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International Journal of Food Science and Technology 2015, 50, 567–577

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Review Gac fruit (Momordica cochinchinensis Spreng.): a rich source of bioactive compounds and its potential health benefits Hoang V. Chuyen,1,2 Minh H. Nguyen,1,3* Paul D. Roach,1 John B. Golding1,4 & Sophie E. Parks1,4 1 2 3 4

School of Environmental and Life Sciences, University of Newcastle, PO Box 127, Brush Road, Ourimbah, NSW 2258, Australia Faculty of Agriculture and Forestry, Tay Nguyen University, 567 Le Duan Street, Buon Ma Thuot, Daklak, Vietnam School of Science and Health, University of Western Sydney, Penrith, NSW 2751, Australia NSW Department of Primary Industries, Ourimbah, NSW 2258, Australia (Received 19 September 2014; Accepted in revised form 12 November 2014)

Summary

Gac (Momordica cochinchinensis Spreng.) is a tropical vine originating from South and South-East Asia. Gac fruit has traditionally been used in Asia to provide red colour for cuisines and enhance visional health. Recently, Gac fruit has emerged as a potential source of carotenoids, especially lycopene and b-carotene. Carotenoids and other identified bioactives from this fruit including phenolics, flavonoids and trypsin inhibitors are associated with many beneficial bioactivities such as antioxidant, anticancer and provitamin A activities. In addition to the traditional utilisation, commercial products like Gac powder and Gac oil have been manufactured as natural colourants and medicinal supplements. This paper is a review of the scientific literature on the nutritional composition, biological activities and processing of Gac fruit.

Keywords

Biological activity, Gac oil, Gac powder, lycopene, b-carotene.

Introduction

Gac (Momordica Cochinchinensis Spreng.) which belongs to the Cucurbitaceae family is a tropical plant. Gac is indigenous to countries in South and SouthEast Asia including Vietnam, China, Thailand and India. Besides the name ‘Gac’ in Vietnam, this plant is called ‘cochinchin gourd’ in English and also known by other names in different countries (Table 1). Gac is a dioecious plant, which has separate male and female plants, and can be cultivated from seeds, branches and roots. Gac usually flowers in the summer and the fruits become ripe approximately 9 or 10 weeks after being pollinated. Gac fruits are normally harvested from autumn to winter when the skin turns to dark orange or red (WHO, 1990). The oily red aril has been reported as the most nutritious portion of Gac fruit with a high amount of oil and extremely high levels of carotenoids including b-carotene and lycopene (West & Poortvliet, 1993; Ishida et al., 2004). Due to its high intensity red colour, Gac aril has long been used in Asia as a natural colourant for traditional cuisines. The seeds of Gac have also been used as a traditional medicine for the treatment of *Correspondent: Fax: +61-2-43494145; e-mail: [email protected]

doi:10.1111/ijfs.12721 © 2014 Institute of Food Science and Technology

various diseases such as mastitis, boils and pyodermas (Huang et al., 1999; Zhao et al., 2012). Many recent studies have demonstrated that Gac fruit has a number of biological activities, which might contribute significant benefits to human health (Vuong et al., 2002; Meng et al., 2012; Mai et al., 2013a,b). In addition, efforts have focused on the processing of Gac fruit to produce Gac powder and Gac oil as a natural food additive and for medical uses. As a result, commercial Gac products have been available on the market such as frozen Gac aril, Gac oil capsules and dried Gac powder. In this review, the potential of Gac fruit as a source of bioactive compounds, especially carotenoids, and its biological activities, processing and utilisation are discussed. Gac fruit anatomy

Each ripe fruit is comprised of black seeds which are covered by an oily red membrane (aril), an orange spongy mesocarp (pulp) and an orange–red peel with spines on the surface (Fig. 1). The edible aril is the most valuable component of the fruit due to its high carotenoid and fatty acid content. However, the aril constitutes only a low proportion of the fruit weight, whereas the pulp, peel and seeds, which make up the

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Table 1 Names of Momordica cochinchinensis Spreng Language

Name

Latin

Momordica cochinchinensis Spreng., Muricia Cochinchinensis Lour. Chinese bitter cucumber, Spiny bitter gourd, Cochinchin gourd Mu Bie, Mu Bie Zi, Teng Tong, Tu Mu Bie Gac, Moc Miet Tu Bat-Khai-Du, Phak-Khao Bhat-Karela, Gangerua, Kakrol, Kantola Khaawz Teruah Buyok-buyok, Sugod-sugod

English Chinese Vietnamese Thai Hindu Laos Malais Tagalog Adapted from Lim (2012).

