Gac (Momordica cochinchinensis Spreng) fruit: A functional food and medicinal resource

Journal of Functional Foods 62 (2019) 103512

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Gac (Momordica cochinchinensis Spreng) fruit: A functional food and medicinal resource

T

Thi Van Thanh Doa, Liuping Fana, , Wildan Suhartinia, Mogos Girmatsionb ⁎

a b

State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, Wuxi, Jiangsu 214122, China Collaborative Innovation Center of Food Safety and Quality Control in Jiangsu Province, Jiangnan University, Wuxi 214122, Jiangsu, China

ARTICLE INFO

ABSTRACT

Keywords: Gac fruit Carotenoids Oil extraction Pharmacological activity Gac products

Knowledge of functional foods and medicine has a specific contribution to improving our health and has grown immensely over the past decade. The relationships between special food components, their physiological functionality, and health benefits need to be explored continuously. These fundamentals could help to reduce current healthcare costs by improving health and disease prevention. This paper provides insight into the emergence of Gac fruit in recent research literature. Gac fruit cultivation, the application of different methods in processing and production, as well as pharmacological activity are discussed. The storage and use of this fruit, as well as its commercial products are also reviewed. Food, agricultural, and medical sciences need to make further progress to meet the demand and deepen the understanding of consumers of Gac fruit. This will also enhance utilization of Gac fruit and reduce waste disposal from Gac processing for use in the food and pharmacological industries.

1. Introduction Gac (Momordica cochinchinensis Spreng.) fruit belongs to the Curcurbitaceae family, originally discovered in Vietnam. The Gac plant is a type of vigorously perennial vines where males and females flower on separate plants. It is native to and grown throughout South and Southeast Asia and Northeastern Australia (USDA, 2019). This tropical and subtropical vine was given the name Muricia cochinchinensis by Loureiro, a Portuguese missionary priest when visited Vietnam in 1790. Later, Sprengel concluded that the plant belonged in the Linnaean genus Momordica and changed the name in 1826 (Vuong, 2000). The species name cochinchinensis is derived from the Cochinchina region in northern Vietnam, although it is grown and consumed in many parts of the world (Vuong, Franke, Custer, & Murphy, 2006). Gac fruit is indigenous to temperate Asia (China, Japan, and Taiwan), the Indian subcontinent (Bangladesh and India in the specific areas such as Assam, Nagaland, Tamil Nadu, Uttar Pradesh, and West Bengal), Papuasia (Papua New Guinea), Indochina (Thailand, Cambodia, Laos, Vietnam, Myanmar), Malesia (Philippines, Malaysia, and Indonesia), and Northeastern Australia (Queensland) (Herklots, 1973; Perry & Metzger, 1980; USDA, 2019). However, Gac fruit is currently only planted as a commercial crop on a limited scale in Vietnam and Thailand. The ripe fruit is normally picked from August to February in outdoor growing systems. To meet Gac fruit demands and ⁎

provide stability all year round, greenhouse growth systems need to be expanded. In recent decades, Gac fruit has emerged as one of the richest natural sources of carotenoids compared to other well-known fruits and vegetables due to the extremely high levels of lycopene and β-carotene in its oily seed membrane (Chuyen, Nguyen, Roach, Golding, & Parks, 2015; Ishida, Turner, Chapman, & McKeon, 2004). Gac is considered to be good for health, and has been utilized traditionally as a food and folk medicine source in Southeast Asia. Many components of Gac such as its seeds, oil, and root are used in traditional medicine (Nhung, Bung, Ha, & Phong, 2010). Gac functional components such as carotenoids, αtocopherol, omega-3 fatty acids, polyphenol compounds, and flavonoids have significant health benefits for humans (Abdulqader, Ali, Ismail, & Esa, 2018a; Ishida et al., 2004). Because of the high phytonutrient value in all its fractions (i.e. aril, seeds, pulp and, peel) and medicinal and pharmaceutical properties, Gac fruit has earned the name “super fruit” or “heaven’s fruit” (Parks, Nguyen, Gale, & Murray, 2013; Wong, Fong, & Ng, 2004). Applications of Gac fruit have focused on producing Gac powder and Gac oil as nutrient supplements, natural colorants, and for medicinal purposes. When Gac oil is applied to wounds, skin infections and burns, it stimulates the growth of new skin and the healing of wounds (Mai & Debaste, 2019). The fruit is also used as a traditional remedy to treat arthritis, cardiovascular disease, and degeneration of the macula (Burke, Smidt, & Vuong, 2005). Commercial Gac products available to global consumers are mostly from

Corresponding author. E-mail address: [email protected] (L. Fan).

https://doi.org/10.1016/j.jff.2019.103512 Received 21 April 2019; Received in revised form 8 August 2019; Accepted 11 August 2019 1756-4646/ © 2019 Elsevier Ltd. All rights reserved.

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Fig. 1. Phytochemical composition, options for processing, and potential health benefits of Gac fruit.

Vietnam and China. These products include frozen Gac aril, Gac powder, Gac oil, Gac oil capsules, and functional beverages (Aamir & Jittanit, 2017). In Vietnam, VNPOFood is the largest manufacturer with a capacity of 3000 tons of Gac fruit per year. In addition to its primary use in food, another potential market for Gac fruit is the cosmetic industry (Parks, Nguyen, et al., 2013). The purpose of this review is to summarize Gac’s cultivation reports, potential bioactive compounds, processing, uses, and storage of whole fruit as well as its products (Fig. 1). Previous published literature is referred to for historical perspective when necessary. Reviews by Chuyen et al. (2015), Kha, Nguyen, Roach, Parks, and Stathopoulos (2013), and Abdulqader et al. (2018a) should be consulted for earlier literature.

can extend to 20 m long. Gac fruit is typically oblong and almost round or ovoid in shape (John et al., 2018; Lim, 2012). The fruit is covered with short spines. There is variety among different fruits with respect to their spines and fruit tips. In some fruits the spines are smooth and dense whereas in others they are hard and widely spaced. The fruit is composed of a peel covered in sparse or dense spines (exocarp), an orange spongy mesocarp (pulp), a red membrane (aril), and brown or black seeds (Fig. 2). Each fruit has an average of between 15 and 20 seeds and Gac seeds which are round, compressed, and sculptured (Vuong, 2000). The color of the fruit changes from green to yellow, orange and finally red when ripening.

2. Characteristics and cultivation of Gac fruit

Seed germination then ground planting is the main propagation method for Gac fruit in Asian countries, though cutting and grafting methods are also utilized. The plant can be cultivated from root tubers as well. Seed germination is a simple process not affected by prolonged dormancy and does not require the deshelling of seeds (Parks, Murray,

2.2. Propagation

2.1. Morphology Gac plants produce flowers about 5–10 cm in length, and the vines 2

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Fig. 2. Anatomy of Gac fruit (a) young fruit and (b) medium ripe fruit (1. Aril, 2. Seed, 3. Pulp, 4. Peel with spines (skin)).

