Evidence-Based Complementary and Alternative Medicine

Evidence-Based Complementary and Alternative Medicine / 2020 / Article

Research Article | Open Access

Volume 2020 |Article ID 6769726 | https://doi.org/10.1155/2020/6769726

Moragot Chatatikun, Wiyada Kwanhian, "Phenolic Profile of Nipa Palm Vinegar and Evaluation of Its Antilipidemic Activities", Evidence-Based Complementary and Alternative Medicine, vol. 2020, Article ID 6769726, 8 pages, 2020. https://doi.org/10.1155/2020/6769726

Phenolic Profile of Nipa Palm Vinegar and Evaluation of Its Antilipidemic Activities

Academic Editor: Riaz Ullah
Received24 Feb 2020
Revised21 Aug 2020
Accepted26 Aug 2020
Published04 Sep 2020

Abstract

Obesity and overweight are strongly associated with dyslipidemia which can promote the development of cardiovascular diseases. Recently, natural products have been suggested as alternative compounds for antioxidant and antilipidemic activity. The objective of this study was to determine the phenolic compounds and assess the inhibitory activities on pancreatic lipase, cholesterol esterase, and cholesterol micellization of nipa palm vinegar (NPV). Total phenolic content was assessed and phenolic compounds were determined using the Folin–Ciocalteu assay and liquid chromatography-mass spectrometry (LC-MS), respectively. Pancreatic lipase and cholesterol esterase inhibitory activities of the NPV were measured using enzymatic colorimetric assays. The formation of cholesterol micelles was assessed using a cholesterol assay kit. The phenolic content of NPV was 167.10 ± 10.15 µg GAE/mL, and LC-MS analyses indicated the presence of gallic acid, isoquercetin, quercetin, catechin, and rutin as bioactive compounds. Additionally, the NPV inhibited pancreatic lipase and cholesterol esterase activities in a concentration-dependent manner. Moreover, the NPV also suppressed the formation of cholesterol micellization. These results suggest that phenolic compounds, especially gallic acid, isoquercetin, quercetin, catechin, and rutin, from NPV may be the main active compounds with possible cholesterol-lowering effects through inhibition of pancreatic lipase and cholesterol esterase activities as well as the inhibition of solubility of cholesterol micelles. Therefore, NPV may delay postprandial dyslipidemia, and it could be used as a natural source of bioactive compounds with antilipidemic activity. However, NPV should be extensively evaluated by animal and clinical human studies.

1. Introduction

Lipid metabolism disorders are commonly found in people who are obese. The prevalence of obesity and overweight has dramatically increased in developed and developing countries due to the increased consumption of high-fat diets and the daily intake of alcohol [1]. Obesity and overweight are associated with hyperglycemia and dyslipidemia in children and adolescents [2]. Dyslipidemia is a group of metabolic disorders and a noncommunicable disease manifested by elevation of serum cholesterol, low-density lipoprotein (LDL) cholesterol, and triglyceride concentrations and a decrease in high-density lipoprotein (HDL) cholesterol concentration. It is one of the major risk factors associated with atherosclerosis which leads to the development of cardiovascular diseases and increased mortality [3]. Orlistat is a weight loss agent which inhibits gastric and pancreatic lipases in the lumen of the gastrointestinal tract delaying absorption of dietary fat that is approved by the Food and Drug Administration for the treatment of obesity. It also improves total cholesterol and low-density lipoprotein for the treatment of dyslipidemia. The major side effects, which occur at an early stage of treatment with orlistat, are mainly gastrointestinal [4]. Simvastatin is a HMG-CoA reductase inhibitor which is commonly used to decrease blood cholesterol and triglyceride levels. The major adverse effects of statins are myositis, myalgia [5], rhabdomyolysis [6], and hepatic disorders [7].

Recently, natural products have been reported to have the potential to be developed faster and cheaper than conventional single drug. For example, curcumin, lycopene, monascin, ankaflavin, oleanolic acid, ursolic acid, berberine, amphene, tanshinone IIA, hesperetin, and naringenin inhibit cholesterol absorption in enterocytes [8]. Thus, natural products, especially phenolic compounds of these products, may inhibit pancreatic lipase, cholesterol esterase, and solubility of cholesterol micelles. Vinegar is generally used as a food condiment and as an alternative medicine for obesity [9], hyperlipidemia [10], hyperglycemia [11], and cancer [12] and as a disinfectant [13]. The nipa palm (Nypa fruticans Wurmb) vinegar has been used by Southeast Asia, and it has showed biological activities, such as antioxidant activity [14], antidiabetic activity [15], and hepatoprotective effects [16]. Therefore, the NPV could be a natural alternative to treat common diseases from contemporary diet. Nevertheless, the antilipidemic activity of this vinegar has not been previously evaluated. This study aimed to investigate phenolic compounds and in vitro inhibitory effects on pancreatic lipase, cholesterol esterase, and cholesterol micellization of nipa palm vinegar.

