Phytochemical constituents and antioxidant, antimicrobial and tyrosinase inhibitory activities of pandanus tectorius extracts - Le Thi Phuong Hoa

TAP CHI SINH HOC 2015, 37(1se): 45-53 DOI: 10.15625/0866-7160/v37n1se. PHYTOCHEMICAL CONSTITUENTS AND ANTIOXIDANT, ANTIMICROBIAL AND TYROSINASE INHIBITORY ACTIVITIES OF Pandanus tectorius EXTRACTS Le Thi Phuong Hoa*, Cao Thi Nhu Hanoi National University of Education, *lephhoa@yahoo.com ABSTRACT: Phytochemical constituents and various biological activities of n-hexane, ethyl acetate and butanol fractions from stem barks, leaves and fruits of Pandanus tectorius were investigated. Among the extracts, fractions from fruits had higher level of phenolics, especially the ethyl acetate fraction (278.33±3.93 mg gallic acid equivalents/g extract). All extracts possessed low flavonoid content. The ethyl acetate fraction from P. tectorius fruits showed highest antioxidant activity by dose-dependent DPPH, 1,1-diphenyl-2-picryl hydrazyl, radical scavenging action (IC50 = 0.280±0.06 mg/ml). P. tectorius extracts, especially ethyl acetate fraction from fruits and leaves, also exhibited strong antimicrobial activity against Staphylococcus aureus, Bacillus subtilis and Salmonella typhimurium. Fruit extracts, particularly the ethyl aceate fraction had remarkable inhibitory effect on L-DOPA (L-3,4-dihydroxyphenylalanine) oxidase activity of tyrosinase in the melanin biosynthesis pathway as well as sunscreen function through UVB and UVA absorption. Further work is suggested to characterize bioactive compounds from fruit extracts, especially the ethyl acetate fraction for pharmaceutical applications. Keywords: Pandanus tectorius, antimicrobial, antioxidant, sunscreen, tyrosinase inhibition. INTRODUCTION In recent years, the search for natural sources for bioactivities has been rising with the global concern for preventive medicine. Vietnam possesses high diversity of plants, among which a number of plants have traditionally been used to treat ailments and consumed as food. They are important reservoirs for modern medicine as a large source of bioactive compounds which exhibit a wide range of biological activities. Pandanus tectorius is a robust, small plant growing in tropical, sub-tropical and warm temperate areas. All parts of P. tectorius tree has been used in traditional medicine in south and southeast Asia and the Pacific islands to treat a wide range of illnesses, including digestive, respiratory and urinary disorders [5, 12]. Several researches have been done to investigate chemical components and biological activities of P. tectorius. P. tectorius contained a wide range of phytochemical compounds such as triterpenes, phytosterols, steroids, phenolics and flavonoids [3, 4, 11, 16]. Some of these exhibited cytotoxicity to KB cell line [3, 4], anti-tubercular activity [11], anti-hyperglycemic and anti-hyperlipidemic activity [14]. However, there is still limited data regarding its antioxidant activity as well as other bioactivities like skin depigmentation. Therefore, this study aims to evaluate phytochemical constituents and antioxidant, antimicrobial, tyrosinase inhibitory activities and sunscreen function of various extracts from Pandanus tectorius. MATERIALS AND METHODS Stem barks, leaves and fruits of Paranus tectorius were collected at Loc Binh commune, Phu Loc district, Thua Thien-Hue province. Microorganisms including Staphylococcus aureus ATCC 13709, Bacillus subtilis ATCC 6633, Salmonella typhimurium, Escherichia coli ATCC 25922 and Candida albicans ATCC 10231 were obtained from the Institute of Natural Product Chemistry, VAST. Chemicals and reagents were of analytical grade and purchased from Sigma Chemicals (MO, USA) and Merck Chemicals (Darmstadt, Germany). Sample preparation Fresh stem barks, leaves and fruits were washed with distilled water to remove adhering debris and dust, and then freeze dried to constant weights. The dried tissues were ground and then extracted with methanol in an ultrasonic bath for 30 mins at room temperature. The extraction was performed in three