Gale, Al-Khawaldeh, & Spohr, 2013). Selecting seeds to grow seed sprouts is important in the germination step of propagation. Robust seeds for germination should be extracted from large and fully ripe fruit, then selecting only seeds that sink in water. Good seed candidates sink because of increased density which indicates they are matured enough to germinate successfully. The selected seeds are laid flat in seed raising mix (2:1:1 pine bark: sand: peat moss) in trays (approximately 10 cm apart), then covered with mix. Trays are placed in open space with enough sunlight in the morning but protected from excessive exposure throughout the day, or are placed in a propagation house with average temperature of 25 °C, and relative humidity of 80%. Seed germination time is around 3 weeks, then the plants are transplanted into 150 mm pots with potting mix (1:1 coir: perlite) and/or grown on land (Parks, Murray, et al., 2013).

above the ground. The plant starts flowering about two months after being planted. In general, flowering occurs from April to July, and sometimes August to September (Vuong, 2000). The plants are pollinated by native bees and insects, but hand pollination is essential to get higher fruit set and yield, especially where its natural pollinators are absent (Maharana, Sahoo, & Tripathy, 1995; Pessarakli, 2016). Dabbing the stamen (male) on the stigma (female) is the method used to handpollinate the female flowers by pollen from male flowers. The pollen can be dusted on receptive stigma by using a paint brush, preferably in the morning for higher fruit setting. Male and female flowers can be identified by their characteristics: male flowers have larger petals and are light in color, while female flowers have a darker yellow flower with 5 simple elliptical petals as shown in Fig. 3 (Parks, Nguyen, et al., 2013).

2.3. Growing medium and fertilizer

2.5. Harvest

Fertilizer and water requirements for Gac fruit are different depending on the method of farming. Hydroponic methods used to grow cucumbers can be used. According to Mason (2000), hydroponic stock solution is prepared in two 60 L containers. The first container contains 4500 g of calcium nitrate, 180 g of iron EDTA, and water is added up to 60 L. The second container contains 6000 g of potassium nitrate, 1200 g of mono-potassium phosphate, 3600 g of magnesium sulphate, 48 g of manganese chelate, 15 g of zinc chelate, 15 g of boric acid, 33 g of copper chelate, 7.2 g of ammonium molybdate, and then water is added up to 60 L. The method for growing in soil is based on field grown bitter melon (Momordica charantia) (Palada & Chang, 2003) which prefers a drained soil with pH range from 6 to 6.5. Before planting a crop, the nutrient status and pH of soil should be determined so fertilizer programs can be adjusted accordingly (Eghball & Power, 1999). Compost and manure may be supplied before planting. Both compost and manure applications are a good organic source of the major elements nitrogen (N), phosphorus (P) and potassium (K) (referred to as NPK), reducing the need of chemical fertilizers for the crop. Gac fruit fertilization can be adjusted to two specific growth stages. The first stage from planting to flowering requires the ratio of NPK per hectare per week as follows: 25 kg N, 5 kg P, and 18 kg K. The second stage from fruit initiation to onwards needs 2 kg N, 5 kg P, 18 kg K, and 5 kg Ca (Traynor, 2005).

The harvest time of Gac fruit differs between countries depending on the desired state of consumption. Fruits reach harvestable maturity 15–20 days after pollination if the whole fruit is to be consumed as vegetables as preferred in India and Bangladesh. Beyond this time, the seeds become hard and the skin becomes leathery (Bharathi & John, 2013). The fruit is harvested at a ripe stage for its red aril at 90–110 days and 45–50 days after pollination as preferred in Vietnam and Malaysia, respectively, when the fruit turns soft quickly after harvesting (Bharathi & John, 2013; Osman, Sulaiman, Saleh, Rahman, & Sin, 2017; Pessarakli, 2016). The crop takes approximately 44 weeks from seed germination to harvest by the greenhouse system used in Australia (Parks, Murray, et al., 2013). The fresh fruit in Malaysia ranged from 390.8 g to 1057.8 g (Osman et al., 2017) while in Australia it ranged between 517 g and 2168 g (Parks, Nguyen, et al., 2013). However, the weight and size of Gac fruit varies depending on the growing area as well as growing system, soil type, and each country may have different specific fruit type. A plant produces 30–60 fruits on average in a season (Vuong, 2000). The highest weight contributing anatomical component of the fruit is the pulp in the range of 49–75% of total weight. The aril in range of 6–31% (Ishida et al., 2004) and the peel is about 17% (Osman et al., 2017). Storage time and growth stage when water loss may occur and contribute to the variation (Nhung et al., 2010). The common name, growing system, and harvest time of the Gac fruit in different countries are listed in Table 1.

2.4. Trellising and pollination

3. Phytonutritient composition of Gac fruit

Gac fruit is a climbing vine crop, which requires to be trellised to allow development and fruit production. Trellising prevents fruit from growing on the ground and rotting when it is ripe and soft. Plants are grown on a horizontal trellis with wires placed at 1 m, 1.8 m, and 2.8 m

Gac fruit contains carotenoids and other bioactive compounds such as phenolics, flavonoids, and vitamin C (Kubola & Siriamornpun, 2011). Carotenoids and bioactive compounds provide health benefits such as 3

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Fig. 3. (a) Male flower and (b) Female flower.

than other fractions and was followed by the pulp (18.1 mg/g) of immature fruit (Kubola & Siriamornpun, 2011). The lutein content did not increase with the development of the fruit (peel: medium ripe > full ripe > immature). The intake of lutein, or a diet supplemented with lutein in fruits and vegetables plays a critical role in the development of the brain and cognitive functions, and are important to reduce the risks of cataract development and macular degeneration (Shegokar & Mitri, 2012). Vitamin E is also found in Gac fruit (Vuong & King, 2003) which plays an important role in protecting the natural polyunsaturated oils in the fruit from oxidization. The content of nutrient and phytochemical composition in Gac fruit differs in fraction, maturity stages, genetic and environmental factors, post-harvest degradation during transportation and storage, and required applied analysis methods (Bhumsaidon & Chamchong, 2016; Nhung et al., 2010; Tran et al., 2016). Furthermore, differences in crop production and harvest time may also be important (Tran, Parks, Nguyen, Roach, & Kha, 2017).

anti-inflammation, anti-oxidant effects, cancer prevention, the maintenance of vision, embryonic development and reproduction, immune modulation, and neuroprotective effects (Chen, Huang, & Chen, 2019; Petyaev, 2016; Saini, Nile, & Park, 2015). Aril of Gac fruit has high carotenoid contents, at levels that surpass those of other main dietary plant sources. There have been several analyses of the widely variable carotenoids in Gac fruit. The discrepant results of aril total carotenoid contents have been determined as 294.5 mg/100 g fresh weight (FW) (Ishida et al., 2004), 49.7 mg/100 g FW (Vuong et al., 2006), 410.7 mg/ 100 g FW (Nhung et al., 2010), 78 mg/100 g FW (Tran, Parks, Roach, Golding, & Nguyen, 2016), and 13.81 mg/100 FW of the color break stage, 36.53 mg/100 g FW of the medium ripe stage and 89.27 mg/ 100 g FW of the fully ripe stage (Bhumsaidon & Chamchong, 2016). The lycopene and beta-carotene contents in the aril were found to be much higher than in the pulp and peel (Aoki, Kieu, Kuze, Tomisaka, & Chuyen, 2002). During fruit development from green stage to full ripe stage, contents of lycopene and β-carotene increased, and the contents of total phenolic and total flavonoid in peel and pulp decreased as reported by Kubola and Siriamornpun (2011). The authors showed the total phenolic content values from greatest to least as aril, peel, pulp, then seed, while the highest total flavonoid content values were obtained for the peel followed by aril, pulp and seed. Gac fruit has a high concentration of linoleic acid omega-6 and omega-3 fatty acids. The main fatty acids in the aril were identified as oleic, palmitic, and linoleic while the predominant fatty acids in the seeds were stearic followed by linoleic, oleic, and palmitic (Ishida et al., 2004). The ascorbic acid content of Gac fruit was 42.57 mg/100 g under wild growing condition (Sarmah, Dutta, & Sarma, 2018). Gac seed is a good source of unsaturated fats (Matthaus, Vosmann, Pham, & Aitzetmuller, 2003; Shang, 2000), and contains multiple trypsin inhibitors which might contribute to its medicinal activity (Jung et al., 2013b). Three major saponins were isolated from ethanol extract of the Gac seed (Fig. 4), including gypsogenin 3-O-β-D-galactopyranosyl(1 → 2)-[α-L rhamnopyranosyl(1 → 3)]-β-D-glucuronopyranoside (compound 1), quilliaic acid 3-O-β-D-galactopyranosyl(1 → 2)-[α-L-rhamnopyranosyl(1 → 3)]β-D-glucuronopyranoside (compound 2), and momordica saponin I (compound 3) (Jung et al., 2016). These compounds have been demonstrated as promising candidates for effective therapeutic intervention in cisplatin-induced renal injury and anti-inflammation (Jung et al., 2013b, 2016; Yu et al., 2017). Gac seeds have been used in China and Vietnam as traditional medicine for treating a range of issues such as diarrhea and dysentery, liver and spleen disorders, haemorrhoids, wounds, bruises, swelling, and pus (Crisp, 2012; IwAMoTo et al., 1985). The pulp and peel contain carotenoids such as β-carotene, lycopene, and lutein. Remarkably, the highest lutein content was found in the peel (52.02 mg/g) of medium ripe fruit which was substantially higher