2. Materials and Methods

2.1. Chemicals and Reagents

All chemicals and reagents were of analytical grade. Folin–Ciocalteu phenol reagent, sodium carbonate, gallic acid, porcine pancreatic lipase, 4-methylumbelliferone, phosphate buffer saline, sodium citrate, orlistat, taurocholic acid, p-nitrophenylbutyrate (p-NPB), sodium phosphate buffer, sodium chloride, porcine pancreatic cholesterol esterase, simvastatin, cholesterol, oleic acid, phosphatidylcholine, methanol, and taurocholate salt were purchased from Sigma-Aldrich (St. Louis, MO).

2.2. Preparation of Nipa Palm Vinegar

Nipa palm sap was collected from Pak Phanang District, Nakhon Si Thammarat, Thailand (8°12′25.1″ N, 100°14′51.7″ E). All parts of the nipa palm were authenticated and a voucher number (Nypa fruticans Wurmb, voucher no. 01518) was deposited at Botanic Garden, Walailak University, Nakhon Si Thammarat, Thailand. The nipa palm sap was collected from cut stalks. The nipa palm sap was fermented to nipa palm vinegar by the local traditional method. In brief, the collected nipa palm sap was placed in terracotta jars for 40 days at room temperature to allow the natural fermentation process to occur. The level of acidity of nipa palm vinegar reaches 4 to 5%.

2.3. Determination of Total Phenolic Content

The total phenolic content was determined by the Folin–Ciocalteu assay as previously described [17]. In brief, 20 µL of each sample was mixed with 100 µL of Folin–Ciocalteu phenol reagent and 80 µl of sodium carbonate solution (75 g/L). After incubation for 30 min at room temperature, the absorbance was measured at 765 nm. A calibration curve was plotted using gallic acid solutions (31.25, 62.5, 125, 250, and 500 µg/mL). Total phenolic content was determined as µg gallic acid equivalent per ml of nipa palm vinegar (µg GAE/mL).

2.4. Determination of Phenolic Compounds by LC-MS Analysis

Nipa palm vinegar was subjected to commercial LC-MS analysis by the Central Laboratory Co., Ltd. (Bangkok, Thailand) essentially as described elsewhere [18]. Mass spectra data were recorded in ionization mode for a mass range of m/z 100–700. Phenolic standards from Sigma-Aldrich (St. Louis, MO) were gallic acid (≥99% purity), tannic acid (≥99% purity) and hydroquinone (≥99% purity), catechin (≥98% purity), rutin (≥94% purity), isoquercetin (98% purity), eriodictyol (98% purity), quercetin (95% purity), apigenin (≥95% purity), and kaempferol (≥97% purity), and their purity was determined by high-performance liquid chromatography (HPLC).

2.5. Pancreatic Lipase Inhibition Assay

Pancreatic lipase inhibition assay was undertaken as described by Adisakwattana et al. [19]. In brief, 25 µL of nipa palm vinegar diluted with distilled water, or positive control (orlistat), was mixed with 25 µL of porcine pancreatic lipase solution and 50 µL of oleate ester of 0.1 mM fluorescent 4-methylumbelliferone (4-MUO) solution in phosphate buffer saline, subsequently. The mixture was incubated at 37oC for 20 min. Reaction was stopped by adding 100 µL of 0.1 M sodium citrate at pH 4.2. The fluorescence of 4-methylumbelliferone released by the lipase was measured at excitation and emission wavelengths of 320 and 450 nm, respectively. Control without sample or orlistat represented 100% pancreatic lipase (PL) activity. The tests were performed in triplicate.

2.6. Pancreatic Cholesterol Esterase Inhibition Assay

The pancreatic cholesterol esterase inhibition assay was performed according to a previously published method [20]. In brief, different concentrations of nipa palm vinegar were incubated with mixtures containing 5.16 mM taurocholic acid, 0.2 mM p-nitrophenylbutyrate (p-NPB) in 100 mM sodium phosphate buffer, and 100 mM NaCl at pH 7.0. Porcine pancreatic cholesterol esterase at concentration of 1 µg/mL was added into the reaction tube, and samples were incubated at 25°C for 5 min. After that, the absorbance of the solutions was measured at 450 nm. Simvastatin served as a positive control. Results were based on triplicate analysis.

