Superfruits in China: Bioactive phytochemicals and their potential health benefits – A Review

Abstract The term “superfruit” usually refers to certain fruits, which are rich in antioxidant components, therefore, are beneficial to human health. In China, there has been the concept of health preservation and dietary therapy through food intake in a long history. However, some other superfruits growing mainly in China have not attracted extensive attention, such as Cili, Goji berry, and sea buckthorn. Many studies suggested all of these superfruits showed strong antioxidant effects and anti‐inflammatory activity in common. However, there are various other advantages and functions in different fruits. This article reviewed the research findings from the existing literature published about major antioxidant bioactive compounds and the potential health benefits of these fruits. The phytochemicals from superfruits are bioaccessible and bioavailable in humans with promising health benefits. More studies are needed to validate the health benefits of these superfruits. It would provide essential information for further research and functional food development.

| 6893 LIU et aL. (Davidson et al., 2018). In recent years, some other fruits with extremely high contents of antioxidants are also called "superfruits," such as açaí, acerola, goji berry, and mangosteen (Felzenszwalb et al., 2013;Oliveira et al., 2012;Pedro et al., 2018;Prakash & Baskaran, 2018;Wittenauer et al., 2016). The health benefits and potential applications of superfruits could be better exploited if more research is available (De Souza Sant'Ana, 2011). Chang et al. (2019) reviewed the phytochemicals, antioxidant efficacies, and health effects of a list of superfruits (açai, acerola, camu-camu, goji berry, jaboticaba, jambolao, maqui, noni, and pitanga). However, due to the abundant geographical and climatic conditions, China is a place of production of several superfruits. This review discusses the bioactive ingredients and their potential health benefits of the selected superfruits in China. It is aimed to arouse researchers' interests in various scientific fields to study superfruits as functional foods or functional food ingredients, and hence, stimulating largescale commercial cultivation ( Figure 1).

| THE SCIENTIFIC MECHANIS M OF PHY TO CHEMI C AL S WITH ANTI OXIDANT AC TIVIT Y OF SUPERFRU ITS
Oxidative stress releases free oxygen radicals in the body to induce many disorders including cardiovascular malfunction, cancers, cataracts, aging, and other immune diseases (Kaur & Kapoor, 2001;Malik et al., 2005). Antioxidant refers to a compound that can delay or inhibit the oxidation of lipids or other molecules through the initiation or spread of oxidative chain reaction that alleviates the oxidative damage in the human body (Tachakittirungrod et al., 2007). In Table 1, the structural features and antioxidant mechanisms of the major groups in fruits are presented. The antioxidants act as scavengers to neutralize the reactive oxygen species (ROS) by donating one of their own electrons retarding to the electron-stealing reaction.
As the antioxidants are capable to bind metal ions such as copper and iron that catalyze oxidation, they are recognized as chelators as well. Some of the phytochemicals halt cancer by blocking enzymes that enhance cancer or preventing various carcinogens that initiate diseases. There are a number of phytochemicals that could damage cells, tissues, and organelles by producing enzymes that destroy carcinogens in the body and others that suppress the reproduction of cells exposed to carcinogens. Meanwhile, antioxidants are supposed to be beneficial in helping to delay initial episodes of general immune disorders by extending the period between infection and clinical appearance (Kaur & Kapoor, 2001

| T YPIC AL SUPERFRU ITS IN China AND THEIR P OTENTIAL HE ALTH B ENEFITS
Some typical superfruits in China are reviewed in this section.
Tables 2 and 3 summarized the main bioactive components and potential health benefits. Various human intervention and animal studies have evaluated the potential health benefits of selected superfruits. All the selected superfruits were reported with antioxidant and anti-inflammatory activity in common, while some of them reported with unique effects such as hepatoprotective (pomegranate and sea buckthorn), radioprotective (Cili), and vision-protective (goji berry). The risk of toxicity of the mentioned superfruits as functional foods requires more investigation. Allergic reactions were reported from goji berry consumption. Further studies into the safety and toxicological properties of these superfruits are urgently needed since they might pose allergenic or chemical toxicity risks, especially for people not from China or Asia.

| Cili
Cili (Rosa roxburghii Tratt) is a kind of specific wild plant in Southwest China. Cili consists of several important components such as superoxide dismutase (SOD), polysaccharide, vitamin C, vitamin E, and some mineral elements (Zn and Ca). Additionally, SOD has long been regarded as a free radical scavenger and ascorbate, which is a highly potent aqueous-phase antioxidant in plasma (Frei, 1991). This fruit has been known to have a number of beneficial effects on atherosclerosis, cancer, aging, and immunity stress. A set of indices, such as the activity of natural killer (NK) cells, free radical metabolism, microcirculation parameters, cognitive function, light reaction time, and cardiovascular function were selected to evaluate the effects of Cili among 50-75 years old people (30 men and 30 women). It demonstrated that Cili was able to enhance natural killer cell activity and strengthen immune function. Furthermore, the supplementation of Cili would significantly improve the antioxidative capacity and then reduce the injury effect on the endothelium of capillary, artery, and brain with the mechanism probably due to its bioactive components such as SOD, polysaccharides, vitamin C, vitamin E, etc ( Ma et al., 1997).
Furthermore, the flavonoids of Cili exhibit radioprotection and anti-apoptosis properties via the Bcl-2(Ca 2+ )/Caspase-3/ PARP-1 pathway in mouse thymus (Xu et al., 2016). In addition, water-soluble polysaccharide (RTFP) from Cili has shown the potential to be a functional ingredient or hypoglycemic agent in food, pharmaceutical, and cosmetic preparations . Later, the same research group reported that the digestion properties of a novel polysaccharide from Cili (RTFP-3) under saliva simulated gastric, and small intestinal conditions were studied. It was proven to be a functional ingredient to improve human health and prevent diseases through regulating gut flora .