4. Processes of Gac fruit Gac fruit contains high levels of carotenoids, α-tocopherol, and fatty acids in its different fractions such as aril, seeds, yellow pulp, and skin. Health benefits and pharmacological actions associated with these compounds have been extensively demonstrated (Bernstein et al., 2016; Bhuvaneswari & Nagini, 2005; Schwarz et al., 2008; Vuong, Dueker, & Murphy, 2002). Therefore, it is very important to exploit and enhance these effective phytochemical resources, process them for extraction, and preserve the bioactive compounds. There currently exist some potential ways to accomplish this including drying processes, oil and bioactive compound extraction, encapsulation, and incorporation of Gac fruits into other foods. 4.1. Drying process for powder production The removal of moisture from a food product is one of the oldest preservation methods. The benefits of drying Gac fruit are to prolong product shelf-life, reduce the costs of transportation and storage, and extend the possibility of out-of-season availability. Furthermore, dried Gac powder can be used as natural food colorant or for subsequent use for further processing (Uearreeloet & Konsue, 2016). Drying not only reduces water activity of raw materials, but also alters other physical, chemical, and biological properties, such as antioxidant capacity, enzymatic activity, aroma, flavor and so on. Hence, the selection of an appropriate drying technology to maintain nutritional value, content of carotenoids, and other bioactive compounds in Gac fruit is critical for the food and pharmaceutical industries. To improve dried product quality and to accelerate the drying 4

Journal of Functional Foods 62 (2019) 103512 (Bhumsaidon & Chamchong, 2016; Kubola & Siriamornpun, 2011) (Osman et al., 2017; Vuong, 2000) (https://www.boombastis.com/manfaat-buah-gac/154102) (Lim, 2012) (Akhter et al., 2014; Lim, 2012) (Bharathi & John, 2013; Lim, 2012) (https://ja.wikipedia.org/wiki/nanbankarasuuri) (Vuong, 2000) (Lim, 2012)

(Ishida et al., 2004; Vuong, 2000) (Chen, 2010; Lim, 2012) (Parks, Murray, et al., 2013; Tran et al., 2017)

process, pretreatment is often employed before drying (Yang, Zhang, Mujumdar, Zhong, & Wang, 2018). Tuyen, Nguyen, and Roach (2011) considered the effects of pretreatments such as blanching, soaking in bisulfite or ascorbic acid on color characteristics, total carotenoid content (TCC) and total antioxidant activity (TAA) in the aril powders. Results showed that pre-soaking in solutions of ascorbic acid or bisulfite prior to hot air drying at the lowest temperature of 40 °C was effective in temperature regimes of 40 °C, 50 °C, 60 °C, 70 °C, and 80 °C. The higher the drying temperature, the greater loss of TCC and TAA was in the powder. Between blanching, blanching in citric acid solution, and steaming, Dien, Minh, and Dao (2013) found steaming for 6 min as the best pretreatment method for the protection and maintenance of TCC in Gac powder dried at 60 °C. Another study by Tran, Nguyen, Zabaras, and Vu (2008) investigated pretreatment using different enzymes and dehydration approaches with different drying techniques. The powder produced with enzymatic pre-treatment had a lower carotenoid content than the enzymatic-untreated powder when applying the same drying method. However, the heat and enzymatic pre-treatments could be applied in seed removal for the mass production of the aril powder. Out of five different drying methods, including oven drying, air drying, vacuum drying and spray drying, freeze-drying whole-seed aril produced Gac powder with the highest carotenoid content and brightest color. It goes without saying that freeze drying is a means for retaining sensory, nutritional, and functional properties of foods, however it is not widely applied in the food industry due to its high operating cost, 4–8 times higher than hot air-drying (Ratti, 2001). Regarding spray drying conditions, a good quality aril powder in terms of color, TCC, and TAA can be retained at an inlet temperature of only 120 °C and adding maltodextrin concentration at 10% w/v (Tuyen, Nguyen, & Roach, 2010). All aforementioned studies (Tran et al., 2008; Tuyen et al., 2010, 2011) for drying of Gac arils focused on drying to a drybased moisture content of 6%. Mai, Truong, Haut, and Debaste (2013) limited dry based water content (db) of 15–18% by air drying or vacuum drying techniques to quantitatively evaluate the interest of limited drying of Gac arils compared with the classical final 6% db. However, the obtained results showed the TCC maintenance was significantly lower than Tran et al. (2008) for similar drying conditions. Tuyen et al. (2011) showed that the total carotenoid loss was the lowest for drying at 40 °C while the study of Mai, Truong, Haut, et al. (2013b) observed an optimal preservation at a higher temperatures (50–60 °C). These differences might be correlated to the choice of final moisture content, local drying conditions, and measurement methods. Gac pulp and peel constitute the major proportion of the whole fruit by weight and also contain a significant content of the carotenoids. Tens of thousands of tons of Gac fruit are processed yearly in Vietnam, thus thousands of tons of Gac peel are estimated to be discarded annually. Moreover, they are easily perishable and degraded if not stored properly. This makes drying an attractive option to utilize the pulp and peel for powder production. Trirattanapikul and Phoungchandang (2016) investigated the effects of both Gac maturity stages and drying methods on the physical, chemical, and antioxidant properties of Gac fruit pulp. The results indicated drying could be applied at both maturity stages of ripe Gac fruit (59–62 days with orange skin and 63–67 days with red skin) to obtain dried product with high quality and high nutritional value. Out of five drying methods including, tray drying, microwave drying, mixed-mode solar drying, freeze drying, and heat pump-assisted dehumidification, the later at 60 °C offered the best quality of dried Gac pulp, reduced drying time by 25%, and increased lutein, total phenolics and antioxidant activity by 12.6%, 32.0% and 0.3%, respectively. Therefore, the most promising drying method for Gac pulp fruit is heat pump-assisted dehumidification drying. It is recommended that Gac peel dried by hot air undergo pretreatment with ascorbic acid prior to drying at a temperature of 70 °C to improve the loss of carotenoid and maximize antioxidant retention in the Gac peel (Chuyen, Roach, Golding, Parks, & Nguyen, 2017a).

