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Functional Properties of Passion Fruit Seed Extract: Comparison
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Please note this is a comparison between Version 3 by Jessie Wu and Version 2 by Jessie Wu.

The genus Passiflora L. is widely cultivated in tropical and subtropical regions. The major species, Passiflora edulis Sims, is known as ‘passion fruit’ and is widely used in processed foods as well as eaten raw. P. edulis fruits are eaten for their pulp together with the seeds; however, the seeds are often discarded when used in processed foods. P. edulis seeds contain a variety of nutrients and functional components, and their industrial use is desirable from the perspective of waste reduction.

  • Passiflora edulis
  • antioxidant
  • seed

1. Introduction

The genus Passiflora L. is a highly diverse plant family with approximately 520 species distributed throughout the tropics of America, Asia, and Africa [1]. More than 90% of Passiflora species are distributed in the Americas; however, they are also widely distributed in India, China, Southeast Asia, Australia, the Pacific islands, and neighboring regions [2]. The Passiflora plant can be divided into pulp, peel, seeds, and bark, the constituents and health benefits of each have been investigated, particularly for P. edulis. The extract of the edible portion reportedly has protective effects against alcoholic liver disease [3]. Moreover, leaf extract has shown a variety of physiological functions, such as being anti-inflammatory [4]; providing intestine protection [5]; and having wound healing [6], antiplatelet [7], and antidepressant effects [8]. It has also been evaluated in animal studies for its safety when administered [9]. P. edulis peel is rich in dietary fiber and functional components, and various physiological effects of P. edulis peel extract have been reported, such as antihypotensive effects [10], hypoglycemic effects [11][12], and metabolic improvement [13][14]. Furthermore, P. edulis bark reportedly has anti-obesity properties [15].

2. Health Benefits of P. edulis Seed Components

2.1. Antioxidant Activity

P. edulis seeds contain a large amount of antioxidants such as polyphenols, and the seed extract has been reported to have high antioxidant activity in the 1,1-diphenyl-2-picrylhydrazyl (DPPH), 2,2′-azino-di-(3-ethylbenzthiazoline sulfonic acid) (ABTS), ferric reducing ability of plasma, oxygen radical absorbance capacity, and the β-carotene bleaching assays [16][17][18]. Santana et al. extracted components from P. edulis seeds under various extraction conditions and investigated the correlation between the component content and antioxidant activity under each condition [16]. The results showed a positive correlation between polyphenol content and antioxidant activity of the extracts, suggesting that polyphenols are a major component responsible for the antioxidant activity. Comparing the antioxidant activity of the seed extract of P. edulis with that of other Passiflora species, the IC50 of P. edulis, P. tripartita, P. ligularis, and P. pinnatistipula were 2.7–132.6, 3.2, 73.9, and 372.2, respectively, as determined via DPPH assay; meanwhile, the IC50s, as revealed by ABTS assays, were 9.0, 96.2, 23.9, and >1000, respectively [16][19][17][18], suggesting that the antioxidant activity of P. edulis is more than equal to that of other Passiflora species.
The polyphenols in P. edulis seeds contain a large amount of piceatannol, which has been reported to have antioxidant activity [20][21]. It is, therefore, considered to be responsible for the antioxidant activity of the seed extracts. In a rat model subjected to streptozotocin-induced oxidative stress, ingestion of ethanol extracts from P. edulis peel and seeds had a protective effect on the heart, liver, and kidneys against oxidative stress by enhancing superoxide dismutase levels and decreasing 2-thiobarbituric acid reactive substance levels [22]. Furthermore, attempts have been made to microencapsulate P. edulis peel and seed extracts in order to maintain and enhance their antioxidant activity in vivo [23]. The microencapsulated extracts showed that their antioxidant activity remained at 60% of the pre-digestion level after the digestion process [23]. Another study demonstrated that encapsulation of P. edulis seed extract using acylated rice starch also maintained antioxidant activity [24]. Hence, microcapsule technology may represent an effective means to transport the extracts into the body while maintaining their activity or to transport them to specific locations in the body to exert their functions.
The high antioxidant activity of P. edulis seed extract has also been applied to processed foods. The addition of an ethanol extract of P. edulis seeds has been studied to prevent lipid oxidation in dairy beverages containing sesame seed oil, which is rich in omega-3 fatty acids; the addition of the extract increased the oxidative stability of the lipids [25]. Oil extracted from P. edulis contains polyphenols as well as α- and β-tocopherol, and extracted oil containing these compounds has been reported to have high antioxidant activity [26]. In addition, oil extracted from P. edulis seeds showed the highest antioxidant activity among the extracted oils of plant seeds such as Caryocar brasiliense Camb., Orbignya phalerata Mart. and Mauritia flexuosa L., which grow in the Amazon [27]. These observations suggest that P. edulis seed oil can also be used as an antioxidant agent.