| Goji berry
Goji (Lycium barbarum L.) berry has been used for centuries in traditional medicine practice in China. It contains mainly polysaccharides, polyphenols, and carotenoids with an ability to exert beneficial effects for the prevention of chronic diseases (cancer, atherosclerosis, obesity, and diabetes), and to promote weight loss and longevity in rats (Amagase & Farnsworth, 2011;Fiorito et al., 2019;Ma et al., 2019;Pedro et al., 2018). Also, there were results that showed that goji berry demonstrated significant reductions in feelings of tiredness after exercise in the human subjects tested. This indicates that goji berry may attenuate stress-related reactivity and facilitate adaptation to physical stressors during exercise (Amagase & Nance, 2011;Chang et al., 2019). The content of polysaccharides in goji berry is more than 40% (Chan et al., 2007). Polysaccharides purified from goji berry were reported to be effective in various potential health benefits. Wang et al. (2002) found that goji polysaccharides were able to protect the seminiferous epithelium from structural damage and apoptosis, in testicular tissue culture and inhibit lipid peroxida-

| Hawthorn
Hawthorn ( Also, they reported a sesquiterpene found in the seeds of hawthorn, which exhibits the ability to inhibit platelet aggregation, thus showing antithrombotic activity. In addition, a series of metabolic syn- Hawthorn has a high pectin content compared with other fruits.
The hawthorn pectin content in fresh fruit is as high as 6.4% and the pectin oligosaccharides from hawthorn showed potential antiglycation activities . Moreover, in vitro antioxidant activity assays indicated that ultrasonic treatment significantly improved the antioxidant activity of pectin ultrasonic treatment and is an effective way to enhance the antioxidant activity. .
In addition, the pericarp of mangosteen showed potential as antioxidant ingredients in cosmetic formulations (Wittenauer et al., 2016).
Xanthones were considered to be really important for chemopreventive or therapeutic functions. Several studies represented that xanthone derivatives, as the major secondary metabolites of mangosteen, demonstrated antibacterial, antifungal, antioxidant, anticancer, antiplasmodial, and cytotoxic activities (Gopalakrishnan et al., 1997;Gutierrez-Orozco & Failla, 2013;Ji et al., 2007;Nakatani et al., 2002;Sakagami et al., 2005;Suksamrarn et al., 2006;Yu et al., 2007). So far, there are more than 68 xanthones isolated from the mangosteen fruit with the majority of them being α-and γ-mangostin (Aizat et al., 2019). Jung et al. (2006) found that α-mangostin, one of the important xanthone derivatives, could inhibit alveolar duct formation in a mouse mammary organ culture model and alleviate the carcinogen-induced formation of aberrant crypt foci in a short-term colon carcinogenesis model. Matsumoto et al. (2004)  ATPase pathway in rat pheochromocytoma PC12 cells. γ-mangostin is a tetraoxygenated diprenylated xanthone derivative. It has been found that γ-mangostin was able to bind to cyclooxygenase and inhibit its activity resulting in reduced production of prostaglandin E 2 (PGE 2 ), which would affect the activities of some cell types, such as neurons, glial, and endothelial cells at a high level (Nakatani et al., 2002). The function of γ-mangostin is supposed to contribute to its anti-inflammatory activity. Moongkarndi et al. (2004) studied the antiproliferative, apoptotic, and antioxidative properties of crude methanolic extract (CME) from mangosteen. The results implied that the CME decreased the intracellular ROS production on