Fakkao, Bai-Khai-Du, Phak-Khao. Teruah Tepurang, teruah, pupia, pakurebu Kakrol Bhat-karela, Gangerua, Kakrol, Kantola. Kusika, Mokubetsushi Balbas-Bakiro, Buyok-Buyok Thailand Malaysia Indonesia Bangladesh India Japan Philippines

May – July 45–50 days after pollination December – January August 15–20 days after pollination December – January September – December

Outdoors/Soil Outdoors/Soil Greenhouses/Substrate Outdoors/Soil Outdoors/Soil Outdoors/Soil Outdoors/Soil Outdoors/Soil Outdoors/Soil Outdoors/Soil Outdoors/Soil August – February August-October Depends on growing system Gac, Moc miet tu Mu bie guo, Mubiezi Gac fruit, baby jackfruit, spiny bitter gourd, cochinchin ground. Vietnam China Australia

Harvest Time Name Country

Table 1 Common name, harvest time, and growing system of Momordica cochinchinensis Spreng in different countries.

Growing system

Reference

T.V.T. Do, et al.

5

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Fig. 4. Chemical structures of compounds 1–3.

pressure of 170 kg/cm2 with 900 g samples to attain the highest extraction efficiency (EE). Furthermore, these authors concluded the optimum extraction conditions of microwave-assisted extraction at 630 W for maximizing EE and carotenoid contents were microwaving time of 62 min, steaming time of 22 min, and a hydraulic pressure of 175 kg/ cm2 (Kha, Nguyen, Phan, Roach, & Stathopoulos, 2013). For comparison in the yield, nutrients, and chemical properties of oil, (Kha, Nguyen, Roach, & Stathopoulos, 2014) continued to conduct further research in oil extraction of the microwave-dried and air-dried samples using both of hydraulic pressing and Soxhlet extraction. The results showed that the oil yield achieved from pressing was lower than that of Soxhlet extraction for dried arils, however, the highest oil quality was obtained by the microwave-drying and pressing method. The same trend was reported by Le, Parks, Nguyen, and Roach (2018) when the Soxhlet method and the supercritical carbon dioxide (SC-CO2) method were compared. A higher oil yield was obtained by Soxhlet extraction than the SC-CO2 oil but with lower oil quality. Microwave irradiation pretreatment is an important procedure to enhance lycopene extraction efficiency of Gac aril for SC-CO2, press, and ethanol extractions due to the effects of the Z-isomerization (Honda et al., 2018). Z-isomers of carotenoids have higher solubility than all-E-isomers (Honda et al., 2017). So increasing content of lycopene Z-isomers contained in the

4.2. Oil and bioactive compound extraction Gac fruit is a potential source of oil and carotenoids. Choosing the correct extraction methods and optimizing extraction conditions are essential to meet requirements of yield and quality, convenience, health concerns, and environmental problems. Many researchers have conducted oil or carotenoid extractions from Gac fruit and their results are summarized in Table 2. Recovery of oil and carotenoids from Gac aril by mechanical pressing is the most widely used method in the oil processing industry (Vuong, 2000). Gac aril was smashed and heated slightly with 5 min of hot steaming before pressing to produce 1L of oil from 100 kg of whole fresh Gac fruit. Batch times of 10–20 min resulted in 50% oil yield and total carotenoids of 5.77 mg/mL (1st analysis) and 3.19 mg/mL (2nd analysis) in Gac oil as reported by Vuong and King (2003). The oil obtained from this press production was well accepted by assessment of local households in Vietnam as a healthful plan oil. To improve oil extraction efficiency by mechanical extraction, Tuyen, Nguyen, Roach, and Stathopoulos (2013) demonstrated that microwave drying pretreatment was superior to air drying pretreatment prior to steam treatment and pressing. The most suitable processing conditions for Gac oil extraction were microwave power of 630 W, microwave time of 65 min, steaming time of 20 min and hydraulic 6

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Table 2 Application of different methods in Gac bioactive compound and oil exaction. Part of Gac fruit

Method of extraction

Extraction objectives

Aril

Microwave-assisted extraction Microwave-assisted extraction Hydraulic press Soxhlet extraction

Oil and oil Oil and oil Oil and content

Organic solvent extraction Organic solvent extraction Organic solvent extraction

Oil and carotenoids in oil Oil Carotenoids in oil

Oil and carotenoids in oil Oil

Aril

Enzyme-assisted extraction Enzyme-assisted extraction Ultrasound-assisted extraction SC-CO2 extraction

Aril

SC-CO2 extraction

Aril

SC-CO2 extraction

Peel

Organic solvent extraction SC-CO2 extraction Soxhlet extraction

Aril Aril

Aril Aril Aril and seed

Aril Aril Aril

Seeds Seeds

Solvent extraction

Solvent extract/Enzyme

Result

Reference

Oil

Bioactives 1.40 mg/mL-C 4.14 mg/mL -L 1.86 mg/mL-C 5.18 mg/mL-L 1.74-C, 5.11-L (mg/mL) 0.62-C, 2.72-L (mg/mL) 1.06-C, 3.22-L (mg/mL) 0.30-C, 1.96-L (mg/mL) 320 mg%-C

carotenoids in

–

EE: 93%

carotenoids in

–

EE: 86%

bioactive in oil

Petroleum ether 60–90 °C

n-hexane

Y: Y: Y: Y: Y:

n-hexane

EE: 81.4%

Chloroform: methanol (2:1 v/v) Petroleum ether Hexane Cellulase, pectinase, protease and α-amylase Viscozyme L

Oil and carotenoids in oil Oil and carotenoid content Oil and carotenoid content Oil and bioactive content in oil Carotenoids and antioxidant capacity Oil

CO2 acetone, ethanol, ethyl acetate and hexane CO2 Hexane

Y: 34.1% Y: 53.02%

Bioactive compounds

Water

–

Water saturated butanol

–

27% - MDB 20% - ADB 31% - MDS 30% - ADS 96.4%

(Tuyen et al., 2013) (Kha et al., 2013) (Kha et al., 2014)

(Thuat, 2010)

–

0.58 mg/g-C 0.16 mg/g-L Aril: 1.18-C, 0.49-L (mg/g)

(Kubola et al., 2013)

– – R: 79.5%

Aril: 0.14-C, 0.3-L (mg/g) Aril: 0.12-C, 0.21-L (mg/g) 5.3 mg/g-TC

(Mai, Truong, & Debaste, 2013)

R: 96.39%

1.96 mg/g-TC

(Nhi & Tuan, 2016)

Deionized water

EE: 90%

(Tuyen et al., 2015)

CO2

Y: 34% EE: 95% R: 95.9% at 70 °C R: 90.1% at 40 °C EE: 80–100%

EE: 84%-C EE: 83%-L 0.83 mg/mL-C 5.08 mg/mL-L ~11,000 ppm- TC at 50 °C

0.3–0.5 mg/g -C 0.1–0.2 mg/g- L 271 mg/100 g dry weight –TC using ethyl acetate – –

(Akkarachaneeyakorn et al., 2017)

CO2

–

581.4 mg trypsin/mgTrypsin inhibitors 71.8 mg aescin equivalents/ g- Saponins

(Aamir & Jittanit, 2017)

(Tuyen, Nguyen, Roach, & Stathopoulos, 2014) (Tai & Kim, 2014)

(Chuyen et al., 2017b) (Le et al., 2018) (Le et al., 2018)