2.2. Effect on Skin

In vitro experiments have shown that ethanol extract of P. edulis seeds increases collagen production when applied to dermal fibroblasts [28]. In addition, ethanol extracts of P. edulis seeds exhibit inhibitory activity against collagenase and elastase [18][29][30]. The skin that covers the surface of human bodies is composed of the epidermis, dermis, and subcutaneous tissue. Approximately 70% of the dermis is composed of collagen, and collagen and elastin play important roles in the formation of the dermis structure; however, the amounts of collagen and elastin decrease with age [31][32]. P. edulis seed extract increases collagen production and inhibits collagen and elastin degradation, which may contribute to the maintenance of the structure of the dermis to retain skin moisture and elasticity. The collagen synthesis-promoting effect of the seed extract disappeared when the polyphenol component in the extract was removed [28], suggesting that the polyphenol component contributes to promoting collagen production.
Skin is directly exposed to UV radiation, and solar UV radiation accelerates skin aging (photoaging), causing symptoms such as coarse wrinkling, blotchy dyspigmentation, and a rough skin texture [33]. UV irradiation increases the expression of matrix metalloproteinase-1 (MMP-1), a collagen-degrading enzyme, and promotes collagen degradation, which contributes to skin aging. P. edulis seeds are rich in piceatannol, which has been shown to suppress UV-induced MMP-1 expression in fibroblasts; it has been suggested that inhibition of the Janus kinase 1 (JAK1) signaling pathway by piceatannol contributes to the suppression of MMP-1 expression [34]. In keratinocytes, UV irradiation does not produce MMP-1 in keratinocytes; however, reactive oxygen species (ROS) are generated by UV irradiation. Excess ROSs in keratinocytes cause oxidative damage, decrease the levels of non-enzymatic antioxidants such as glutathione (GSH), and activate complex signaling pathways that affect fibroblasts and strongly induce MMPs [35][36]. Ethanol extract of P. edulis seeds or piceatannol increases GSH levels in a dose-dependent manner in keratinocytes [37]. Furthermore, MMP-1 activity increased when the medium of UV-irradiated keratinocytes was applied to fibroblasts; however, the increase in MMP-1 was suppressed in the medium of keratinocytes treated with piceatannol [37]. P. edulis seed extract and its polyphenolic components are expected to suppress excessive ROS increase in human skin and inhibit photoaging.
Human study has been conducted to examine the effects of P. edulis seed extract on skin moisture and elasticity. A randomized, placebo-controlled, double-blind study was conducted to evaluate the effects of P. edulis seed extract (rich in piceatannol) on the skin of healthy women [38]. The results showed that the water content and elastic recovery from the pretrial were significantly increased 8 weeks after ingestion of the seed extract compared with the placebo. These results indicate that intake of P. edulis seed extract containing piceatannol is effective for improving skin hydration and elasticity.
The ethanol extract of P. edulis seeds has also been reported to inhibit tyrosinase activity [18] and inhibit melanin synthesis when applied to melanoma cells [28]. The inhibitory effect of melanin synthesis disappeared when the polyphenol fraction in the seed extract was removed, suggesting the involvement of polyphenols such as piceatannol, which has been reported to exhibit higher tyrosinase inhibitory activity than kojic acid or resveratrol [39]. Piceatannol and other stilbene compounds have been identified not only in ethanol and acetone extracts of P. edulis seed, but also in extracted seed oil [40], and P. edulis seed oil extracted by ultrasound showed tyrosinase inhibitory activity [41]. Furthermore, nanostructured lipid carrier-based hydrogels with P. edulis seed oil showed high tyrosinase inhibitory activity and low skin irritation; therefore, P. edulis seed oil has been considered for use as a cosmetic [42]. In human studies, most subjects noticed significant improvement in acne vulgaris after 8 weeks of application of a 10% P. edulis seed extract cream [43]. P. edulis seed extract exhibits antibacterial activity against Propionibacterium acnes [44], and this antibacterial activity of the extract may have contributed to the improvement of acne vulgaris in the human studies. In addition, another human study demonstrated that application of a cream containing 6% P. edulis seed extract improved the symptoms of striae distensae, a common form of skin scarring [45]. Evidently, P. edulis seed extract can contribute to the improvement of skin disorders such as acne vulgaris and striae distensae when applied to the skin.