Figure 1 Anatomical components of Gac fruit (1. Seed, 2. Pulp, 3. Aril, 4. Peel with spines).

bulk of the fruit, are usually discarded in processing. Kha et al. (2013a) reported that the proportion of aril in a Gac fruit is <31% while that of pulp, peel and seeds constitute up to 90% of the total weight of a fruit. In a later study, Parks et al. (2013) showed a similar result with the proportion of the aril ranging from 6% to 31% and found a correlation between the increase in fruit size and weight and the higher proportion of aril. Other studies also showed wide variations in the proportion of aril in Gac fruit but that it was not above 30% of fruit weight. The variation in the proportion of Gac aril might be due to differences in variety, growing conditions and maturity of the investigated fruits (Ishida et al., 2004; Nhung et al., 2010). Although the pulp, peel and seeds are normally discarded in Gac processing, it was reported that the pulp and peel contain a significant amount of carotenoids such as b-carotene, lycopene and especially lutein, a xanthophyll which is widely used in the treatment of eye diseases (Kubola & Siriamornpun, 2011). Gac seed has also been used in traditional Chinese medicine and reported to contain multiple trypsin inhibitors, which might contribute to its medicinal activity (Wong et al., 2004). Consequently, it is necessary to further examine potential applications of bioactive compounds from these parts (pulp, peel and seed) of Gac fruit other than the aril to avoid wasting a natural resource as well as to resolve potential environmental issues caused by their disposal. Phytochemical composition of Gac fruit

Gac fruit is not only rich in b-carotene, lycopene and essential fatty acids but also contains significant levels of other carotenoids and bioactive compounds such as a-tocopherol (vitamin E), phenolic compounds and flavonoids (Ishida et al., 2004; Kubola & Siriamornpun, 2011). These compounds significantly contribute to the health benefits of Gac fruit through their

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provitamin A, antioxidant and antimicrobial activities (Vuong et al., 2002; Innun, 2012; Mai et al., 2013a,b). Carotenoids

The edible red aril (seed membrane) of Gac fruit contains a very high concentration of carotenoids including lycopene and b-carotene. It was reported that the b-carotene content in Gac aril is five times greater than the levels measured in carrots, and the lycopene content eight times greater compared to the levels measured in tomatoes (Mangels et al., 1993; Singh et al., 2001; Aoki et al., 2002). A concentration of 892 lg g 1 fresh weight (FW) of total carotenoids was identified in Gac aril, which includes 188 lg g 1 FW of b-carotene (West & Poortvliet, 1993). A later study on the carotenoid composition of Gac fruit showed much higher levels of carotenoid, which were 718 and 2227 lg g 1 FW of b-carotene and lycopene, respectively (Ishida et al., 2004). Other studies on Gac fruit also observed a very high content of carotenoids in the aril but results from the studies varied widely (Table 2). These observed variations in carotenoid level might be due to differences in the materials used for the studies in of variety, maturity, growing conditions and storage conditions. Therefore, effects of the above factors on the level of carotenoids in Gac fruit need further investigation. In addition to b-carotene and lycopene, other carotenoids like lutein, zeaxanthin and b-cryptoxanthin have also been identified to be present at considerable levels in Gac fruit. Aoki et al. (2002) showed concentrations of 9 lg zeaxanthin g 1 FW and 2 lg b-cryptoxanthin g 1 FW in Gac aril and 1.6 lg zeaxanthin g 1 FW and 3.5 lg b-cryptoxanthin g 1 FW in Gac pulp. Lutein was found to be present in all portions of the fruit, especially at very high concentrations in the peel and pulp (12 480 and 1448 lg g 1 FW, respectively) (Kubola & Siriamornpun, 2011; Kha et al., 2013a). This

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Table 2 Carotenoid content of Gac aril (lg g

1

fresh weight)

Total carotenoids

b-carotene

Lycopene

References

892 977 481 – 497 – –

188 175 101 718 83 379 1600

–

West & Poortvliet (1993) Vuong et al. (2002) Aoki et al. (2002) Ishida et al. (2004) Vuong et al. (2006) Nhung et al. (2010) Kubola & Siriamornpun (2011) Kubola et al. (2013)

–

45

802 380 2227 408 3728 1400 9

observation suggests that Gac peel and pulp should be regarded as a potential source of lutein instead of being discarded as a waste product of Gac processing. Oil and fatty acids

Several studies have demonstrated that the aril of Gac contains a high concentration of oil that is composed of several types of fatty acids. For example, fresh Gac aril was found to contain 10.2% mg of oil, which is comparable with other oil-rich fruits like avocadoes (G omezL opez, 2002; Vuong et al., 2002). Kha et al. (2013b) determined that the total oil content in Gac aril ranged from 18% to 34% dry basis using Soxhlet extraction with petroleum ether. In another study which used supercritical CO2 fluid extraction, a concentration of 37–42% dry basis of oil was found in Gac aril (Kha et al., 2014a). Although the extraction method might affect the amount of extracted oil, these differences in the oil content of Gac aril might also be caused by variations in variety and growing conditions of the materials as for other oil-rich fruits (G omez-L opez, 2002). In further studies on the fatty acid composition of Gac, the extracted oil has been analysed by gas chromatography. Oleic, palmitic and linoleic were identified as the predominant fatty acids in Gac aril, while stearic followed by linoleic, oleic and palmitic were the main fatty acids in the seeds (Ishida et al., 2004). These results are consistent with data reported by Vuong et al. (2002) and Mai et al. (2013a,b) (Table 3). The significant amount of oleic and linoleic acids in the oil may potentially contribute to the benefits of Gac oil for human health by reducing LDL-cholesterol and having anti-atherogenic effects (Pariza, 2004; Lopez-Huertas, 2010). The composition of fatty acids and high level of carotenoids in Gac oil (Vuong & King, 2003) suggest that Gac fruit is a good source of oil having high nutritional value. Other bioactive compounds

Gac fruit is not only rich in carotenoids but it is also high in other bioactive compounds, which may contribute to its beneficial bioactivities.

