Antioxidant and α-Glucosidase Inhibitory Activities ... - ACS Publications

Sep 8, 2014 - Although Malaysia is blessed with a diverse tropical fruit heritage, only a small percentage of its native fruit trees are commercially ...
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Antioxidant and α‑Glucosidase Inhibitory Activities of 40 Tropical Juices from Malaysia and Identification of Phenolics from the Bioactive Fruit Juices of Barringtonia racemosa and Phyllanthus acidus Shaida Fariza Sulaiman* and Kheng Leong Ooi School of Biological Sciences, Universiti Sains Malaysia, 11800 USM Pulau Pinang, Malaysia ABSTRACT: The present study compared pH, total soluble solids, vitamin C, and total phenolic contents, antioxidant activities, and α-glucosidase inhibitory activities of 40 fresh juices. The juice of Baccaurea polyneura showed the highest yield (74.17 ± 1.44%) and total soluble solids (32.83 ± 0.27 °Brix). The highest and lowest pH values were respectively measured from the juices of Dimocarpus longan (6.87 ± 0.01) and Averrhoa bilimbi (1.67 ± 0.67). The juice of Psidium guajava gave the highest total phenolic (857.24 ± 12.65 μg GAE/g sample) and vitamin C contents (590.31 ± 7.44 μg AAE/g sample). The juice of Phyllanthus acidus with moderate contents of total phenolics and vitamin C was found to exhibit the greatest scavenging (613.71 ± 2.59 μg VCEAC/g sample), reducing (2784.89 ± 3.93 μg TEAC/g sample), and α-glucosidase inhibitory activities (95.37 ± 0.15%). The juice of Barringtonia racemosa was ranked second in the activities and total phenolic content. Gallic and ellagic acids, which were quantified as the major phenolics of the respective juices, are suggested to be the main contributors to the antioxidant activities. The α-glucosidase inhibitory activity of the juices could be derived from myricetin and quercetin (that were previously reported as potent α-glucosidase inhibitors) in the hydrolyzed juice extracts. The juice of Syzygium samarangense, which was found to be highest in metal chelating activity (82.28 ± 0.10%), also was found to have these phenolics. KEYWORDS: juice, phenolics, vitamin C, antioxidant activity, α-glucosidase inhibitory activity, Barringtonia racemosa, Phyllanthus acidus

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and diabetic.2 Fresh juices are a rich source of vitamin C and phenolics. Among the classes of phenolics reported in various fresh fruit juices are flavonols, flavanones, hydroxycinnamic acids, and phenolic acids.3 These compounds (either synergistically or individually) were reported to play a major role as antioxidants and α-glucosidase inhibitors.4 To date, many comparative antioxidant evaluations on wild, rare, exotic, indigenous, underutilized, and commonly consumed tropical fruits from different regions including Malaysia have been documented.5−12 Various solvents were used to extract antioxidants from the fruits such as 70% acetone,5 50% ethanol,7 and 80% methanol.8,12 The fruits were also sequentially extracted with 50% methanol and 70% acetone to increase the recovery of antioxidants.10 However, to our knowledge no comparative report is available on the antioxidant activity as well as vitamin C and total phenolic contents of the tropical fresh juices used in this study. This information is important for the public to rank the antioxidant capacity of the juices. Therefore, this study is the first to comparatively measure the antioxidant activities of the juices. Consumption of some antioxidant-rich fruits and vegetables also was reported to induce postprandial hyperglycemia.13 It is therefore crucial to identify juices that possess antioxidant activities with no adverse effect on blood glucose level.

INTRODUCTION Although Malaysia is blessed with a diverse tropical fruit heritage, only a small percentage of its native fruit trees are commercially cultivated for both domestic and export markets. The well-known examples are Durio zibethinus (durian), Nephelium lappaceum (rambutan), Garcinia mangostana (manggis), and Lansium domesticum (dokong). Two main constraints restricting further expansion of our local fruit industries are that (1) most of these fruits are seasonal and (2) they are categorized into climacteric type, with a short shelf life. The majority of large-scale fruit plantations in Malaysia are allocated to nonseasonal tropical fruits that are not native to our region, particularly Psidium guajava (guava), Carica papaya (papaya), Musa acuminata (banana), and Ananas comosus (pineapple). There are also many rare fruit species that are found wild in our forests. Among the rare fruits that are endemic and native to Malaysia are Cynometra cauliflora (nam nam), Syzygium malaccense (jambu bol), Bouea macrophylla (remia), and Baccaurea polyneura (jentik) (Table 1).1 Fresh juices are obtained from succulent plant parts, mostly from the fruit parts. Commercially available processed fruit juices are mainly produced from temperate fruits such as apple and orange and several tropical fruits such as Psidium guajava (guava), Mangifera indica (mango), and Ananas comosus (pineapple). However, fresh juices are more preferred by health-conscious consumers. They are generally consumed for their cooling, refreshing, detoxifying, and diuretic properties. Some of these juices are used as therapeutic remedies to reduce blood cholesterol level as well as to treat dysentery, diarrhea, © XXXX American Chemical Society

