrochalcones, anthocyanins, and other derivatives [1,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20]. In the Salix babylonica (L.) plant, major flavonoids such as apigenin glycoside (apigenin-7-O-galactoside [15]) and chrysoeriol [20]; luteolin [20,21] and its glycosides such as luteolin-6-C-β-D-glucopyranoside (iso-orientin) [21], luteolin-4′-O-glucoside, luteolin-7-O-β-D-glucopyranoside [15], and kaempferol-7-O-glucoside [3]; and flavan-3-ols such as (epi)catechin gallate and (epi)gallocatechin gallate [19] have been reported. For phenolics and its derivatives of the Salix plant, more than 90 compounds have been reported. 4-(Hydroxymethyl)phenyl β-D-glucopyranoside [3], salicin [15], salidroside [8], tremuloidin [21], triandrin [18], trichocarpin, 2′-O-acetyltrichocarpin [15], and vimalin [8] of Salix babylonica (L.) were isolated as major chemical compositions, and this is also the main group of compounds found in plants of the genus Salix. The phenolic acids in Salix plants are either benzoic or cinnamic acid or hydroxycinnamic acid derivatives. Salix plants are rich resources of phenolic acids, among which S. purpurea L. and S. alba L. bark have been identified with the highest number of phenolic acids [22]. Terpenes, volatile terpenes, and lignans have been detected in many species of the Salix genus. S. cheilophila C. K. Schneid. twigs [23]; S. tetrasperma Roxb. leaves, bark, and flowers [2,24]; S. subserrata Willd. [25]; S. babylonica L. [3,26,27]; S. caprea L. [28]; S. egyptiaca L. [29]; and S. alba L. [30] have been found to contain more terpenes, volatile terpenes, and lignans. In Salix babylonica leaves collected in Egypt, depending on the comparisons of retention time or mass spectral data, Salem et al. [26] discovered 59 compounds in their sample. The main compositions were tritetracontane (an aliphatic hydrocarbon: 15.2%), 9-octadecenoic acid, 1,2,3-propanetriyl ester, (E,E,E, atrioleoylglycerol: 11.1%), hexadecanoic acid-methylester (a saturated fatty acid: 10.5%), 1,3-dioxane-4-(hexadecyloxy)-2-pentadecyl (a heterocyclic organic compound: 10.3%), phytol (3,7,11,15-tetramethy-2-hexadecen-1-ol: 9.7%), and aliphatic hydrocarbons such as nonadecane (1.2%) and hexatriacontane (0.8%) [26].
Total extracts and the isolated compounds of Salix species have been applied to treat headache, rheumatic diseases, menstrual cramps, and toothache in traditional medicine [31]. In recent research, extracts and the isolated compounds of Salix species confirmed many useful biological activities such as anticancer, anti-inflammatory, anti-microbial, anti-diabetic, anti-oxidant, neuroprotective, and hepatoprotective activities [27,28,29,30,31,32,33,34]. Antimicrobial activities of Salix plants have been observed as the most evident by limiting the activity of multidrug-resistant bacteria, which are high-risk species of bacteria, and these bacteria are used for research to provide a great opportunity for the treatment of disease and the discovery of new substances of natural resources that have the ability to inhibit bacteria, especially against multidrug-resistant bacteria [9,27,29,30,31,32,33,34,35]. The extracts of S. babylonica L. from leaves were experimented against bacterial strains by using twofold serial dilutions on Mueller–Hinton agar and using the Agar-gel diffusion method. The results showed that the average diameter of the inhibition zone was 13.38 ± 2.22 mm and the value of MIC50 was 70.4 ± 17.41 mg/mL against E. coli and Salmonella enterica, respectively [35]. The inhibitory activities of extract fractions from hydroalcoholic and subfractions of S. babylonica L. against two bacterial strains were determined by using the broth microdilution method to afford MIC values of Listeria monocytogenes and S. aureus of 0.78 mg/mL and 0.39 mg/mL, respectively [4]. In addition, through in vitro assay, Salix extracts were tested against cancer cell lines such as PC3 cells (prostate cancer cells), human acute lymphoblastic leukemia (ALL cells), Hep G2 cells (liver cancer cells), MCF7 (breast cancer cells), HCT116 (colorectal cancer cells), A549 (adenocarcinomic human alveolar basal epithelial cells), SW2 (small-cell lung cancer) cells, and H1299 (human lung cancer cell line) [34,36,37,38]. A fraction of Salix extracted by ether and chloroform was effective against AML cells (acute myeloid leukemia), while a fraction of extract from the young leaves of S. safsaf effectively reduced the tumor growth of cancer cell lines [37]. On other hand, the Salix plant also exhibited anti-HIV (human immunodeficiency virus) activity infection that causes acquired immunodeficiency syndrome (AIDS), which represents a major global health problem. In fact, chemical agents are usually used as an anti-retroviral therapeutic method for AIDS patients, but it has many side-effects and drug resistance for many of them. Recently, natural anti-retroviral factors have been discovered from natural resources to have the potential to replace synthetic drugs. Eftekhari et al. inspected the anti-retroviral effects of S. egyptiaca L. extract by using the cell proliferation kit II (XTT assay), which is a colorimetric assay for the nonradioactive quantification of cellular proliferation, viability, and cytotoxicity. As a result of that study and bioinformatics analyses, it was suggested that the S. egyptiaca L. had anti-HIV properties and could be a viable choice for AIDS patients [39]. Reactive oxygen species (ROS) have been identified as the cause of a few human infections, such as cardiovascular diseases, inflammation, viral infections, diabetes, and cancer [26,27,28,29,30,31,32,33,34]. The most important activities of Salix species such as good antioxidant activities were responsible for phenolic compounds. The extract of Salix and their antioxidant activities were mainly estimated through DPPH, FRAP, ABTS, the Folin–Ciocalteu method, total antioxidant capacity (TAC) assays, β-carotene bleaching, lipid peroxidation activities, linoleic acid anti-oxidation, alkyl radical scavenging assays, and superoxide anion radical scavenging [14,15,16,17,18,24,25,26,28]. A recent study showed that S. tetrasperma Roxb. extract exhibited antioxidant effects on neuropathic pain and its mechanism of action was useful in vitro and in vivo [24]. Furthermore, S. atrocinerea Brot., S. fragilis L., and S. viminalis L. displayed antioxidant activities from the polyphenolic compounds [40], and the extracts from S. subserrata Willd. leaf contained major compositions such as isorhamnetin-3-O-β-D-rutinoside, aromadendrin, gallocatechin, tremuloidin, triandrin, chrysoeriol-7-O-glucuronid, and salicin, also exhibiting antioxidant effects against the oxidative stress process in Caenorhabditis elegans [41]. In Vietnam, besides being used as an ornamental tree, the S. babylonica plant is also used in many traditional remedies such as healing painful tendon and bone injuries, treating internal anger, transferring heat pain to another location, or treating convulsions in limbs: boil and drink 40–60 g of Rhizophora leaves [42]; treating prince’s pimples and allergies to chewing gum: boil 100–150 g of young leaves and branches in water, drink, and wash; curing boils in the breast: use jade talisman—it will feel hot at first, continue to build up, become normal, and then go away [42]; curing tooth decay: use rubber tree branches [42]; treating diseases and coughing up blood: crush dried capers and take 4 g each time; treating children with saw-toothed orange: use the stamens of the Rhizome flower (do not cut into ash), grind it with a little musk or ice, and rub it on the roots of the teeth [42].
Currently, in Vietnam, there are no studies on the chemical components and biological activity of the EOs of this plant, so in this study, we determine the phytochemical components and antibacterial and anticancer activities of the EOs extracted from the S. babylonica collected in the mountainous area of Northern Vietnam.

