Antioxidant Properties of Stingless Bee Honey and Its Effect on the Viability of Lymphoblastoid Cell Line
Two Approaches of Simulated Central Vein Cannulation
Vol. 14 No. 1 : 2019 (91-105)
Abstract
Research on the medical benefit of stingless bee honey (kelulut honey) is rather new although it has been used as traditional food and additive for ages. The primary objective of our study was to evaluate the antioxidant properties of kelulut honey and its effect on lymphoblastoid cell line. We analysed the antioxidant properties of kelulut honey by ferric reducing antioxidant potential assay, total phenolic and flavonoid contents using UV spectrophotometry. The total phenolic content, total flavonoid content and ferric reducing antioxidant potential of Malaysian kelulut honey produced by Trigona spp. were found to be 844.45 mg RE/kg honey, 78.29 mg RE/kg honey and 1132.66 mM FE/kg honey, respectively. Our findings showed a strong correlation between total phenolics and flavanoids contents with its antioxidant potential at R2 = 0.920 and R2 = 0.951, respectively. The effect of honey on cell viability of lymphoblastoid cell line (LCL) was also investigated. The cells were cultured in RPMI-1640 medium supplemented with 0 - 500 μg/mL of kelulut honey for 24 hours. Cell viability was quantitated using 3-(4,5-dimethylthiazol-2-yl)-5-(3-carboxymethoxyphenyl)-2-(4-sulfophenyl)-2H-tetrazolium, MTS assay showed that honey supplementation boosted the viability of LCL up to 164.64% (p< 0.01). The significant increase in cell viability might be modulated by the antioxidant properties of kelulut honey.
Keywords :
Antioxidant,
flavonoid,
kelulut honey,
lymphoblastoid cell line,
phenolic,
stingless bee,
Correspondance Address
Norwahidah Abdul Karim. Department of Biochemistry, Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Centre, Jalan Yaacob Latif, Bandar Tun Razak, 56000 Cheras, Kuala Lumpur, Malaysia. Tel: +603-91459555 Email: wahida2609@gmail.com
References
A-Rahaman, N.L., Chua, L.S., Sarmidi, M.R., Aziz, R. 2013. Physicochemical and radical scavenging activities of honey samples from Malaysia. Agricultural Sciences 4: 46-51.
Abd Jalil, M.A., Kasmuri, A.R., Hadi, H. 2017. Stingless bee honey, the natural wound healer: a review. Skin Pharmacol Physiol 30(2): 66-75.
Abdullah, B., Lazim, N.M., Salim, R. 2015. The effectiveness of Tualang honey in reducing post-tonsillectomy pain. Kulak Burun Bogaz Ihtis Derg 25(3): 137-43.
Adekoya, A.A., Ahmad, S., Maziah, M. 2016. Assessment of total phenolic compounds and in vitro free radical scavenging potentials of water extracts of ten selected species of Zingiberaceae rhizomes use in folkloric medicine. Pak J Pharm Sci 29(3): 979-84.
Afanas’ev, I.B., Dorozhko, A.I., Brodskii, A.V., Kostyuk, V.A., Potapovitch, A.I. 1989. Chelating and free radical scavenging mechanisms of inhibitory action of rutin and quercetin in lipid peroxidation. Biochem Pharmacol 38(11): 1763-9.
Al-Mamary, M., Al-Meeri, A., Al-Habori, M. 2002. Antioxidant activities and total phenolics of different types of honey. Nutr Res 22(9): 1041-7.
Al-Rahbi, B., Zakaria, R., Othman, Z., Hassan, A., Mohd Ismail, Z.I., Muthuraju, S. 2014. Tualang honey supplement improves memory performance and hippocampal morphology in stressed ovariectomized rats. Acta Histochem 116(1): 79-88.
Aziz, C.B., Ismail, C.A., Hussin, C.M., Mohamed, M. 2014. The antinociceptive effects of tualang honey in male sprague-dawley rats: a preliminary study. J Tradit Complement Med 4(4): 298-302.