Received: June 19, 2014 Revised: September 5, 2014 Accepted: September 8, 2014

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Table 1. Juices Used in This Study scientific name Averrhoa bilimbi Averrhoa carambola cv. B10 Barringtonia racemosa Cynometra cauliflora Garcinia atroviridis Myristica f ragrans Phyllanthus acidus Psidium guajava cv. GU8 Sandoricum koetjape Spondias pinnata Syzygium malaccense Syzygium samarangense Zizyphus mauritiana Bouea macrophylla Carica papaya cv. Batu Arang Citrullus lanatus cv. New Dragon Citrus aurantifolia Citrus maxima cv. PO52 Citrus microcarpa Cucumis melo cv. Inodorus Mangifera indica cv. Malgoa

common name

local name

scientific name

status

Mature Flesh bilimbi belimbing buluh star fruit belimbing segi hippo apple putat nam nam nam nam, katak puru Malabar gelugor tamarind nutmeg pala Indian cermai gooseberry guava jambu batu santol, sentul kechapi wild mango, kedondong, hog plum amra Malay apple jambu susu, jambu bol wax apple jambu semarang Indian jujube bidara Ripe Flesh gandaria kundang, remia papaya betik

native and endemic introduced

watermelon

tembikai

introduced

lime pommelo calamansi melon mango

limau nipis limau bali limau kasturi honeydew mangga

native native native introduced native

Manilkara zapota cv. CM19 (mega) Musa acuminata cv. Mas

native native native native and endemic native

Annona muricata Annona squamosa Artocarpus heterophyllus cv. J33 (tekam yellow) Baccaurea montleyana Baccaurea polyneura

native native introduced native

Dimocarpus longan cv. Edaw Garcinia mangostana Lansium domesticum Nephelium lappaceum cv. R191 (Anak sekolah) Nephelium ramboutan-ake Salacca edulis cv. Z6 (Raja) Sandoricum koetjape

native native and endemic native introduced

Cocos nucifera cv. Pandan wangi Ananas comosus cv. Moris Apium graveolens Saccharum off icinarum Daucus carota

common name Ripe Flesh sapodilla

local name

status

ciku

introduced

pisang

native

durian belanda nona

introduced

nangka

native

rambai jentik

rambai jentik

longan mangosteen dokong rambutan

mata kucing manggis dokong rambutan

native native and endemic introduced native native native

banana Ripe Aril sour sop sugar-apple, sweetsop jackfruit

pulasan pulasan snake fruit salak santol, sentul kechapi Young Endosperm coconut kelapa Ripe Peduncle pineapple Stem celery sugar cane Root carrot

introduced

native native native

introduced

nenas

introduced

saleri tebu

introduced introduced

lobak merah

introduced

search indicated that, to date, there have only been four reports on the α-glucosidase inhibitory activity of 10 fruits selected for this study, which are 99.5% ethanol extracts of dried mature fleshes of Phyllanthus acidus (Indian gooseberry), Spondias pinnata (hog plum), Zizyphus mauritiana (Indian jujube), and Manilkara zapota (sapodilla) and Artocarpus heterophyllus (jackfruit);19 70% methanol extracts of lyophilized ripe fleshes of Averrhoa carambola (star fruit) and Annona muricata (sour sop);15 aqueous extracts of fresh ripe fleshes of Averrhoa carambola, Phyllanthus acidus, Spondias pinnata, Zizyphus mauritiana, Manilkara zapota, Annona squamosa (sugar-apple), and Dimocarpus longan (longan);20 and 70% methanol extract of lyophilized ripe flesh of Carica papaya (papaya).17 Different extraction solvents and sample matrices were used in these studies. The aims of the present study were to comparatively analyze the total phenolic contents and vitamin C as well as antioxidant and α-glucosidase inhibitory activities of 40 fresh and pure juices from juicy and fleshy fruit parts, stems, and roots that are commonly consumed in Malaysia. The results were correlated with each other, and the unknown phenolic compounds in the juices with higher activities were identified.

Elevation of blood sugar level (hyperglycemia) can be minimized to normal (euglycemia) by inhibiting the carbohydrate-digesting enzymes such as α-glucosidase. α-Glucosidase is known to catalyze the final step in the digestion of carbohydrate to absorbable monosaccharides. Thus, in this study the juices were also screened for their α-glucosidase inhibitory activity to determine their antihyperglycemic effect. Due to the doselimiting side effects of oral antihyperglycemic drugs, we hypothesized that consumption of the antioxidant-rich juices with α-glucosidase inhibitory activity prior to a meal is a safer and appropriate alternative for the treatment of hyperglycemia. On the basis of the published data from various comparative studies of phenolic-rich extracts from fruits, several tropical fruits were proven to be effective against α-glucosidase, such as Pouteria lucuma (lucuma), a native Peruvian fruit;14 Campomanesia phaea (cambuci) and Eugenia dysenterica (cagaita), which are native to Brazil;15 Eugenia uniflora (pinanga), which is native to tropical America;16 and Aristotelia chilensis (maqui), a Latin-American fruit.17 However, all of these fruits are not found in Malaysia, and no earlier study on α-glucosidase inhibitory activity of tropical juices had been reported. To the best of our knowledge, there was only one comparative study that had determined the α-glucosidase inhibitory activity of five juice samples from fruits and vegetables that are commonly consumed in Korea.18 However, the highest percentage of inhibition, 30.4% (indicated by the juice from lotus root), was considered very low. Our literature

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MATERIALS AND METHODS

Plant Materials. Table 1 shows a list of 40 juices that were used in this study. For several fruit crops, the information about the cultivars or clones used were also included in Table 1. The juicy parts at their B

