Uchuva Overview PDF
Uchuva Overview PDF
Uchuva Overview PDF
Review
Bioactive phytochemicals, nutritional value, and functional properties of cape gooseberry (Physalis peruviana): An overview
Mohamed Fawzy Ramadan
Department of Biochemistry, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt
a r t i c l e
i n f o
a b s t r a c t
Exotic fruits play an important role in nutrition as an excellent base for low calorie and dietetic products. Highly valued for its unique avor, texture and color, recent research has shown cape gooseberry (Physalis peruviana) to be high in many benecial compounds. The diversity of functional applications to which P. peruviana can be put gives this fruit great importance. The food industry has used cape gooseberry in different products including beverages, yogurts and jams. With the rapidly growing popularity of this unique fruit it is important to have a comprehensive reference for its nutritional benets. This review provides a valuable source for current knowledge on bioactive phytochemicals and further development of P. peruviana for functional foods as well as nutraceutical and pharmaceutical industries. 2011 Elsevier Ltd. All rights reserved.
Article history: Received 22 September 2010 Accepted 28 December 2010 Keywords: Physalis peruviana Phytochemicals Fruit pomace Functional foods
Contents Introduction . . . . . . . . . . . . . . . . . General chemical composition of P. peruviana . P. peruviana juice . . . . . . . . . . . . . . . P. peruviana lipids . . . . . . . . . . . . . . P. peruviana pomace . . . . . . . . . . . . . Bioactive phytochemicals . . . . . . . . . . . 6.1. Withanolides . . . . . . . . . . . . . 6.2. Carotenoids . . . . . . . . . . . . . . 7. P. peruviana volatiles and aroma compounds . . 8. Health benets of P. peruviana extracts . . . . 8.1. Anti-hepatotoxic activity . . . . . . . . 8.2. Anti-inammatory activity . . . . . . . 8.3. Anti-hepatoma activity . . . . . . . . . 8.4. Health benets of P. peruviana oil . . . . 9. Medical and edible applications of P. peruviana . 10. Future trends for P. peruviana . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . 1. 2. 3. 4. 5. 6. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1830 1831 1831 1831 1832 1833 1833 1834 1834 1834 1834 1835 1835 1835 1835 1835 1835
1. Introduction Berries have been shown to provide signicant health benets because of their high antioxidants, vitamins, minerals and ber (Zhao, 2007). Cape gooseberries are annuals or short-lived perennials, and are
Tel.: +20 55 2320282, +20 129782424; fax: +20 55 2287567, +20 55 2345452. E-mail address: hassanienmohamed@yahoo.com. 0963-9969/$ see front matter 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodres.2010.12.042
more or less hairy. The owers are bell-shaped, but the most distinctive feature is the fruiting calyx which enlarges to cover the fruit and hangs downwards like a lantern. Cape gooseberry forms a domed shrub that can grow to 1 m. The owers, produced in winter, are yellow with purple blotches. Physalis peruviana is an herbaceous, semi-shrub, that is upright, perennial in subtropical zones, and can grow until it reaches 0.9 m. The fruit (Fig. 1) with an approximate weight of 45 g is protected by an accrescent calyx and covered by a brilliant yellow peel (Mayorga, Knapp, Winterhalter, & Duque, 2001). It is somewhat tomato-like in
1831
avor and appearance, though the taste (sweet and sour) is much richer with a hint of tropical luxuriance. The plant is fairly adaptable to wide variety of soils and good crops are obtained on poor sandy ground (Popenoe et al., 1990???; Ramadan & Mrsel, 2004, 2007). Cape gooseberry (P. peruviana Linn., Solanaceae) has been grown in Egypt, South Africa, India, New Zealand, Australia and Great Britain (McCain, 1993; Morton, 1987; Ramadan & Mrsel, 2003; Rehm & Espig, 1991). Functional foods represent an emerging market of growing economic importance. International markets exist for many exotic fruits and recently the processing of tropical fruits started in many countries (Ramadan & Mrsel, 2007). In 2005, there were more than 1.8 million acres of berry crops worldwide including 966 acres of gooseberries (Strik, 2007). Cultivation in Colombia is steadily increasing to satisfy the growing export demands, ranking it second after banana fruit exports (Mayorga et al., 2001). A single plant may yield 300 fruit and carefully tended plants can provide 20 to 33 tons per hectare. Fruits are long-lasting, can be stored for several months and also freeze well. Given research indicates that goldenberry could become a fruit of particular interest to the food industry. This is the strategy that established markets for kiwifruits in the 1960s and led to a multimillion dollar annual crop. 2. General chemical composition of P. peruviana The fruit has been used as a good source of provitamin A, minerals, vitamin C and vitamin B-complex. The fruit contain 15% soluble solids (mainly sugars) and its high level of fructose makes it valuable for diabetics. The phosphorus level is high for a fruit (Table 1). Its high content of dietary ber is of importance, wherein fruit pectin acts as an intestinal regulator (McCain, 1993; Ramadan & Mrsel, 2003). 