2.3. Effect on Fat Metabolism

The effect of P. edulis seed extract on fat metabolism has also been examined. In vivo experiments showed that rats fed a high-fat diet showed signs of cardiovascular disease with abnormal serum profiles, whereas high-fat diets containing ethanol extracts of P. edulis seed improved liver enlargement, blood triglyceride, cholesterol levels, and cardiac function [46]. It has also been demonstrated that ovariectomized mice fed a high-fat diet showed marked weight gain and visceral fat accumulation, however, these effects were significantly suppressed when mice were fed a high-fat diet containing 0.05% piceatannol extracted from P. edulis seeds [47]. Piceatannol is considered to be a major polyphenol that exhibits anti-obesity effects among the compounds in P. edulis seed extract, and compared to high-fat fed mice, intake of piceatannol-containing high-fat diets decreased the weights of liver, spleen, perigonadal, and retroperitoneal fat [48].
Human studies on fat metabolism have been conducted, and a double-blind, placebo-controlled, crossover study showed that a food containing 10 mg piceatannol from P. edulis seeds for 1 week significantly reduced the respiratory quotient at rest and during very light exercise [49]. Moreover, the mean amount of fat burning at rest was increased by 39.5% during piceatannol intake compared to placebo intake (Figure 1). Another study showed that even during moderate-intensity exercise, intake of 10 mg of piceatannol from P. edulis seeds for 2 weeks significantly increased fat burning and decreased the respiratory quotient compared to the placebo [50]. These results show that P. edulis seed extract containing piceatannol can promote fat burning both at rest and during exercise.
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Figure 1. Fat-burning effect of ingestion of piceatannol from Passiflora edulis seed [49]. Data are shown as the mean ± SEM (n = 9).
The mechanism of action of piceatannol (which is abundant in P. edulis seeds) on fat metabolism has been investigated in vitro and in vivo, and enhancement of fat metabolism via SIRT and the peroxisome proliferator-activated receptor alpha (PPARα) is suggested to be the mechanism of action. The SIRT1-inducing effect of P. edulis seed extract and piceatannol has been reported in vitro and in vivo [51][52], and SIRT1 is thought to activate fatty acid β-oxidation by deacetylating peroxisome proliferator-activated receptor transcriptional coactivator γ1α [53]. Furthermore, piceatannol has been reported to increase PPARα in fatty liver-induced HepG2 hepatocytes [54]. Treatment of HepG2 cells with piceatannol increased PPARα, farnesoid X receptor, and carnitine palmitoyltransferase 1α and promoted β-oxidation of fatty acids. In in vivo experiments, male C57BL/6J mice fed piceatannol orally for 4 weeks showed an increase in PPARα as well as induction of SIRT1 expression [52]. In addition, piceatannol has been shown to strongly inhibit lipid synthesis and fat accumulation in human mesenchymal stem cells by suppressing the expression of fatty acid synthase and glucose transporter type 4, which are important factors in the adipogenic pathway [55]. Piceatannol improves fat metabolism through various pathways related to fat metabolism, and P. edulis seed extract containing piceatannol may improve fat metabolism in a similar manner.
It has been reported that not only the polyphenols in P. edulis seeds, but also those in extracted oil, are expected to have an inhibitory effect on fat accumulation. P. edulis seed oil extracted with hexane contains high amounts of linoleic and oleic acids, and the administration of this oil resulted in significant reductions in triglycerides, total cholesterol, and low-density lipoprotein-cholesterol in high-fat-diet-induced rats [56], suggesting that P. edulis oil is also expected to have anti-obesity effects.