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Table 2. Yield of Juice from 20 g of Sample, pH Values, and Total Soluble Solidsa scientific name Averrhoa bilimbi Averrhoa carambola Barringtonia racemosa Cynometra cauliflora Garcinia atroviridis Myristica f ragrans Phyllanthus acidus Psidium guajava Sandoricum koetjape Spondias pinnata Syzygium malaccense Syzygium samarangense Zizyphus mauritiana Bouea macrophylla Carica papaya Citrullus lanatus Citrus aurantifolia Citrus maxima Citrus microcarpa Cucumis melo Mangifera indica Manilkara zapota Musa acuminata Annona muricata Annona squamosa

juice yield (%)

pH

Mature Flesh 57.5 ± 2.50ef 1.67 ± 0.67δ 64.17 ± 1.44bc 3.68 ± 0.01r

total soluble solids (°Brix) 1.03 ± 0.01w 11.74 ± 0.14p

56.67 ± 2.89efg

3.77 ± 0.02q

7.14 ± 0.14u

50.01 ± 5.00hi

2.75 ± 0.03z

11.26 ± 0.14q

49.17 ± 1.44hi

1.81 ± 0.01ε

11.26 ± 0.14q

57.05 60.04 51.67 36.67

± ± ± ±

0.87efg 2.50cde 2.89hi 1.44l

3.08 2.80 4.15 3.06

± ± ± ±

0.02v 0.02y 0.01o 0.01v

7.88 1.04 12.06 13.63

± ± ± ±

2.91 ± 0.04x 3.00 ± 0.02w

1.01 ± 0.01w 1.01 ± 0.01w

63.50 ± 3.61bcd

3.16 ± 0.04u

1.01 ± 0.01w

62.50 ± 2.50bcd

2.66 ± 0.01β

7.99 ± 0.30t

Ripe Flesh 2.50ij 4.37 2.50ij 5.09 2.89a 5.48 1.44l 2.47 2.89fgh 3.38 0.58n 2.34 2.89fgh 6.21 2.75jk 3.36 2.89hi 5.53 1.26p 5.09 Ripe Aril 26.67 ± 2.89m 3.36 14.50 ± 0.50° 5.78 ± ± ± ± ± ± ± ± ± ±

± ± ± ± ± ± ± ± ± ±

0.01n 0.01i 0.01h 0.01τ 0.03s 0.01σ 0.01d 0.01s 0.03g 0.01i

± 0.01s ± 0.01f

3.25 16.26 12.77 10.06 13.71 11.26 7.72 28.83 29.13 13.71

± ± ± ± ± ± ± ± ± ±

Artocarpus heterophyllus Baccaurea montleyana Baccaurea polyneura Dimocarpus longan Garcinia mangostana Lansium domesticum Nephelium lappaceum Nephelium ramboutan-ake Salacca edulis Sandoricum koetjape

0.14t 0.01w 0.14p 0.14n

50.17 ± 1.26hi 56.67 ± 5.20efg

47.50 47.50 71.67 35.83 53.33 19.67 53.33 43.17 48.33 6.33

scientific name

Cocos nucifera Ananas comosus

0.30v 0.13m 0.14° 0.14s 0.14n 0.14q 0.14t 0.27d 0.27d 0.14n

Apium graveolens Saccharum off icinarum Daucus carota

juice yield (%)

pH

total soluble solids (°Brix)

Ripe Aril 39.17 ± 1.44kl 4.97 ± 0.01j

22.52 ± 0.28i

67.00 ± 0.87b

3.07 ± 0.01v

29.76 ± 0.28c

74.17 ± 1.44a

2.71 ± 0.01α

32.83 ± 0.27a

66.67 ± 2.87b

6.87 ± 0.01a

30.99 ± 0.27b

50.00 ± 5.00hi

2.92 ± 0.01x

24.90 ± 0.28h

50.83 ± 1.44hi

3.69 ± 0.01r

27.89 ± 0.27f

59.17 ± 1.44de

4.98 ± 0.01j

27.89 ± 0.27f

65.83 ± 1.44b

4.64 ± 0.01l

25.85 ± 0.27g

42.50 ± 2.50k 11.67 ± 1.44o

4.53 ± 0.01m 3.26 ± 0.01t

29.13 ± 0.27d 28.36 ± 0.28e

Young Endosperm 52.50 ± 2.50gh 6.56 ± Ripe Peduncle 53.33 ± 2.89fgh 3.86 ± Stem 53.33 ± 2.89fgh 5.96 ± 63.33 ± 2.89bcd 4.94 ±

0.02b

10.86 ± 0.14qr

0.01p

20.28 ± 0.28k

0.01e 0.01k

2.90 ± 0.15v 21.08 ± 0.28j

Root 43.33 ± 2.89jk 6.46 ± 0.01c

10.62 ± 0.14r

Values are means ± standard deviations of triplicate analyses. Results from different analyses were analyzed separately. Values per each analysis followed by different letters are significantly different (p < 0.05). a

19.32 ± 0.28l 30.66 ± 0.72b

at room temperature (27 ± 1 °C). The pure puree from the second group and the diluted puree (from the first group of puree) were then filtered using a clean muslin cloth and centrifuged using a Hittech EBA 20 centrifuge (Japan) at 704g for 15 min. The yields of the pure juices (%) were calculated. Concentration of the obtained diluted juice was referred to fresh sample weight resulting in 200 mg/mL (w/v). The pure juices and diluted juices were stored at 4 °C in the dark until further analysis. The interval between extraction process and experimental work was specified to be 1000 μg AAE/g sample in this fruit.5−7 The differences may result from the cultivars and methodologies used to extract and quantify vitamin C from the fresh sample matrices. The juices of Spondias pinnata and Dimocarpus longan were also found to contain >300 μg AAE/g sample, and the values were respectively higher than that of Kubola et al.12 (90 μg AAE/g sample) and Mahattanatawee et al.6 (140 μg AAE/g sample). Moreover, Isabelle et al.9 reported 633.9 μg AAE/g sample from Dimocarpus longan and had identified Psidium guajava and Dimocarpus longan as fruits with high vitamin C contents. Contents ranging from 200 to 300 μg AAE/g sample were measured from the juices of Citrus maxima, Garcinia atroviridis, Carica papaya, Citrus aurantifolia, and Citrus microcarpa. Previous studies had reported higher vitamin C contents from the fleshes of Carica papaya cv. Exotica,5 cv. Red Lady,6 and cv. Solo.7 Other aforementioned fruits are believed D