3. P. peruviana juice Cape gooseberry juice yield is 72.6% of the berry weight. Enzymatic treatment resulted in an increase in the macro- and micro-component levels. Application of enzymes leads to juice with higher pulp content, acidity and total soluble solids. On the other side, enzyme-treated juice was characterized by lower alcohol insoluble solids and pHvalues (Ramadan & Mrsel, 2007). The amount of alcohol insoluble solids in fresh juice was found to be 0.62 g/100 g juice. The total acid content in cape gooseberry juice is 0.91.0% and the pH of the juice is low (3.793.86). Total sugar content in the juice is 4.9 g/100 g and the preponderant compounds are sucrose (35 g/100 g sugar) and fructose (29 g/100 g sugar), which are comparable to the sugar content in
Table 1 Levels of nutrients, minerals and water-soluble bioactives in Physalis peruviana pulp. Source: Ramadan and Mrsel (2004). Moisture (g/100 g) Protein (g/100 g) Lipid (g/100 g) Carbohydrate (g/100 g) Fiber (g/100 g) Ash (g/100 g) Calcium (mg/100 g) Phosphorus (mg/100 g) Iron (mg/100 g) Carotene (mg/100 g) Thiamine (mg/100 g) Riboavin (mg/100 g) Niacin (mg/100 g) Ascorbic acid (mg/100 g) 78.9 0.050.3 0.150.2 19.6 4.9 1.0 8.0 55.3 1.2 1.6 0.1 0.03 1.70 43.0
common juices. The sugar content in common juices was reported to be 9.8% in pear, 7.0% in orange, 11.1% in apple, 8.5% in peach, and 5.7% in strawberry (Belitz & Grosch, 1999; Gurrieri et al., 2000). Ascorbic acid level in cape gooseberry (46 mg/100 g) turns out to be higher than in most fruits such as pear (4 mg/100 g), apple (6 mg/100 g), peach (7 mg/100 g), and somewhat comparable with orange (50 mg/ 100 g) and strawberry (60 mg/100 g) (Belitz & Grosch, 1999). Phenolics in fruits are of great interest owing to their important pharmacological properties (Meyer, 1999). In gooseberry, quercetin is the main phenolic compound, followed by myricetin and kaempferol (Hkkinen, Krenlampi, Heinonen, Mykknen, & Riitta, 1999). Good amounts of phenolics were estimated in cape gooseberry juice, wherein the level of total phenols was 6.30 mg/100 g juice as caffeic acid equivalents (Ramadan & Mrsel, 2007). Fruit juice was found to contain 0.2% oil, wherein linoleic acid, oleic acid, palmitic acid, -linolenic (GLA) acid and palmitoleic acid were the main fatty acids (Table 2). The total level of trienes was ca. 22.7% and the oil is characterized by high level of GLA (18.8%), while -3 fatty acid (-linolenic acid) and dihomo--linolenic (DHGLA) were found in lower levels. The juice could be a source of polyunsaturated fatty acids. Interest in polyunsaturated fatty acids as health-promoting nutrients has expanded in recent years with growing literature illustrating their benets (Riemersma, 2001). The major phytosterols (ST) were 5avenasterol and campesterol (Table 2). Vitamin E level was high, wherein - and -tocopherols were the main constituents. High amounts of -carotene were detected also in the juice (Table 2). Therefore, cape gooseberry juice could be a novel source of functional drinks without a need of fortication with fat-soluble bioactives (Ramadan & Mrsel, 2007). The antioxidant activity of cape gooseberry juice was assessed by means of a 1,1-diphenyl-2-picrylhydrazyl (DPPH) test. Fresh juice produce a 78% decrease vs the absorbance of DPPH radicals' control solution while enzyme-treated juice resulted in an 82% decrease (Ramadan & Mrsel, 2007). Phenolics are responsible for the antioxidant activity of juices and wines, while ascorbic acid plays a minor role in the antioxidant efciency of juices (Meyer, Yi, Pearson, Waterhouse, & Frankel, 1995; Rapisarda et al., 1999). Miller and RiceEvans (1997) underlined the signicant contributory role of phenols to the antioxidant activity of orange juice, even if vitamin C was the most abundant antioxidant. The presence of a good amount of phenolics in cape gooseberry juice, could contribute to the high level of antioxidant capacity. 4. P. peruviana lipids
Fig. 1. Physalis peruviana in opened calyx. The fruit is a berry, 0.5 to 0.75 in. (1.252 cm) wide, with smooth, waxy, orange-yellow skin and juicy pulp containing numerous small yellowish kernels. The part of the goldenberry that can be used is composed of husk (5%) and berry (95%). The berries can be further subdivided into seeds (ca. 17%) and pulp/peel fraction (ca. 83%), the latter being the basis for fruit and juice products.