2.7. Cholesterol Micellization Assay

Cholesterol micelles served as a model system for in vitro cholesterol micellization and were prepared according to a previous method [21]. In brief, the micelle solution (2 mM cholesterol, 1 mM oleic acid, and 2.4 mM phosphatidylcholine) was dissolved in methanol and then dried under nitrogen. After that, 15 mM phosphate-buffered saline (PBS) solution containing 6.6 mM taurocholate salt, pH 7.4, was added onto the dried micelles. The emulsion was sonicated twice for 30 min using a sonicator. The micelle solution was incubated overnight at 37°C. Various concentrations of nipa palm vinegar or equivalent PBS as a control were added into the micelle solutions, and samples were incubated for 2 h at 37°C. This mixture was then centrifuged at 16,000 rpm for 20 min. The supernatant of the mixture was collected for determination of cholesterol using total cholesterol test kits (Human Diagnostics Worldwide, Weisbaden, Germany). Gallic acid served as a positive control. All tests were taken in triplicate analysis.

2.8. Data Analysis

All analyses were carried out in triplicate, and data are expressed as mean ± standard deviation. The correlation coefficient (R2) was evaluated by using SigmaPlot version 12.2 software.

3. Results

3.1. Determination of Total Phenolic Content

The amount of total phenolics in nipa palm vinegar (NPV) was determined using the Folin–Ciocalteu method. The value was determined as µg gallic acid equivalent per ml of NPV (µg GAE/mL). The phenolic content of NPV was determined to be 167.10 ± 10.15 µg GAE/mL.

3.2. Phenolic Profile of Nipa Palm Vinegar Determined by LC-MS

LC-MS was used to identify of phenolic compounds. Gallic acid, tannic acid and hydroquinone, catechin, rutin, isoquercetin, eriodictyol, quercetin, apigenin, and kaempferol were used as standards (as shown in Table 1). The contents of gallic acid (peak 1), isoquercetin (peak 5), quercetin (peak 8), catechin (peak 2), and rutin (peak 4) were 14.14, 11.27, 10.33, 8.61, and 6.67 µg/mL in NPV, respectively (as shown in Figure 1), while hydroquinone, tannic acid, eriodictyol, apigenin, and kaempferol were not detected in NPV.


PeakCompoundsRetention time (min)[M + H]+ (m/z)Contents (µg/mL)

1Gallic acid5.60 ± 0.99188.014.14 ± 0.07
2Catechin12.40 ± 0.08185.08.61 ± 0.32
3Tannic acid12.82 ± 0.04503.0ND
4Rutin15.05 ± 0.17649.06.67 ± 0.03
5Isoquercetin16.12 ± 0.21329.011.27 ± 0.12
6Hydroquinone24.56 ± 0.20289.0ND
7Eriodictyol30.71 ± 0.55327.0ND
8Quercetin33.02 ± 0.36341.010.33 ± 0.16
9Apigenin41.08 ± 0.40271.0ND
10Kaempferol42.37 ± 7.97287.0ND

ND: not detected; data are expressed as mean ± standard deviation in triplicate.
3.3. Pancreatic Lipase Inhibitory Activity of Nipa Palm Vinegar

The inhibitory activity of nipa palm vinegar against pancreatic lipase is shown in Figure 2. The nipa palm vinegar inhibited pancreatic lipase activity by 9.55, 12.51, 19.65, 28.14, 50.53, and 60.22% at concentrations of 3.13, 6.25, 12.50, 25.00, 50.00, and 100.00 µL/mL, respectively. The nipa palm vinegar had an IC50 value of 69.95 µL/mL. Orlistat served as a pancreatic lipase inhibitor control, and a concentration of 2 µg/mL reduced activity by 53.67%. These results show that the NPV showed a lipase inhibiting activity.

3.4. Pancreatic Cholesterol Esterase Inhibitory Activity of Nipa Palm Vinegar

The nipa palm vinegar inhibited cholesterol esterase by 8.78, 16.33, 19.48, 23.02, 26.22, and 36.66% at concentrations of 3.13, 6.25, 12.50, 25.00, 50.00, and 100.00 µL/mL, respectively (Figure 3). Simvastatin at a concentration of 300 µg/mL was used as a positive control which inhibited cholesterol esterase by 41.66%. These findings show that the NPV has the ability to inhibit cholesterol esterase in a dose-dependent manner.