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FRAP assays were used to measure the direct involvement of an extract as a primary antioxidant. As indicated in Table 4, the juice of Phyllanthus acidus was found to exhibit the greatest scavenging and reducing activities. This was followed by the juice of Barringtonia racemosa. To date, the phytochemical and antioxidant evaluations of these two species were mainly focused on the leaf extracts.27,28 Only a pentacyclic triterpenoid, bartogenic acid, was isolated from Barringtonia racemosa fruit extract,29 and 46 volatile compounds were identified from Phyllanthus acidus fruit.30 In Malaysia, Barringtonia racemosa fruit is traditionally consumed to treat asthma, sore throat, and stomachache, and Phyllanthus acidus fruit is used as a diuretic.2 Interestingly, the juice of Psidium guajava demonstrated the third highest values of DPPH and FRAP. This fruit juice was found to have the richest in TPC and vitamin C contents (Table 3). The major contents of flavonols such as rutin and flavones such as luteolin in Psidium guajava12 may also be responsible for the activities. Meanwhile, the juice of Ziziphus mauritiana, with a low content of vitamin C and moderate TPC, ranked fourth best in DPPH value. The activity might be contributed by p-hydroxybenzoic acid that was reported to be the most abundant phenolic compound in the fruit extract.31 The juices of the ripe aril of Salacca edulis and the mature flesh of Sandoricum koetjape were found to rank in the top six for both activities. Shui and Leong32 had identified chlorogenic acid, epicatechin, and proanthocyanidins as the major antioxidants in Salacca edulis. The antioxidant activities of Sandoricum koetjape could be associated with its high TPC. However, no phenolic compound was previously identified from its flesh. The only phytochemical that was isolated from the flesh is a triterpenoid, bryononic acid.33 Other juices that gave DPPH values of >280 μg VCEAC/g sample and FRAP values of >800 μg TEAC/g sample were obtained from Spondias pinnata and Citrus maxima. It is found that the activities of the juices were well-correlated with their TPCs and vitamin C contents (Table 3). The major contents of ferulic and syringic acids in the fruit of Spondias pinnata12 and naringin (a flavanone glycoside) in the juice of Citrus maxima25 might act synergistically or individually to enhance the antioxidant activities of the juices. Furthermore, the FRAP value >750 μg TEAC/g sample was also measured from the juice of Manilkara zapota. This could be due to the presence of several polyphenolics such as methyl 4-O-galloylchlorogenate, 4-O-galloylchlorogenic acid, methyl chlorogenate, dihydromyricetin, quercitrin, myricitrin, (+)-catechin, (−)-epicatechin, (+)-gallocatechin, and gallic acid in the fruit.34 The metal chelating assay assesses the indirect involvement of an extract as a secondary antioxidant by binding the ferrous (Fe(II)) ion that catalyzes oxidation and subsequently prevents the formation of the Fe(II)−ferrozine complex. The highest metal chelating activity was detected from the juice of Syzygium samarangense. This was followed by the juices of Averrhoa bilimbi and Averrhoa carambola with no significant difference. Lim et al.7 reported lower activity (only 30%) of the 50% ethanol extract of Averrhoa carambola at 100 mg/mL. This might be due to higher contents of metal chelating compounds in the juice compared to the extract. With the exception of the juices of Averrhoa carambola and Barringtonia racemosa, the juices with >50% of activity were found to contain low TPCs (Table 3). Thus, the results revealed the minor contribution of TPC to the chelating activity. Besides, the activity of polyphenols is related to the presence of an o-dihydroxy moiety in their chemical structures

Table 3. Total Phenolic Content (TPC) and Vitamin C Content of the Juicesa scientific name Averrhoa bilimbi Averrhoa carambola Barringtonia racemosa Cynometra cauliflora Garcinia atroviridis Myristica f ragrans Phyllanthus acidus Psidium guajava Sandoricum koetjape Spondias pinnata Syzygium malaccense Syzygium samarangense Zizyphus mauritiana Bouea macrophylla Carica papaya Citrullus lanatus Citrus aurantifolia Citrus maxima Citrus microcarpa Cucumis melo Mangifera indica Manilkara zapota Musa acuminata Annona muricata Annona squamosa Artocarpus heterophyllus Baccaurea montleyana Baccaurea polyneura Dimocarpus longan Garcinia mangostana Lansium domesticum Nephelium lappaceum Nephelium ramboutanake Salacca edulis Sandoricum koetjape Cocos nucifera Ananas comosus Apium graveolens Saccharum of f icinarum Daucus carota

TPC (μg GAE/g sample) Mature Flesh 251.83 ± 0.79p 699.67 ± 2.24c 790.40 ± 0.23b 52.59 ± 0.53σ 117.28 ± 0.40y 658.76 ± 4.04d 204.75 ± 4.99s 857.24 ± 12.65a 617.04 ± 2.23f 421.64 ± 0.32j 81.51 ± 0.06α 374.83 ± 4.03m 396.96 ± 7.77k Ripe Flesh 372.35 ± 1.43m 377.43 ± 1.10m 104.97 ± 0.19z 463.08 ± 8.48h 606.50 ± 0.22g 453.47 ± 1.38i 162.72 ± 0.81v 79.72 ± 2.77α 255.88 ± 0.91p 120.37 ± 0.85y Ripe Aril 185.80 ± 0.59t 134.35 ± 1.43x 319.01 ± 1.02o 149.49 ± 3.06w 417.14 ± 3.41j 399.13 ± 5.15k 647.59 ± 9.52e 386.82 ± 5.53l 223.75 ± 0.57r 199.07 ± 2.18s 175.99 ± 0.94u 60.96 ± 1.44τ Young Endosperm 71.85 ± 7.84β Ripe Peduncle 359.28 ± 2.53n Stem 200.99 ± 0.34s 116.55 ± 0.30y Root 236.02 ± 0.57q

vitamin C (μg AAE/g sample) 154.14 85.39 108.16 106.01 280.91 139.10 102.58 590.31 98.28 396.93 100.43 72.50 84.10