Lipid composition of the Colombian cultivar of P. peruviana was studied (Ramadan & Mrsel, 2003). Whole berries contained ca. 2.0% oil, in which seed oil (SO) comprised ca. 90% (1.8% oil of the berry weight) and pulp/peel oil (PO) constituted ca. 10% (0.2% oil of the
1832
M.F. Ramadan / Food Research International 44 (2011) 18301836 Table 4 Levels of lipid classes (g/100 g total lipids) in Physalis peruviana oils. Source: Ramadan and Mrsel (2003). MAG WBO SO PO 1.23 1.04 2.76 DAG 1.65 1.36 2.46 TAG 78.2 84.0 60.3 FFA 3.13 2.12 5.16 STE 0.49 0.34 0.65 PL 4.15 2.99 7.34
Table 2 Levels of fatty acids, phytosterols, fat-soluble vitamins and -carotene in the Egyptian Physalis peruviana juice (pulp oil). Source: Ramadan and Mrsel (2007). Compound C12:0 C14:0 C16:0 C16:1n-7 C18:0 C18:1n-9 C18:2n-6 C18:3n-6 C20:0 C18:3n-3 C20:1n-9 C20:3n-6 C22:1n-9 C24:0 C24:1n-9 S/U ratio (%)a
a
% 0.25 1.09 19.3 7.52 1.87 22.2 22.7 18.8 0.21 0.63 0.15 2.31 0.91 0.65 1.12 29.4
Compound Ergosterol Campesterol Stigmasterol Lanosterol -Sitosterol 5-Avenasterol 7-Avenasterol Total sterols -Tocopherol -Tocopherol -Tocopherol -Tocopherol Total vitamin E -Carotene
g/kg 9.23 12.2 6.23 6.55 5.23 12.5 3.71 55.6 28.3 15.2 45.5 1.50 90.5 4.32
Abbreviations: MAG, monoacylglycerols; DAG, diacylglycerols; TAG, triacylglycerols; FFA, free fatty acids; STE, sterol esters; PL, polar lipids.
berry weight). In whole berry oil (WBO), SO and PO linoleic, oleic, palmitic, stearic and -linolenic (GLA) were the main fatty acids (Table 3). Pulp/peel oil was characterized by a high amount of saturated fatty acids which comprised more than 16%. The content of PUFA in PO was about 11.7% and the oil was characterized by a high level of GLA (8.66%), while -3 fatty acid (-linolenic acid) and DHGLA were estimated in lower levels. WBO and SO contained more neutral lipids (NL, ca. 95% of total lipids) than polar lipids (PL). Triacylglycerols (TAG) were the predominant NL class and constituted ca. 81.6, 86.6 and 65.1% of NL in WBO, SO and PO, respectively (Table 4). MAG, DAG and FFA were found in higher levels in the PO comparing with the SO and WBO. Saturated fatty acids were detected in high amounts in all lipid classes especially MAG which are characterized by high levels of palmitic acid (N 25%). The oils contain nine TAG molecular species, but three species, C54:3, C52:2 and C54:6 accounted for ca. 91% or above (Ramadan & Mrsel, 2003). Plant sterols were estimated in high levels and there were no remarkable differences between WBO and SO in terms of sterol content and composition while PO was characterized by a higher level of sterols. In WBO and SO, campesterol and -sitosterol were the sterol markers while the major sterols in PO were, 5-avenasterol and
campesterol. Recently, there has been a rise of interest in plant sterols. Most of this interest has focused on cholesterol-lowering properties of 4-desmethyl plant sterols and phytostanols, and evidence of this phenomenon includes clinical studies on plant sterols products, patents on phytosterol products, and many commercial plant sterols products (Costa, Ballus, Teixeira-Filho, & Godoy, 2010). Vitamin E level was high in PO (ca. 8.6% of TL) whereas estimated in low amounts in WBO and SO. - and -Tocopherols were the major components in WBO and SO, while - and -tocopherols were the main constituents in PO. Tocopherols are the best-known antioxidants in nature to protect lipids from oxidation (Toyosaki, Sakane, & Kasai, 2008). -Carotene was measured in the highest level in PO (0.32% of TL) followed by WBO (0.22%) then SO (0.13%), the latter being characterized by light yellow hues. Besides their potential benecial health effect, carotenoids are used as pigments to color food in the industries. Since the consumer purchase decision of food is, inter alia, based on the color, the market position of a product can be improved, in particular by application of natural pigments in contrast to synthetic colorant, since there is an increased demand for natural mild processed food (Wackerbarth, Stoll, Gebken, Pelters, & Bindrich, 2009). Cape gooseberry oils were characterized by a high level of vitamin K1 (phylloquinone), which comprised more than 0.2% of the total lipids in PO (Ramadan & Mrsel, 2003). Vitamin K1 (Fig. 2) level is very low in most food (b 10 mg/100 g), and the majority of the vitamin is obtained from a few green and leafy vegetables (e.g. spinach) (Jakob & Elmadfa, 2000; Piironen, Koivu, Tammisalo, & Mattila, 1997).
