Sains Malaysiana 47(12)(2018): 3069–3075
http://dx.doi.org/10.17576/jsm-2018-4712-17
Antioxidant Activity of Pitcher Extracts
from Three Nepenthes Species
(Aktiviti Antioksidan Ekstrak Kendi bagi Tiga Spesis
Nepenthes)
MUHAMMAD
AQIL FITRI ROSLI, KAMALRUL AZLAN AZIZAN & HOE-HAN GOH*
Metabolomics Research Laboratory, Institute
of Systems Biology (INBIOSIS), Universiti Kebangsaan Malaysia, 43600 UKM Bangi,
Selangor Darul Ehsan, Malaysia
Diserahkan: 14 September 2018 /Diterima:
19 September 2018
ABSTRACT
Nepenthes, locally known as 'periuk
kera' in Malaysia, is a fascinating species due to uniqueness
in their morphology in having pitcher organ for carnivorous diet.
The pitcher plant has been used for cooking traditional delicacies
and as traditional remedies to treat illness. Hence, this species
might possess beneficial health properties. This study aimed to
compare the antioxidant activity of the pitcher extracts from
Nepenthes ampullaria, Nepenthes rafflesiana and
their hybrid, Nepenthes × hookeriana. The samples
were extracted using methanol:chloroform:water (3:1:1) via sonication
assisted extraction and the extracts were subjected to three different
antioxidant assays, namely 2,2-diphenyl-1-picrylhydrazyl (DPPH), ferric reducing power (FRAP)
and total phenolic content (TPC). Extract from N. ampullaria
exhibited the strongest radical scavenging activity (0.148
± 0.04 mg/mL) with the highest ferric reducing power (0.009
± 0.003 mg GA/mg dry weight) among the three species, whereas
that of N. rafflesiana possessed the highest phenolic content
(0.057 ± 0.017 mg GA/mg
dry weight). However, the antioxidant capacities of the pitcher
extracts were not significantly different (p>0.05) between
the three species and were much lower than the gallic acid as
a standard reference.
Keywords: Antioxidants activity; DPPH
assay; ferric reducing power assay; Nepenthes sp.;
total phenolic content
ABSTRAK
Nepenthes, lebih dikenali sebagai
'periuk kera' di Malaysia merupakan suatu spesies yang menakjubkan
kerana keunikan morfologinya dalam mempunyai organ seperti kendi
untuk diet karnivor. Tumbuhan berkendi ini telah digunakan dalam
masakan tradisi dan juga sebagai ubat-ubatan tradisi untuk merawat
penyakit. Oleh itu, spesies ini mungkin memiliki kandungan yang
bermanfaat untuk kesihatan. Kajian ini bertujuan untuk membandingkan
aktiviti antioksidan ekstrak kendi daripada Nepenthes ampullaria,
Nepenthes rafflesiana dan hibrid mereka, Nepenthes
× hookeriana. Setiap sampel telah diekstrak dengan menggunakan
metanol:kloroform:air (3:1:1) melalui pengekstrakan dengan bantuan
sonikasi dan telah diasai dengan tiga asai antioksidan yang berbeza,
iaitu 2,2-diphenyl-1-picrylhydrazyl (DPPH), kuasa penurunan ferik (FRAP)
dan jumlah kandungan fenolik (TPC). Ekstrak daripada N.
ampullaria menunjukkan aktiviti pelupusan radikal yang terkuat
(0.148 ± 0.04 mg/mL) dan mempunyai kuasa penurunan ferik
yang tertinggi (0.009 ± 0.003 mg GA/mg
berat kering) antara ketiga-tiga spesies ini, namun begitu N.
rafflesiana mempunyai kandungan fenolik yang tertinggi (0.057
± 0.017 mg GA/mg berat kering). Walau bagaimanapun, tiada
perbezaan signifikan terhadap kebolehan antioksidan ekstrak kendi
daripada tiga spesies yang dikaji dan ternyata jauh lebih rendah
daripada asid galik yang merupakan piawai rujukan dalam kajian
ini.
Kata
kunci: Aktiviti antioksidan; asai DPPH; asai jumlah
kandungan fenolik; asai kuasa penurunan ferik; Nepenthes sp.
RUJUKAN
Adam, J.H. & Hamid,
H.A. 2007. Pitcher plants (Nepenthes) recorded from Universiti Kebangsaan
Malaysia, Bangi, Selangor, Malaysia. International Journal of Botany 3(1):
71-77.
Adhikari, S., Joshi, R.,
Patro, B., Ghanty, T., Chintalwar, G., Sharma, A., Chattopadhyay, S. &
Mukherjee, T. 2003. Antioxidant activity of bakuchiol: Experimental evidences
and theoretical treatments on the possible involvement of the terpenoid chain. Chemical
Research in Toxicology 16(9): 1062-1069.
Ahmad, R., Baharum,
S.N., Bunawan, H., Lee, M., Mohd Noor, N., Rohani, E.R., Ilias, N. & Zin,
N.M. 2014. Volatile profiling of aromatic traditional medicinal plant, Polygonum
minus in different tissues and its biological activities. Molecules 19(11):
19220-19242.