± ± ± ± ± ± ± ± ± ± ± ± ±

6.44h 3.72no 1.49k 3.24kl 7.44d 3.72i 6.44klm 7.44a 3.72m 3.94b 3.72lm 3.72pqr 2.68no

156.29 268.02 61.75 259.42 285.21 227.20 74.64 121.06 72.50 72.50

± ± ± ± ± ± ± ± ± ±

3.72h 7.44e 3.72stu 7.44f 7.44d 3.72g 3.72pq 1.28j 3.72pqr 3.72pqr

104.72 98.28 72.50 67.34 149.85 380.61 66.91 87.54 60.89 65.62

± ± ± ± ± ± ± ± ± ±

3.72klm 3.72m 1.97pqr 0.744qrst 3.72h 1.49c 3.24rst 3.72n 0.74tu 1.49rst

98.28 ± 3.72m 120.19 ± 1.97j 51.87 ± 0.74v 78.94 ± 3.72op 56.60 ± 0.74uv 79.80 ± 1.49op 63.04 ± 1.49stu

Values are means ± standard deviations of triplicate analyses. Results from different analyses were analyzed separately. Values per each analysis followed by different letters are significantly different (p < 0.05). a

to be native to Southeast Asia, and this study apparently was the first comparative evaluation that revealed higher vitamin C contents of their juices. Antioxidant Activities. The antioxidant activities of the juices were evaluated using DPPH free radical scavenging, ferric reducing power (FRAP), and metal chelating assays. DPPH and E

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Table 4. Antioxidant Activities of the Juicesa scientific name

DPPH (μg VCEAC/g sample)

Averrhoa bilimbi Averrhoa carambola Barringtonia racemosa Cynometra cauliflora Garcinia atroviridis Myristica f ragrans Phyllanthus acidus Psidium guajava Sandoricum koetjape Spondias pinnata Syzygium malaccense Syzygium samarangense Zizyphus mauritiana

156.92 111.88 534.09 105.28 115.14 242.54 613.71 517.95 418.22 289.00 137.11 149.77 460.58

± ± ± ± ± ± ± ± ± ± ± ± ±

0.58o 1.36uv 1.41b 0.41vw 1.15u 1.08i 2.59a 6.06c 5.17e 3.25g 2.07q 2.61op 17.93d

Bouea macrophylla Carica papaya Citrullus lanatus Citrus aurantifolia Citrus maxima Citrus microcarpa Cucumis melo Mangifera indica Manilkara zapota Musa acuminata

258.17 202.78 74.64 170.14 397.68 185.83 98.13 133.75 116.55 123.47

± ± ± ± ± ± ± ± ± ±

4.25h 0.61l 0.70zα 5.32n 4.21f 7.40m 1.18wxy 9.61qr 0.74tu 0.91st

Annona muricata Annona squamosa Artocarpus heterophyllus Baccaurea montleyana Baccaurea polyneura Dimocarpus longan Garcinia mangostana Lansium domesticum Nephelium lappaceum Nephelium ramboutan-ake Salacca edulis Sandoricum koetjape

132.57 145.57 127.76 96.88 233.21 61.37 225.70 111.27 94.17 49.19 421.56 116.20

± ± ± ± ± ± ± ± ± ± ± ±

1.67qr 1.50p 1.35rs 0.34xy 0.55j 0.48β 9.23k 1.10uv 1.60y 0.68δ 8.61e 0.46tu

Cocos nucifera

102.79 ± 4.64wx

Ananas comosus

105.55 ± 1.42vw

Apium graveolens Saccharum of f icinarum

78.00 ± 0.72z 124.37 ± 1.97s

Daucus carota

69.91 ± 0.67α

FRAP (μg TEAC/g sample) Mature Flesh 192.66 ± 0.23s 154.55 ± 3.32u 2129.66 ± 2.04b 60.86 ± 1.18α 168.27 ± 0.74t 229.74 ± 0.85q 2784.89 ± 3.93a 1924.34 ± 1.65c 933.39 ± 2.21e 866.82 ± 10.69f 189.94 ± 2.95s 625.18 ± 0.84j 484.79 ± 4.68l Ripe Flesh 133.31 ± 0.70w 469.44 ± 1.05m 37.81 ± 0.39β 347.61 ± 3.71n 834.22 ± 7.28g 262.31 ± 1.40p 123.44 ± 1.11x 311.13 ± 2.66o 759.90 ± 17.34h 554.94 ± 4.55k Ripe Aril 210.80 ± 3.18r 146.92 ± 0.09v 142.94 ± 1.16v 116.64 ± 0.67x 210.71 ± 3.24r 694.56 ± 4.76i 171.48 ± 0.79t 120.27 ± 0.41x 96.85 ± 1.37y 73.06 ± 0.29z 1556.79 ± 8.73d 97.01 ± 0.70y Young Endosperm 174.93 ± 0.82t Ripe Peduncle 172.45 ± 1.99t Stem 59.78 ± 0.11α 159.01 ± 0.65u Root 76.14 ± 0.30z

metal chelatingb (%)