replicates. The extracts were mixed and concentrated in a rotary evaporator at 40°C, and then lyophilized. The crude extract was further fractionated in n-hexane, ethyl acetate and butanol. The three fractions were concentrated by vacuum evaporation and freeze dried. All of the extracts were stored at -20°C until use. Thin layer chromatography The extracts were prepared at the concentration of 20 mg/ml in absolute ethanol. Each extract was applied as a single spot in a row along one side of the pre-coated silica gel aluminum plate 60F254, about 2 cm from the edge, using capillary tubes. Solvent including toluene, ethyl acetate, acetone and formic acid at a ratio of 5:3:1:1 was used as the mobile phase. The plate was sprayed with 10% sulfuric acid, heat dried, and observed under white light and UV (ultra violet) radiation at 365 nm. A qualitative evaluation of the plate was done by determining the migration behavior of the separated substances given in the form of Rf value. Determination of total phenolic content The total phenolic content was estimated employing the method of Waterhouse (2002) [13], using Folin-Ciocalteau reagent with gallic acid as the standard. Sample solutions were prepared in ethanol at a concentration of 1 mg/ml and standard solutions were from 0-0.5 mg/ml. Sample or standard solution (10 mL) was mixed with Folin-Ciocalteu reagent (50 ml) and water (790 ml). After 5 min, 150 ml of 10% sodium carbonate was added. The mixture was kept at room temperature for 90 min. The absorbance was then measured at 725 nm. The amounts of total phenolics were calculated using a gallic acid calibration curve. The results were expressed as mg gallic acid equivalents (GAE) per g dry weight of each extract. Determination of total flavonoid content The total flavonoid content of each extract was determined making used of the method described by Sapkota et al. (2010) [9] using quercetin as the standard. Extracts were diluted with 80% aqueous ethanol to arrive at a concentration of 1 mg/ml. Quercetin solutions were prepared in the same manner to the range of 0-0.3 mg/ml. Different quercetin and extract solutions (100 mL) were mixed with 20 µL 10% Al(NO3)3, 20 µL1M K-acetate and 860 µL 80% ethanol. After standing for 40 min at room temperature, the absorbance of the mixture was determined spectrophotometrically at 415 nm. The results were expressed in mg quercetin equivalents (QE) per gram dry weight using a quercetin standard curve. Antioxidant activity Antioxidant activity was evaluated by determining DPPH radical scavenging potential according to Blois (1958) [2]. The reaction mixture contained 20 µL of extract solutions at various concentrations ranging from 0.05-2 mg/ml in ethanol and 180 µL of 0.3 mM DPPH solution. The samples were allowed to stand in a dark place at room temperature for 30 min. The control was prepared with ethanol instead of extracts. Ascorbic acid was used for comparison with extracts at the concentration range of 0.005-0.5 mg/ml. The reduction of DPPH free radicals was measured at 517 nm. DPPH radical scavenging capacity was calculated using the following formula: DPPH scavenging capacity (%) = [(Acontrol – Asample)/(Acontrol)]× 100 where Acontrol represents the absorbance of the control and Asample is the absorbance of the test sample. Antimicrobial activity The antimicrobial activity was tested using the agar well diffusion method. The 24 hour culture broth of the test microorganisms (approximately 1×108 CFU/ml) was spread onto petri plates containing MPA (meat-peptone-agar) for bacteria and Hansen medium for fungi. Wells of 10 mm diameter were made aseptically in the inoculated plates. Each extract was dissolved in methanol to a final concentration of 10 mg/ml. Methanol served as a negative control and 0.4% chloramphenicol was used as the positive control. Aliquots of 100 µL of the extracts and controls were added into the respectively labeled wells. The plates were incubated at 30°C for 24 hrs for bacteria and 36 hrs for fungi in an upright position. Antimicrobial activity was determined by measuring