Baba, S.A., Malik, S.A. 2015. Determination of total phenolic and flavonoid content, antimicrobial and antioxidant activity of a root extract of Arisaema jacquemontii Blume. J Taibah Univ Sci 9(4): 449-54.
Benzie, I.F., Strain, J.J. 1996. The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1): 70-6.
Beretta, G., Granata, P., Ferrero, M., Orioli, M., Maffei Facino, R. 2005. Standardization of antioxidant properties of honey by a combination of spectrophotometric/fluorimetric assays and chemometrics. Anal Chim Acta 533(2): 185-91.
Beretta, G., Orioli, M., Facino, R. M. 2007. Antioxidant and radical scavenging activity of honey in endothelial cell cultures (EA.hy926). Planta Med 73(11): 1182-9.
Bertoncelj, J., Doberšek, U., Jamnik, M., Golob, T. 2007. Evaluation of the phenolic content, antioxidant activity and colour of Slovenian honey. Food Chem 105(2): 822-8.
Bogdanov, S., Jurendic, T., Sieber, R., Gallmann, P. 2008. Honey for nutrition and health: a review. J Am Coll Nutr 27(6): 677-89.
Breen, M.S., White, C.H., Shekhtman, T., Lin, K., Looney, D., Woelk, C.H., Kelsoe, J.R. 2016. Lithium-responsive genes and gene networks in bipolar disorder patient-derived lymphoblastoid cell lines. Pharmacogenomics J 16(5): 446-53.
Budin, S.B., Jubaidi, F.F., Mohd Noor Azam, S.N.F., Mohamed Yusof, N.L., Taib, I.S., Mohameda, J. 2017. Kelulut honey supplementation prevents sperm and testicular oxidative damage in streptozotocin-induced diabetic rats. Diagnostic & Applied Health Sciences 79(3): 89-95.
Chang, C.C., Yang, M.H., Wen, H.M., Chern, J.C. 2002. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal 10(3): 178-82.
Chua, L.S., Rahaman, N.L., Adnan, N.A., Eddie Tan, T.T. 2013. Antioxidant Activity of Three Honey Samples in relation with Their Biochemical Components. J Anal Methods Chem 2013: 313798.
Cianciosi, D., Forbes-Hernández, Y.T., Afrin, S., Gasparrini, M., Reboredo-Rodriguez, P., Manna, P.P., Zhang, J., Bravo Lamas, L., Martínez Flórez, S., Agudo Toyos, P., Quiles, L.J., Giampieri, F., Battino, M. 2018. Phenolic compounds in honey and their associated health benefits: a review. Molecules 23(9): pii: E2322.
Delhalle, S., Deregowski, V., Benoit, V., Merville, M.P., Bours, V. 2002. NF-kappaB-dependent MnSOD expression protects adenocarcinoma cells from TNF-alpha-induced apoptosis. Oncogene 21(24): 3917-24.
Erejuwa, O.O., Sulaiman, S.A., Ab Wahab, M.S. 2012. Honey: a novel antioxidant. Molecules 17(4): 4400-23.
Fatima, I.J., Mohd Hilmi, A.B., Salwani, I., Lavaniya, M. 2018. Physicochemical characteristics of malaysian stingless bee honey from trigona species. IMJM 17: 187-91.
Ferreres, F., Andrade, P., Tomás-Barberán, F.A. 1994. Flavonoids from Portuguese heather honey. Z Lebensm Unters Frosch 199(1): 32-7.
Gheldof, N., Wang, X., Engeseth, N. 2002. Identification and quantification of antioxidant components of honeys from various floral sources. J Agric Food Chem 50(21): 5870-7.
Goon, J.A., Gunasekaran, G., Muhamad Fitri, C.A., Chandrashegkar, S., Hajar Amalnina, A.B., Raishan, S., Nurul Faiznani, Z., Ismail, N.A.S., Mohd Yusof, Y.A. 2017. Effects of gelam honey on oxidative stress in lung cancer cells. Med Health 12(2): 202-9.
Hassan, H., Abdul Karim, N. 2018. Honey as versatile remedy: a focus on selected honeys. Int J Food Nutr Sci 6(1): 1-6.