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Table 3 Composition of main fatty acids in aril of Gac fruit (% total fatty acid) Palmitic (16:0)

Stearic (18:0)

Oleic (18:1D9)

Linoleic (18:2 D9,12)

References

22.0 26.4–32.1 17.3

7.1 3.2–12.2 7.5

34.1 30.8–33.7 59.5

31.4 27.5–28.7 13.98

Vuong et al. (2002) Ishida et al. (2004) Mai et al. (2013a,b)

Phenolic compounds have been found to be present in Gac fruit and especially in green fruit. Bharathi et al. (2014) recently showed that immature Gac fruit at 25-days of age, which is regarded as a vegetable in India, contains 26 mg of gallic acid equivalents of total phenolics and 1.3 mg catechin equivalents of total flavonoids in 100 g of fresh fruit. A study on the phytochemical composition of Gac fruit also reported that the pulp of green fruits and the aril of ripe fruits contained 181 and 90 mg g 1 dry weight (DW) of total phenolic content, respectively (Kubola & Siriamornpun, 2011). In addition, p-hydroxybenzoic acid and ferulic acid were determined as the major phenolic acids present in the fruit. The highest amount of total flavonoids was found in the aril (376 mg g 1 DW) followed by the pulp of red fruits (302 mg g 1 DW) and green fruits (285 mg g 1 DW). Among the flavonoids, apigenin and rutin were the predominant compounds in the pulp and the aril, respectively. Antioxidant assays on hydrophilic extracts, which do not contain carotenoids, showed a correlation between increases in antioxidant activity and total phenolic as well as flavonoid content. This result suggests that these bioactive groups significantly contribute to the antioxidant capacity of Gac fruit (Kubola & Siriamornpun, 2011). In of lipophilic extracts, vitamin E (a-tocopherol) was determined in Gac oil at a concentration of 357 lg mL 1 and in Gac aril at 76 lg g 1 FW (Vuong & King, 2003). At these levels of vitamin E, consuming foods with added Gac oil or Gac aril could significantly contribute to the daily intake of vitamin E (Vuong et al., 2006). Gac seed, which has been used for more than 1000 years as a drug called mubiezhi in China, has been found to contain trypsin inhibitors (Meng et al., 2012). Although trypsin inhibitors may cause growthretardation in animals by inhibiting intestinal proteolysis and limiting the bioavailability of essential amino acids (Booth et al., 1960; Khayambashi & Lyman, 1966), these compounds have been reported to possess both in vitro and in vivo anticarcinogenic effects on cancer cells (Kennedy & Troll, 1993). Huang et al. (1999) isolated a trypsin inhibitor from Gac seed having a molecular weight of 3479 Da, which was found to belong to the squash family inhibitors. In a later study, five more trypsin inhibitors with molecular

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weights of 5100, 4800, 4400, 4100 and 3900 Da were also determined to be present in Gac seeds (Wong et al., 2004). The findings on the phytochemical composition of Gac fruit show that its nutritional value is not only contributed to by the high content of lycopene and bcarotene in the aril but also by significant amounts of other bioactive compounds including lutein, phenolics and flavonoids in the pulp and peel and trypsin inhibitors in the seeds. The presence of these valuable compounds in Gac fruit should provide positive effects on human health due to their reported bioactivities. Biological activities

Many biological activities associated with Gac fruit including provitamin A, antioxidant, anticancer and antimicrobial properties have been reported. Provitamin A activity

Red Gac aril has been regarded as one of the best sources of vitamin A due to its high content of b-carotene, which is a precursor for this vitamin. In Vietnam, Gac aril and Gac oil have been traditionally added to foods like steamed rice (xoi gac) to promote healthy vision and assist the treatment of eye diseases caused by the lack of vitamin A (Vo-Van-Chi, 1997). Vuong et al. (2002) investigated the influence of a diet supplemented with b-carotene from Gac aril on the plasma b-carotene and retinol concentration in Vietnamese children. After 30 days consuming steamed rice with added Gac aril containing 3.5 mg b-carotene per serving, the plasma retinol concentration of the treated group was significantly higher than that of the control group (consuming normal steamed rice) and even higher than that of the group consuming steamed rice supplemented with 5 mg of synthetic b-carotene. The

higher level of plasma retinol of the group treated with Gac aril compared to the group treated with synthetic b-carotene can be explained by the higher absorption of b-carotene from the Gac-added rice compared to that from the other diet. An increase of 2.11 lmol L 1 of plasma b-carotene was recorded in the Gac aril treated group while it was 1.67 lmol L 1 in the group treated with synthetic b-carotene. The higher bioavailability of b-carotene in the Gac-added rice might be induced by other components in Gac fruit, including the effects of a significant amount of fat, which has been reported to promote the intestinal absorption of b-carotene in humans (Yeum & Russell, 2002; Brown et al., 2004). Antioxidant activity