2. Materials and Methods

2.1. Materials

Amounts of 20 kg of fresh leaves and 10 kg of fresh bark of S. babylonica were collected in May 2021 from each Bac Giang and Thai Nguyen province, Vietnam. The samples were authenticated by Dr. S.D. Thuong, Faculty of Biology, Thai Nguyen University of Education. All solvents and reagents used in this work were purchased from Merck & Co., Inc., Rahway, NJ, USA.

2.2. Extraction of Essential Oils through Steam Distillation Extraction

The extraction of essential oils in 5 kg of fresh samples was carried out via steam distillation method for 6 h. Essential oils (50 mL from leaves, 27 mL from barks), which were extracted using a separatory funnel, had a light-yellow color and strong scent, and were dried by Na2SO4. Essential oils were preserved in a glass vial at 4–5 °C prior to the following analysis.

2.3. GC/FID and GC/MS Analysis

GC/MS analysis was conducted using a Hewlett Packard 5890 Series II w/HP 5971 MSD GC/MS System coupled with a quadrupole MS system. The system was equipped with an electron impact source operating at 200 °C. A fused silica-capillary column with an apolar stationary phase HP5-MS (30 m × 0.25 mm, 0.25 µm film thickness) was used. The gas chromatographic (GC) conditions used helium (0.9 mL/min) as a carrier gas for the separation of compounds in essential oils and oven heating rates around 3 to 5 °C/min, and compounds were identified via a flame ionization detector (FID) (GC-FID) [27]. The electron impact spectra were recorded at an ion voltage of 70 eV, covering a scan range of 30–600 uma [27]. The identification of compounds was accomplished by comparing their retention indices (Ris) on an HP-5MS column and cross-referencing them with the data available in the NIST Chemistry WebBook (http://webbook.nist.gov/chemistry/ Accessed on 18–22 December 2022). Additionally, the mass spectra of the compounds were compared with those stored in the Wiley NBS75K.L and NIST/EPA/NIH mass spectral libraries for further confirmation.

2.4. Antibacterial Activity

Gram-negative strains included Pseudomonas aeruginosa (PA) and Escherichia coli, and Gram-positive strains included Staphylococcus aureus (SA), which were provided by Dr. Nguyen Thi Ngoc Lan (Dean of Faculty of Biology, Thai Nguyen University of Education). The antibacterial action of the essential oil was determined using the disc agar diffusion method [43], and the diameter of the inhibition zones around the wells was measured to evaluate the oil’s antibacterial effectiveness. Essential oils were diluted with DMSO solution at concentrations of 25 mg/mL, 50 mg/mL, and 100 mg/mL. The studied bacterial strains were cultured on nutrient medium supplemented with agar at 30 °C for 24 h. Microbial suspensions were diluted with sterile distilled water to a concentration of about 108 CFU/mL. An amount of 0.1 mL of the microorganism suspension was spread onto a plate with nutrient agar, 5 wells were made in the agar (diameter 6 mm), and then 50 µL of essential oils in DMSO was added to each well for 1 h at 4 °C. The bacteria were nurtured at 37 °C for 24 h. After nurture, the results were observed by measuring the diameter of inhibition zones in centimeters. The negative control was DMSO without test material. The positive control was ampicillin 50 mg/mL. The experiments were performed in triplicate.

