The most commonly used spices in Thai traditional medicine: in vitro evaluation of anti-hyperglycemic, antioxidant, polyphenol content, and nitric oxide production inhibitory activities

Chadchom Choockong , Arunporn Itharat , Weerachai Pipatrattanaseree, Theeraphong Ninlaor, Krit Piwngam, Ninnart Intharit, Supon Sukkhum, Neal M. Davies

Abstract


Background and purpose: Diabetes mellitus is a persistent hyperglycemic condition. Thai cuisine and medicine incorporate spices: nutmeg, mace, clove buds, cardamom, cinnamon, and coriander. The in vitro impacts of these spices on anti-diabetic, antioxidant, anti-inflammatory, and total phenolic and flavonoid content were assessed.

Experimental approach:  Alpha-amylase and alpha-glucosidase inhibition assays were conducted. Antioxidant potential was measured through DPPH and ABTS assays. Anti-inflammatory activity was determined by inhibiting nitric oxide generation in RAW 264.7 cells. Total phenolic content was quantified using the Folin Ciocalteu method, while total flavonoid content was estimated via the aluminum chloride colorimetric method.

Findings/Results: Ethanolic and aqueous extracts of a blend of spices (Siam cardamom, nutmeg, mace, and clove buds), denoted as 4-GlurE and 4-GlurA, displayed concentration-dependent inhibition of alpha-glucosidase, with IC50 values of 0.373 and 0.435 mg/mL, respectively.  4-GlurE and 4-GlurA exhibited antioxidant activity, by ABTS•+ radical and DPPH scavenging capabilities.  4-GlurE demonstrated anti-inflammatory potential by reducing nitric oxide generation (IC50: 43.95 ± 2.47 μg/mL). 4-GlurE and 4-GlurA possessed total phenolic content (TPC) of 122.47 ± 1.12 and 148.72 ± 0.14 mg GAE/g, respectively.  4-GlurE exhibited a higher total flavonoid content (TFC) compared to the aqueous extract (340.33 ± 4.77 and 94.17 ± 3.36 mg QE/g). Cinnamon and clove aqueous extracts were more potent than acarbose in alpha-glucosidase inhibition with the highest antioxidant activity.  Polyphenol levels (TPC and TFC) exhibited strong correlations with antioxidant capacity.

Conclusions and implications: Findings are consistent with the traditional use of 4-Glur, with cinnamon, for diabetes prevention and treatment.


Keywords


Alpha-amylase; Alpha-glucosidase; Antioxidant; Diabetic; Spices.

Full Text:

PDF

References


Dalal S, Beunza JJ, Volmink J, Adebamowo C, Bajunirwe F, Njelekela M, et al. Non-communicable diseases in sub-Saharan Africa: what we know now. Int J Epidemiol. 2011;40(4):885-901. DOI: 10.1093/ije/dyr050.

The global health observatory. Noncommunicable diseases: Mortality. Available on: https://www.who.int/data/gho/data/themes/topics/topic-details/GHO/ncd-mortality

IDF Diabetes Atlas 2021 | IDF Diabetes Atlas. IDF Diabetes Atlas 2021 | IDF Diabetes Atlas. Available on: https://www.diabetesatlas.org.

Tripathi BK, Srivastava AK. Diabetes mellitus: complications and therapeutics. Med Sci Monit. 2006;12(7):RA130-RA147.PMID: 16810145.

Vincent AM, Callaghan BC, Smith AL, Feldman EL. Diabetic neuropathy: cellular mechanisms as therapeutic targets. Nat Rev Neurol. 2011;7(10): 573-583. DOI: 10.1038/nrneurol.2011.137.

Wang H, Shen Y, Zhao L, Ye Y. 1-Deoxynojirimycin and its derivatives: a mini review of the literature. Curr Med Chem. 2021;28(3):628-643. DOI: 10.2174/0929867327666200114112728.

Dirir AM, Daou M, Yousef AF, Yousef LF. A review of alpha-glucosidase inhibitors from plants as potential candidates for the treatment of type-2 diabetes. Phytochem Rev. 2022;21(4):1049-1079. DOI: 10.1007/s11101-021-09773-1.

Chiasson JL, Josse RG, Gomis R, Hanefeld M, Karasik A, Laakso M, et al. Acarbose for prevention of type 2 diabetes mellitus: the STOP-NIDDM randomised trial. Lancet. 2002;359(9323): 2072-2077. DOI: 10.1016/S0140-6736(02)08905-5.

Mohd Bukhari D, Siddiqui M, Shamsudin SH, Rahman MdM, So’ad SZM. α-Glucosidase inhibitory activity of selected Malaysian plants. J Pharm Bioallied Sci. 2017;9(3):164-170. DOI: 10.4103/jpbs.JPBS_35_17.

Tapsell LC, Hemphill I, Cobiac L, Sullivan DR, Fenech M, Patch CS, et al. Health benefits of herbs and spices: the past, the present, the future. Med J Aust. 2006;185(S4): S1-S24. DOI: 10.5694/j.1326-5377.2006.tb00548.x.