Gac aril and products from Gac aril have been demonstrated to have very high antioxidative activity because of their extremely high levels of carotenoids, especially lycopene. Lycopene has been reported as one of the most bioactive carotenoids which contributes to a variety of health benefits by having anticancer, cardioprotective and anti-inflammatory effects (Bhuvaneswari & Nagini, 2005; Mordente et al., 2011; Hazewindus et al., 2012). There are many studies which have focused on the antioxidant activity of Gac fruit as well as on the changes in antioxidant activity of the processed products (Table 4). For example, Kubola & Siriamornpun (2011) investigated the ferric-reducing antioxidant power (FRAP) of extracts from different parts of Gac fruits at different stages of maturity. The extract from aril of the fully ripe fruits exhibited the highest antioxidant activity, while the lowest activity was identified in the extract from the seeds. These results were explained by the correlation between the antioxidant capacity and the total phenolic content of the

Table 4 Antioxidant activity of Gac fruit and products Material

Assay

Result

References

Ethanol extracts of Gac aril, pulp and peel

DPPH & FRAP

Kubola & Siriamornpun (2011)

Methanol extract of immature Gac fruit

DPPH & FRAP

Spray-dried Gac aril powder Air-dried Gac aril powder

ABTS ABTS & DPPH

Vacuum dried Gac aril

ABTS & DPPH

Aril: IC50 = 3.66 mg g 1; FRAP: 531 lmol FeSO4 g 1 Pulp: IC50 = 2.53 mg g 1 FRAP: 466 lmol FeSO4 g 1 Peel: IC50 = 2.56 mg g 1; FRAP: 472 lmol FeSO4 g 1 DPPH: 45.1 mg AAE/100 g FRAP: 5.9 mg AEAC/100 g 1.4 mM TE g 1 ABTS: 0.37 mM TE g 1 DPPH: 0.33 mM TE g 1 ABTS: 162 mM TE g 1 DW DPPH: 124 mM TE g 1 DW

Bharathi et al. (2014) Kha et al. (2010) Kha et al. (2011) Mai et al. (2013a,b)

FRAP, ferric-reducing antioxidant power.

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corresponding extracts. In a recent study, Bharathi et al. (2014) studied the FRAP and DPPH radical scavenging activities of a methanol extract from a homogenised sample of whole immature Gac fruit. The assays showed that the antioxidant activity of the extract from 100 g Gac fruit was equivalent to 5.8 and 45.1 mg ascorbic acid for FRAP and DPPH, respectively. The all trans-lycopene extracted from Gac aril and its cis-isomer were also investigated for antioxidant capacity (Phan-Thi & Wache, 2014). The ABTS assay demonstrated that 1 lmol of the all trans-lycopene had an antioxidant power equivalent to 2.4 lmol of Trolox, and that the antioxidant activity of the heated extract, which contained more cis-lycopene, increased to a maximum value of 3.7 lmol Trolox equivalents. This result suggests that the isomerisation of lycopene from Gac fruit during extraction processes might result in a higher antioxidant activity for the extracts. The antioxidant activity of a Gac aril powder, which was prepared with 10% maltodextrin by spray drying at 120 °C to a moisture content of 4.9%, was shown to be equivalent to 1.4 mmol Trolox per gram in an ABTS assay (Kha et al., 2010). However, in a later study, these authors found a much lower antioxidant activity for Gac aril powder having a moisture content of 6%, which was obtained by air drying (Kha et al., 2011). To improve the retention of carotenoids and antioxidant activity of dried Gac aril, Mai et al. (2013a,b) produced a semi-dried Gac aril (15–18% moisture content) using a vacuum dryer at 60 °C. This semi-dried aril retained 81% and 87% of the total antioxidant capacity of the fresh aril in the DPPH and ABTS assays, respectively. Anticancer activity

Due to the high content of carotenoids and phenolic compounds of Gac fruit, several studies have been conducted on the anticancer activity of this fruit. These studies have demonstrated that extracts from the whole green fruit, the aril and especially the seeds possess significant anticancer abilities (Table 5). The antitumour activity of a water extract from the whole green Gac fruit was investigated by the treatment of Balb/c mice transplanted with the colon 26-20 adenocarcinoma and HepG2 cell lines (Tien et al., 2005). The results showed that the extract led to a significant decrease in the proliferation of colon 26-20 and HepG2 cells and a reduction of tumour weight in the treated mice. Furthermore, it was found that the Gac extract inhibited the tumour growth via inducing necrosis rather than apoptosis. Specifically, the downregulation of cyclin A, Cdk2, p27waf1/Kip1 was observed, while no decrease in p21waf1/Cip1 protein level was recorded. In other studies on Gacavit, a