2.5. Cytotoxicity Activities

The cytotoxicity of essential oils against HepG2 cells (human hepatocarcinoma), MCF-7 cells (human breast carcinoma), and A549 cells (adenocarcinomic human alveolar basal epithelial cells) was determined by using MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) assay at the Institute of Biotechnology, Vietnam Academy of Science and Technology. The MTT assay is a colorimetric assay and relies on the cellular reduction of tetrazolium salts to their formazan crystals. The MTT assay is one of main methods to measure cell metabolic activity, cell proliferation, and viability, and is the main standard for cytotoxicity testing in vitro [37].
The culture media for this experiment were DMEM (Dulbecco’s Modified Eagle Medium) with L-glutamine, sodium pyruvate, NaHCO3, penicillin/streptomycin, 10% FBS (Fetal Bovine Serum), and Trypsin-EDTA (0.05%). The detailed test steps were described by Khang et al. [44]. Optical density of plates was read on a microplate reader at a wavelength of 550 nm. IC50 values were calculated using the logarithm formula.

2.6. Statistical Analysis

All experiments were repeated three times, and data in this work were afforded from two-way ANOVA and are presented as mean ± standard deviation, with p-value < 0.05 being considered as a statistically significant difference.

3. Results and Discussions

S. babylonica essential oil obtained via steam distillation was a liquid, had a pale-yellow color, and was lighter than water. In this research, the chemical components of the EOs of S. babylonica collected in two provinces of Bac Giang and Thai Nguyen were determined and compared with each other. The results of the chemical composition, molecular formula, RI, and relative content of the S. babylonica essential oil of leaves and S. babylonica bark collected in two provinces are shown in Table 1 and Table 2.
There were 28 compounds (in leaves’ essential oils) and 31 compounds (in bark essential oils) that were determined in the S. babylonica essential oils collected from Bac Giang and Thai Nguyen provinces. Camphene (7.3%), 2-(4-methyl-3-cyclohexen-1-yl)-2-propanol (4.5%), 3,7-dimethyl-1,6-octadien-3-ol (5.4%), geranyl acetate (5.2%), α-humulene (14.5%), and pentacosane (32.2%) were the major chemical compositions in essential oils of S. babylonica leaves. Trans-carvone oxide (4.3%), thymol (4.5%), trans-caryophyllene (24.5%), α-humulene (30.2%), cadinol (5.5%), and farnesol (4.8%) were the major chemical compositions in essential oils of S. babylonica bark. These results demonstrated the affordance of conditional growth of the plants on the essential oils’ chemical composition.
From the above results, we found that some main chemical components were new components discovered for the first time in S. babylonica species collected in Vietnam: α-humulene (14.5, 30.2%), pentacosane (32.2%), trans-carvone oxide (4.3%), and trans-caryophyllene (24.5%). Pentacosane’s concentration in the bark was smaller than those of its leaves’ essential oils. These compositions have been proven to have many good biological activities and have been of good value as a starting material for the synthesis of other substances to serve in medicine. From the Vietnam samples, we found that the main components in oil samples were different from those of Mu et al.’ [27] and Salem et al.’s [26]. Salem et al. [26] utilized S. babylonica samples collected in Mexico and extracted using an organic solvent system such as methanol/acetone/n-hexane at a ratio of 1/1/1 (v/v/v), while our study extracted essential oils via the steam distillation method [16]. According to Mu et al.’s work [27], they experimented with S. babylonica samples collected in China and determined pentacosane’s derivatives, finding that salicylic acid derivatives are the major components in essential oils. Meanwhile, the research group of Zeid et al. [21] analyzed the composition of substances in essential oils extracted via steam distillation from S. babylonica samples collected in Egypt, and the results showed that many components were similar to samples collected in Vietnam, but the main composition of samples collected in Vietnam and Egypt was also different. For S. babylonica samples collected in Egypt, essential oils had α-pinene, β-cedrene, salicylaldehyde, Cis-4-hexen-1-ol, linalool, and 1,2-cyclohexanedione as the main components, while S. babylonica samples collected in Vietnam had camphene, 2-(4-methyl-3-cyclohexen-1-yl)-2-propanol, 3,7-dimethyl-1,6-octadien-3-ol, geranyl acetate, α-humulene, pentacosane, trans-carvone oxide, thymol, trans-caryophyllene, α-cadinol, and farnesol as the derivatives of the substances in the samples collected in Egypt as the main chemical components. This also demonstrates the influence of geological and growing conditions on the chemical components of the plant, especially the composition of substances contained in their essential oils. This is the basis to promote research on the chemical components of EOs to serve life.