5. P. peruviana pomace Fruit processing industry produces a large amount of byproducts which are a rich source of bioactive compounds. Cape gooseberry pomace (seeds and skins) represent a large portion of the waste generated during juice processing (ca. 27.4% of fruit weight). The pomace contains 19.3% oil, 17.8% protein, 3.10% ash, 28.7% crude ber and 24.5% carbohydrates. Aqueous enzymatic extraction was investigated for recovery of oil from the fruit pomace (Ramadan & Mrsel, 2007, 2009). Different extraction techniques (Fig. 3) were checked for the best pomace oil yield. Enzymatic treatment with Pectinases and Cellulases followed by centrifugation in an aqueous system (EAE) or followed by solvent extraction (ESE) was investigated for recovery of oil from fruit pomace. Enzymatic hydrolysis of pomace followed by solvent extraction reduced the extraction time and enhanced oil extractability up to ca. 7.60% (Ramadan, Sitohy, & Mrsel, 2008).
Table 3 Fatty acid compositions of Colombian Physalis peruviana oils. Source: Ramadan and Mrsel (2003). Fatty acid Whole berry oil (WBO) Relative content C12:0 C14:0 C16:0 C16:1n-7 C18:0 C18:1n-9 C18:2n-6 C18:3n-6 C20:0 C18:3n-3 C20:1n-9 C20:3n-6 C22:1n-9 C24:0 C24:1n-9 S/U ratio (%)b
a b
0.49 1.00 8.62 0.63 2.57 13.0 70.5 1.79 0.28 0.11 0.01 0.22 0.26 0.22 0.30 15.1
0.35 1.00 7.29 0.52 2.51 11.7 76.1 0.31 0.20 0.02 n.d.a n.d. n.d. n.d. n.d. 12.8
0.91 0.50 9.58 1.06 2.92 20.1 44.4 8.66 0.40 1.09 0.22 1.95 2.70 1.85 3.66 19.2
O
n.d.(not detected). Ratio of saturated fatty acids to unsaturated fatty acids. Fig. 2. Vitamin K1 (phylloquinone).
1833
6. Bioactive phytochemicals 6.1. Withanolides Withanolides are a group of steroidal lactones which have been isolated from the genera Acnistus, Datura, Jaborosa, Lycium, Physalis and Withania of the family Solanaceae. Withanolides have a limited distribution, having been rst isolated from Withania somnifera and subsequently being found in 12 genera of the Solanaceae (Glotter, 1991; Ray & Gupta, 1994). Withanolides exhibited a broad spectrum of biological properties and signicant pharmacological activities, including insect-antifeedant, insect-repellent activities, hepatoprotective, immunomodulatory, antibacterial, anti-inammatory, antitumor, cytotoxic activity, and protection against CCl4-induced hepatoxicity (Glotter, 1991; Lan et al., 2009; Veleiro, Oberti, & Burton, 2005). An insect-antifeedant property of withanolide E isolated from P. peruviana has been demonstrated against Spodoptera littoralis larvae (Ascher et al., 1980). Withanolide E and 4-hydroxywithanolide E have been tested as anticancer agents (Cassady & Suffness, 1980). 28-hydroxywithanolide E (Fig. 4) was isolated from the calyces of P. peruviana. In addition, two withanolides isolated from the whole plant material of P. peruviana have been characterized as (20R,22R)5 ,6 ,14 ,20,27-pentahydroxy-1-oxowith-24-enolide and
OH
R2
OH O
OH
R1
R1 1- 4-hydroxywithanolide E. 2- 28-hydroxywithanolide E. 3- Withanolide E. -OH -H -H R2 Me -CH2OH Me
1834
(20S,22R)-5,6-epoxy-4,14,15-trihydroxy-1-oxowith-2,24-dienolide (Dinan, Sarker, & Sik, 1997). Lan et al. (2009) investigated the extracts of P. peruviana and characterized seven new withanolides, phyperunolide A (1), phyperunolide B (2), phyperunolide C (3), phyperunolide D (4), peruvianoxide (5), phyperunolide E (16), and phyperunolide F (17) together with ten known withanolides. 6.2. Carotenoids
HO
HO HO
O OH O
HO
OH
HO O
A positive correlation was observed between ingestion of vegetables and fruits containing carotenoids and prevention of several chronic-degenerative diseases (Coyne et al., 2005; Fraser, Lee, & Binns, 2005). Carotenoids from Physalis were determined by HPLC-PDA-MS/ MS and 22 compounds have been identied. all-trans--Carotene was the major carotenoid, contributing 76.8% to the total carotenoid, followed by 9-cis--carotene and all-trans--cryptoxanthin, contributing around 3.6 and 3.4% (De Rosso & Mercadante, 2007). The level of carotenoid esters calculated as lutein dimyristate equivalents was (b 0.5 mg/100 g) (Breithaupt & Bamedi, 2001). 7. P. peruviana volatiles and aroma compounds As natural progenitors of cinnamic acid-derived volatiles in fruits, l-O-trans-Cinnamoyl--D-glucopyranosyl-(1 6)--D-glucopyranose (Fig. 5) was isolated (47.8 mg/kg) from P. peruviana (Latza, Ganber, & Berger, 1996). Structure elucidation by NMR and optical rotation enabled the identication of (1S,2S)-1-phenylpropane-1,2-diol 2-O-D-glucopyranoside (1) and p-menth-4(8)-ene-1,2-diol 1-O--Larabinopyranosyl-(1-6)--D-glucopyranoside (2). Both glycosides (Fig. 6) have been identied for the rst time in nature. They could be considered as immediate precursors of 1-phenylpropane-1,2-diol and p-menth-4(8)-ene-1,2-diol, typical volatiles found in cape gooseberry (Mayorga et al., 2001). Mayorga, Duque, Knapp, and Winterhalter (2002) analyzed hydroxyester glycoconjugates which could liberate volatile hydroxyesters as a mechanism of aroma generation. Characterization of three new hydroxyester glycosides (Fig. 7): 3-O--D-glucopyranosyl-(1 6)--D-glucopyranoside of ethyl 3-hydroxyoctanoate (1); 3-O--L-arabinopyranosyl-(1 6)-D-glucopyranoside of butyl (3R)-hydroxybutanoate (2); and 3-O--Larabinopyranosyl-(1 6)--D-glucopyranoside of butyl (3S)-hydroxybutanoate (3) was reported. 