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pharmaceutical product mainly comprised of Gac oil, the anticancer activity of oil from Gac aril was also demonstrated by its antitoxic effect on mice injected with dioxin and the inhibition of hepatocellular carcinoma hcc development in high-risk patients (Mao et al., 1992; Trinh, 1993). In addition to the aril and pulp, interest in the anticancer activity has also focused on the seeds due to the recent findings of saponins and several trypsin inhibitors in this fruit fraction. Ethanol extracts from Gac seeds showed a potential anticancer activity on a variety of cancer cell lines including lung carcinoma, breast carcinoma, oesophageal carcinoma and melanoma cells by the significant inhibition on the proliferation of these cell lines in a dose-dependent manner (Zhao et al., 2010). Ethyl ester extracts from Gac seeds also induced differentiation and suppressed the growth of mouse melanoma B16F1 cells and inhibited cell proliferation significantly even at a very low dose (5 lg mL 1). Moreover, the high cell viability and the increases in typical dendrite-like cellular protrusions and elongated cells suggest that the antiproliferative effect of the extract was caused by promoting cell differentiation rather than by inducing apoptosis (Zhao et al., 2012). To investigate the mechanism of action for the antiproliferative effect of Gac seed on cancer cells, the proliferation, apoptosis and cell cycle of human breast cancer MDA-MB-231 cells treated with Gac seed extract were analysed (Meng et al., 2012). The results showed that Gac seed extract dramatically inhibited the growth of the breast cancer cells in a dose- and time-dependent manner. The appearance of typical apoptotic morphology in the treated cells demonstrated that treatment with Gac seed extract induces apoptosis in the cell line. In addition, the extract also resulted in cell cycle arrest at the G2/M phase, which can trigger the proliferation inhibition of cancer cells (Chao et al., 2004). In a further study, Liu et al. (2012) found two pathways by which a Gac seed ethanol extract induced apoptosis and cell cycle arrest in human SGC7901 and MKN-28 gastric cancer cell lines. The treatment with the Gac seed extract resulted in a significant ratio of apoptotic cells and blocked the cells at the G0/G1 and G2/M phases. In addition, it was demonstrated that a decrease in the level of the nuclear enzyme PARP and an increase in the tumour suppressor gene p53 were likely to participate in the antiproliferative effect of the extract. Antimicrobial activity

The antimicrobial activity of Gac aril and pulp extracts was studied on both gram negative and positive bacteria. The water extract of the pulp exhibited prohibition of the growth of some bacteria, while no inhibition zone was determined in the treatment with

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Table 5 Anticancer activity of Gac fruit and products Material Water extract of Gac fruit

Treatment

Water extract of Gac seeds

0.75 mg DW of fruit g body weight 10–100 mg L 1

Ethyl ester extract of Gac seeds

5–200 lg mL 1, 72 h

Ethanol extract of Gac seeds

0.4 mg mL 1, 48 h

Ethanol extract of Gac seeds

0.8 mg mL 1, 48 h

1

Result

References

Reduction of 26% wet colon tumour weight

Tien et al. (2005)

Significant antiproliferative effect on lung (a549), breast (MDA-MB-231), oesophageal (TE-13) carcinoma cells and melanoma cell (B16) Significant antiproliferative effects on melanoma B16F1 cells via cell differentiation Significant inhibition on growth of human breast cancer MDA-MB-231 cells (30% apoptotic cells) Inhibition of 55% on cell viability of SGC7901 and 63% on MKN-28 human gastric cancer cells

Zhao et al. (2010)

water extract of the aril. For the ethanol extracts, both the extract from pulp and the extract from aril had significantly higher inhibitions on the growth of Micrococcus luteus 745 compared to the water extracts with inhibition zone diameters of 20 and 19 mm, respectively (Innun, 2012). The biological activities of Gac fruit illustrate that it might contribute significant benefits for human health. Thus, to exploit this bioactive resource more effectively, techniques for the isolation of bioactive compounds from Gac fruit as well as processes for the preparation of Gac products should be developed. Processing of Gac fruit

Because fresh Gac aril is very susceptible to oxidation and degradation by environmental conditions including oxygen, light, temperature and especially microorganisms, it needs to be processed to preserve the valuable carotenoids. In traditional processing, fresh Gac aril is usually exposed to sunlight until it is dry. The seeds are then removed before the dried aril is packaged and stored to use as a food colourant or a traditional medicine (Vuong et al., 2002). This method might cause significant loss of lycopene and b-carotene in the aril through degradation caused by the direct exposure to sunlight and oxygen. Therefore, several methods have been developed for processing Gac fruit, which can be classified into two major approaches: (i) dehydration to produce dried aril powder and (ii) extraction of oil from the aril, which contains a high concentration of carotenoids. Gac powder production

The effects of various drying methods and drying factors on the physiochemical properties, carotenoid content and antioxidant activity of Gac aril have been investigated for the production of Gac aril powder.

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Zhao et al. (2012) Meng et al. (2012) Liu et al. (2012)

Tran et al. (2008) studied the effects of enzyme pretreatments and drying methods on the degradation of carotenoids during the production of Gac powder. Although the enzyme treatments (Pectinex and Maxoliva) allowed the aril to be more easily separated from the seeds, they caused significant losses of carotenoids in the dried aril compared to the untreated samples. The dried Gac aril produced by freeze drying showed the highest total carotenoid content (7577 lg g 1) followed by that obtained from vacuum drying (5523 lg g 1), air drying (5426 lg g 1), oven drying (4825 lg g 1) and spray drying (380 lg g 1). The highest degradation of carotenoids in the spray drying process was explained by the use of a very high temperature for the inlet air (200 °C). For this reason, various temperatures and the use of maltodextrin as a drying assisting agent were investigated to reduce the loss of carotenoids during the preparation of Gac aril powder (Kha et al., 2010). An inlet-air temperature of 120 °C and a maltodextrin concentration of 10% w/v were found to be the most suitable conditions for retaining the carotenoids and total antioxidant activity of the dried powder. In a later study by these authors, different temperatures for air drying were investigated simultaneously with pretreatments for the retention of carotenoid content and antioxidant activity of Gac aril (Kha et al., 2011). An inverse association between the total carotenoid content of dried Gac aril and drying temperature was found when temperature was increased from 40 to 80 °C. Although most of the previous studies on drying Gac aril attempted to produce Gac aril powder having a moisture content of 6% or less, Mai et al. (2013a,b) carried out a limited drying process, which only dehydrated Gac aril to a moisture content of 15–18%, to maintain the nutritional value of the Gac aril. Interestingly, the optimal temperature for reducing carotenoid loss was 60 °C among the investigated range of 40–80 °C instead of the lowest temperature as reported previously by Kha et al. (2011). Carotenoids were more protected when the aril