In addition, the antibacterial action of the EOs of S. babylonica bark and leaves was determined using the disc agar diffusion method [14]. The results are given in Table 3.
From Table 3, the results indicate that both essential oils derived from the leaves and bark of S. babylonica exhibit antibacterial action against the tested bacteria. The inhibitory effects of the oils increase with higher concentrations of the samples. Furthermore, under the experimental conditions, the antibacterial activity of the S. babylonica EO surpasses that of antibiotics. The essential oils demonstrate stronger inhibitory activity against P. aeruginosa and S. aureus compared to E. coli. In conclusion, the essential oil from Thai Nguyen province exhibits a noticeably stronger antibacterial action than the EOs from Bac Giang province.
In the previous work, the cytotoxic activities of the Salix plant were mainly studied on ethanol and aqueous extracts, and essential oils [27,28,29,30,31,32,33,34,35,36,37,38]. The results showed that the aqueous extract of parts of the Salix plant had proliferative activity of all compounds in the rich flavonoids and proanthocyanidin fractions with 50% maximal growth inhibitory concentrations (GI(50)) between 33.3 and 103.3, and 50.0–243.0 microg/mL, respectively [36]. The extract from the leaves of Salix safsaf for action against human carcinoma cells in vitro, and in vivo in mice, decreased tumor growth [37] and reduced the majority of the blasts of acute myeloid leukemia after 24 h of incubation [38]. Herein, the inhibition activity of EOs of the bark and leaves of S. babylonica were experimented against MCF-7, A549, and HepG2 cancer cell lines. The conclusion is presented in Table 4.
Table 4 presents the test results of the EOs of S. babylonica samples, which displayed medium inhibitory activity against the three tested cancer cell lines with IC50 values ranging from 45.4 to 95.3 µg/mL. Ellipticine was the positive control in the experiment. In addition, the essential oils of leaves exhibited inhibitory activities compared to its bark.
The bioactivity of essential oils commonly causes breakdown of the key chemical constituents present in that essential oil [7,8,9,10,11]. In the samples of the S. babylonica plant, which was collected in Vietnam, compounds with relatively large amounts (>3%) were found such as camphene, 2-(4-methyl-3-cyclohexen-1-yl)-2-propanol, 3,7-dimethyl-1,6-octadiene-3-ol, geranyl acetate, α-humulene, pentacosane, trans-carvone oxide, thymol, trans-caryophyllene, α-cadinol, and farnesol derivatives. Pentacosane is an n-alkane, which was the main component obtained in the leaf samples of S. babylonica that we collected in Vietnam. Recently, Pentacosane was found as the major component in the acetone extract from Curcuma raktakanda and Malus domestica [45]. Pentacosane exhibits anti-cancer activities against C-6, A549 (lung carcinoma), Hep-G2, KB, CHOK1 (ovarian), and THP-1 (acute monocytic leukemia) cells [45,46]. A plant rich in n-alkane, Moringa oleifera (including pentacosane), collected in Mozambique and Taiwan containing pentacosane and phytol, has major compositions similar to its plant species, which we used in this study, and it showed good inhibitory activity against two Gram-positive strains (Bacillus cereus, Staphylococcus aureus), two Gram-negative strains (Escherichia coli, Pseudomonas aeruginosa), and five fungal strains (Penicillium aurantiogriseum, Penicillium expansum, Penicillium citrinum, Penicillium digitatum, and Aspergillus niger spp.) of bacteria [46]. Meanwhile, β-caryophyllene (BCP) is a natural compound, in the bicyclic sesquiterpene group, and is one of the major components of essential oils extracted from medicinal and food plants, typically in the following plant genera: Ocimum spp., Cinnamomum spp., Piper spp., Syzygium spp., Cannabis spp., Lavandula spp., Origanum spp., and Rosmarinus spp. Its biological effects include anti-inflammatory [47,48,49], anticarcinogenic [50], antimicrobial [50], antioxidative [5], and anticancer activities [51,52]. Thus, the above content is analyzed and compared with previous studies to show that S. babylonica essential oil from Vietnam contains valuable biologically active compounds, which is the basis for the use of this species. This plant is used to make medicine to improve quality of life.