MDB: microwave-drying before pressing; ADP: air-drying before pressing; MDS: microwave-drying before Soxhlet extraction; ADS: air-drying before Soxhlet extraction; EE: extraction efficiency; Y: yield; R: recovery; TC: total carotenoid; C: β-carotene content; L: lycopene content;

raw material could increase the solubility of lycopene in extraction solvents and ultimately improve lycopene extraction efficiency. According to (Gamlieli-Bonshtein, Korin, & Cohen, 2002) the solubility of (9Z)-β-carotene in SC-CO2 was approximately four times higher than that of the (all-E)-isomer. Moreover, the lycopene extraction with high bioactivity can be obtained by moderate heat treatment. The effect of heating on cis-isomerization of oil-free lycopene from Gac aril in the alltrans form induced an increase in the antioxidant properties (Phan-Thi & Waché, 2014). Solvent extraction is commonly used to extract oil and bioactive compounds from plants. Thuat (2010) investigated oil extraction from commercially dried Gac aril by n-hexane solvent and an IKA magnetic stirrer. Remarkably, the oil yield in optimal extract conditions obtained was higher than 96%. To consider effects of ohmic heating on Gac aril oil extraction using n-hexane in comparison with conventional heating, three extraction stages with the ratio of Gac aril powder to n-hexane and extraction times 1:7(7 h), 1:6 (6 h) and 1:5 (5 h) were treated with ohmic heating at 50 °C (Aamir & Jittanit, 2017). The ohmic heating method resulted in significantly higher oil EE than the conventional heating method which was conducted by using an IKA magnetic stirrer with heating plate, enhanced color characteristics, and increased βcarotene and lycopene contents of extraction oil. Extraction of bioactive compounds from Gac fruit has also been attractive to researchers. Kubola, Meeso, and Siriamornpun (2013) evaluated the lycopene and β-

carotene concentration in aril oil by different extracting solvents and drying methods. Chloroform: methanol (2:1 v/v) provided higher carotenoid content in aril oil and seed oil (1.67 and 0.11 mg/g) than petroleum ether and hexane. Among three different drying methods, hot air drying resulted in the highest content of lycopene, low relative humidity air drying gave the highest β-carotene content, while far-infrared radiation drying resulted in moderate results for both lycopene and β-carotene. Other technologies to be considered to improve the yield, oil quality, and flavoring from Gac fruit are enzyme-assisted aqueous extraction and ultrasound-assisted extraction. Advantages of these methods are environmentally friendly, solvent-free, and a convenient solution for application in developing countries. The maximal oil recovery and total carotenoid content attained under optimal conditions of the enzyme ratio of 14.6% (w/v), incubation time of 127 min, temperature of 58 °C, and stirring speed of 162 rpm was reported by Mai, Truong, and Debaste (2013). The parameters were an enzyme concentration of 0.15%, incubation time of 100 min, and a drying temperature of 60 °C after enzyme-treated arils extracted by Viscozyme L enzyme assistance (Nhi & Tuan, 2016). Ultrasound assisted aqueous extraction of oil and carotenoids from microwave-dried aril powder was investigated by Tuyen, Nguyen, Roach, and Stathopoulos (2015). In the findings, the best extraction efficiencies were achieved when applied ultrasound power of aril powder, extraction time, powder particle sizes, a ratio of water to powder and a centrifugal force by 32 W/g, 20 min, 7

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0.3–0.5 mm, 9 g/g and 6750 g respectively. SC-CO2 extraction has been proven as a promising alternative method to mechanical pressing and traditional solvent extraction. Research has been conducted to develop models and contribute insight on the mechanisms and optimization of Gac oil extraction using SC-CO2 (Akkarachaneeyakorn, Boonrattanakom, Pukpin, Rattanawaraha, & Mattaweewong, 2017; Tuyen, Phan-Tai, & Nguyen, 2014). Mathematical modelling of oil solubility data was applied to calculate the oil loading capacity of SC-CO2. The results showed that after 120 min of extraction, the oil recovery exceeded 95% by specific flow rate of 70 kg/h CO2 per kg of Gac aril, a pressure of 400 bar, and a temperature of 70 °C (Tai & Kim, 2014). Akkarachaneeyakorn et al. (2017) reported that temperature range of 50–60 °C and pressure range of 200–250 bar were the optimal conditions for oil extraction, which resulted in an EE of 80–100%, 60–80% iodine values, and an acidity of 0–4 mg potassium hydroxide. Optimization of technical and economic aspects of the Gac oil production process was investigated by Martins, De Melo, and Silva (2015). At 400 bar, 60 °C and 1 h gave the minimal oil manufacturing cost of 8 euro/kg but the minimal manufacturing cost of extraction of carotenes at 400 bar, 50 °C, and 1 h was 755 euro/kg.

5.1. Antioxidant activity The antioxidant activity of Gac fruit has been determined using diphenyl-picrylhydrazyl (DPPH) radical scavenging, ferric reducing antioxidant power (FRAP), and 2,2′-azino-bis (3-ethylbenzothiazoline6-sulphonic acid) (ABTS). Bharathi, Singh, Shivashankar, Ganeshamurthy, and Sureshkumar (2014) reported that 500 g of fruit samples collected at 25-day maturity post-pollination contained 45.06 mg ascorbic acid equivalent (AAE)/100 g by using DPPH assay and 5.84 mg ascorbic acid equivalent anti-oxidant capacity (AEAC)/ 100 g by using FRAP assay. The different fractions of Gac fruit exhibited different antioxidant capacities. The greatest antioxidant activities of ethanolic extract from the aril of ripe Gac fruit were 4.87 mg AAE/g fresh weight (FW) and 0.016 mg AAE/g FW compared to peel and pulp extract when examined by DPPH and FRAP (Tinrat, Akkarachaneeyakorn, & Singhapol, 2014). Kubola and Siriamornpun (2011) concluded that the aril fraction had the greatest antioxidant capacity, followed by peel, pulp, and then seed. The antioxidant capacity of peel and pulp extracts decreased from the immature stage to the ripe stage, whereas that in the seed extracts increased from mature stage to ripe stage. The significant decrease in phenolic levels during the development stage of fruit might cause the decrease of antioxidant activity. Further storage and processing probably have an impact on the bioactive compounds and antioxidant activity of Gac fruit. Drying is one of the key processes that results in antioxidant activity reduction (Mai, Truong, Haut, et al., 2013b). However, several researchers demonstrated that pretreatment before drying, or applying a suitable drying method with optimal operation parameters could preserve antioxidant properties in the aril (Mai, Truong, Haut, et al., 2013b; Tuyen et al., 2010, 2011). The antioxidant activity values for the seed oil tend to be higher when the oil is extracted using SC-CO2 than when Soxhlet extraction is applied (Le et al., 2018). The extraction conditions and different extract solvents exhibited different extraction yields of antioxidant capacity reported by Chuyen, Roach, Golding, Parks, and Nguyen (2017b). These authors determined the extraction time of 150 min, temperature of 40.7 °C with the ratio of 80:1 (mL ethyl acetate per g solid) were the optimal conditions and solvent for recovering antioxidant capacity from the peel. The seeds of Gac fruit possess a novel potato type I chymotrypsin inhibitor which showed antioxidant activities in rat hepatocyte culture subjected to tert-butyl hydroperoxide (t-BHP)-induced oxidative stress (Tsoi, Ng, & Fong, 2005; Tsoi, Wong, Ng, & Fong, 2004).