| Pomegranate
The fruit known as pomegranate (Punica granatum) originated from the Middle East, then extended to Mediterranean areas, as well as in countries such as Iran, India, China, Japan, and Russia. Pomegranate presented that punicalagin, EA, and total pomegranate tannin could reduce the cell number of human oral, prostate, and colon tumor cells. Furthermore, when concentrations of those compounds rose up to an equivalent level (w/w) with pomegranate juice, they were able to induce apoptosis in HT-29 cells. Punicalagin is supposed to be the most potent antioxidant ingredient for its antioxidant properties. The radical scavenging ability of punicalagin was because of polyphenolic hydroxyl groups that enhance the antioxidative activity through additional resonance stability and o-quinone or p-quinone formation (Kulkarni et al., 2004). In addition, pomegranate juice consumption resulted in antiatherogenic influence with a remarkable reduction in oxidative stress in serum and monocytesmacrophages, and macrophage uptake of oxidized LDL and then cellular cholesterol biosynthesis (Fuhrman et al., 2005;Rosenblat, Hayek, & Aviram, 2006). Some studies showed that both pomegranate flower and juice might prevent diabetic sequelae via peroxisome proliferator-activated receptorγ binding and nitric oxide production. Antidiabetic compounds included oleanolic, ursolic, and gallic acids (Katz, Newman, & Lansky, 2007). Pomegranate juice was also reported to decrease the potent downregulation of NOSⅢ induced by the oxidation of LDL in human coronary endothelial cells (Nigris et al., 2007). It has been considered that this fruit juice may be useful in Alzheimer's disease, as supplementation of mice with PJ led to significantly less accumulation of soluble Aβ42 and amyloid deposition in the hippocampus (Hartman et al., 2006).
However, the total content of anthocyanins in pomegranate juice was reported to be higher than any other fruit juice tested for antioxidant activity. Pomegranate juice increased the biological actions of NO by protecting NO against oxidative destruction but reversed proatherogenic effects induced by perturbed shear stress (de Nigris et al., 2007;Ignarro et al., 2006).
The result from Kohno et al. (2004) suggested that administration of pomegranate seed oil (PSO) that was rich in c9, t11, and c13-CLN could inhibit azoxymethane-induced colon carcinogenesis, while Yamasaki et al. (2006) found that PSO promoted Ig production by mouse splenocytes. In addition, emerging evidence has suggested that nutraceutical ingredients like PSO possessed health-promoting effects in cell and animal models. However, these health benefits

| Sea buckthorn
Sea buckthorn (Hippophae rhamnoides L.) belongs to the Elaeagnaceae family, which is naturally distributed throughout Eurasia from the Baltic Sea and the North Sea in the west to Central Asia in the east (Guliyev et al., 2004;Negi et al., 2005;Nelson & Olas, 2018). This fruit is elliptic or oval in shape, and it is a yellowish-orange berry with silvery dust particles covered surface, and sour in taste (Guliyev et al., 2004). Sea buckthorn consists of series of chemical compounds including vitamins, carotenoids, flavonoids, etc. It is found that the juice is rich in vitamin E, vitamin C, and flavonoids that are 13.3, 1,540, and 1,182 mg/L, respectively. More than 75% of the total vitamin E is in the form of α-tocopherol, and isorhamnetin is one of the most active flavonol aglycones in sea buckthorn juice (Eccleston et al., 2002;Teng et al., 2006). All parts of the plant have been used as a good source of bioactive substances treating diseases in traditional medicine (Geetha et al., 2003). Nowadays, scientific studies have reported pharmacological effects of sea buckthorn. In vitro studies and in vivo human and animal models, have found that the juices, jams, and oils derived from this fruit and seeds have a wide range of beneficial anti-inflammatory, anticancer, antioxidant, and anti-atherosclerotic effects. These were attributed to the presence of phenolics, vitamins, minerals, amino acids, fatty acids, and phytosterols (Nelson & Olas, 2018). Eccleston et al. (2002) demonstrated that supplementation of sea buckthorn juice showed a moderate decrease in the susceptibility of LDL to oxidation and, therefore, its rate of accumulation by macrophages. Teng et al. (2006) studied isorhamnetin, which was the metabolite of quercetin (Ader et al., 2000), and the result illustrated potent cytotoxicity against human hepatocellular carcinoma cells (BEL-7402).
The antioxidant activity of leaf extract of sea buckthorn was also detected by Geetha et al. (2003) studying chromium(VI)-induced oxidative stress in albino rats. They revealed that the ethanolic leaf extract at a concentration of 100 and 250 mg/kg body weight significantly reduced the chromium-induced oxidative damage in animals.
Meanwhile, methanol extract of sea buckthorn seed exhibited high antibacterial and antioxidant capacity, which is supposed to be due to its high phenolic contents (Negi et al., 2005). Oil extracted from sea buckthorn has high concentrations of lipophilic constituents, predominantly unsaturated fatty acids in triglyceride form, and phytosterols and vitamins A and E have a positive influence on human health, especially on the cardiovascular system (Olas, 2016).

| CON CLUS ION
This review has focused on the potential human health benefits of superfruits in China. Evidently, the functional properties are due to their abundant or unique components with high nutrition and medical value. In vivo and in vitro studies have found that the bioactive phytochemicals present in superfruits have been useful in antioxidant, anti-inflammatory, and reducing the risk of various diseases, such as heart diseases, various cancers, and brain diseases. Complementary research is also needed to enhance the potential functionalities of the by-products of these superfruits in China, as such by-products contain numerous phytochemicals that may be beneficial to human health. In the future, the studies of functional food development of these superfruits could not only benefit the health of consumers but also promote the development of China's fruit industry.

ACK N OWLED G M ENTS
This work was funded by the National Natural Science Foundation

CO N FLI C T S O F I NTE R E S T
The authors declare that they have no conflicts of interest.