4. Conclusions

In conclusion, we extracted essential oil and determined that S. babylonica essential oil from Vietnam has many new chemical components discovered for the first time in this plant. The results from this research indicate that both essential oils demonstrated antibacterial activity against the tested bacteria and anti-cancer activity against three cancer cell lines. The evaluation of the ability to inhibit three strains of microorganisms and to inhibit the growth of three cancer cell lines was first conducted with essential oils extracted from the plant species S. babylonica collected in Asia, which will be the basis for using essential oils of this plant in medicine.

Author Contributions

Conceptualization, P.H.H. and V.K.P.; methodology, P.H.H.; software, P.H.H.; writing—original draft preparation, P.H.H., T.H.T. and V.K.P.; supervision, V.K.P. and T.H.T. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data are contained within the article.

Acknowledgments

University of Thai Nguyen University of Education, Thai Nguyen, Vietnam (TNUE.2022.08).

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Tawfeek, N.; Mahmoud, M.F.; Hamdan, D.I.; Sobeh, M.; Farrag, N.; Wink, M.; El-Shazly, A.M. Phytochemistry, Pharmacology and Medicinal Uses of Plants of the Genus Salix: An Updated Review. Front. Pharmacol. 2021, 12, 593856. [Google Scholar] [CrossRef]
  2. El-Shazly, A.; El-Sayed, A.; Fikrey, E. Bioactive secondary metabolites from Salix tetrasperma Roxb. Z. Naturforschung C J. 2012, 67, 353–359. [Google Scholar] [CrossRef]
  3. Singh, H.; Raturi, R.; Badoni, P.P. Isolation of secondary metabolites from the roots of Salix babylonica. Mater. Sci. Eng. 2017, 225, 012094. [Google Scholar] [CrossRef]
  4. González-Alamilla, E.N.; Gonzalez-Cortazar, M.; Valladares-Carranza, B.; Rivas-Jacobo, M.A.; Herrera-Corredor, C.A.; Ojeda-Ramírez, D.; Zaragoza-Bastida, A.; Rivero-Perez, N. Chemical constituents of Salix babylonica L. and their antibacterial activity against Gram-positive and Gram- negative animal bacteria. Molecules 2019, 24, 2992. [Google Scholar] [CrossRef]
  5. Du, Q.; Jerz, G.; Shen, L.; Xiu, L.; Winterhalter, P. Isolation and structure determination of a lignan from the bark of Salix alba. Nat. Prod. Res. 2007, 21, 451–454. [Google Scholar] [CrossRef]
  6. Du, Q.; Jerz, G.; Winterhalter, P. Preparation of three flavonoids from the bark of Salix alba by high-speed countercurrent chromatographic separation. J. Liq. Chromatogr. Relat. Technol. 2004, 27, 3257–3264. [Google Scholar] [CrossRef]
  7. Balbaa, S.; Khafagy, S.; Haggag, M.; Sahsah, N. Phytochemical study of certain Salix species cultivated in Egypt. J. Pharmacol. Sci. 1979, 20, 153–164. [Google Scholar]
  8. Binns, W.W.; Blunden, G.; Woods, D.L. Distribution of leucoanthocyanidins, phenolic glycosides and imino-acids in leaves of Salix species. Phytochemistry 1968, 7, 1577–1581. [Google Scholar] [CrossRef]
  9. Fayaz, M.; Sivakumaar, P.K. Phytochemical Analysis and antimicrobial activity of Salix alba against dental biofilm forming bacteria. Int. J. Pharm. Biol. Sci. Arch. 2014, 5, 137–140. [Google Scholar] [CrossRef]
  10. Fernandes, C.C.; Cursino, L.M.D.C.; Novaes, J.D.A.P.; Demetrio, C.A.; Pereira Júnior, O.L.; Nunez, C.V.; Amaral, I.L.D. Salicylates isolated from leaves and stems of Salix martiana Leyb. (Salicaceae). Química Nova 2009, 32, 983–986. [Google Scholar] [CrossRef]
  11. Freischmidt, A.; Jürgenliemk, G.; Kraus, B.; Okpanyi, S.; Müller, J.; Kelber, O. Phenolic compounds in the ethyl acetate fraction of a standardized willow bark extract. Planta Medica 2010, 76, P283. [Google Scholar] [CrossRef]
  12. Gasecka, M.; Mleczek, M.; Jutrzenka, A.; Golinski, P.; Stuper-Szablewska, K. Phenolic compounds in leaves of Salix species and hybrids growing under different soil conditions. Chem. Ecol. 2017, 33, 196–212. [Google Scholar] [CrossRef]
  13. Han, L.K.; Sumiyoshi, M.; Zhang, J.; Liu, M.X.; Zhang, X.F.; Zheng, Y.N. Anti-obesity action of Salix matsudana leaves (Part 1). Anti-obesity action by polyphenols of Salix matsudana in high fat-diet treated rodent animals. Phytother. Res. 2003, 17, 1188–1194. [Google Scholar] [CrossRef]
  14. Han, L.K.; Sumiyoshi, M.; Zheng, Y.N.; Okuda, H.; Kimura, Y. Antiobesity action of Salix matsudana leaves (Part 2). Isolation of anti-obesity effectors from polyphenol fractions of Salix matsudana. Phytother. Res. 2003, 17, 1195–1198. [Google Scholar] [CrossRef]