4.3. Encapsulation Encapsulation of carotenoids and other bioactive compounds have demonstrated a significant improvement in the protection, stability, and slow release of encapsulated ingredients (Rocha, Fávaro-Trindade, & Grosso, 2012). Spray drying, coacervation and emulsion solidification are available methods of encapsulating food nutrients. Amongst these technologies, spray-drying encapsulation is one of the most widely used and suitable technologies due to its auxiliary production, industrial convenience, and efficiency (Shu, Yu, Zhao, & Liu, 2006). As previously discussed, the extracted oil contains high levels of bioactive compounds and potential antioxidant activities (Le et al., 2018; Tai & Kim, 2014; Tuyen et al., 2013). However, it is very susceptible to oxidants, light, and heat during storage (Boon, McClements, Weiss, & Decker, 2010; Vuong & King, 2003). Technological condition optimization for encapsulation of Gac oil has been reported by several researchers (Chuyen, Roach, Golding, Parks, & Nguyen, 2019; Kha et al., 2014b, 2014a). Kha et al. (2014a) and Kha et al. (2014b) predicted the optimization of wall material concentration, oil load, and spray drying conditions by using response surface methodology. The results showed that the wall concentration of 29.5%, oil load of 0.2 w/w, inlet temperature of 154 °C and outlet temperature of 80 °C were optimal conditions of encapsulation efficiencies for Gac aril oil. The response variable of the encapsulation efficiencies in terms of the oil, β-carotene, lycopene, encapsulation yield, moisture content, water solubility index, and peroxide value were predicted and validated as 87.22%, 82.76%, 84.29%, 52.78%, 4.90%, 90.29%, and 4.06 meq/kg, respectively (Kha et al., 2014b). With the same purpose, a recent report found inlet temperature of 160 °C using a spray drier and feeding rate of 180 mL/h for emulsion at 24.5% total solids (a mixture of whey protein and gum Arabic) containing the ratio of 3:10 (oil/wall material) resulted in 80% of carotenoid and 82% of antioxidant capacity. These optimal conditions were determined for carotenoid- rich oil encapsulation from Gac peel (Chuyen et al., 2019).

5.2. Antimicrobial activity The extract of Gac fruit showed potent antimicrobial activity against both Gram positive and Gram-negative bacteria. Ethanolic extract from peel, pulp, and aril of ripe Gac fruit was evaluated for antimicrobial activity against six pathogenic strains (Tinrat et al., 2014). The extracts from peel and pulp fractions with minimum inhibitory concentration (MIC) value of 1.562 mg/mL proved the most bacteriotoxicity for E. coli ATCC 25,922 while the aril extract with MIC value of 3.125 mg/mL proved the most bacteriotoxicity for P. aeruginosa ATCC 27853. This demonstrated that the effectiveness of antibacterial activity depends on which part of the fruit is extracted and bacterial strain tested. In another study, parts of aril and pulp were extracted using 95% ethanol, ether and distilled water to determine inhibitive properties against twelve bacterial strains (Innun, 2013). The pulp extracts with distilled water and the aril extracts with ethanol had the strongest inhibition against Staphylococcus aureus and Micrococcus luteus, respectively. However, the extracts of pulp and aril with ether had no antimicrobial activity. The seed of the fruit has also been found to possess strong antiviral activity, with extracts significantly reducing the infectivity of influenza A virus H3N8 in vitro by using at a high concentration of 0.5% extract. From the result obtained, Gac seed could be a promising potential source of new antiviral drugs (Oyuntsetseg et al., 2014).

5. Pharmacological activities of Gac fruit Many researches have indicated that Gac fruit has a wide variety of biological functions including anti-oxidation, anticancer, anti-inflammation, antimicrobial, immunomodulatory properties, and other activities. Fig. 5 briefly summarizes mechanisms of action of Gac fruit on human health. However, a detailed discussion of findings is presented below. 8

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Fig. 5. Schematic representation of main mechanisms and outcomes of Gac fruit on human health. Abbreviations: ↑ – increase, upregulation, enhancement, or stimulation compared to control; ↓ – decrease or inhibition compared to control; GSH – glutathione; GSSG – oxidized glutathione; t-BHP – tert-Butyl hydroperoxide; PARP – poly (ADP-ribose) polymerase; Bcl 2 – B-cell lymphoma 2; PI-3K/Akt – phosphoinositide 3-kinase/phosphorylation; matrix metalloproteinase – MMP; pERK – phosphorylated extracellular signal-regulated kinase; LPS – lipopolysaccharide; NO – nitric oxide; iNOS – inducible NO synthase; NF-κB – Nuclear factor kappa; IκBα – inhibitor of NF-κB; VEGF – vascular endothelial growth factor; IL – interleukin; MAPK – mitogen-activated protein kinase; HG – high glucose; ROS – reactive oxygen species; PEDF – pigmented epithelium-derived factor.

5.3. Anticancer activity

angiogenic activities of the crude water extract from aril. 1.24 mg/mL of aril water extract inhibited colon and liver cancer cells by 38 and 45%, respectively. The bioactive antitumor component in Gac aril was a protein with molecular weight of 35 kDa, which was the water-soluble high molecular weight. Another study (Wimalasiri, Piva, & Huynh, 2016) also reported the cytotoxicity of crude water extracts of aril was the greatest with extracts of fruits from northern Vietnam with 60% and 71% mortality on breast cancer (MM418C1, D24) and melanoma (MCF7) cells, respectively. Cancer cell viability was reduced significantly by the aril extract. It could be through necrotic or apoptotic cellular pathways as indicated with by analysis of morphology and biochemical tests. Petchsak and Sripanidkulchai (2015) investigated the anti-estrogenic effects and underlying mechanism of apoptosis-inducing effects of Gac aril extract on MCF-7 human breast cancer cells. The aril extract has anticancer abilities on human MCF-7 breast cancer cells by both intrinsic and extrinsic apoptosis pathways.

The anticancer activities of Gac fruit have been investigated in vitro and in vivo. Many studies demonstrated that extract from the seed and aril have anticancer abilities. Researchers have recently focused on anticancer activity of the seeds because recent reports showed some special saponins containing disaccharide chains, trypsin inhibitors, and a chymotrypsin inhibitor. The seed extract exhibited inhibition against the proliferation of human SGC7901 and MKN-28 gastric cancer cells (Liu et al., 2012). The mechanism in antiproliferation activities of the seed extract was explained to be due to apoptosis promotion by increasing enzyme activities of caspase-3 and caspase-9 and via poly (ADP-ribose) polymerase and p53 signal pathways. Similarly, the ethanolic seed extracts were capable of suppressing the proliferation of A549 lung cancer cells due to apoptosis induction verified through the activation of p53 and inactivation of PI-3K/Akt signaling, as well as metastasis inhibition by regulating multiple molecular targets (Shen, Meng, Sun, Zhu, & Liu, 2015). The development of an inhibitory treatment for breast cancer may also be found in the seed extract. The migration, adhesion, and invasion of ZR-75-30 cancer cells were inhibited by the seed extract (Zheng, Zhang, Zhan, & Liu, 2014). In a recent study, Gac seed extract showed high anticancer potential against two melanoma cell lines (MM418C1 and D24) (Le, Huynh, Parks, Nguyen, & Roach, 2018). Gac aril extract has been demonstrated to suppress the viability of cancer cell lines. Tien et al. (2005) assessed the antitumor and anti-

5.4. Anti-inflammatory activity Gac fruit is rich in lycopene which has a protective effect against inflammation (Hazewindus, Haenen, Weseler, & Bast, 2012). Jung et al. (2013a) indicated Gac seed extract has anti-gastritis effects in ethanoland diclofenac-induced gastritis in rats. Treatment with the seed extract had more preventive efficacy compared to a rebamipide treatment. These authors found momordica saponin I of the seed might be used as an active marker compound. Gac seeds contain several triterpenoids 9