Ainsworth, E.A. &
Gillespie, K.M. 2007. Estimation of total phenolic content and other oxidation
substrates in plant tissues using Folin–Ciocalteu reagent. Nature
Protocols 2(4): 875-877.
Aung, H., Chia, L., Goh,
N., Chia, T., Ahmed, A., Pare, P. & Mabry, T. 2002. Phenolic constituents
from the leaves of the carnivorous plant Nepenthes gracilis. Fitoterapia 73(5):
445-447.
Azlim Almey, A.A., Ahmed
Jalal Khan, C., Syed Zahir, I., Mustapha Suleiman, K., Aisyah,
M.R. & Kamarul Rahim, K. 2010. Total phenolic content and
primary antioxidant activity of methanolic and ethanolic extracts
of aromatic plants' leaves. International Food Research Journal
17(4): 7.
Barros, L., Ferreira,
M.J., Queiros, B., Ferreira, I.C. & Baptista, P. 2007. Total phenols,
ascorbic acid, β-carotene and lycopene in Portuguese wild edible mushrooms
and their antioxidant activities. Food Chemistry 103(2): 413-419.
Carocho, M. &
Ferreira, I.C. 2013. A review on antioxidants, prooxidants and related
controversy: Natural and synthetic compounds, screening and analysis
methodologies and future perspectives. Food and Chemical Toxicology 51:
15-25.
Clarke, G., Ting, K.N.,
Wiart, C. & Fry, J. 2013. High correlation of 2, 2-diphenyl-1-picrylhydrazyl
(DPPH) radical scavenging, ferric reducing activity potential and total
phenolics content indicates redundancy in use of all three assays to screen for
antioxidant activity of extracts of plants from the Malaysian rainforest. Antioxidants 2(1): 1-10.
Diplock, A., Charuleux,
J.L., Crozier-Willi, G., Kok, F., Rice- Evans, C., Roberfroid, M., Stahl, W.
& Vina-Ribes, J. 1998. Functional food science and defence against reactive
oxidative species. British Journal of Nutrition 80(1): 77-112.
Goh, H.H., Khairudin,
K., Sukiran, N.A., Normah, M.N. & Baharum, S.N. 2016. Metabolite profiling
reveals temperature effects on the VOCs and flavonoids of different plant
populations. Plant Biology 18: 130-139.
Grassmann, J. 2005.
Terpenoids as plant antioxidants. Vitamins & Hormones 72: 505-535.
Huda-Faujan, N.,
Noriham, A., Norrakiah, A. & Babji, A.S. 2009. Antioxidant activity of
plants methanolic extracts containing phenolic compounds. African Journal of
Biotechnology 8(3): 484-489.
Ismail, N., Kamariah,
A., Lim, L. & Ahmad, N. 2015. Phytochemical and pharmacological evaluation
of methanolic extracts of the leaves of Nepenthes bicalcarata Hook. f. International
Journal of Pharmacognosy and Phytochemical Research 7(6): 1127-1138.
Khalaf, N.A., Shakya,
A.K., Al-Othman, A., El-Agbar, Z. & Farah, H. 2008. Antioxidant activity of
some common plants. Turkish Journal of Biology 32(1): 51-55.
Kliebenstein, D. 2004.
Secondary metabolites and plant/ environment interactions: A view through Arabidopsis
thaliana tinged glasses. Plant, Cell & Environment 27(6):
675-684.
Kopjar, M.,
Lončarić, A. & Pichler, A. 2016. Synergistic effect of sugars and
phenolics on antioxidant activity of pomegranate juice. IFT 13, Annual
meeting and Food expo, hlm. 1.utg.
Kuda, T. & Yano, T.
2009. Changes of radical-scavenging capacity and ferrous reducing power in chub
mackerel Scomber japonicus and Pacific saury Cololabis saira during
4°C storage and retorting. LWT-Food Science and Technology 42(6):
1070-1075.
Lätti, A.K., Riihinen, K.R. &
Jaakola, L. 2011. Phenolic compounds in berries and flowers of a natural hybrid
between bilberry and lingonberry (Vaccinium × intermedium Ruthe). Phytochemistry 72(8): 810-815.
Likhitwitayawuid, K., Kaewamatawong, R.,
Ruangrungsi, N. & Krungkrai, J. 1998. Antimalarial naphthoquinones from Nepenthes
thorelii. Planta Medica 64(03): 237-241.
Maisuthisakul, P., Suttajit, M. &
Pongsawatmanit, R. 2007. Assessment of phenolic content and free
radical-scavenging capacity of some Thai indigenous plants. Food Chemistry 100(4):
1409-1418.
Mehta, S.K. & Gowder, S.J.T. 2015.
Members of antioxidant machinery and their functions. In Basic Principles
and Clinical Significance of Oxidative Stress, edited by Gowder, S.J.T.
IntechOpen. DOI: 10.5772/6188.
Moran, J.A., Hawkins, B.J., Gowen, B.E.