  15. Khatoon, F.; Khabiruddin, M.; Ansari, W. Phenolic glycosides from Salix babylonica. Phytochemistry 1988, 27, 3010–3011. [Google Scholar] [CrossRef]
  16. Kim, C.S.; Kwon, O.W.; Kim, S.Y.; Choi, S.U.; Kim, J.Y.; Han, J.Y. Phenolic glycosides from the twigs of Salix glandulosa. J. Nat. Prod. 2014, 77, 1955–1961. [Google Scholar] [CrossRef]
  17. Kim, C.S.; Subedi, L.; Park, K.J.; Kim, S.Y.; Choi, S.U.; Kim, K.H. Salicin derivatives from Salix glandulosa and their biological activities. Fitoterapia 2015, 106, 147–152. [Google Scholar] [CrossRef]
  18. Kompantsev, V.; Gaidash, P.; Dauksha, A. Phenolic compounds of the bark of Salix alba× babylonica. Chem. Nat. Compd. 1974, 10, 839. [Google Scholar] [CrossRef]
  19. Kompantsev, V.; Shinkarenko, A. Phenolic glycosides of the roots of Salix pentandroides. Chem. Nat. Compd. 1973, 9, 127. [Google Scholar] [CrossRef]
  20. Liu, K.Y.; Liu, H.J.; Zhou, B.; Han, L.K. Studies on chemical constituents from Salix babylonica L. and their stimulating lipolysis activity. J. Fudan Univ. 2018, 4, 022. [Google Scholar]
  21. Zeid, A.; Hifnawy, M.; Saleh, M.; Sleem, A.; Mohamed, R. Phenolics, volatiles and biological activities of Salix babylonica L. leaves and stem bark. Planta Medica 2006, 72, 335. [Google Scholar] [CrossRef]
  22. Agnolet, S.; Wiese, S.; Verpoorte, R.; Staerk, D. Comprehensive analysis of commercial willow bark extracts by new technology platform: Combined use of metabolomics, high-performance liquid chromatography–solid-phase extraction–nuclear magnetic resonance spectroscopy and high-resolution radical scavenging assay. J. Chromatogr. A 2012, 1262, 130–137. [Google Scholar] [CrossRef]
  23. Shen, T.; Tian, Y.Q.; Liu, W.X.; Zheng, S.Z. Acyclic diterpene-γ-lactones and flavonoid from Salix cheilophila Omitted. J. Chin. Chem. Soc. 2008, 55, 401–405. [Google Scholar] [CrossRef]
  24. Sobeh, M.; Mahmoud, M.F.; Rezq, S.; Alsemeh, A.E.; Sabry, O.M.; Mostafa, I. Salix tetrasperma roxb. Extract alleviates neuropathic pain in rats via modulation of the NF-κB/TNF-α/NOX/iNOS pathway. Antioxidants 2018, 8, 482. [Google Scholar] [CrossRef]
  25. Hussain, H.; Badawy, A.; Elshazly, A.; Elsayed, A.; Krohn, K.; Riaz, M. Chemical constituents and antimicrobial activity of Salix subserrata. Rec. Nat. Prod. 2011, 5, 133–137. [Google Scholar]
  26. Salem, A.; Salem, M.; Gonzalez-Ronquillo, M.; Camacho, L.; Cipriano, M. Major chemical constituents of Leucaena leucocephala and Salix babylonica leaf extracts. J. Trop. Agric. 2011, 49, 95–98. [Google Scholar]
  27. Mu, D.; Liu, Z.; Tao, Y.; Zhou, L.; Wang, J.; Xu, W.; Luo, G. Analysis of volatile compounds of Salix babylonica by GC-MS. J. Chin. Med. Mater. 2014, 37, 1001–1005. [Google Scholar]
  28. Ahmed, A.; Akbar, S.; Shah, W.A. Chemical composition and pharmacological potential of aromatic water from Salix caprea inflorescence. Chin. J. Integr. Med. 2017. ahead of print. [Google Scholar] [CrossRef]
  29. Karimi, I.; Hayatgheybi, H.; Kamalak, A.; Pooyanmehr, M.; Marandi, Y. Chemical composition and effect of an essential oil of Salix aegyptiaca L., Salicaceae, (musk willow) in hypercholesterolemic rabbit model. Rev. Bras. Farmacogn. 2011, 21, 407–414. [Google Scholar] [CrossRef]
  30. Zarger, M.S.S.; Khatoon, F.; Akhtar, N. Phytochemical investigation and growth inhibiting effects of Salix alba leaves against some pathogenic fungal isolates. World J. Pharmacol. 2014, 3, 1320–1330. [Google Scholar]
  31. Highfield, E.S.; Kemper, K.J. Long Wood Herbal Task Force White Willow Bark (Salix alba). Available online: https://www.yumpu.com/en/document/read/51822299/white-willow-bark-salix-alba-longwood-herbal-task-forcet (accessed on 13 July 1999).
  32. Mahdi, J.G. Medicinal potential of willow: A chemical perspective of aspirin discovery. J. Saudi Chem. Soc. 2010, 14, 317–322. [Google Scholar] [CrossRef]
  33. Van Wyk, B.E.; Wink, M. Medicinal Plants of the World; CABI: Pretoria, South Africa, 2014; p. 648. [Google Scholar]
  34. Tuberoso, C.I.; Jerkovic, I.; Bifulco, E.; Marijanovi, Z. Biodiversity of Salix spp. honeydew and nectar honeys determined by RP-HPLC and evaluation of their antioxidant capacity. Chem. Biodivers. 2011, 8, 872–879. [Google Scholar] [CrossRef]
  35. Popova, T.P.; Kaleva, M.D. Antimicrobial effect in vitro of aqueous extracts of leaves and branches of willow (Salix babylonica L). Int. J. Curr. Microbiol. Appl. Sci. 2015, 4, 146–152. [Google Scholar]