α-glucosidase inhibitionb (%)

81.33 78.94 56.56 63.61 36.22 28.61 18.67 44.06 24.67 24.83 22.67 82.28 22.11

± ± ± ± ± ± ± ± ± ± ± ± ±

0.17a 0.42a 0.77d 1.11c 1.67fg 2.43hi 0.44k 2.80e 0.44ij 0.17ij 0.29jk 0.10a 1.68jk

0d 0d 93.75 88.59 65.94 86.98 95.37 0d 46.15 64.85 0d 79.44 0d

23.00 7.89 32.89 11.56 0n 38.39 0n 25.33 0n 40.22

± ± ± ±

0.25jk 5.97l 4.62gh 0.42l

83.44 ± 0.10ab 0d 0d 0d 0d 75.24 ± 0.71ab 0d 0d 0d 0d

0n 24.56 0n 10.78 23.89 0n 71.83 58.22 3.39 72.78 0n 56.72

± 0.75f ± 1.33ij ± 1.36ef

± 0.35ij ± 1.11l ± 4.89ij ± ± ± ±

1.17b 5.51d 1.92m 1.13b

± 1.18d

± ± ± ± ±

0.14a 0.34a 0.32bc 0.23ab 0.15a

± 5.22c ± 3.24bc ± 0.45ab

0d 0d 0d 0d 0d 0d 85.20 ± 0.59ab 0d 0d 0d 0d 0d

28.56 ± 1.92hi

0d

9.11 ± 4.52l

0d

21.33 ± 0.50jk 71.00 ± 0.17b

0d 0d

38.06 ± 3.78f

0d

Values are means ± standard deviations of triplicate analyses. Results from different assays were analyzed separately. Values for each assay followed by different letters are significantly different (p < 0.05). bResulted from assay using pure juices. a

0.01 (in Garcinia atroviridis) to 4.37 ± 0.01 (in Bouea macrophylla). This indicated no effect of the juice pH on the assay system. The highest α-glucosidase inhibitory percentage (95.37 ± 0.15%) was measured from the juice of Phyllanthus acidus. The value was not significantly different from the juices of Barringtonia racemosa, Cynometra caulif lora, Myristica f ragrans, Garcinia mangostana, Bouea macrophylla, Syzygium samarangense, and Citrus microcarpa. The α-glucosidase inhibitory activity of these fruit parts (excluding Phyllanthus acidus) was highlighted for the first time in this study. It is

or those bearing catechol or galloyl groups.35 Polyphenolics that were previously isolated from Syzygium samarangense fruit pulps such as reynoutrin, hyperin, myricitrin, quercitrin, quercetin, guaijaverin, gallic acid, and ellagic acid36 and from Averrhoa carambola, which are chlorogenic, caffeic acids,24 catechin, epicatechin, and gallic acid,37 were found having these characteristics. α-Glucosidase Inhibitory Activity. As indicated in Table 4, only 11 juices mostly obtained from the mature fleshes show positive results. The pH values of juices ranged from 1.81 ± F

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Figure 1. UPLC chromatograms (at 350 nm) of the juices of (a) Barringtonia racemosa and (b) Phyllanthus acidus. The UV spectra of several peaks generated by a photodiode array detector are indicated.

fruit parts of Myristica f ragrans, which are the methanol extract of the mace (aril)43 and the water extract of nutmeg (seed),44 were previously reported to possess a moderate α-glucosidase inhibitory activity. Furthermore, three prenylated xanthones (αmangostin, γ-mangostin, and gartanin) that were identified as α-glucosidase inhibitors were abundantly quantified from the ethanol extract of the seedcase of Garcinia mangostana.45 The major phenolic compound in the 80% methanol extract of the aril of Garcinia mangostana was p-hydroxybenzoic acid,46 and in the juice of Citrus microcarpa was p-coumaric acid.47 However, according to Kwon et al.,42 these compounds have a low capacity to inhibit α-glucosidase. Therefore, the low contents of protocatechuic acid and vanillic acid that were also quantified from the extract of Garcinia mangostana46 and caffeic acid in the juice of Citrus microcarpa47 may be responsible for the activity.42 On the basis of the comparative α-glucosidase inhibitory activity of various flavonoids, Tadera et al.48 had suggested that unsaturated C-ring, hydroxylation on the C-ring at the 3-position, and an increase in the number of hydroxyl group on the B-ring might enhance the inhibitory activity. Therefore, quercetin, four quercetin glycosides (quercitrin, guaijaverin, reynoutrin, and hyperin), and a myricetin glycoside (myricitrin) that were previously isolated from Syzygium samarangense fruit pulps could be attributed with the activity.36

interesting to note that Cynometra caulif lora and Bouea macrophylla fruits that are endemic and native to Malaysia were also found to have higher activity. To date, no compound was identified from Cynometra caulif lora fruit, and only volatile components were identified from Bouea macrophylla fruit. The major volatile components of this fruit are (E)-β-ocimene (68.59%) and α-pinene (8.04%).38 These compounds were also detected in the essential oil of black pepper (Piper guineense) seeds, which was reported to inhibit α-glucosidase.39 A very low α-glucosidase inhibitory activity was determined from the extracts of Phyllanthus acidus in two earlier investigations.19,20 This might be due to higher contents of α-glucosidase inhibitors in the juice compared to the extracts. The activity of the juices of Barringtonia racemosa, Myristica fragrans, and Garcinia mangostana is in line with their high TPCs (>600 μg GAE/g sample; Table 3). Bartogenic acid, which was also isolated in the fruit29 and the seed of Barringtonia racemosa, was reported to possess α-glucosidase inhibitory activity.40 Caffeic acid and catechin, which were found in the mature flesh of Myristica f ragrans,41 were identified as potent α-glucosidase inhibitors from the phenolic group.42 The present study in fact is the first to determine the αglucosidase inhibitory activity of the flesh of Myristica f ragrans and the aril of Garcinia mangostana. Extracts from another two G

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Figure 2. UPLC chromatograms (at 350 nm) of the hydrolyzed juice extracts of (a) Barringtonia racemosa and (b) Phyllanthus acidus. The identified compounds of the labeled peaks are shown in Table 5.