& Robbins, S.L. 2010. Ion fluxes across the pitcher walls of three Bornean
Nepenthes pitcher plant species: Flux rates and gland distribution patterns
reflect nitrogen sequestration strategies. Journal of Experimental Botany 61(5):
1365-1374.
Onoja, S.O., Omeh, Y.N., Ezeja, M.I.
& Chukwu, M.N. 2014. Evaluation of the in vitro and in vivo antioxidant
potentials of Aframomum melegueta methanolic seed extract. Journal of
Tropical Medicine 2014: 159-343.
Öztürk, M. 2012. Anticholinesterase and
antioxidant activities of savoury (Satureja thymbra L.) with identified
major terpenes of the essential oil. Food Chemistry 134(1): 48-54.
Patel, V.R., Patel, P.R. & Kajal,
S.S. 2010. Antioxidant activity of some selected medicinal plants in western
region of India. Advances in Biological Research 4(1): 23-26.
Reddy, A. & Grace, J.R. 2016. In
vitro evaluation of antioxidant activity of methanolic extracts of selected
mangrove plants. Medicinal and Aromatic Plants 5(3): 250-255.
Rosli, M.A.F., Azizan, K.A., Baharum,
S.N. & Goh, H.H. 2017. Mass spectrometry data of metabolomics analysis of
Nepenthes pitchers. Data in Brief 14: 295-297.
Sampaio, B.L., Edrada-Ebel, R. & Da
Costa, F.B. 2016. Effect of the environment on the secondary metabolic profile
of Tithonia diversifolia: A model for environmental metabolomics of
plants. Scientific Reports 6: 29265.
Sanusi, S.B., Bakar, M.F.A., Mohamed, M.,
Sabran, S.F. & Mainasara, M.M. 2017. Ethnobotanical, phytochemical, and
pharmacological properties of Nepenthes species: A review. Asian Journal of
Pharmaceutical and Clinical Research 10(11): 16-19.
Schwallier, R., De Boer, H.J., Visser,
N., Van Vugt, R.R. & Gravendeel, B. 2015. Traps as treats: A traditional
sticky rice snack persisting in rapidly changing Asian kitchens. Journal of
Ethnobiology and Ethnomedicine 11(24): 1-9.
Shian, T.E. & Abdullah, A. 2012.
Antioxidant properties of three banana cultivars (Musa acuminata ‘Berangan’,‘Mas’
and ‘Raja’) extracts. Sains Malaysiana 41(3): 319-324.
Shil, D., Mohanty, J., Das, T., Bhuyan,
N., Uriah, T. & Saleem, T. 2010. Protective role of pitcher of Nepenthes
khasiana Hook against dexamethazone induced hyperlipidemia and insulin
resistance in rats. International Journal of Research in Pharmaceutical
Science 1(2): 195-198.
Shin, K.S., Lee, S.K. & Cha, B.J.
2007. Antifungal activity of plumbagin purified from leaves of Nepenthes
ventricosa × maxima against phytopathogenic fungi. The
Plant Pathology Journal 23(2): 113-115.
Thao, N.P., Luyen, B.T.T., Koo, J.E.,
Kim, S., Koh, Y.S., Thanh, N.V., Cuong, N.X., Kiem, P. V., Minh, C.V. &
Kim, Y.H. 2016. In vitro anti-inflammatory components isolated from the
carnivorous plant Nepenthes mirabilis (Lour.) Rafarin. Pharmaceutical
Biology 54(4): 588-594.
Van Thanh, N., Thao, N.P., Huong, P.T.T.,
Lee, S.H., Jang, H.D., Cuong, N.X., Nam, N.H., Van Kiem, P., Kim, Y.H. &
Van Minh, C. 2015. Naphthoquinone and flavonoid constituents from the
carnivorous plant Nepenthes mirabilis and their anti-osteoporotic and
antioxidant activities. Phytochemistry Letters 11: 254-259.
Van Thanh, N., Thao, N.P., Huong, P.T.T.,
Lee, S.H., Jang, H.D., Cuong, N.X., Nam, N.H., Van Kiem, P., Van Minh, C. &
Kim, Y.H. 2015. Two new naphthalene glucosides and other bioactive compounds
from the carnivorous plant Nepenthes mirabilis. Archives of Pharmacal
Research 38(10): 1774- 1782.
Wang, L., Zhou, Q., Zheng, Y. & Xu,
S. 2009. Composite structure and properties of the pitcher surface of the
carnivorous plant Nepenthes and its influence on the insect attachment
system. Progress in Natural Science 19(12): 1657-1664.
Yehye, W.A., Rahman, N.A., Ariffin, A.,
Abd Hamid, S.B., Alhadi, A.A., Kadir, F.A. & Yaeghoobi, M. 2015.
Understanding the chemistry behind the antioxidant activities of butylated
hydroxytoluene (BHT): A review. European Journal of Medicinal Chemistry 101:
295-312.
Zulkefli, H.N., Mohamad, J. & Abidin,
N.Z. 2013. Antioxidant activity of methanol extract of Tinospora crispa and Tabernaemontana corymbosa. Sains Malaysiana 42(6): 697-706.
*Pengarang untuk
surat-menyurat; email: gohhh@ukm.edu.my