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was dried at 60 °C because the drying time (5 h) was significantly shorter than that of drying at 40 and 50 °C (10–12 h). Because of the significant loss of carotenoids during the drying of Gac aril, a number of pretreatments and antioxidative agents have been investigated for protection of these carotenoids. For example, presoaking Gac aril with ascorbic acid or sodium bisulphite prior to drying significantly reduced the loss of carotenoids and antioxidant power of dried Gac aril prepared by hot air drying (Kha et al., 2011). In addition, blanching in citric acid and steaming exhibited a protective effect on carotenoids when drying at 60 °C was used to produce Gac aril powder having a moisture content of 6% (Dien et al., 2013). The blanching of Gac aril for 2 min at 80 °C with 0.04% citric acid and the steaming at 100 °C for 6 min prior to drying resulted in dried powders with 8.6% and 24.0% higher carotenoid content than the untreated sample, respectively. The use of a maltodextrin–gelatin mixture (1:1) in this study as a drying carrier also led to a remarkable protection against carotenoid loss. The obtained dried Gac powder had a 28.4% higher carotenoid content compared to the control. Other antioxidant agents including vitamin C and vitamin E were then investigated for their protective effects on the stability of b-carotene and lycopene during the drying of Gac aril (Minh & Dao, 2013). The addition of these vitamins into the drying carrier at a concentration of 0.2% resulted in a significant prevention of carotenoid loss in Gac aril during the drying process. These results suggest that pretreatments and drying assisting agents might be applied to achieve better retention of carotenoids in dried Gac aril. Gac oil production

As Gac aril has been shown to contain high levels of carotenoid-rich oil, a variety of processes to extract oil from the aril have been reported. The use of a manual single hydraulic press (1 kg Gac aril per batch), which can be used by homemakers, was investigated for the pressing of Gac oil (Vuong & King, 2003). The pressing of 5-min steamed aril produced 1 L of oil from 100 kg of ripe Gac fruit. The obtained oil was reported to have very high total carotenoid content (5770 mg L 1), which was comprised of 2710, 3020 and 334 mg L 1 of b-carotene, lycopene and atocopherol, respectively. In addition, the Gac oil was highly accepted by the local famers in Vietnam for daily consumption. To improve the extraction yield of oil from the aril, treatments of aril with microwaves (630W, 65 min) and steam (20 min) prior to the use of hydraulic pressing were investigated (Kha et al., 2013a). A very high extraction efficiency of oil (93%) was achieved from

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pressing (170 kg cm 2) of the treated Gac aril, which contained 414 and 140 mg L 1 of lycopene and b-carotene, respectively. The levels of these carotenoids in Gac oil were then significantly increased to 511 mg L 1 for lycopene and 174 mg L 1 for b-carotene by pressing of the microwave-dried aril instead of air-dried aril (Kha et al., 2014b). In addition to the use of pressing, the extraction of Gac oil by different solvents has been studied. Extractions using a chloroform:methanol mixture, petroleum ether and hexane were studied for improvement of lycopene and b-carotene content in the extracted Gac oil (Kubola et al., 2013). The use of different solvents resulted in significantly different amounts of carotenoids in the extracted oils. The oil extracted with the mixture of chloroform:methanol (2:1) contained the highest lycopene and b-carotene concentrations (0.49 and 1.18 mg g 1, respectively), while the hexaneextracted oil contained the lowest levels of these carotenoids (0.21 and 0.12 mg g 1, respectively). In this study, the application of hot air, low relative humidity air and far-infrared irradiation for the drying of Gac aril prior to the solvent extraction also led to remarkable increases in the carotenoid content of the extracted oil. While hot air drying resulted in the highest increase in lycopene content (166%), the highest increase in b-carotene was obtained from the drying using far-infrared irradiation (Kubola et al., 2013). In an attempt to extract Gac oil using water instead of organic solvents, various enzymatic treatments and the optimisation of the extraction factors were investigated (Mai et al., 2013a,b). In this study, dried Gac aril was ground and then mixed with water in a beaker. The mixture was then added with enzymes before being incubated with stirring. Finally, the mixture was centrifuged and dried to remove water and obtain the oil. Among the treatments with protease, cellulase, pectinase and a-amylase individually or in combination at different ratios, the combination of all enzymes at the ratio 1:1:1:1 resulted in the highest oil extraction yield (62.4%) with the highest carotenoid content (4.25 mg g 1). This result was six times higher than the oil yield obtained from the control sample (10%, no enzyme treatment), and it was explained by the breaking of the Gac aril cell wall seen by microscope observation. The optimal extraction conditions were determined as 14.6% (v/w) for the enzymes, 58 °C for the extraction temperature, 127 min for the incubation time and 162 rpm for the stirring. The extraction efficiency and the total carotenoid content from the optimal conditions were 79.5% and 5.3 mg g 1, respectively. Recently, supercritical carbon dioxide fluid has been investigated for the extraction of oil from Gac aril. Effects of enzymatic treatments, drying conditions, particle sizes of the Gac aril powder after grinding and extraction conditions on oil extraction