  36. Hostanska, K.; Jürgenliemk, G.; Abel, G.; Nahrstedt, A.; Saller, R. Willow bark extract (BNO1455) and its fractions suppress growth and induce apoptosis in human colon and lung cancer cells. Cancer Detect. Prev. 2007, 31, 129–139. [Google Scholar] [CrossRef] [PubMed]
  37. El-Shemy, H.A.; Aboul-Enein, A.M.; Aboul-Enein, K.M.; Fujita, K. Willow leaves’ extracts contain anti-tumor agents effective against three cell types. PLoS ONE 2007, 2, e178. [Google Scholar] [CrossRef]
  38. El-Shemy, H.A.; Aboul-Enein, A.M.; Aboul-Enein, M.I.; Issa, S.I.; Fujita, K. The effect of willow leaf extracts on human leukemic cells in vitro. J. Biochem. Mol. Biol. 2003, 36, 387–389. [Google Scholar] [CrossRef] [PubMed]
  39. Eftekhari, Y.; Rustaiyan, A.; Monajjemi, M.; Khavari-nejad, R.A. (Study of anti-retroviral effects of Salix aegyptiaca L. herbal extract on HIV-1 in-vitro. Int. J. Mol. Clin. Microbiol. 2014, 1, 398–405. [Google Scholar]
  40. Ramos, P.A.B.; Moreirinha, C.; Silva, S.; Costa, E.M.; Veiga, M.; Coscueta, E.; Santos, S.A.O.; Almeida, A.; Pintado, M.M.; Freire, C.S.R.; et al. The Health-Promoting Potential of Salix spp. Bark Polar Extracts: Key Insights on Phenolic Composition and In Vitro Bioactivity and Biocompatibility. Antioxidants 2019, 8, 609. [Google Scholar] [CrossRef] [PubMed]
  41. Tawfeek, N.; Sobeh, M.; Hamdan, D.I.; Farrag, N.; Roxo, M.; El-Shazly, A.M.; Wink, M. Phenolic Compounds from Populus alba L. and Salix subserrata Willd. (Salicaceae) Counteract Oxidative Stress in Caenorhabditis elegans. Molecules 2019, 24, 1999. [Google Scholar] [CrossRef] [PubMed]
  42. Do Tat, L. Vietnamese Medicinal Plants and Herbs; Medicine Pubishing House: Hanoi, Vietnam, 2015. [Google Scholar]
  43. Hadacek, F.; Greger, H. Testing of antifungal natural products: Methodologies, comparability of results and assay choice. Phytochem. Anal. 2000, 11, 137–147. [Google Scholar] [CrossRef]
  44. Khang, P.; Truong, M.; Hiep, H.; Thuong, S.; Shen, S. Extraction, chemical compositions, and cytotoxic activities of essential oils of Thevetia peruviana. Toxicol. Environ. Chem. 2020, 102, 124–131. [Google Scholar] [CrossRef]
  45. Mishra, S.; Verma, S.S.; Rai, V.; Awasthee, N.; Arya, J.S.; Maiti, K.K.; Gupta, S.C. Curcuma raktakanda Induces Apoptosis and Suppresses Migration in Cancer Cells: Role of Reactive Oxygen Species. Biomolecules 2019, 9, 159. [Google Scholar] [CrossRef] [PubMed]
  46. Marrufo, T.; Nazzaro, F.; Mancini, E.; Fratianni, F.; Coppola, R.; De Martino, L.; Agostinho, A.B.; De Feo, V. Chemical Composition and Biological Activity of the Essential Oil from Leaves of Moringa oleifera Lam. Cultivated in Mozambique. Molecules 2013, 18, 10989–11000. [Google Scholar] [CrossRef] [PubMed]
  47. Klaudyna, F.; Anna, F.; Leon, S.; Antoni, S. β-caryophyllene and β-caryophylleneoxide—Natural compounds of anticancer and analgesic properties. Cancer Med. 2016, 5, 3007–3017. [Google Scholar] [CrossRef]
  48. Legault, J.; Pichette, A. Potentiating effect of β-caryophyllene on anticancer activity of α-humulene, isocaryophyllene and paclitaxel. J. Pharm. Pharmacol. 2007, 59, 1643–1647. [Google Scholar] [CrossRef]
  49. Sain, S.; K Naoghare, P.; Saravana Devi, S.; Daiwile, A.; Krishnamurthi, K.; Arrigo, P.; Chakrabarti, T. Beta caryophyllene and caryophyllene oxide, isolated from Aegle marmelos, as the potent anti-inflammatory agents against lymphoma and neuroblastoma cells. AntiInflamm. Anti-Inflamm. Anti-Allergy Agents Med. Chem. 2014, 13, 45–55. [Google Scholar] [CrossRef]
  50. Sabulal, B.; Dan, M.; Kurup, R.; Pradeep, N.; Valsamma, R.; George, V. Caryophyllene-rich rhizome oil of Zingiber nimmonii from South India: Chemical characterization and antimicrobial activity. Phytochemistry 2006, 67, 2469–2473. [Google Scholar] [CrossRef]
  51. Klauke, A.L.; Racz, I.; Pradier, B.; Markert, A.; Zimmer, A.M.; Gertsch, J.; Zimmer, A. The cannabinoid CB 2 receptor-selective phytocannabinoid beta-caryophyllene exerts analgesic effects in mouse models of inflammatory and neuropathic pain. Eur. Neuropsychopharmacol. 2014, 24, 608–620. [Google Scholar] [CrossRef]
  52. Chicca, A.; Caprioglio, D.; Minassi, A.; Petrucci, V.; Appendino, G.; Taglialatela-Scafati, O.; Gertsch, J. Functionalization of β-caryophyllene generates novel polypharmacology in the endocannabinoid system. ACS Chem. Biol. 2014, 9, 1499–1507. [Google Scholar] [CrossRef]