National Drug System Development Committee. National list of essential medicines 2013. The Agricultural Cooperative Federation of Thailand Limited; 2013. Available on: https://ttm.skto. moph.go.th/document_file/pr008.pdf.

Makchuchit S, Rattarom R, Itharat A. The antiallergic and anti-inflammatory effects of Benjakul extract (a Thai traditional medicine), its constituent plants and its some pure constituents using in vitro experiments. Biomed Pharmacother. 2017;89:1018-1026. DOI: 10.1016/j.biopha.2017.02.066.

Yamasaki K, Hashimoto A, Kokusenya Y, Miyamoto T, Sato T. Electrochemical method for estimating the antioxidative effects of methanol extracts of crude drugs. Chem Pharm Bull (Tokyo). 1994;42(8): 1663-1665. DOI: 10.1248/cpb.42.1663.

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C. Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med. 1999;26(9-10):1231-1237. DOI: 10.1016/s0891-5849(98)00315-3.

Wongnawa, M, Tohkayomatee, R, Bumrungwong, N, Wongnawa, S. Alpha-glucosidase inhibitory effect and inorganic constituents of Phyllanthus amarus Schum. & Thonn. ash. Songklanakarin J Sci Technol. 2014;36(5):541-546.

Lordan S, Smyth TJ, Soler-Vila A, Stanton C, Ross RP. The α-amylase and α-glucosidase inhibitory effects of Irish seaweed extracts. Food Chem. 2013;141(3):2170-2176. DOI: 10.1016/j.foodchem.2013.04.123.

Folin O, Ciocalteu V. On tyrosine and tryptophane determinations in proteins. J Biol Chem. 1927;73(2):627-650. DOI: 10.1016/s0021-9258(18)84277-6.

Zhu H, Wang Y, Liu Y, Xia Y, Tang T. Analysis of flavonoids in Portulaca oleracea L. by UV-Vis spectrophotometry with comparative study on different extraction technologies. Food Anal Methods. 2009;3(2):90-97.DOI: 10.1007/s12161-009-9091-2.

Ning W, Wei Y, Gao L, Han C, Gou Y, Fu S, et al. HemI 2.0: an online service for heatmap illustration. Nucleic Acids Res. 2022;50(W1): W405-W411.DOI: 10.1093/nar/gkac480.

Deng W, Wang Y, Liu Z, Cheng H, Xue Y. HemI: a toolkit for illustrating heatmaps. PLoS One. 2014;9(11): e111988,1-5. DOI: 10.1371/journal.pone.0111988.

Fernando IT, Perera KI, Athauda SBP, Sivakanesan R, Kumar NS, Jayasinghe L. Heat stability of the in vitro inhibitory effect of spices on lipase, amylase, and glucosidase enzymes. Food Sci Nutr. 2019;7(2):425-432. DOI: 10.1002/fsn3.797.

Sham Shihabudeen HM, Priscilla DH, Thirumurugan K. Cinnamon extract inhibits α-glucosidase activity and dampens postprandial glucose excursion in diabetic rats. Nutr Metab (Lond). 2011;8(1):46,1-11. DOI: 10.1186/1743-7075-8-46

Rao PV, Gan SH. Cinnamon: a multifaceted medicinal plant. Evid Based Complement Alternat Med. 2014;2014:642942,1-13. DOI: 10.1155/2014/642942.

Subash Babu P, Prabuseenivasan S, Ignacimuthu S. Cinnamaldehyde-a potential antidiabetic agent. Phytomedicine. 2007;14(1):15-22. DOI: 10.1016/j.phymed.2006.11.005.

Lu T, Sheng H, Wu J, Cheng Y, Zhu J, Chen Y. Cinnamon extract improves fasting blood glucose and glycosylated hemoglobin level in Chinese patients with type 2 diabetes. Nutr Res. 2012;32(6):408-412. DOI: 10.1016/j.nutres.2012.05.003.

Seetaloo AD, Aumeeruddy MZ, Rengasamy Kannan RR, Mahomoodally MF. Potential of traditionally consumed medicinal herbs, spices, and food plants to inhibit key digestive enzymes geared towards diabetes mellitus management - a systematic review. S AFR J BOT. 2019;120:3-24. DOI: 10.1016/j.sajb.2018.05.015.

Khathi A, Serumula MR, Myburg RB, Van Heerden FR, Musabayane CT. Effects of Syzygium aromaticum-derived triterpenes on postprandial blood glucose in streptozotocin-induced diabetic rats following carbohydrate challenge. PLoS One. 2013;8(11):e81632,1-8. DOI: 10.1371/journal.pone.0081632

Wang X, Ye XL, Liu R, Chen HL, Bai H, Liang X, et al. Antioxidant activities of oleanolic acid in vitro: possible role of Nrf2 and MAP kinases. Chem Biol Interact. 2010;184(3):328-337. DOI: 10.1016/j.cbi.2010.01.034.

Ngubane PS, Masola B, Musabayane CT. The effects of Syzygium aromaticum-derived oleanolic acid on glycogenic enzymes in streptozotocin-induced diabetic rats. Ren Fail. 2011;33(4):434-439. DOI: 10.3109/0886022X.2011.568147.