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efficiency were studied (Kha et al., 2014a). The pretreatments of the Gac aril and extraction time, temperature and pressure significantly influenced the oil extraction yield as well as the carotenoid level of the oil. The highest extraction efficiency of oil (95%) was achieved from the extraction at 200 bar, 50 °C for 120 min of the aril powder having a particle size of 0.45 mm, which was treated with 0.1% pectinase prior to being dried at 50 °C. Although lycopene and b-carotene are the most important bioactive compounds in Gac oil, they are very susceptible to storage conditions and can degrade rapidly during storage (Vuong & King, 2003). For this reason, the protection of the bioactive compounds in Gac oil has been studied. Kha and co-authors (2014c, d) recently investigated the encapsulation of Gac oil by spray drying. To improve the encapsulation efficiency of the oil, the spraying conditions and the wall materials were optimised. The use of a protein–polysaccharide matrix as wall material at 29.5% (v/v) relative to the Gac oil, for the microencapsulation by spray drying with inlet and outlet temperatures of 154 and 80 °C, respectively, was found as the optimal process for the production of encapsulated Gac oil powder. In the powder produced by the above optimal conditions, 92%, 80% and 74% of oil, b-carotene and lycopene in the oil were encapsulated by the wall matrix. The high encapsulation efficiencies of oil and the carotenoids suggest that the oxidation of Gac oil and carotenoid loss during storage can be reduced significantly by protection from the storage environment. In addition, the encapsulated powder showed an attractive orange–red colour and high solubility in water, which makes the powder easy to incorporate into various foods (Kha et al., 2014c,d). The results from the processing of Gac oil and Gac powder suggest that Gac fruit is a potential material for producing high-quality commercial products for food and medicinal uses. However, in addition to the development of products from Gac aril, the processing of the pulp, peel and seed should also be considered to further exploit the biological potential of compounds in these sources. Storage of Gac fruit and Gac products

The most valuable part of Gac fruit is the red aril due to its high concentration of carotenoids, which are very susceptible to degradation by environmental and storage conditions such as light, oxygen and temperature. Thus, one of the important issues for the storage of Gac products is the prevention of carotenoid loss. Because the harvesting period of Gac fruit is usually from October to the next February in Vietnam, farmers usually sun-dry the Gac aril and store it in tight containers under the absence of light for year round consump-

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tion. Recently, as the popularity of fridge-freezer units in households has increased, Gac aril is separated from the seeds, divided and packed into serving amounts and then stored in the freezer until being used. The frozen Gac aril can maintain its palatability from the end of a harvesting season to the beginning of the next or even for up to 1 year. Although Gac fruit has been reported as one of the richest carotenoid sources, there has been a limited number of investigations into the effects of storage on the nutritional quality and carotenoid content of Gac fruit and its products. In a study on the storage of fresh Gac fruit, changes in the carotenoid content of Gac fruit were investigated for 2 weeks under ambient conditions (Nhung et al., 2010). After 1 week of storage, the lycopene content significantly increased in the fruits at the green maturity stage, while b-carotene increased in both green and ripe fruits. However, a remarkable decline in the carotenoids was found after 2 weeks of storage at ambient temperatures with 2.7and 9-fold reductions seen for lycopene and b-carotene, respectively. The storage of Gac oil was also investigated in this study at different temperatures with and without antioxidant treatments. The storage of Gac oil at 45 and 60 °C significantly increased the degradation of both lycopene and b-carotene compared to storage at 5 °C and at the ambient temperature (20–25 °C). The addition of 0.02% (w/w) butylated hydroxytoluene (BHT) into the oil and the use of a nitrogen stream to exclude oxygen lowered carotenoid loss during storage at 5 °C and at the ambient temperature but had no effects during storage at the higher temperatures (Nhung et al., 2010). In an earlier study, Gac oil obtained from an extraction by a manual press was stored under ambient conditions in the local farmers’ kitchens for 3 months. Although 45% of the total carotenoid was lost during storage, the oil still provided 3190 mg L 1 of carotenoids and was highly accepted by the local farmers for making the glutinous rice dish, mixing with vegetable dishes and soups, and even for skin care (Vuong & King, 2003). For the storage of Gac powder, dried Gac powder was stored in vacuum packages under the absence of light at 5, 25 and 37 °C to examine the influence of temperature on the stability of the carotenoids in the powder (Tran et al., 2008). The results showed that the loss of total carotenoids was significantly decreased at low storage temperatures. The powder stored at 5, 25 and 37 °C retained 75%, 70% and 46% of its total carotenoids after 4 months, respectively. Similarly, for the storage of semi-dried aril (15–18% moisture content), only a negligible loss of the carotenoids was observed after 3 weeks in a refrigerator, and the level of microorganisms remained within the accepted limit for 21 weeks (Mai et al., 2013a,b). The addition of antioxidative agents during the drying of Gac aril not