8. Health benets of P. peruviana extracts Epidemiological studies from other parts of the world indicate that increased consumption of fruits and vegetables are associated with lower risk of chronic degenerative diseases (Reddy, Sreeramulu, & Raghunath, 2010). Various bioactive compounds (withanolides and phenolics) are reported to be present in P. peruviana (Dinan et al., 1997). Some of these compounds have a strong antioxidant property and prevent peroxidative damage to liver microsomes and hepatocytes (Wang, Lin-Shiau, & Lin, 1999). 8.1. Anti-hepatotoxic activity Water, ethanol and hexane (500 mg/kg body weight) leaves extracts of P. peruviana showed antihepatotoxic activities against
HO HO O HO OH O
Fig. 5. l-O-trans-cinnamoyl--D-glucopyranosyl-(1 6)--D-glucopyranose.
HO OH HO O HO OH OH O O
Fig. 6. Structures of newly identied glycosides of Physalis peruviana: (1S,2S)-1phenylpropane-1,2-diol 2-O--D-glucopyranoside (1); p-menth-4(8)-ene-1,2-diol 1O--L-arabinopyranosyl-(1-6)--D-glucopyranoside (2).
CCl4-induced hepatotoxicity (DeLeve & Kaplowitz, 1995). The antioxidant property is claimed to be one of the mechanisms of hepatoprotective impact (Bhatt & Bhatt, 1996). Histopathological changes induced by CCl4 were also signicantly reduced by the extract (Arun & Asha, 2007).
HO HO
O
HO OH HO HO OH
O O O O O
1
HO
HO OH HO HO OH
O O O O O
2
HO
HO OH HO HO OH
O O O O O
3
Fig. 7. Hydroxyester glycosides isolated from Physalis peruviana
1835
8.2. Anti-inammatory activity Supercritical carbon dioxide (SFE-CO2) extracts of P. peruviana contained high levels of avonoid (234 mg/g) and phenol (90 mg/g). At concentrations 0.130 g/mL, SFE-CO2 extracts demonstrated strong xanthine oxidase inhibitory effect. At 30 g/mL, SFE-CO2 extracts prevented lipopolysaccharide (LPS; 1 g/mL)-induced cell cytotoxicity in murine macrophage cells and remarkably blocked the LPS induction of inducible nitric oxide synthase and cyclooxygenase-2 expression (Wu et al., 2006). 8.3. Anti-hepatoma activity Apoptosis is dened by a number of morphological and biochemical changes including membrane bubbling, cell shrinkage, DNA fragmentation and appearance of phosphatidylserine in the outer side of the plasma membrane (Park et al., 2002). Reactive oxygen species (ROS) are generated during mitochondrial respiration and recognized as mediators of the apoptotic signaling pathway (Li et al., 2003). Cellular generation of ROS has been associated with human disease states such as inammatory diseases, neurodegenerative diseases, cancer and aging (Yang, Addona, Nair, Qi, & Ravikumar, 2003). Ethanolic extract of P. peruviana (EEPP) inhibits growth and induces apoptotic death of human Hep G2 cells in culture, whereas proliferation of the mouse liver cells was not affected. The results concluded that EEPP possesses potent antihepatoma activity and its effect on apoptosis is associated with mitochondrial dysfunction. A detailed study to dene the molecular mechanism of EEPP-induced apoptosis in Hep G2 cells was recently published (Wu, Ng, Chen, et al., 2004; Wu, Ng, Lin, Wang & Lin, 2004). 8.4. Health benets of P. peruviana oil A high level of vitamin K1 is the most unique health promoting characteristic of cape gooseberry oil. Vitamin K functions as a coenzyme and is involved in the synthesis of a number of proteins participating in blood clotting and bone metabolism (Damon, Zhang, Haytowitz, & Booth, 2005; Shearer, 1992). Vitamin K reduces the risk of heart disease, kills cancer cells, and enhances skin health and may have antioxidant properties (Otles & Cagindi, 2007). High phylloquinone intakes are markers of a dietary and lifestyle pattern that is associated with lower coronary heart disease (CHD) risk (Erkkil, Booth, Hu, Jacques, & Lichtenstein, 2007). The phylloquinone requirement of the adult human is extremely low. Vitamin K1 is obtained from a few green and leafy vegetables (e.g. spinach and broccoli). Among edible oils, the best sources of phylloquinone were rapeseed oil (ca 1.5 ug/g) and soybean oil (ca 1.30 ug/g) (Piironen et al., 1997). Cape gooseberry oil appears to be nutritionally valuable, as the high content of linoleic acid is associated with the prevention of cardiovascular diseases (CVD) and linoleic acid is known to be the precursor of structural components of plasma membranes and of some metabolic regulatory compounds. The level of tocopherols which is signicantly high identies the oil as nutritionally valuable. 