the diameter (mm) of the inhibition zone formed around the well. Tyrosinase inhibitory activity Tyrosinase inhibition assay was carried out according to the procedure described by Yagi et al. (1987) [15] using L-DOPA as the substrate. Kojic acid was used for comparison with concentration ranging as 0.005-0.5 mg/ml in a 0.175 M phosphate buffer at pH 6.8. Extract concentrations ranged from 0.05-2 mg/ml. One hundred µL of each test sample was mixed with 20 µL of phosphate buffer pH 6.8 and 40 µL of 5 mM L-DOPA before added with 40 µL of 110 UI/ml mushroom tyrosinase. The reaction mixture was incubated at 30oC for 2 min. The amount of DOPAchrome was determined at 475 nm. The percentage inhibition of tyrosinase activity was calculated as follows: Tyrosinase inhibitory capacity (%) = [(A – B)/A]× 100 where A stands for the absorbance at 475 nm without the test sample, and B is the absorbance at 475 nm with the test sample. IC50 values were calculated based on the logarithm curve of tyrosinase inhibitory activity vs. sample concentration. Sunscreen function The sunscreen function of extracts was evaluated according to Sapkota et al. (2010) [9]. Kojic acid and quercetin were used as positive controls. The extracts and positive controls were dissolved in methanol-water solution at a ratio of 1:4 to a concentration of 0.1 mg/ml. The absorbance was measured at several UVB and UVA wavelength from 280 nm to 400 nm using a UV-visible spectrophotometer. Statistical analysis For statistical analysis, data were analyzed using Microsoft Excell software and Student’s t-test. Results were expressed as means ± standard deviation. A level of p value less than0.05 was considered to be significant. RESULTS AND DISCUSSION Thin layer chromatography Phytochemical constituents of the crude methanol extract and fractions of Pandanus tectorius were subjected to thin layer chromatography (TLC) analysis using 5:3:1:1 toluene-ethyl acetate-acetone-formic acid solvent system. The chromatograms were visualized by 10% H2SO4 spraying and observed under white light and 365 nm as shown in figure 1. TLC chromatograms of P. tectorius extracts allowed the identification of various compounds. The dominant compounds are terpenoids, revealed by pink and purple bands under white light, chrolophylls as green bands and flavonoids as yellow and orange bands (data not shown). UV detection at 365 nm demonstrated the difference in phytochemical composition of stem bark, leaf and fruit extracts. Red bands were dominant in leaf extracts, correlating to leaf pigment components. Light and dark blue bands appeared in all extracts especially in ethyl acetate fractions of stem barks and fruits, indicating the presence of phenolic compounds. There were some blue fluorescence bands defined as phenol carboxylic compounds. The purple band in the ethyl acetate fraction of leaves represented terpenoids. However, yellow or orange bands were not detectable under 365 nm. As shown in the figure, the ethyl acetate fractions had the highest number of bands as compared to other fractions, which requires further characterization. Various compounds such as triterpenes, steroids and various phenolic and flavonoid compounds have been isolated from P. tectorius extracts [3, 4, 11, 16]. Total phenolic and flavonoid content Phenolic compounds are commonly found in various parts of all sorts of plants. They have been widely investigated in many medicinal plants and plant foods because they are responsible for multiple biological effects [8, 10]. The level of phenolic compounds and flavonoids in P. tectorius extracts are shown in table 1 and 2. As shown in table 1, total phenolic content of fractions from P. tectorius fruits were higher than fractions from stem barks and leaves. Among various fractions, the ethyl acetate fraction had significantly high level of phenolic compounds. The ethyl acetate fraction of P. tectorius fruits possessed the highest amount of phenolics (278.33±3.93 mg GAE/g), approximately 1.4 times higher than the same fraction from stem barks and 2.6 times higher than the fraction