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only prevented carotenoid loss in the processed Gac powder but also significantly protected the carotenoids during the storage of the product (Minh & Dao, 2013). Specifically, Gac powder dried with supplements of vitamin C or vitamin E maintained 70% of its carotenoids after 3 months of storage at 10 °C in the absence of light and oxygen. These studies demonstrate that carotenoids in Gac fruit and its products are very easily degraded by the impact of storage conditions including light, temperature and oxygen. Therefore, further studies need to focus on the influence of these factors on Gac products so that a better preservation of their carotenoids can be achieved. Utilisation of Gac fruit

Gac aril has long been used by Asian people as a natural colour for traditional foods. In Vietnam, the aril is used widely to provide red colour, a lustrous appearance and an oil-rich taste for the glutinous steamed rice dish (xoi gac), a traditional food of Vietnamese people for important occasions such as weddings and the Lunar New Year. In addition to the use in xoi gac, Gac aril is added into other kinds of foods such as stir-fried dishes and soups to improve their appearance as well as to provide a nutritional supplement for the foods. The aril and the oil obtained from the aril are also used as supplements for the treatment of ‘dry eyes’ (xerophthalmia) and night blindness, which are caused by the lack of vitamin A, as well as for promoting healthy vision (Vo-Van-Chi, 1997). Recently, commercial Gac products such as frozen Gac aril, Gac oil and dried Gac aril powder have been introduced into the market for food, medicinal and cosmetic uses. In general, only the red aril of Gac fruit is used for food, medicine and cosmetics, while the other parts including seeds, pulp and peel are discarded. The pulp and the peel removed from the processing of Gac are usually treated to produce organic fertiliser or used for feeding cattle. The seeds from Gac have been used as a traditional Chinese medicine called mubiezhi for the treatment of cancers in the Inner Mongolian tribe areas and various other diseases such as mastitis, boils and pyodermas (Huang et al., 1999; Zhao et al., 2012). Although Gac fruit is mostly consumed at the fully ripe stage, the green fruit is commonly used as a vegetable for cooking in Thailand and India. At the immature stage, the fruit meat, which has a flavour similar to papaya, is consumed with chilli paste after being boiled or used in curries (Kubola & Siriamornpun, 2011). Conclusion

Gac fruit, which has been used in traditional Asian cuisine and medicine, has been demonstrated to

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contain very high levels of beneficial carotenoids including lycopene, b-carotene and lutein. In recent decades, this fruit has emerged as a potential material for the functional food industry due to its biological activities and the success of the presently available products. However, there are still many obstacles, which need to be resolved through research for the development of the Gac processing industry to be assured. For example, inconsistent and sometimes conflicting data on the carotenoid content and the bioactivity of Gac fruit have been reported. Although several bioactivities have been reported for Gac fruit, there has been no study on the contribution of its individual bioactive compounds to these activities. In addition, after the removal of the aril, the disposal of Gac pulp and peel, which constitute the major proportion of the whole fruit by weight and which have a significant content of the carotenoids, especially lutein, needs to be addressed. This resource should be more effectively utilised to avoid potential environmental issues and to prevent the wasting of an important source for the carotenoids. If the above problems are resolved successfully and economically, Gac fruit will become one of the most important carotenoid-rich sources for the food and medicinal industries. References Aoki, H., Kieu, N.T., Kuze, N., Tomisaka, K. & Van Chuyen, N. (2002). Carotenoid pigments in GAC fruit (Momordica cochinchinensis Spreng). Bioscience, Biotechnology, and Biochemistry, 66, 2479–2482. Bharathi, L.K., Singh, H.S., Shivashankar, S., Ganeshamurthy, A.N. & Sureshkumar, P. (2014). Assay of nutritional composition and antioxidant activity of three dioecious Momordica species of South East Asia. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences, 84, 31–36. Bhuvaneswari, V. & Nagini, S. (2005). Lycopene: a review of its potential as an anticancer agent. Current Medicinal Chemistry: Anti-Cancer Agents, 5, 627–635. Booth, A.N., Robbin, D.J., Ribelin, W.E. & DeEds, F. (1960). Effect of raw soybean meal and amino acids on pancreatic hypertrophy in rats. Proceedings of the Society for Experimental Biology and Medicine, 104, 681–683. Brown, M.J., Ferruzzi, M.G., Nguyen, M.L. et al. (2004). Carotenoid bioavailability is higher from salads ingested with full-fat than with fat-reduced salad dressings as measured with electrochemical detection. American Journal of Clinical Nutrition, 80, 396–403. Chao, J.I., Kuo, P.C. & Hsu, T.S. (2004). Down-regulation of survivin in nitric oxide-induced cell growth inhibition and apoptosis of the human lung carcinoma cells. Journal of Biological Chemistry, 279, 20267–20276. Dien, L.K.L., Minh, N.P. & Dao, D.T.A. (2013). Investigation different pretreatment methods and ratio of carrier materials to maintain carotenoids in Gac (Momordica Cochinchinensis Spreng) powder in drying process. International Journal of Scientific & Technology Research, 2, 360–371. G omez-L opez, V.M. (2002). Fruit characterization of high oil content avocado varieties. Scientia Agricola, 59, 403–406. Hazewindus, M., Haenen, G.R.M.M., Weseler, A.R. & Bast, A. (2012). The anti-inflammatory effect of lycopene complements

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