Table 5. Content of Phenolic Compounds in Hydrolyzed Juice Extracts of Barringtonia racemosa and Phyllanthus acidus (Milligrams per 100 g of Extract) peak

phenolic

retention time (min)

1 2 3 4 5 6

gallic acid dihydroquercetin (taxifolin) ellagic acid myricetin quercetin kaempferol

1.709 2.919 3.217 3.661 3.919 4.407

B. racemosa

P. acidus 230.69 ± 3.31 103.33 ± 9.31

1269.48 ± 33.82 265.57 ± 2.45 61.70 ± 1.97

85.42 ± 6.51 142.68 ± 12.49 4.54 ± 0.19

The UV spectra of myricetin (a flavonol) were detected at the peaks with retention times of 2.868 and 3.138 min, and this indicated the presence of different glycosidic myricetins in Phyllanthus acidus and Barringtonia racemosa juices, respectively. The presence of three glycosidic quercetins (also a flavonol) was detected by the UV spectra of peaks at retention times of 2.733 and 3.510 min in the chromatogram of Phyllanthus acidus and 3.955 min in the Barringtonia racemosa chromatogram. The UV spectra of glycosidic dihydroquercetin (a flavanone) and kaempferol (a flavonol) were observed at peaks with retention times of 2.796 and 3.177 min, respectively, in the Phyllanthus acidus chromatogram. Due to the diversity of unknown glycosidic flavonoids and/or bound phenolics found in these two fresh juices, we quantified the polyphenolics as aglycones, after hydrolysis. Moreover, glycosylation of flavonoids was reported to decrease the antioxidant49 and α-glucosidase inhibitory activities.50 Figure 2 shows the UPLC chromatograms of the hydrolyzed juice extracts of Barringtonia racemosa and Phyllanthus acidus (at 350 nm) and six labeled peaks that were positively identified by comparison with standards. The contents of these compounds in the extracts are summarized in Table 5. Ellagic acid (peak 3, Figure 2) was identified as the major compound in the hydrolyzed juice extract of Barringtonia racemosa. The hydrolyzed juice extract of

Identification and Quantification of Phenolic Compounds in Barringtonia racemosa and Phyllanthus acidus. The fruit juices of Barringtonia racemosa and Phyllanthus acidus have indicated the highest FRAP, DPPH, and α-glucosidase inhibitory activities (Table 4). This is considered the first comparative evaluation to highlight the pronounced activities of these juices. We hypothesized that polyphenolics are the major contributors of the activities. However, no polyphenolics had been previously identified from these two fruits. Thus, polyphenolics were separated from the juices using UPLC, and different chromatograms were obtained when different mobile phases and gradient modes were used. Figure 1 shows one of the UPLC chromatograms that indicated a good separation of polyphenolics of the juices (detected at 350 nm) using solvent A (0.5% acetic acid) and solvent B (acetonitrile) as the mobile phase. The juices were separated using a gradient mode that was initially set at an A/B ratio of 80:20 and then linearly increased to 60:40 at 1 min, to 30:70 at 2 min, and to 10:90 at 4.5 min until 5.5 min. The UV spectrum of each separated peak was detected by the photodiode array detector. Only the peaks of gallic acid in Phyllanthus acidus chromatogram and ellagic acid in Barringtonia racemosa chromatogram (at retention times of 1.731 and 2.646 min, respectively) were positively identified by comparing the retention times and UV spectra of the peaks with the standards. H