3.5. Effect of Nipa Palm Vinegar on Cholesterol Micellization

The inhibition of cholesterol micellization by NPV at various concentrations is shown in Figure 4. The NPV suppressed cholesterol micellization by 13.46, 19.23, 25.00, 38.46, and 46.15% at concentrations of 12.50, 25.00, 50.00, 100.00, and 200.00 µL/mL, respectively. Gallic acid at a concentration of 200 µg/mL was used as a positive control which inhibited cholesterol micellization by 84.62%. These results show that the NPV can inhibit the formation of cholesterol micellization in a dose-dependent manner.

3.6. Correlation Analyses of Pancreatic Lipase Inhibition, Pancreatic Cholesterol Esterase Inhibition, and Cholesterol Micellization Inhibition of Nipa Palm Vinegar

The linear regression analysis and correlation coefficients between the variables are presented in Figure 5. There were strongly positive correlations between % pancreatic lipase inhibition and % cholesterol esterase inhibition (R2 = 0.8801) at concentrations of 3.13, 6.25, 12.50, 25.00, 50.00, and 100.00 µL/mL (Figure 5(a)). A strongly positive correlation was also found between the % pancreatic lipase inhibition and % cholesterol micellization inhibition (R2 = 0.8919) at concentrations of 12.50, 25.00, 50.00, and 100.00 µL/mL (Figure 5(b)). Moreover, a positive correlation was also observed between % cholesterol micellization inhibition and % cholesterol (Figure 5(c)) esterase inhibition (R2 = 0.9943).

4. Discussion

Dyslipidemia is a key risk factor in the development of cardiovascular diseases which leads to increased morbidity and mortality [8]. Natural products have been used as an alternative medicine for the prevention and management of cardiovascular diseases [22]. There are many risk factors for dyslipidemia including genetic factors, hormonal abnormalities, and lifestyle factors. A diet especially high in fat is believed to be one of the greatest risk factors for the development of dyslipidemia [23]. Normally, pancreatic lipase is a key enzyme that hydrolyses ester linkages of triglyceride [24]. Therefore, pancreatic lipase inhibition is a goal to reduce fat absorption to control dyslipidemia. Pancreatic cholesterol esterase is an enzyme which hydrolyses cholesterol esters, so inhibition of pancreatic cholesterol esterase can reduce cholesterol absorption and may be useful for therapeutics for controlling cholesterol [25]. Moreover, the reduction of micelle formation is a target for lowering blood cholesterol level [21]. This study evaluated nipa palm vinegar for its total phenolic content and the presence of phenolic compounds as well as determined its ability to inhibit pancreatic lipase, inhibit cholesterol esterase, and inhibit cholesterol micellization.

Natural phenolic compounds as secondary metabolites of plants consist of phenolic acids, flavonoids, tannins, stilebenes, curcuminoids, coumarins, lignans, quinones, and others [26]. Phenolic compounds have been shown to have several pharmacological effects including antioxidant [27], anti-hyperlipidemic activity [28], anti-hypertensive activity [29], antimutagenic activity [30], anti-inflammatory activity [31], antidiabetic effect [32], and anticancer [33]. The total phenolic content in NPV was determined by the Folin–Ciocalteu assay. In this study, the NPV contained 167.10 ± 10.15 µg GAE/mL. According to a previous study, nipa sap vinegar produced by surface fermentation contained a phenolic content of 253.98 ± 0.14 µg GAE/mL and showed antioxidant activity against DPPH free radicals [34]. Moreover, phenolic compounds were determined by LC-MS, and the results showed that nipa palm vinegar contains gallic acid, isoquercetin, quercetin, catechin, and rutin.

Orlistat is a well-known pancreatic lipase inhibitor which is produced from Streptomyces toxytricini. It reacts with lipases at the active site serine by forming a covalent bond and thus inactivating the ability of these enzymes to hydrolyse dietary fat in the small intestine [35]. Adverse effects of orlistat are liquid stools, steatorrhea, fecal urgency, incontinence, flatulence, abdominal cramping, and fat-soluble vitamin deficiencies [36]. Recently, many researchers have been focused on the effects of natural products for the treatment of dyslipidemia [37]. Our study determined the inhibitory activity of NPV towards pancreatic lipase, and the results showed that NPV can inhibit pancreatic lipase in a concentration-dependent manner with an IC50 value of 69.95 µL/mL. In a previous study, an aqueous extract of NPV was able to significantly reduce blood glucose in streptozotocin-induced diabetic rats [15]. The aqueous extract of NPV also stimulated insulin secretion in RIN-5F cells [16]. Moreover, nipa palm sap and its syrup inhibited α-glucosidase which hydrolyses polysaccharides [38].