from leaves. However, the flavonoid content in all P. tectorius extracts were at low level. The results confirmed the TLC analysis on phytochemical constituents of P. tectorius extracts. Some of P. tectorius biological effects could be attributed to thepresence of these valuable constituents. Zhang et al. (2008) [16] isolated 10 phenolic compounds from P. tectorius fruits with several biological activities such as antioxidant, tyrosinase inhibitory, anti-inflammatory, cholesterol-lowering activity. In another research, Wu et al. (2014) [14] indicated that P. tectorius fruit extract was rich in caffeoylquinic acid, a phenolic carboxylic acid and had antioxidant activity, antihyperglycemic and antihyperlipidemic activities. According to Huyen et al. (2013) [4], three compounds purified from n-hexane and ethyl acetate fractions of P. tectorius roots belonging to phenolic group were cytotoxic to KB cell line. Table 1. Total phenolics content of P. tectorius extracts Fractions Total phenolics content (mg GAE/g) Stem bark Leaf Fruit n-Hexane 13.14±7.34a* 24.38±13.38a* 26.58±1.64b* Ethyl acetate 193±6.71a** 105.6±10.4b** 278.33±3.93c** Butanol 88.45±8.12a*** 111.2±9.63b** 124.2±8.53b*** Table 2. Total flavonoid content of P. tectorius extracts Fractions Total flavonoid content (mg GAE/g) Stem bark Leaf Fruit n-Hexane 7.74±2.31a* 5.64±3.7a* 6.49±1.15a* Ethyl acetate 10.6±0.93a* 15.66±1.52b** 8.48±2.77a* Butanol 7.93±1.87a* 35.79±8.88b*** 4.71±1.09c* a,b,c: Significant difference among same fractions from stem barks, leaves and fruits; *,**,***: significant difference among fractions of stem bark or leaf or fruit extracts at p<0.05. Antioxidant activity Antioxidants are believed to be highly effective in the management of tissue impairment caused by reactive oxygen species, such as superoxide, hydrogen peroxide and hydroxyl radicals [8, 10]. Antioxidant activity of P. tectorius extracts was estimated by DPPH radical scavenging assay and expressed as IC50 values in table 3. It was observed that extracts of P. tectorius had low DPPH radical scavenging capacity. IC50 value was not determined for n-hexane fractions due to poor scavenging capacity (<35%) at highest experimental concentration (2 mg/ml). The ethyl acetate fraction of fruits showed significantly highest activity (IC50=0.280±0.06 mg/ml). The scavenging capacity of this fraction was around 77.1% at the concentration of 2 mg/ml, nearly equal to the scavenging capacity of ascorbic acid at 0,1 mg/ml. The DPPH scavenging capacity of the ethyl acetate fraction of P. tectorius fruits may be due to high phenolic content as compared with other fractions. Phenolics have redox properties, adsorbing and neutralizing free radicals, quenching singlet and triplet oxygen, or decomposing peroxides [8, 10]. The antioxidant activity of P. tectorius extracts showed a high correlation (R2=0.95) to their phenolic content as shown in figure 2. Table 3. DPPH scavenging capacity of P. tectorius extracts Fractions IC50 (mg/ml) Stem bark Leaf Fruit n-Hexane - - - Ethyl acetate 0.468±0.09a* 1.008±0.06b* 0.280±0.06c* Butanol 0.865±0.01a** 1.204±0.01b** 0.842±0.07a** (-): not determined; a,b,c: Significant difference among same fractions from stem barks, leaves and fruits; *,**: significant difference among fractions of stem bark or leaf or fruit extracts at p < 0,05 1 2 3 1 2 3 1 2 3 Stem bark Leaf Fruit Figure 1. TLC chromatograms of Pandanus tectorius extracts in a toluene/ethyl acetate/acetone/formic acid 5:3:1:1 solvent system 1: n-hexane fraction; 2: ethyl acetate fraction; 3: butanol fraction. Figure 2. Relationship between DPPH scavenging capacity and total phenolic content of P. tectorius extracts Antimicrobial activity Extracts of P. tectorius were subjected to a screening of antimicrobial activity using agar well diffusion method. The results were recorded as the absence or presence and the diameter of zones of microbial growth inhibition around the wells, as shown in table 4. The results showed that all P. tectorius extracts exhibited no inhibition against E. coli and C. albicans. Ethyl