2.4. Hypoglycemic Effect

Anti-diabetic effects of P. edulis seeds have been investigated, and oral administration of P. edulis peel and seed extract for >7 days was reported to significantly improve blood glucose levels in a rat model subjected to streptozotocin-induced oxidative stress [22]. Experiments using a genetic diabetic mouse model (db/db mice) also showed a significant reduction in blood glucose levels after a single dose of both P. edulis seed extract and its abundant component, piceatannol [57]. Regarding the mechanism of blood glucose regulation by P. edulis seed extract, a study examined the blood glucose-lowering effect of piceatannol from P. edulis seeds in freely moving healthy rats [58]. In this study, intravascularly administered piceatannol reduced blood glucose levels during both fasting and glucose tolerance tests, and piceatannol increased the insulin secretion index during the glucose tolerance test, suggesting that piceatannol from P. edulis seed improves glucose tolerance by promoting the initial secretion of insulin. In C57BL/6J mice fed a high-fat diet, administration of 10 mg piceatannol/kg body weight/day for 4 weeks decreased the area under the curve of blood glucose during the oral glucose tolerance test [52]. In this study, piceatannol increased the levels of insulin receptors and AMP-activated protein kinase in the liver and increased the levels of Sirt1, Sirt3, Sirt6, and two downstream targets of SIRTs, peroxisome proliferator-activated receptor gamma coactivator 1-alpha, and forkhead box O1. Evidently, piceatannol-rich seed extract can improve blood glucose levels via factors related to SIRTs and its downstream targets, as well as insulin signaling.
The seed extracts of P. pinnatistipula and P. tripartita have also exhibited α-amylase and α-glucosidase inhibitory activity in vitro [19]; however, no reports have verified its hypoglycemic effect in vivo or in human studies. Meanwhile, among the polyphenols detected in P. edulis seeds, stilbenes—such as piceatannol—have been shown to exhibit α-glucosidase inhibitory activity [59]. Although it remains unclear whether P. edulis seed has a stronger hypoglycemic effect than other species, P. edulis seed has shown many positive results and can be expected to exhibit hypoglycemic effects.
The effect of seed extract on glucose metabolism has been studied in human trials. Intake of 20 mg/day of piceatannol from P. edulis seed for 8 weeks in overweight men reduced serum insulin levels, homeostasis model assessment-insulin resistance, blood pressure, and heart rate [60]. P. edulis seeds are expected to be effective in improving insulin sensitivity.

2.5. Other Physiological Effects

The antihypertensive potential of P. edulis seeds was evaluated in vivo [61]. This investigation demonstrated that the ethanolic extracts obtained from P. edulis f. edulis seeds prevented hypertension induced by nitric oxide deficiency in rats. The mechanism of the antihypertensive effect of P. edulis seed extracts was suggested to be the synthesis of nitric oxide and inhibition or antagonism of angiotensin-II.
The anti-cancer potential of P. edulis seeds has also been investigated. It has been reported that P. edulis seed extract inhibits cancer cell proliferation via human glyoxalase I, the rate-limiting enzyme for the detoxification of methylglyoxal in both NCI-H522 cells and HCT116 cells [62]. P. edulis seed extract by ethanol also shows antitumor activity in MCF-7 cells, and the mechanism of antitumor activity is suggested to be induction of apoptosis via the mitochondrial pathway [63]. An in vivo study demonstrated that when an aqueous extract of P. edulis seeds was administered for 10 weeks, the extract affected the protein levels of p21, cyclin D1, and cyclin-dependent kinase 4; delayed disease progression in the transgenic adenocarcinoma of the mouse prostate model; and decreased the incidence of preneoplastic lesions [64]. A number of preclinical studies have shown that piceatannol can prevent the growth of cancers in various organs [65]. Cumulatively, this evidence shows that P. edulis seed extracts are a potential source of anti-cancer activity.

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