Pancreatic cholesterol esterase exerts important functions in controlling the bioavailability of cholesterol from dietary cholesterol esters, contributing to the incorporation of cholesterol into mixed micelles, and in helping to transport free cholesterol to enterocytes [25]. It has previously been reported that inhibition of pancreatic cholesterol esterase and the solubility of cholesterol micelles by gallic acid, catechin, and epicatechin from grape seed extract results in delaying the absorption of cholesterol [20]. The current findings revealed that NPV inhibited pancreatic cholesterol esterase and the solubility of cholesterol micelles in a concentration-dependent manner. There was a positive correlation between pancreatic lipase inhibition and pancreatic cholesterol esterase inhibition. Moreover, cholesterol micellization inhibition had a positive correlation with pancreatic lipase inhibition and pancreatic cholesterol esterase inhibition. Therefore, it could be hypothesized that the NPV can inhibit pancreatic cholesterol esterase and may protect against cholesterol micellization.

There are several reports demonstrating anti-dyslipidemia activity of natural compounds. Gallic acid has been reported to decrease levels of serum triglycerides, total cholesterol, and low-density lipoprotein in high-fat induced dyslipidemia in rats [39]. Similarly, quercetin had a strong inhibitory activity on pancreatic lipase [40], and it also reduced serum levels of triglycerides and cholesterol in a rabbit model of high-fat diet-induced atherosclerosis [41]. Moreover, isoquercetin, a glucoside derivative of quercetin, improved hepatic lipid accumulation through activating the AMPK pathway and inhibiting TGF- signalling in a high-fat diet-induced nonalcoholic fatty liver disease rat model [42]. A previous study showed that green tea catechin suppressed cholesterol absorption in the small intestine and reduced serum cholesterol concentrations [43]. Other studies have also demonstrated the antiobesity effects of rutin by decreasing serum lipid profiles and leptin [44].

According to our in vitro finding, it can be hypothesized that phenolic compounds including gallic acid, isoquercetin, quercetin, catechin, and rutin from NPV may be the main active compounds with possible cholesterol-lowering effects through inhibition of pancreatic lipase and cholesterol esterase activities as well as the inhibition of solubility of cholesterol micelles. More in vivo studies in animal and clinical human studies are required to determine the anti-dyslipidemia activity of NPV and to confirm its mechanism for the aim of application in the prevention and treatment of dyslipidemia.

5. Conclusion

Our results indicate that nipa palm vinegar may delay the digestion of a high-fat diet and absorption through small intestine through mechanisms such as the inhibition of pancreatic lipase and cholesterol esterase activities as well as through the inhibition of solubility of cholesterol micelles. These results indicate that NPV could be used as a natural source of bioactive compounds with antilipidemic activity. Nevertheless, NPV should be extensively evaluated by animal and clinical human studies.

Data Availability

The data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

This study was supported by Walailak University and Thailand Research Fund (grant no. WU-TRF_ABC60_11) and partially supported by the New Strategic Research (P2P) Project, Walailak University, Thailand. We would like to thank the Center of Excellence Research for Melioidosis (CERM) and School of Allied Health Sciences, Walailak University, Nakhon Si Thammarat 80161, Thailand, for providing the equipment. Finally, we would also like to thank Professor Duncan R. Smith (Institute of Molecular Biosciences, Mahidol University) for reviewing our manuscript.