Hussain, T., Mulherkar, R. 2012. Lymphoblastoid Cell lines: a Continuous in Vitro Source of Cells to Study Carcinogen Sensitivity and DNA Repair. Int J Mol Cell Med 1(2): 75-87.
Isla, M.I., Craig, A., Ordoñez, R., Zampini, C., Sayago, J., Bedascarrasbure, E., Alvarez, A., Salomón, V., Maldonado, L. 2011. Physico chemical and bioactive properties of honeys from Northwestern Argentina. LWT Food Sci Technol 44(9): 1922-30.
Iurlina, M.O., Saiz, A.I., Fritz, R., Manrique, G.D. 2009. Major flavonoids of Argentinean honeys. Optimisation of the extraction method and analysis of their content in relationship to the geographical source of honeys. Food Chem 115(3): 1141-9.
Jubri, Z., Rahim, N.B., Aan, G.J. 2013. Manuka honey protects middle-aged rats from oxidative damage. Clinics 68(11): 1446-54.
Kassim, M., Achoui, M., Mustafa, M.R., Mohd, M.A., Yusoff, K.M. 2010. Ellagic acid, phenolic acids, and flavonoids in Malaysian honey extracts demonstrate in vitro anti-inflammatory activity. Nutr Res 30(9): 650-9.
Kek, S.P., Chin, N.L., Yusof, Y.A., Tan, S.W., Chua, L.S. 2014. Total phenolic contents and colour intensity of Malaysian honeys from the Apis spp. and Trigona spp. bees. Agric Agric Sci Procedia 2: 150-5.
Kharsa, B.E. 2017. Physiochemical and antioxidant properties of Malaysian Trigona and tualang bee honey. (Master of Health Sciences (Nutrition Sciences)), International Islamic University Malaysia.
Kishore, R.K., Halim, A.S., Syazana, M.S., Sirajudeen, K.N. 2011. Tualang honey has higher phenolic content and greater radical scavenging activity compared with other honey sources. Nutr Res 31(4): 322-5.
LeBlanc, J.G., Chain, F., Martín, R., Bermúdez-Humarán, L.G., Courau, S., Langella, P. 2017. Beneficial effects on host energy metabolism of short-chain fatty acids and vitamins produced by commensal and probiotic bacteria. Microb Cell Fact 16(1): 79.
Machado De-Melo, A.A., Almeida-Muradian, L. B.d., Sancho, M.T., Pascual-Maté, A. 2018. Composition and properties of Apis mellifera honey: A review. J Apic Res 57(1): 5-37.
Martinotti, S., Bucekova, M., Majtan, J., Ranzato, E. 2018. Honey: an effective regenerative medicine product in wound management. Curr Med Chem.
Martinotti, S., Ranzato, E. 2018. Honey, Wound Repair and Regenerative Medicine. J Funct Biomater 9(2): pii: E34.
Mohan, A., Quek, S.-Y., Gutierrez-Maddox, N., Gao, Y., Shu, Q. 2017. Effect of honey in improving the gut microbial balance. Food Qual Saf 1(2): 107-15.
Morrison, G., Lenkala, D., LaCroix, B., Ziliak, D., Abramson, V., Morrow, P. K., Forero, A., Van Poznak, C., Rugo, H.S., Nanda, R., O’Donnell, P.H., Huang, R.S. 2016. Utility of patient-derived lymphoblastoid cell lines as an ex vivo capecitabine sensitivity prediction model for breast cancer patients. Oncotarget 7(25): 38359-66.
Niu, N., Schaid, D.J., Abo, R.P., Kalari, K., Fridley, B. L., Feng, Q., Jenkins, G., Batzler, A., Brisbin, A. G., Cunningham, J.M., Li, L., Sun, Z., Yang, P., Wang, L. 2012. Genetic association with overall survival of taxane-treated lung cancer patients - a genome-wide association study in human lymphoblastoid cell lines followed by a clinical association study. BMC Cancer 12: 422.