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(4) Xiao, J.; Kai, G.; Yamamoto, K.; Chen, X. Advance in dietary polyphenols as α-glucosidases inhibitors: a review on structure-activity relationship aspect. Crit. Rev. Food Sci. Nutr. 2013, 53, 818−836. (5) Luximon-Ramma, A.; Bahorun, T.; Crozier, A. Antioxidant actions and phenolic and vitamin C contents of common Mauritian exotic fruits. J. Sci. Food Agric. 2003, 83, 496−502. (6) Mahattanatawee, K.; Manthey, J. A.; Luzio, G.; Talcott, S. T.; Goodner, K.; Baldwin, E. A. Total antioxidant activity and fiber content of select Florida-grown tropical fruits. J. Agric. Food Chem. 2006, 54, 7355−7363. (7) Lim, Y. Y.; Lim, T. T.; Tee, J. J. Antioxidant properties of several tropical fruits: a comparative study. Food Chem. 2007, 103, 1003− 1008. (8) Ikram, E. H. K.; Eng, K. H.; Jalil, A. M. M.; Ismail, A.; Idris, S.; Azlan, A.; Nazri, H. S. M.; Diton, N. A. M.; Mokhtar, R. A. M. Antioxidant capacity and total phenolic content of Malaysian underutilized fruits. J. Food Compos. Anal. 2009, 22, 388−393. (9) Isabelle, M.; Lee, B. L.; Lim, M. T.; Koh, W.-P.; Huang, D.; Ong, C. N. Antioxidant activity and profiles of common fruits in Singapore. Food Chem. 2010, 123, 77−84. (10) Rufino, M. d. S. M.; Alves, R. E.; Brito, E. S. d.; Pérez-Jiménez, J.; Saura-Calixto, F.; Mancini-Filho, J. Bioactive compounds and antioxidant capacities of 18 non-traditional tropical fruits from Brazil. Food Chem. 2010, 121, 996−1002. (11) Contreras-Calderón, J.; Calderón-Jaimes, L.; Guerra-Hernández, E.; García-Villanova, B. Antioxidant capacity, phenolic content and vitamin C in pulp, peel and seed from 24 exotic fruits from Colombia. Food Res. Int. 2011, 44, 2047−2053. (12) Kubola, J.; Siriamornpun, S.; Meeso, N. Phytochemicals, vitamin C and sugar content of Thai wild fruits. Food Chem. 2011, 126, 972− 981. (13) Tiwari, A. K.; Reddy, K. S.; Radhakrishnan, J.; Kumar, D. A.; Zehra, A.; Agawane, S. B.; Madhusudana, K. Influence of antioxidant rich fresh vegetable juices on starch induced postprandial hyperglycemia in rats. Food Funct. 2011, 2, 521−528. (14) Pinto Mda, S.; Ranilla, L. G.; Apostolidis, E.; Lajolo, F. M.; Genovese, M. I.; Shetty, K. Evaluation of antihyperglycemia and antihypertension potential of native Peruvian fruits using in vitro models. J. Med. Food 2009, 12, 278−291. (15) Goncalves, A.; Franco, M. L.; Genovese, M. I. Chemical composition and antioxidant/antidiabetic potential of Brazilian native fruits and commercial frozen pulps. J. Agric. Food Chem. 2010, 58, 4666−4674. (16) Correia, R. T. P.; Borges, K. C.; Medeiros, M. F.; Genovese, M. I. Bioactive compounds and phenolic-linked fuctionality of powdered tropical fruit residues. Food Sci. Technol. Int. 2012, 18, 539−547. (17) Girones-Vilaplana, A.; Baenas, N.; Villano, D.; Speisky, H.; Garcia-Viguera, C.; Moreno, D. A. Evaluation of Latin-American fruits rich in phytochemicals with biological effects. J. Funct. Foods 2014, 7, 599−608. (18) Park, J.-H.; Kim, R.-Y.; Park, E. Antidiabetic activity of fruits and vegetables commonly consumed in Korea: inhibitory potential against α-glucosidase and insulin-like action in vitro. Food Sci. Biotechnol. 2012, 21, 1187−1193. (19) Hossain, S. J.; Tsujiyama, I.; Takasugi, M.; Islam, M. A.; Biswas, R. S.; Aoshima, H. Total phenolic content, antioxidative, anti-amylase, anti-glucosidase and antihistamine release activities of Bangladeshi fruits. Food Sci. Technol. Res. 2008, 14, 261−268. (20) Das, S.; Das, S.; De, B. In vitro inhibition of key enzymes related to diabetes by aqueous extracts of some fruits of West Bengal, India. Curr. Nutr. Food Sci. 2012, 8, 19−24. (21) Sulaiman, S. F.; Ooi, K. L. Polyphenolic and vitamin C contents and antioxidant activities of aqueous extracts from mature-green and ripe fruit fleshes of Mangifera sp. J. Agric. Food Chem. 2012, 60, 11832−11838. (22) Ooi, K. L.; Muhammad, T. S. T.; Tan, M. L.; Sulaiman, S. F. Cytotoxic, apoptotic and anti-α-glucosidase activities of 3,4-di-Ocaffeoyl quinic acid, an antioxidant isolated from the polyphenolic-rich

Phyllanthus acidus was found to contain the highest content of gallic acid (peak 1, Figure 2). These compounds respectively bear catechol and galloyl groups that might be responsible for enhancing the antioxidant activity of the juices. However, these compounds were reported to possess low α-glucosidase inhibitory activity.42 Two flavonols, myricetin (peak 4, Figure 2) and quercetin (peak 5, Figure 2), were also quantified from these hydrolyzed juice extracts. The contents of these compounds in Barringtonia racemosa are respectively more than 3-fold higher and 2-fold lower than Phyllanthus acidus. These flavonols with structural configurations of 2−3 double bonds conjugated with the 4-oxo function and hydroxyl groups at the 3-, 5-, 7-, 3′-, and 4′-positions play a major role in enhancing the antioxidant49 and α-glucosidase inhibitory activities.48 As indicated in Table 5, a low content of kaempferol (a flavonol) and a moderate content of dihydroquercetin were also detected from the hydrolyzed juice extract of Phyllanthus acidus. With the exception of kaempferol, all of the quantified compounds have an o-dihydroxy moiety in their chemical structures. This may indicate the major contribution of the compounds to increase the activities of the juices. Our results indicate that various tropical fruit juices serve as rich sources of antioxidants and α-glucosidase inhibitors. The activities can be associated with the combined effect of polyphenolics in the juices or the structure−activity relationships of the major polyphenolics. The results obtained from this study were in line with several earlier comparative antioxidant studies that highlighted higher primary antioxidant activities of Psidium guajava fruit compared with other tropical fruits. However, the activities were found lower than those of Phyllanthus acidus and Barringtonia racemosa. These two medicinal fruits are native to Southeast Asia and were also found to have higher α-glucosidase inhibitory activity. The new information obtained by this study would be useful for promoting their consumption and the development of functional foods.

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AUTHOR INFORMATION

Corresponding Author

*(S.F.S.) Phone: +60-4-6534095. Fax: +60-4-6565125. E-mail: [email protected]. Funding

We acknowledge financial support provided by the Universiti Sains Malaysia (Research University Grant 1001/PBIOLOGI/ 813049). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We acknowledge the Universiti Sains Malaysia for providing laboratory facilities.

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J

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