References

  1. T. Darebo, A. Mesfin, and S. Gebremedhin, “Prevalence and factors associated with overweight and obesity among adults in Hawassa city, southern Ethiopia: a community based cross-sectional study,” BMC Obesity, vol. 6, no. 1, 2019. View at: Publisher Site | Google Scholar
  2. C. P. Reuter, P. T. da Silva, J. D. P. Renner et al., “Dyslipidemia is associated with unfit and overweight-obese children and adolescents,” Arquivos Brasileiros de Cardiologia, vol. 106, no. 3, pp. 188–193, 2016. View at: Publisher Site | Google Scholar
  3. B. Klop, J. Elte, and M. Cabezas, “Dyslipidemia in obesity: mechanisms and potential targets,” Nutrients, vol. 5, no. 4, pp. 1218–1240, 2013. View at: Publisher Site | Google Scholar
  4. A. M. Heck, J. A. Yanovski, and K. A. Calis, “Orlistat, a new lipase inhibitor for the management of obesity,” Pharmacotherapy, vol. 20, no. 3, pp. 270–279, 2000. View at: Publisher Site | Google Scholar
  5. A. Selva-O’Callaghan, M. Alvarado-Cardenas, I. Pinal-Fernández et al., “Statin-induced myalgia and myositis: an update on pathogenesis and clinical recommendations,” Expert Review of Clinical Immunology, vol. 14, no. 3, pp. 215–224, 2018. View at: Google Scholar
  6. S. Ezad, H. Cheema, and N. Collins, “Statin-induced rhabdomyolysis: a complication of a commonly overlooked drug interaction,” Oxford Medical Case Reports, vol. 2018, no. 3, 2018. View at: Publisher Site | Google Scholar
  7. J. Jose, “Statins and its hepatic effects: newer data, implications, and changing recommendations,” Journal of Pharmacy and Bioallied Sciences, vol. 8, no. 1, pp. 23–28, 2016. View at: Publisher Site | Google Scholar
  8. X. Ji, S. Shi, B. Liu et al., “Bioactive compounds from herbal medicines to manage dyslipidemia,” Biomedicine & Pharmacotherapy, vol. 118, Article ID 109338, 2019. View at: Publisher Site | Google Scholar
  9. J. Y. Kim, E. Ok, Y. J. Kim, K.-S. Choi, and O. Kwon, “Oxidation of fatty acid may be enhanced by a combination of pomegranate fruit phytochemicals and acetic acid in HepG2 cells,” Nutrition Research and Practice, vol. 7, no. 3, pp. 153–159, 2013. View at: Publisher Site | Google Scholar
  10. H. Seo, B.-D. Jeon, and S. Ryu, “Persimmon vinegar ripening with the mountain-cultivated ginseng ingestion reduces blood lipids and lowers inflammatory cytokines in obese adolescents,” Journal of Exercise Nutrition and Biochemistry, vol. 19, no. 1, pp. 1–10, 2015. View at: Publisher Site | Google Scholar
  11. S. N. Yun, S. K. Ko, K. H. Lee, and S. H. Chung, “Vinegar- processed ginseng radix improves metabolic syndrome induced by a high fat diet in ICR mice,” Archives of Pharmacal Research, vol. 30, no. 5, pp. 587–595, 2007. View at: Publisher Site | Google Scholar
  12. N. Baba, Y. Higashi, and T. Kanekura, “Japanese black vinegar “Izumi” inhibits the proliferation of human squamous cell carcinoma cells via necroptosis,” Nutrition and Cancer, vol. 65, no. 7, pp. 1093–1097, 2013. View at: Publisher Site | Google Scholar
  13. T. M. S. Pinto, A. C. C. Neves, M. V. P. Leão, and A. O. C. Jorge, “Vinegar as an antimicrobial agent for control of Candida spp. in complete denture wearers,” Journal of Applied Oral Science, vol. 16, no. 6, pp. 385–390, 2008. View at: Publisher Site | Google Scholar
  14. B. K. Beh, N. E. Mohamad, S. K. Yeap et al., “Polyphenolic profiles and the in vivo antioxidant effect of nipa vinegar on paracetamol induced liver damage,” RSC Advances, vol. 6, no. 68, pp. 63304–63313, 2016. View at: Publisher Site | Google Scholar
  15. N. A. Yusoff, M. F. Yam, H. K. Beh et al., “Antidiabetic and antioxidant activities of Nypa fruticans Wurmb. vinegar sample from Malaysia,” Asian Pacific Journal of Tropical Medicine, vol. 8, no. 8, pp. 595–605, 2015. View at: Publisher Site | Google Scholar
  16. N. Yusoff, V. Lim, B. Al-Hindi et al., “Nypa fruticans Wurmb. Vinegar’s aqueous extract stimulates insulin secretion and exerts hepatoprotective effect on STZ-induced diabetic rats,” Nutrients, vol. 9, no. 9, p. 925, 2017. View at: Publisher Site | Google Scholar