Nordin, A., Omar, N., Sainik, N.Q.A.V., Chowdhury, S.R., Omar, E., Saim, A., Idrus, R. 2018. Low dose stingless bee honey increases viability of human dermal fibroblasts T that could potentially promote wound healing. Wound Medicine 23: 22-27.
Othman, Z., Shafin, N., Zakaria, R., Hussain, N. H., Mohammad, W.M. 2011. Improvement in immediate memory after 16 weeks of tualang honey (Agro Mas) supplement in healthy postmenopausal women. Menopause 18(11): 1219-24.
Pisoschi, A.M., Negulescu, G.P. 2011. Methods for total antioxidant activity determination: a review. Biochem Anal Biochem 1(106): 1-10.
Prior, R.L., Wu, X., Schaich, K. 2005. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53(10): 4290-302.
Putri Shuhaili, S., Haszianaliza, H., Muhammad Fairuz, A., Zar Chi, T. 2016. Gelam honey: a review of its antioxidant, anti-inflammatory, anticancer and wound healing aspects. Med Health 11(2): 105-16.
Ranneha, Y., Ali, F., Zareia, M., Md Akimb, A., Abd Hamid, H., Khazaai, H. 2018. Malaysian stingless bee and Tualang honeys: A comparative characterization of total antioxidant capacity and phenolic profile using liquid chromatography-mass spectrometry. LWT - Food Science and Technology 89: 1-9.
Sahhugi, Z., Hasenan, S.M., Jubri, Z. 2014. Protective effects of gelam honey against oxidative damage in young and aged rats. Oxid Med Cell Longev 2014: 673628.
Saiful Yazan, L., Muhamad Zali, M.F., Mohd Ali, R., Zainal, N.A., Esa, N., Sapuan, S., Ong, Y. S., Tor, Y. S., Gopalsamy, B., Voon, F. L., Syed Alwi, S.S. 2016. Chemopreventive properties and toxicity of Kelulut Honey in Sprague Dawley Rats induced with azoxymethane. Biomed Res Int 2016: 4036926.
Sawazaki, T., Nakajima, Y., Urai, T., Mukai, K., Ohta, M., Kato, I., Kawaguchi, A., Kinoshita, Y., Kumagai, Y., Sakashita, A., Yamazaki, A., Nakatani, T. 2018. Efficacy of Honeydew Honey and Blossom Honey on Full-thickness Wound Healing in Mice. Wounds 30(7): 197-204.
Sie, L., Loong, S., Tan, E.K. 2009. Utility of lymphoblastoid cell lines. J Neurosci Res 87(9): 1953-9.
Singleton, V.L., Orthofer, R., Lamuela-Raventós, R. M. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299: 152-78.
Stagos, D., Soulitsiotis, N., Tsadila, C., Papaeconomou, S., Arvanitis, C., Ntontos, A., Karkanta, F., Adamou-Androulaki, S., Petrotos, K., Spandidos, D.A., Kouretas, D., Mossialos, D. 2018. Antibacterial and antioxidant activity of different types of honey derived from Mount Olympus in Greece. Int J Mol Med 42(2): 726-34.
Yazan, L.S., Zainal., N.A., Ali, R.M., Zali, M.F.S.M., Ong, Y.S., Tor, Y.S., Gopalsamy, B., Ling, V.F., Sapuan, S., Esa, N., Haron, A.S., Ansar, F.H.Z., Mokhtar, A.M.A. and Alwi, S.S.S, 2018. Antiulcer properties of kelulut honey against ethanol-induced gastric ulcer. Pertanika J Sci Technol 26(1): 121-32.
Zainol, M.I., Mohd Yusoff, K., Mohd Yusof, M. Y. 2013. Antibacterial activity of selected Malaysian honey. BMC Complement Altern Med 13: 129.
Zivkovic, L., Bajic, V., Dekanski, D., Cabarkapa-Pirkovic, A., Giampieri, F., Gasparrini, M., Mazzoni, L., Potparevic, B. S. 2018. Manuka honey attenuates oxidative damage induced by H2O2 in human whole blood in vitro. Food Chem Toxicol 119: 61-5.