9. Medical and edible applications of P. peruviana Cape gooseberry is used in folk medicine for treating diseases such as malaria, asthma, hepatitis, dermatitis, diuretic and rheumatism (Wu, Ng, Chen, et al., 2004; Wu, Ng, Lin, et al., 2004). Many medicinal properties have been attributed to cape gooseberry, including antiasthmatic, antiseptic, and strengthener for the optic nerve, treatment of throat affections and elimination of intestinal parasites, amoebas as well as albumin from kidneys. It has an anti-ulcer activity and it is effective in reducing cholesterol level (Arun & Asha, 2007; Mayorga et al., 2001). In addition to having a future as a fresh fruit, the fruit can be consumed in many ways as an ingredient in salads, cooked
dishes, dessert, jam, natural snack and preservers. Its extract can also be used for preparing a health drink (Popenoe et al., 1990???; Rehm & Espig, 1991). 10. Future trends for P. peruviana Cape gooseberry was known for centuries, but the potential of this fruit for intensive cultivation has only just begun to be explored. Cape gooseberry should attract great interest because of their nutritional and industrial properties. Because of its unique storage properties, wherein the fruits can be kept for a long time, cape gooseberry could be a suitable plant for different food applications. The development of adequate agro-technical methods can make this fruit a promising protable new crop for arid regions. Cape gooseberry can be a very interesting candidate for the processing of new functional foods and drinks. The yield of the juice is extremely high and the juice is a rich source of sugars as well as water- and fat-soluble bioactives. The preparation of new alcoholic, nonalcoholic and alpha-tocopherolbeta-carotene drinks based on the cape gooseberry could greatly extend the distribution and marketing of this delicious fruit. Cape gooseberry pulp, seed and pomace oils might serve as excellent dietary sources for vitamin K1, -linoleic acid, essential fatty acids, tocopherols, and carotenoids. On the other side, P. peruviana is a promising candidate plant for the development of a phytomedicine against many diseases. Useful information for the industrial application of cape gooseberry is provided. This will be important as an indication of the potentially nutraceutical and economical utility of cape gooseberry as a new source of bioactive phytochemicals and functional foods. References
Arun, M., & Asha, V. V. (2007). Preliminary studies on antihepatotoxic effect of Physalis peruviana Linn. (Solanaceae) against carbon tetrachloride induced acute liver injury in rats. Journal of Ethnopharmacology, 111, 110114. Ascher, K. R. S., Nemny, N. E., Eliyahu, M., Kirson, I., Abraham, A., & Glotter, E. (1980). Insect antifeedant properties of withanolides and related steroids from Solanaceae. Experientia, 36, 998999. Belitz, H. D., & Grosch, W. (1999). Food chemistry. Berlin, Germany: Springer-Verlag. Bhatt, A. D., & Bhatt, N. S. (1996). Indigenous drugs and liver disease. Indian Journal of Gastroenterology, 15, 6367. Breithaupt, D. E., & Bamedi, A. (2001). Carotenoid esters in vegetables and fruits: A screening with emphasis on -cryptoxanthin esters. Journal of Agricultural and Food Chemistry, 49, 20642070. Cassady, J. M., & Suffness, M. (1980). Terpenoid antitumor agents. In J. M. Cassady, & J. D. Douros (Eds.), Anticancer agents based on natural product models (pp. 201269). New York: Academic Press. Costa, P. A., Ballus, C. A., Teixeira-Filho, J., & Godoy, H. T. (2010). Phytosterols and tocopherols content of pulps and nuts of Brazilian fruits. Food Research International, 43, 16031606. Coyne, T., Ibiebele, T. I., Baadr, P. D., Dobson, A., McClintock, C., Dunn, S., et al. (2005). Diabetes mellitus and serum carotenoids: Findings of a population-based study in Queensland. The American Journal of Clinical Nutrition, 82, 685693. Damon, M., Zhang, N. Z., Haytowitz, D. B., & Booth, S. L. (2005). Phylloquinone (vitamin K1) content of vegetables. Journal of Food Composition and Analysis, 18, 751758. De Rosso, V. V., & Mercadante, A. Z. (2007). Identication and quantication of carotenoids, by HPLC-PDA-MS/MS, from Amazonian fruits. Journal of Agricultural and Food Chemistry, 55, 50625072. DeLeve, L. D., & Kaplowitz, N. (1995). Mechanisms of drug-induced liver disease. Gastroenterology Clinics of North America, 24, 787810. Dinan, L., Sarker, S., & Sik, V. (1997). 