  17. G. Sharma, S. Dubey, N. Sati, and J. Sanadya, “Phytochemical screening and estimation of total phenolic content in aegle marmelos seeds,” International Journal of Pharmaceutical and Clinical Research, vol. 3, no. 2, pp. 27–29, 2011. View at: Google Scholar
  18. M. Junsi, S. Siripongvutikorn, C. T. Yupanqui, and W. Usawakesmanee, “Phenolic and flavonoid compounds in aqueous extracts of thunbergia laurifolia leaves and their effect on the toxicity of the carbamate insecticide methomyl to murine macrophage cells,” Functional Foods in Health and Disease, vol. 7, no. 7, pp. 529–544, 2017. View at: Publisher Site | Google Scholar
  19. S. Adisakwattana, J. Intrawangso, A. Hemrid, B. Chanathong, and K. Mäkynen, “Extracts of edible plants inhibit pancreatic lipase, cholesterol esterase and cholesterol micellization, and bind bile acids,” Food Technology and Biotechnology, vol. 50, no. 1, pp. 11–16, 2012. View at: Google Scholar
  20. S. Ngamukote, K. Mäkynen, T. Thilawech, and S. Adisakwattana, “Cholesterol-lowering activity of the major polyphenols in grape seed,” Molecules, vol. 16, no. 6, pp. 5054–5061, 2011. View at: Publisher Site | Google Scholar
  21. A. Duangjai, N. Limpeanchob, K. Trisat, and D. Amornlerdpison, “Spirogyra neglecta inhibits the absorption and synthesis of cholesterol in vitro,” Integrative Medicine Research, vol. 5, no. 4, pp. 301–308, 2016. View at: Publisher Site | Google Scholar
  22. W. H. El-Tantawy and A. Temraz, “Natural products for controlling hyperlipidemia: review,” Archives of Physiology and Biochemistry, vol. 125, no. 2, pp. 128–135, 2019. View at: Publisher Site | Google Scholar
  23. S.-A. Kim, H. Joung, and S. Shin, “Dietary pattern, dietary total antioxidant capacity, and dyslipidemia in Korean adults,” Nutrition Journal, vol. 18, no. 1, p. 37, 2019. View at: Publisher Site | Google Scholar
  24. S. Liu, D. Li, B. Huang, Y. Chen, X. Lu, and Y. Wang, “Inhibition of pancreatic lipase, α-glucosidase, α-amylase, and hypolipidemic effects of the total flavonoids from Nelumbo nucifera leaves,” Journal of Ethnopharmacology, vol. 149, no. 1, pp. 263–269, 2013. View at: Publisher Site | Google Scholar
  25. J. E. Heidrich, L. M. Contos, L. A. Hunsaker, L. M. Deck, and D. L. Vander Jagt, “Inhibition of pancreatic cholesterol esterase reduces cholesterol absorption in the hamster,” BMC Pharmacology, vol. 4, no. 1, 2004. View at: Publisher Site | Google Scholar
  26. W. Y. Huang, Y. Z. Cai, and Y. Zhang, “Natural phenolic compounds from medicinal herbs and dietary plants: potential use for cancer prevention,” Nutrition and Cancer, vol. 62, no. 1, pp. 1–20, 2010. View at: Google Scholar
  27. N. Pourreza, “Phenolic compounds as potential antioxidant,” Jundishapur Journal of Natural Pharmaceutical Products, vol. 8, no. 4, pp. 149-150, 2013. View at: Publisher Site | Google Scholar
  28. S. Sharma, R. Asija, R. S. Kumawat, P. Chaudhary, and P. K. Sharma, “A study of anti-hyperlipidemic acitivity of marketed formulations of Terminalia arjuna powder using experimetnal animal model,” Journal of Biomedical and Pharmaceutical Research, vol. 4, no. 1, 2015. View at: Google Scholar
  29. E. A. d. Figueiredo, N. F. B. Alves, M. M. d. O. Monteiro et al., “Antioxidant and antihypertensive effects of a chemically defined fraction of syrah red wine on spontaneously hypertensive rats,” Nutrients, vol. 9, no. 6, p. 574, 2017. View at: Publisher Site | Google Scholar
  30. A. Pandey, T. Belwal, S. Tamta, I. D. Bhatt, and R. S. Rawal, “Phenolic compounds, antioxidant capacity and antimutagenic activity in different growth stages of in vitro raised plants of Origanum vulgare L,” Molecular Biology Reports, vol. 46, no. 2, pp. 2231–2241, 2019. View at: Publisher Site | Google Scholar
  31. J. C. Ruiz-Ruiz, A. J. Matus-Basto, P. Acereto-Escoffié, and M. R. Segura-Campos, “Antioxidant and anti-inflammatory activities of phenolic compounds isolated from Melipona beecheii honey,” Food and Agricultural Immunology, vol. 28, no. 6, pp. 1424–1437, 2017. View at: Publisher Site | Google Scholar