Fernando IT, Perera KI, Athauda SBP, Sivakanesan R, Kumar NS, Jayasinghe L. Heat stability of the in vitro inhibitory effect of spices on lipase, amylase, and glucosidase enzymes. Food Sci Nutr. 2019;7(2):425-432. DOI: 10.1002/fsn3.797.

Hayward NJ, McDougall GJ, Farag S, Allwood JW, Austin C, Campbell F, et al. Cinnamon shows antidiabetic properties that are species-specific: effects on enzyme activity inhibition and starch digestion. Plant Foods Hum Nutr. 2019;74(4): 544-552. DOI: 10.1007/s11130-019-00760-8.

Adefegha SA, Oboh G. In vitro inhibition activity of polyphenol-rich extracts from Syzygium aromaticum (L.) Merr. & Perry (Clove) buds against carbohydrate hydrolyzing enzymes linked to type 2 diabetes and Fe2+-induced lipid peroxidation in rat pancreas. Asian Pac J Trop Biomed. 2012;2(10):774-781. DOI: 10.1016/S2221-1691(12)60228-7.

Lee SY, Mediani A, Ismail IS, Maulidiani, Abas F. Antioxidants and α-glucosidase inhibitors from Neptunia oleracea fractions using 1H NMR-based metabolomics approach and UHPLC-MS/MS analysis. BMC Complement Altern Med. 2019;19(1):7,1-15. DOI: 10.1186/s12906-018-2413-4.

Schober P, Boer C, Schwarte LA. Correlation coefficients: : appropriate use and interpretation. Anesth Analg. 2018;126(5):1763-1768. DOI: 10.1213/ane.0000000000002864.

Rice-Evans C, Miller N, Paganga G. Antioxidant properties of phenolic compounds. Trends Plant Sci. 1997;2(4):152-159.

DOI: 10.1016/S1360-1385(97)01018-2.

Zeb A. Concept, mechanism, and applications of phenolic antioxidants in foods. J Food Biochem. 2020;44(9):e13394,1-22. DOI: 10.1111/jfbc.13394.

Kumaran A, Karunakaran RJ. In vitro antioxidant activities of methanol extracts of five Phyllanthus species from India. LWT Food Sci Technol. 2007;40(2):344-352. DOI: 10.1016/j.lwt.2005.09.011.

Muflihah YM, Gollavelli G, Ling YC. Correlation study of antioxidant activity with phenolic and flavonoid compounds in 12 Indonesian indigenous herbs. Antioxidants (Basel). 2021;10(10): 1530,1-15. DOI: 10.3390/antiox10101530.

Yu L, Haley S, Perret J, Harris M, Wilson J, Qian M. Free radical scavenging properties of wheat extracts. J Agric Food Chem. 2002;50(6):1619-1624. DOI: 10.1021/jf010964p.

Jo SH, Ka E, Lee H, Apostolidis E, Jang HD, Kwon Y. Comparison of antioxidant potential and rat intestinal a-glucosidases inhibitory activities of quercetin, rutin, and isoquercetin. International Int J Appl Res Nat Prod. 2009;2:52-60.

Li YQ, Zhou FC, Gao F, Bian JS, Shan F. Comparative evaluation of quercetin, isoquercetin and rutin as inhibitors of alpha-glucosidase. J Agric Food Chem. 2009;57(24):11463-11468. DOI: 10.1021/jf903083h.

Adewole SO, Caxton-Martins EA, Ojewole JAO. Protective effect of quercetin on the morphology of pancreatic β-cells of streptozotocin-treated diabetic rats. Afr J Tradit Complement Altern Med. 2006;4(1):64-74. DOI: 10.4314/ajtcam.v4i1.31196.

Ayuraved-Wittayarai Foundation. Thai Traditional Medicine Textbook (Paet-Saat-Song-Kror). Vol. 1, 1st edition. Ministry of Public Health: Thailand. 1998.

Paswan VK, Singh CS, Kukreja G, Bunkar DS, Bhinchhar BK. Health benefits and functional and medicinal properties of some common Indian spices. In: Ahmad RS. Herbs and Spices-New Processing Technologies. 2021. pp. 1-18.DOI: 10.5772/intechopen.98676.

Jayaprakasha GK, Rao LJM. Chemistry, biogenesis, and biological activities of Cinnamomum zeylanicum. Crit Rev Food Sci Nutr. 2011;51(6):547-562. DOI: 10.1080/10408391003699550.

Salehi P, Asghar B, Esmaeili MA, Deghan H, Ghazi I. α-Glucosidase and α-amylase inhibitory effect and antioxidant activity of ten plant extracts traditionally used in Iran for diabetes. J Med Plants Res. 2013;7(6):257-266. DOI: 10.5897/JMPR11.1320.


Refbacks

  • There are currently no refbacks.


Creative Commons LicenseThis work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License which allows users to read, copy, distribute and make derivative works for non-commercial purposes from the material, as long as the author of the original work is cited properly.