acetate and butanol fractions of P. tectorius had inhibitory effect on S. aureus and S. typhimurium while n-hexane fractions hardly showed the effect except the n-hexane fraction of leaves on S. aureus. Only ethyl acetate and butanol fractions from leaves show inhibition on the growth of B. subtilis. Among fractions, ethyl acetate fractions expressed stronger activity, especially the ethyl acetate fraction from leaves. Ethyl acetate fraction from fruits showed similar inhibition on S. aureus and S. typhimurium. The antibacterial activity of P. tectorius extracts may be related to the action of phenolic compounds like flavonoids and terpenoids, which were reported to have antiviral and antibacterial activities [10]. According to Bajpai et al. (2008) [1], phenolic compounds might interact with membrane proteins or change bacterial cell permeability and obstruct membrane functions including electron transport, nutrient uptake, protein and nucleic acid synthesis and enzyme activity. Table 4. Antimicrobial activity of P. tectorius extracts Microorganism Inhibition zone diameter (mm) B. subtilis S. aureus S. typhimurium E. coli C. albicans Control (+) 38.00±7.21 34.67±8.08 34.67±8.08 31.33±1.54 - Control (-) - - - - - Fruit n-Hex - - - - - Et - 13.33±4.61 12.67±4.62 - - Bu - 8.00±3.46 9.00±1.41 - - Stem bark n-Hex - - - - - Et - 5.77±3.46 13.33±5.77 - - Bu - - - - - Leaf n-Hex - 10.00±0.00 - - - Et 11.33±2.31 13.33±5.77 15.00±7.07 - - Bu 6.67±3.05 13.33±5.77 7.00±4.24 - - (-): no inhibition; n-Hex: n-Hexane fraction; Et: Ethyl acetate fraction; Bu: Butanol fraction. Table 5. Tyrosinase inhibitory activity of P. tectorius extracts Fractions IC50 (mg/ml) Stem bark Leaf Fruit n-Hexane 0.039±0.01a* 0.049±0.01a* 0.036±0.01a* Etyl acetate 0.43±0.21a** 0.57±0.13a** 0.07±0.0004b** Butanol - - 0.036±0.004* Acid kojic 0.0015±0.0001 (-): not determined; a,b: Significant difference among the same fractions from stem barks, leaves and fruits; *,**: significant difference among fractions of stem bark or leaf or fruit extracts at p<0,05. Tyrosinase inhibitory activity Melanin synthesis in human skin is regulated by tyrosinase, the enzyme catalyzing the two first reactions in the biosynthesis pathway of melanin. One is the hydroxylation of tyrosine to form L-DOPA, and the next is the oxidation of L-DOPA to DOPAquinone which leads to the polymerizing of brown pigments [7, 9]. Over the years, tyrosinase inhibitors have attracted strong interest in both the food and cosmetic industries. In order to further characterize biological effects of P. tectorius, we attempted to test tyrosinase inhibitory activity of P. tectorius extracts. The result was shown in table 5. Data in table 4 indicated that P. tectorius extracts had inhibitory effects on the DOPA oxidase activity of mushroom tyrosinase. Among fractions, n-hexane fraction exhibited significantly stronger activity with IC50 ranging from 0.036-0.049 mg/ml (p<0.05). Fractions from fruits had stronger activity than fractions from other parts of P. tectorius. The ethyl acetate fraction of fruits had remarkable activity (IC50= 0.07 mg/ml). Zhang et al. (2012) [16] isolated and purified vanillin from P. tectorius fruits, which had tyrosinase inhibitory activity. According to the research of Masuda et al. (2005) [6] the methanol extract of P. tectorius leaves inhibited 26,7% of tyrosinase activity at the concentration of 0,5 mg/ml. The activity of P. tectorius fruit extracts was much stronger, suggesting potential source for depigmentation agents. Sunscreen function Exposure of skin to UV radiation inducesextensive generation of reactive oxygen species and a number of biological responses, including development of erythema, sunburn cell formation, hyperplasia, immune suppression, DNA damage, photoaging and melanogenesis. Most solar radiation reaching the earth’s surface is UVB and UVA [10]. P. tectorius extracts were tested with sunscreen function through UVB (280-320 nm) and UVA (320-400 nm) absorption ability. The result was presented in figure 3. a b c Figure 3. UVB and UVA absorption ability of