28-Hydroxywithanolide E from Physalis Peruviana. Photochemistry, 44, 509512. Erkkil, A. T., Booth, S. L., Hu, F. B., Jacques, P. F., & Lichtenstein, A. H. (2007). Phylloquinone intake and risk of cardiovascular diseases in men. Nutrition, Metabolism, and Cardiovascular Diseases, 17, 5862. Fraser, M. L., Lee, A. H., & Binns, C. W. (2005). Lycopene and prostate cancer: Emerging evidence. Expert Review of Anticancer Therapy, 5, 847854. Glotter, E. (1991). Withanolides and related ergostane-type steroids. Natural Product Reports, 8, 415440. Gurrieri, S., Miceli, L., Lanza, M., Tomaselli, F., Bonomo, R. P., & Rizzarelli, E. (2000). Chemical characterization of Sicilian prickly pear (Opuntia cus indica) and perspective for the storage of its juice. Journal of Agricultural and Food Chemistry, 48, 54245431. Hkkinen, S. H., Krenlampi, S. O., Heinonen, I. M., Mykknen, H. M., & Riitta, A. T. (1999). Content of the avonols quercetin, myricetin, and kaempferol in 25 edible berries. Journal of Agricultural and Food Chemistry, 47, 22742279.
1836
M.F. Ramadan / Food Research International 44 (2011) 18301836 Ramadan, M. F., Sitohy, M. Z., & Mrsel, J. -T. (2008). Solvent and enzyme-aided aqueous extraction of goldenberry (Physalis peruviana L.) pomace oil: Impact of processing on composition and quality of oil and meal. European Food Research and Technology, 226, 14451458. Rapisarda, P., Tomaino, A., Lo Cascio, R., Bonina, F., De Pasquale, A., & Saija, A. (1999). Antioxidant effectiveness as inuenced by phenolic content of fresh orange juices. Journal of Agricultural and Food Chemistry, 47, 47184723. Ray, A. B., & Gupta, M. (1994). Withasteroids, a growing group of naturally occurring steroidal lactones. In W. Herz, G. W. Kirby, R. E. Moore, W. Steglich, & Ch. Tam (Eds.), Progress in the chemistry of organic natural products, Vol. 63. (pp. 1106) New York: Springer Verlag. Reddy, C. V. K., Sreeramulu, D., & Raghunath, M. (2010). Antioxidant activity of fresh and dry fruits commonly consumed in India. Food Research International, 43, 285288. Rehm, S., & Espig, G. (1991). Fruit. In R. Sigmund, & E. Gustav (Eds.), The cultivated plants of the topics and subtropics, cultivation, economic value, utilization (pp. 169245). Weikersheim (Germany): Verlag Josef Margraf. Riemersma, R. A. (2001). The demise of the n 6 to n 3 fatty acid ratio? A dossier. European Journal of Lipid Science and Technology, 103, 372373. Shearer, M. J. (1992). Vitamin K metabolism and nutriture. Blood, 6, 92104. Strik, B. C. (2007). Berry crops: Worldwide area and production systems. In Y. Zhao (Ed.), Berry fruit, value-added products for health promotion. NW (USA): CRC Press08493-5802-7. Toyosaki, T., Sakane, Y., & Kasai, M. (2008). Oxidative stability, trans, trans-2, 4decadienals, and tocopherol contents during storage of dough fried in soybean oil with added medium-chain triacylglycerols (MCT). Food Research International, 41, 318324. Veleiro, A. S., Oberti, J. C., & Burton, G. (2005). Chemistry and bioactivity of withanolides from South American Solanaceae. Studies in Natural Products Chemistry, (Part L) Bioactive Natural Products, 32, 10191052. Wackerbarth, H., Stoll, T., Gebken, S., Pelters, C., & Bindrich, U. (2009). Carotenoid protein interaction as an approach for the formulation of functional food emulsions. Food Research International, 42, 12541258. Wang, I. K., Lin-Shiau, S. Y., & Lin, J. K. (1999). Induction of apoptosis by apigenin and related avonoids through cytochrome c release and activation of caspase-9 and caspase-3 in leukaremia HL-60 cells. Eurpean Journal of Cancer, 35, 15171525. Wu, S. J., Ng, L. T., Chen, C. H., Lin, D. L., Wang, S. S., & Lin, C. C. (2004). Antihepatoma activity of Physalis angulata and Physalis peruviana extracts and their effects on apoptosis in human Hep G2 cells. Life Sciences, 74, 20612073. Wu, S. J., Ng, L. T., Lin, D. L., Wang, S. S., & Lin, C. C. (2004). Physalis peruviana extract induces apoptosis in human Hep G2 cells through CD95/CD95L system and the mitochondrial signaling transduction pathway. Cancer Letters, 215, 199208. Wu, S. J., Tsai, J. Y., Chang, S. P., Lin, D. L., Wang, S. S., Huang, S. N., et al. (2006). Supercritical carbon dioxide extract exhibits enhanced antioxidant and antiinammatory activities of Physalis peruviana. Journal of Ethnopharmacology, 108, 407413. Yang, W. L., Addona, T., Nair, D. G., Qi, L., & Ravikumar, T. S. (2003). Apoptosis induced by cryo-injury in human colorectal cancer cells is associated with mitochondrial dysfunction. International Journal of Cancer, 103, 360369. Zhao, Y. (2007). In Y. Zhao (Ed.), Berry fruit, value-added products for health promotion. NW (USA): CRC Press0-8493-5802-7.