Table 1. Chemical components of S. babylonica leaves’ essential oils.
Table 1. Chemical components of S. babylonica leaves’ essential oils.
NoCompoundMolecular FormulaRIRelative Content (%)
Thai Nguyen SampleBac Giang Sample
1.α-PineneC10H169173.50.1
2.CampheneC10H169477.30.3
3.Nonan-4-olC9H20O10782.50.1
4.LinaloolC10H18O11040.60.1
5.CitronellalC10H18O11580.40.2
6.2-(4-methyl-3-cyclohexen-1-yl)-2-propanolC10H18O11900.54.5
7.3,7-dimethyl-1,6-octadien-3-olC11H18O21215.41.55.4
8.Methyl citronellateC11H20O212622.84.6
9.Trans-Carvone oxideC10H14O212791.10.4
10.Salicylic acidC7H6O312972.80.2
11.Dihydrocarvyl acetateC12H20O213040.42.7
12.α-Terpinyl acetateC12H20O213671.40.5
13.Geranyl acetateC12H20O213865.20.2
14.MethyleugenolC11H14O214100.40.3
15.CedreneC15H2414220.32.2
16.Trans-CaryophylleneC15H2414445.29.3
17.α-HumuleneC15H2414524.514.5
18.α-FarneseneC15H2415071.03.1
19.Gamma—CadineneC15H2815181.10.2
20.TridecanalC13H26O15190.22.2
21.NerolidolC15H26O15311.32.8
22.Dodecanoic acidC12H24O215620.32.5
23.Benzoic acid, hexyl esterC13H18O215760.22.1
24.(-)-SpathulenolC15H24O15820.22.3
25.HexadeceneC16H3215920.12.1
26.Farnesyl acetateC17H28O218180.35.3
27.PhytolC20H40O21225.64.2
28.PentacosaneC25H52250032.211.3
Table 2. Chemical compositions of S. babylonica bark essential oils.
Table 2. Chemical compositions of S. babylonica bark essential oils.
NoCompoundMolecular FormulaRIRelative Content (%)
Thai Nguyen SampleBac Giang Sample
1.α-PineneC10H169170.30.1
2.CampheneC10H169470.40.2
3.Nonan-4-olC9H20O10780.10.2
4.LinaloolC10H18O11040.20.1
5.CitronellalC10H18O11580.40.2
6.2-(4-methyl-3-cyclohexen-1-yl)-2-propanolC10H18O11900.10.6
7.3,7-dimethyl-1,6-octadien-3-olC11H18O21215.41.71.8
8.Methyl citronellateC11H20O212623.82.6
9.Trans-Carvone oxideC10H14O212790.14.3
10.ThymolC10H14O12970.34.5
11.Dihydrocarvyl acetateC12H20O213040.40.7
12.α-Terpinyl acetateC12H20O213671.01.2
13.Geranyl acetateC12H20O213861.32.8
14.MethyleugenolC11H14O214100.40.3
15.CedreneC15H2414220.30.5
16.Trans—CaryophylleneC15H24144416.524.5
17.α-HumuleneC15H24145230.216.5
18.Alpha-FarneseneC15H2415072.02.1
19.Gamma—CadineneC15H2815181.81.2
20.TridecanalC13H26O15191.20.5
21.NerolidolC15H26O15311.30.8
22.Dodecanoic acidC12H24O215622.00.9
23.Benzoic acid, hexyl esterC13H18O215761.80.7
24.(-)-SpathulenolC15H24O15821.50.9
25.HexadeceneC16H3215920.22.1
26.trans-MuurololC15H26O16520.24.5
27.CadinolC15H26O16790.25.5
28.FarnesolC15H26O16950.34.8
29.Farnesyl acetateC17H28O218186.61.3
30.PhytolC20H40O21220.60.5
31.PentacosaneC25H5225000.10.2
Table 3. Antibacterial action of the S. babylonica EOs.
Table 3. Antibacterial action of the S. babylonica EOs.
Test SampleConcentrationEscherichia coliPseudomonas aeruginosaStaphylococcus aureus
LeavesBarkLeavesBarkLeavesBark
Ampicillin50 mg/mL221714
DMSO-000000
Thai Nguyen sample25 mg/mL202124202124
50 mg/mL313038343433
100 mg/mL353739343635
Bac Giang sample25 mg/mL242325272829
50 mg/mL303229293131
100 mg/mL322632323434
Negative control (0): DMSO; positive control (+); Unit of antibacterial circle diameter in mm.
Table 4. Inhibition activities of the EOs of S. babylonica collected in Thai Nguyen, Vietnam.
Table 4. Inhibition activities of the EOs of S. babylonica collected in Thai Nguyen, Vietnam.
Cancer Cell LinesEssential Oil SamplesIC50 (µg/mL)
A549Leave45.4 ± 1.1
Bark65.3 ± 1.5
Ellipticine0.53 ± 0.05
MCF-7Leave86.1 ± 1.5
Bark95.3 ± 1.3
Ellipticine0.53 ± 0.05
HepG2Leave77.1 ± 1.4
Bark>100
Ellipticine0.53 ± 0.05
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Hoang, P.H.; Tran, T.H.; Pham, V.K. Analysis of Essential Oil of Salix babylonica Collected in Vietnam: Phytochemical Components and Antibacterial and Anticancer Activity. Processes 2024, 12, 33. https://doi.org/10.3390/pr12010033

AMA Style

Hoang PH, Tran TH, Pham VK. Analysis of Essential Oil of Salix babylonica Collected in Vietnam: Phytochemical Components and Antibacterial and Anticancer Activity. Processes. 2024; 12(1):33. https://doi.org/10.3390/pr12010033

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Hoang, Phu Hiep, Thien Hien Tran, and Van Khang Pham. 2024. "Analysis of Essential Oil of Salix babylonica Collected in Vietnam: Phytochemical Components and Antibacterial and Anticancer Activity" Processes 12, no. 1: 33. https://doi.org/10.3390/pr12010033

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