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and saponins. Among the triterpenoidal saponins isolated, momordica saponin I was confirmed to be inhibitory against nitric oxide (NO) production and transcriptional activation of inflammatory genes, as well as suppression against the activation of inflammatory signaling proteins (Yu et al., 2017). The other saponin is a quillaic acid glycoside, inhibiting the induction of IL-6 and iNOS expression and NO synthesis in RAW 264.7 cells (Jung et al., 2013b). These studies provide evidence that the Gac seed could be useful in treating inflammatory diseases.

aril extract could change the density of the 70 kDa testicular tyrosine protein and improve the aril extract-treated group. The neurotrophic effects of Gac seed were investigated by assessing for neurite length, neurite count/cell and min/max neurite length (Mazzio, Georges, McTier, & Soliman, 2015). The results showed the maximum lengths were 41.93 ± 3.14 µm (nerve growth factor (NGF) of 0.5 µg/mL), 40.20 ± 2.72 µm (seed extract treatment of 138 µg/ mL), and 3.58 ± 0.42 µm (controls). The seed extract presented the same behavior with NGF as the neurotrophic effects through early pERK signaling and morphological changes in structural proteins associated with neurite branching and outgrowth. Mazzio et al. (2018) further investigated the nature of the unknown NGF within the seed that was responsible for neurite outgrowth in PC-12 cells. In conclusion, the neuritogenic factor was a stable protein having a mass of 17 kDa. This is compatible with previous reports in that neurotrophins are proteins, and mimetics tend to be dimeric peptides or cleaved peptide products (Antipova, Gudasheva, & Seredenin, 2011). Recently, two triterpenoidal saponins (compounds 1 and 2) in Gac seed have proven to possess renoprotective effects against cisplatin-induced injury in cultured LLC-PK1 cells by blocking the MAPKs-caspase-3 signaling cascade (Jung et al., 2016). The extracts from Gac fruit parts (peel, pulp, seed, and aril) reduced ARPE-19 cell viability, decreased reactive oxygen species and vascular endothelial growth factor productions, induced morphological changes, and increased pigmented epithelium-derived factor levels in high glucose conditions at 30 mmol/L. These results provide evidence for the use of Gac fruit as a potential treatment against high glucose-related diabetic retinopathy disease (Abdulqader, Ali, Ismail, & Esa, 2018b).

5.5. Immunomodulatory activity Tsoi, Ng, and Fong (2006) investigated the effects of Gac seed on splenocytes, splenic lymphocytes, neutrophils, bone marrow cells and macrophages of the immune system. The proliferation of splenocytes, lymphocytes and bone marrow cells was increased by a chymotrypsinspecific inhibitor from the seeds. This chymotrypsin inhibitor also suppressed the production of H2O2 in both neutrophils and macrophages. These results demonstrate immunomodulatory action of the seed. Moreover, immune responses were enhanced by the supplement of seed extract in Newcastle disease vaccine in chickens (Xiao, Bao, & Hu, 2009) and foot-and-mouth disease vaccine in female guinea pigs (Chenwen Xiao, Rajput, Liu, & Hu, 2007). 5.6. Pro-vitamin A activity Influence of β-carotene supplementation from Gac aril was assessed by participation of preschoolers (Vuong et al., 2002). Three groups were fed one of the following steamed glutinous rice variations: one with added 3.5 mg β-carotene per serving from Gac aril, one with 5.0 mg synthetic β-carotene powder per serving, and one without fortification. After 30-days of consumption, the increase in plasma retinol concentration of the Gac aril group was significantly higher than in the control and β-carotene powder groups. The oil rich aril is a key factor in improving β-carotene absorption which caused the greater increase in plasma β-carotene and retinol concentrations compared to the group treated with synthetic β-carotene. In the findings of Muller-Maatsch et al. (2017), liberation and bioaccessibility of carotenoids were up to eight times higher in Gac fruit aril than in carrot root and tomato fruit. Their hypothesis explained that the small carotenoid aggregates of Gac fruit aril could possess a much higher surface-to-volume ratio in the deposition form than the large crystalloid aggregates of carrot and tomato, hence dissolving more rapidly in dietary lipids during digestion, and ultimately enhancing carotenoid bioaccessibility.

6. Commercial Gac products and uses of Gac fruit Gac fruit has potential to be utilized by the pharmaceutical, cosmetic, and food industries. Gac fruit is processed for components to be used as ingredients or fortification. Recently, commercial Gac products such as frozen aril, puree, Gac oil, dried Gac aril powder, and Gac juice have been introduced into the market. The Gac products serve domestic and international markets such as the countries as listed in Table 3. Food manufacturers could take the bulk of Gac fruit and utilize it in a range of mainstream food such as fruit bars, yogurt, breakfast cereal, or in specific health food such as juices, jams, natural colorants, and health supplements. Gac fruit has been commonly used in its native countries, China and Vietnam, mainly as food and traditional medicine for more than 1200 years (Xiao, Hu, & Rajput, 2007). Gac seed is called “mubiezhi” in China and is used to provide a variety of therapeutic benefits, including relief from boils, rheumatic pain, muscular spasm, hemorrhoids, and hemangiomas (Huang, Ng, Fong, Wan, & Yeung, 1999; Zhao et al., 2012). In Vietnam, Gac aril is mixed with sticky rice as a natural colorant and steam to make “xoi gac”. This nutritious dish is served at weddings, Lunar New Year, or other important celebrations. The Gac crop is widely cultivated for production of its fruits, although the young leaves, leafy shoots, and flowers are also eaten as a vegetable, blanched and served with chili sauce, or added to soups in developing countries (Lim, 2012; Mukherjee, Sarkar, & Barik, 2014). Young and immature green fruit is boiled, stuffed, stir-fried with pork or shrimp, or cooked in curries in India, Thailand, and Bangladesh (Bharathi & John, 2013; Kubola & Siriamornpun, 2011) while fresh ripe aril is used for juice and ice cream processing in Thailand. Honey and lemon are mixed with ripe aril and blended into a fresh juice in Indonesia, the Philippines, and Malaysia.

5.7. Other activities Gac seed showed gastric ulcer healing and angiogenesis, as reported by Kang et al. (2010). Ulcer size in the seed extract- treated group was significantly smaller by days 7 and 14 compared to the vehicle group. The mRNA expression at day 7 and vascular endothelial growth factor protein at day 14 were higher than in the vehicle treated rats. Moreover, the seed extract resulted in a wound healing effect on cutaneous injury at 50 µg/mouse, which is supposedly responsible for increasing the gastroprotective effect (Jung et al., 2013a). The adverse effects of valproic acid (VPA) treatment include reductions of sperm concentration and seminiferous tubule diameters. A study considered protective activity of aril extract on reproductive parameters of male rats induced with VPA (Sukhorum, Sampannang, Sripanidkulchai, & Iamsaard, 2016). The groups treated with aril extract and VPA showed an increase of sperm concentration, seminiferous tubular diameter, and prevention of testicular tissue damage as compared to VPA group. Antioxidants in aril extract could be ascribed to testosterone production and spermatogenesis and could improve hyperglycemia and male reproductive damages in streptozotocin-induced hyperglycemia mice as reported by Sampannang et al. (2017). The 70 kDa testicular protein was interrupted in sperm production of a hyperglycemic mice group while the

7. Storage of Gac fruit and Gac products Study of the changes of postharvest Gac fruit quality and product shelf life, as well as optimum storage conditions is an important issue for quality management. Intrinsic factors such as variety, stage of 10

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Table 3 List of Gac suppliers by country and their products (https://www.alibaba.com/showroom/gac-fruit.html) (https://www.alibaba.com/gac-fruit-suppliers.html). Country