Jakob, E., & Elmadfa, I. (2000). Rapid and simple HPLC analysis of vitamin K in food, tissue and blood. Food Chemistry, 68, 219221. Lan, Y. -H., Chang, F. -R., Pan, M. -G., Wu, C. -C., Wu, S. -J., Chen, S. -L., et al. (2009). New cytotoxic withanolides from Physalis peruviana. Food Chemistry, 116, 462469. Latza, S., Ganber, D., & Berger, R. G. (1996). Carbohydrate esters of cinnamic acid from fruits of Physalis peruviana, Psidium guajava and Vaccinium vitis-idaea. Phytochemistry, 43, 481485. Li, N., Ragheb, K., Lawler, G., Sturgis, J., Rajwa, B., Melendez, J. A., et al. (2003). DPI induces mitochondrial superoxide-mediated apoptosis. Free Radical Biology & Medicine, 34, 465477. Mayorga, H., Duque, C., Knapp, H., & Winterhalter, P. (2002). Hydroxyester disaccharides from fruits of cape gooseberry (Physalis peruviana). Phytochemistry, 59, 439445. Mayorga, H., Knapp, H., Winterhalter, P., & Duque, C. (2001). Glycosidically bound avor compounds of cape gooseberry (Physalis peruviana L.). Journal of Agricultural and Food Chemistry, 49, 19041908. McCain, R. (1993). Goldenberry, passionfruit and white sapote: Potential fruits for cool subtropical areas. In J. Janick, & J. E. Simon (Eds.), New Crops (pp. 479486). New York: Wiley and Sons. Meyer, A. S. (1999). Antioxidant activity of phenolic compounds in grape juice and prune juice on human low-density lipoproteins. Fruit-processing, 11, 426430. Meyer, A. S., Yi, O. S., Pearson, D. A., Waterhouse, A. L., & Frankel, E. N. (1995). Inhibition of human low-density lipoprotein oxidation in relation to composition of phenolic antioxidants in grapes (Vitis vinifera). Journal of Agricultural and Food Chemistry, 45, 16381643. Miller, N. J., & Rice-Evans, C. A. (1997). The relative contributions of ascorbic acid and phenolic antioxidants to the total antioxidant activity of orange and apple fruit juices and blackcurrant drink. Food Chemistry, 60, 331337. Morton, J. F. (1987). Cape gooseberry. In J. F. Morton (Ed.), Fruits of warm climates (pp. 430434). Winterville, NC: Creative Resource Systems Inc. Otles, S., & Cagindi, O. (2007). Determination of vitamin K1 content in olive oil, chard and human plasma by RP-HPLC method with UVVis detection. Food Chemistry, 100, 12201222. Park, W. H., Lee, M. S., Park, K., Kim, E. S., Kim, B. K., & Lee, Y. Y. (2002). Monensinmediated growth inhibition in acute myelogenous leukemia cells via cell cycle arrest and apoptosis. International Journal of Cancer, 101, 235242. Piironen, V., Koivu, T., Tammisalo, O., & Mattila, P. (1997). Determination of phylloquinone in oils, margarines and butter by high-performance liquid chromatography with electrochemical detection. Food Chemistry, 59, 473480. Ramadan, M. F., & Mrsel, J. -T. (2003). Oil goldenberry (Physalis perviana L.). Journal of Agricultural and Food Chemistry, 51, 969974. Ramadan, M. F., & Mrsel, J. -T. (2004). Goldenberry: A novel fruit source of fat soluble bioactives. Inform, 15, 130131. Ramadan, M. F., & Mrsel, J. -T. (2007). Impact of enzymatic treatment on chemical composition, physicochemical properties and radical scavenging activity of goldenberry (Physalis peruviana L.) juice. Journal of the Science of Food and Agriculture, 87, 452460. Ramadan, M. F., & Mrsel, J. -T. (2009). Oil extractability from enzymatically-treated goldenberry (Physalis peruviana L.) pomace: Range of operational variables. International Journal of Food Science & Technology, 44, 435444.