P. tectorius extracts a. stem bark extracts; b. leaf extracts; c. fruit extracts; AK: kojic acid; QE: quercetin; T: stem bark; L: leaf; Q: fruit; 1: n – hexane fraction; 2: ethyl acetate fraction; 3: butanol fraction. As shown in figure 3, UV radiation absorption ability of P. tectorius extracts was lower at UVB range but higher at UVA range as compared to kojic acid. Especially, the ethyl acetate fraction of P. tectorius fruits had highest absorption ability, which was comparable with kojic acid, a widely used component in sunscreen cosmetics. Polyphenols can absorb all UVB radiation and a part of UVA radiation, resulting in reduction of inflammation and oxidative damage to skin [10]. The activity of ethyl acetate fraction P. tectorius fruits may be due to the presence of high phenolic content. CONCLUSION Our study indicated that P. tectorius extracts, especially fruit extracts had good antioxidant activity by DPPH radical scavenging in correlation with high phenolic content. P. tectorius fruit extracts also exhibited remarkable antibacterial activity against Gram-positive and Gram-negative bacteria as well as tyrosinase inhibitory activity and sunscreen function. The ethyl acetate fraction of P. tectorius fruits had significantly stronger activity than other fractions The present findings encourage further characterization of bioactive compounds in fruit extracts, especially the ethyl acetate fraction, and their mechanism of actions for better application as natural antioxidants, antibiotics and whitening. REFERENCES Bajpai V. K., Rahman A., Dung N. T., HuhM. K., Kang S. C., 2008. In vitro inhibition of food spoilage and food borne pathogenic bacteria by essential oil and leaf extracts of Magnolia lilifloria Desr. J. Food Sci., 73: 214-329. Blois M. S., 1958. Antioxidant determination by the use of a stable free radical. Nature, 181: 1199-1200. Hoa N. T ., Dien P. H., Quang D. N,, 2014. Cytotoxic steroids from the stem barks of Pandanus tectorius. Research journal of phytochemistry, 8(2): 52-56. Huyen T. T, Yen H. T. L, Quang D. N, Dien H. P., 2013. A cytotoxicity of Pandanus tectorius plant extracts and isolated metabolites. 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Yagi A., Kanbara T., Morinobu N., 1987, Inhibition of mushroom-tyrosinase by aloe extract. Planta Med., 53(6): 515-517. Zhang X., Guo P., Sun G., Chen S., Yang M., Fu N., Wu H., Xu X., 2012. Phenolic compounds and flavonoids from the fruits of Pandanus tectorius Soland. Journal of Medicinal Plants Research, 6(13): 2622. MỘT SỐ THÀNH PHẦN HÓA HỌC VÀ HOẠT TÍNH CHỐNG OXY HÓA, KHÁNG VI SINH VẬT VÀ ỨC CHẾ TYROSINASE CỦA CÁC CHIẾT XUẤT TỪ Pandanus tectorius Lê Thị Phương Hoa, Cao Thị Nhu Trường Đại học Sư phạm Hà Nội TÓM TẮT Một số thành phần hóa học và hoạt tính sinh học của các phân đoạn n-hexane, ethyl acetate và butanol từ các cao chiết vỏ thân, lá và quả của dứa dại Pandanus tectorius đã được nghiên cứu. Trong các chiết xuất, các phân đoạn của quả có hàm lượng các hợp chất phenol cao hơn đặc biệt là phân đoạn ethyl acetate (278,33±3,93 mg đương lượng acid gallic/g cao chiết). Tất cả các chiết xuất đều có hàm lượng flavonoid thấp. Cao phân đoạn ethyl acetate của quả P. tectorius có hoạt tính chống oxy hóa mạnh nhất thông qua hoạt động quét gốc tự do DPPH, 1,1-diphenyl-2-picryl hydrazyl, phụ thuộc nồng độ (IC50=0,280±0,06 mg/ml). Các chiết xuất của P. tectorius, đặc biệt cao phân đoạn ethyl acetate từ quả và lá, có hoạt tính kháng mạnh các chủng vi khuẩn Staphylococcus aureus, Bacillus subtilis và Salmonella typhimurium. Các cao phân đoạn từ quả trong đó là cao phân đoạn ethyl aceate fraction đã ức chế đáng kể hoạt tính L-DOPA (L-3,4-dihydroxyphenylalanine) oxidase của tyrosinase trong con đường sinh tổng hợp melanin cũng như có tác dụng chống nắng thông qua khả năng hấp thụ tia UVB và UVA. Cần tiến hành nghiên cứu các hợp chất có hoạt tính sinh học từ quả P. tectorius đặc biệt cao phân đoạn ethyl acetate nhằm ứng dụng trong dược mỹ phẩm. Từ khóa: Pandanus tectorius, chống oxy hóa, kháng vi sinh vật, chống nắng, ức chế tyrosinase. Ngày nhận bài: 22-10-2014