Manufacturers/Trading companies

Gac products

Vietnam

VNPOFood Hanfimex Moocos Vietnam Co., Ltd. Rita Food & Drink Co., Ltd. Sunrise Viet Nam Technology Joint Stock Company Viet Nam Herbal Oil Joint Stock Company Hangenco., JSC Viet Delta Industrial Co., Ltd. Dong Duong JSC Tri Long Trade and Production Limited Company Domesco Medical Import Export Joint Stock Corporation Nam Viet Phat Food Co.,Ltd. Mekong Herbals Corporation Safimex Joint Stock Company

Puree Gac Concentrate Frozen Aril Juice Extract Powder Gac Oil Gac Fruit Jam Gac Oil Capsules Tea Biscuits Soap Skin Balm Gac seed alcohol

China

Xian Aladdin Biological Technology Co., Ltd. Xi'an Chen Lang Biological Technology Co., Ltd. Hunan Greenland Plant Resource Development Co., Ltd. Shaanxi Guanjie Technology Co., Ltd. Honhun Health International Co., Ltd. Shaanxi Joryherb Bio-Technology Co., Ltd. Xian Pincredit Bio-Tech Co., Ltd. Xi'an Le Sen Bio-Technology Co., Ltd. Xi'an DN Biology Co., Ltd. Xian Lucky Clover Biotech Co., Ltd. Guangxi Nanning Yue Yin Import And Export Trade Co., Ltd.

Gac Fruit Enzyme Drink Extract Powder Juice

Thailand

MagnaGac Phusirath Company Limited D2 Holding Company Limited P.O.P. Siam Golden Fruit Limited Partnership Lycopenelover Co,. Ltd. Chaichada Co., Ltd.

Extract Powder Juice Blend Skin Balm Soap

maturity, and the extrinsic influences like growing and storage conditions have potential effects on the nutritional quality of Gac fruit. For short-time postharvest storage and quick consumption, Gac fruit should be harvested at the fully ripe stage which is higher quality than medium ripe fruits in terms of their carotenoids (Kubola & Siriamornpun, 2011) and oil concentrations (Tran et al., 2016). However, the shelf life of fully ripe fruit at ambient temperature conditions is short. According to the report of Bhumsaidon and Chamchong (2016), Gac fruit at the fully ripe stage showed the highest lycopene content (50.11 ± 1.59 mg/ 100 g FW) after 6 day storage at 26 ± 1 °C while the β-carotene was found to be highest (39.16 ± 1.29 mg/100 g FW) in the aril which became rotten with spoilage after 15 days of storage. The previous study suggested that Gac fruit harvested prior to full maturity can increase the nutritional qualities in terms of the contents of oil, lycopene, and β-carotene in aril and is suitable for long term storage (Tran et al., 2017). These authors concluded the whole fruit firmness and total soluble solid of aril are simple indices for the quality management of Gac fruit. High temperature was one of the factors with a strong effect on the degradation kinetics of carotenoids in food (Boon et al., 2010). Storage at low temperatures in the absence of oxygen and light has been considered the most efficient method to maintain the quality of Gac fruit and Gac products. Fruit stored at 10 °C and 13 °C had a shelf life of 30 days while the shelf life at 25 °C was 15 days, however lower temperature storage of 4 °C resulted in fruit that could not ripen normally

and had both external and internal symptoms of chilling injury (Win, Buanong, Kanlayanarat, & Wongs-Aree, 2015; Win, Kanlayanarat, Buanong, & Wongs-Aree, 2013). Gac powder samples (6% db) after pretreatment and dehydration with different drying technologies retained the best quality with over 4 months in vacuum storage below 25 °C (Tran et al., 2008). The vacuum dried samples had higher moisture content (15–18% db) was found to enhance subsequent storage at 2 °C in a sealed container for 21 weeks (Mai, Truong, Haut, et al., 2013b). The addition of antioxidant factors combined with storage at low temperature better preserved the total carotene content in the powder (Minh & Dao, 2013) but not in the oil, which could result in reduction of carotenoid content (Nhung et al., 2010). The phenomenon was logically explained by authors as the precipitation of β- carotene at the bottom of the glass tubes at 5 °C, which was not the final result with the oil. Vitamin C supplementation (2000 ppm) and mixing carrier (maltodextrin: gelatin, 0.5:0.5 (w/w)) incorporated with Gac aril powder maintained 70% of carotene content for three months at 10 °C or five months at 5 °C in the absence of oxygen and light (Minh & Dao, 2013). To date, the encapsulation of Gac oil from the peel has also shown an improvement in the retention of carotenoid content compared to that of the non-encapsulated oil during the storage. However, great losses of the encapsulated carotenoids were also observed at both storage temperatures tested (Chuyen et al., 2019). Storage at 5 °C and 20 °C could retain 65.3% and 41.5% of total carotenoid in encapsulated powder respectively after 6 months. Further investigations on the packaging 11

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and storage of Gac oil should be carried out to improve the stability of carotenoids.

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8. Conclusion Gac fruit has shown to be rich in nutrients, containing very high levels of carotenoids, fatty acids, α-tocopherol, vitamin C, polyphenol compounds and flavonoids. The pharmacological activities of the seed have been demonstrated through both in vitro and in vivo studies. Recently, the food industries of countries where Gac fruit grows natively have been processing it for consumers to utilize, however, a larger variety of Gac products needs to be developed and Gac fruit needs to be more widely available throughout the year. There are still many unresolved issues blocking the development of Gac agriculture at an industrial processing scale in non-native locations due to limited cultivation area and insufficient seed stock. Optimal Gac processing methods including drying, oil and bioactive compound extraction, and encapsulation have been conducted by researchers. However, research into oil and bioactive compound extraction has focused mainly on the aril of Gac fruit. It is highly important to also investigate the extraction of oil and bioactive compounds from Gac peel and seed for the food and medicine industries. In addition, large amounts of peel and pulp are discarded yearly after Gac processing which should instead be utilized to avoid the waste of a potentially valuable carotenoid source. The different parts of Gac fruit require different drying methods to maintain dried product quality. Moreover, pre-treatment before drying Gac fruit should be applied to enhance dried product quality as well. To obtain high quality Gac oil with storage stability, the combination of SC-CO2 extraction and encapsulation is essential. Although the most effective storage conditions for Gac fruit and products are at low temperature in the absence of oxygen and light. However, it is important to note that storage of Gac fruit and oil in the temperature range of 4–5 °C results in a deterioration of quality. Application of Gac fruit for functional beverage production is a potential prospect for the food industry. To our knowledge, studies on Gac juices and beverages have not been reported. Thus, this is an area where more research needs to be conducted. The review presented here provides many suggestions concerning the technological processing and agricultural research of Gac as well as its medicinal and functional properties that serves as a resource for students and professionals seeking information or a basis for future investigations. Ethical statements This work did not include any human subjects and animal experiments. Declaration of Competing Interest The authors declared no conflicts of interest. Acknowledgements This research was subsidized by the Jiangsu Agriculture Science and Technology Innovation Fund (CX (18)3070), China National Natural Science Foundation (31871840), the Six-Talent Peaks Project in Jiangsu Province and QingLan Project, which has enabled us to accomplish this study. References Aamir, M., & Jittanit, W. (2017). Ohmic heating treatment for Gac aril oil extraction: Effects on extraction efficiency, physical properties and some bioactive compounds. Innovative Food Science & Emerging Technologies, 41, 224–234. Abdulqader, A., Ali, F., Ismail, A., & Esa, N. (2018). Gac (Momordica cochinchinensis Spreng.) fruit and its potentiality and superiority in-health benefits. Journal of Contemporary Medical Sciences, 4(4), 179–186.

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