  32. T. R. Dias, M. G. Alves, S. Casal, P. F. Oliveira, and B. M. Silva, “Promising potential of dietary (poly) phenolic compounds in the prevention and treatment of diabetes mellitus,” Current Medicinal Chemistry, vol. 24, no. 4, pp. 334–354, 2017. View at: Google Scholar
  33. M. Carocho and I. Ferreira, “The role of phenolic compounds in the fight against cancer - a review,” Anti-Cancer Agents in Medicinal Chemistry, vol. 13, no. 8, pp. 1236–1258, 2013. View at: Publisher Site | Google Scholar
  34. P. Saithong, S. Nitipan, and J. Permpool, “Optimization of vinegar production from nipa (Nypa fruticans Wurmb.) sap using surface culture fermentation process,” Appiled Food Biotechnology, vol. 6, no. 3, p. 8, 2019. View at: Google Scholar
  35. B. Kaila and M. Raman, “Obesity: a review of pathogenesis and management strategies,” Canadian Journal of Gastroenterology, vol. 22, no. 1, pp. 61–68, 2008. View at: Publisher Site | Google Scholar
  36. N. Aktar, N. K. Qureshi, and H. S. Ferdous, “Obesity: a review of pathogenesis and management strategies in adult,” Delta Medical College Journal, vol. 5, no. 1, pp. 35–48, 2017. View at: Publisher Site | Google Scholar
  37. A. Seyyedan, M. Alshawsh, M. Al-Shagga, S. Koosha, and Z. Mohamed, “Medicinal plants and their inhibitory activities against pancreatic lipase: a review,” Evidence-based Complementary and Alternative Medicine, vol. 2015, Article ID 973143, 2015. View at: Publisher Site | Google Scholar
  38. R. Phetrit, M. Chaijan, S. Sorapukdee, and W. Panpipat, “Characterization of nipa palm’s (Nypa fruticans Wurmb.) sap and syrup as functional food Ingredients,” Sugar Tech, vol. 22, 2019. View at: Google Scholar
  39. C.-L. Hsu and G.-C. Yen, “Effect of gallic acid on high fat diet-induced dyslipidaemia, hepatosteatosis and oxidative stress in rats,” British Journal of Nutrition, vol. 98, no. 4, pp. 727–735, 2007. View at: Publisher Site | Google Scholar
  40. A. I. Martinez-Gonzalez, E. Alvarez-Parrilla, Á.G. Díaz-Sánchez et al., “In vitro inhibition of pancreatic lipase by polyphenols: 
a kinetic, fluorescence spectroscopy and molecular docking study,” Food Technology and Biotechnology, vol. 55, no. 4, pp. 519–530, 2017. View at: Publisher Site | Google Scholar
  41. S. Juzwiak, J. Wójcicki, K. Mokrzycki et al., “Effect of quercetin on experimental hyperlipidemia and atherosclerosis in rabbits,” Pharmacological Reports, vol. 57, pp. 604–609, 2005. View at: Google Scholar
  42. G. Qin, J. Ma, Q. Huang et al., “Isoquercetin improves hepatic lipid accumulation by activating AMPK pathway and suppressing TGF-β signaling on an HFD-induced nonalcoholic fatty liver disease rat model,” International Journal of Molecular Sciences, vol. 19, no. 12, p. 4126, 2018. View at: Publisher Site | Google Scholar
  43. M. Kobayashi and I. Ikeda, “Mechanisms of inhibition of cholesterol absorption by green tea catechins,” Food Science and Technology Research, vol. 23, no. 5, pp. 627–636, 2017. View at: Publisher Site | Google Scholar
  44. C.-L. Hsu, C.-H. Wu, S.-L. Huang, and G.-C. Yen, “Phenolic compounds rutin ando-coumaric acid ameliorate obesity induced by high-fat diet in rats,” Journal of Agricultural and Food Chemistry, vol. 57, no. 2, pp. 425–431, 2009. View at: Publisher Site | Google Scholar

Copyright © 2020 Moragot Chatatikun and Wiyada Kwanhian. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


More related articles

 PDF Download Citation Citation
 Download other formatsMore
 Order printed copiesOrder
Views162
Downloads54
Citations

Related articles

We are committed to sharing findings related to COVID-19 as quickly as possible. We will be providing unlimited waivers of publication charges for accepted research articles as well as case reports and case series related to COVID-19. Review articles are excluded from this waiver policy. Sign up here as a reviewer to help fast-track new submissions.