Abstract Acerola (Malpighia emarginate DC.) is one of the richest natural sources of ascorbic acid and contains a plethora of phytonutrients like carotenoid phenolics, anthocyanins, and flavonoids. There is an upsurge of interest in this fruit among the scientific community and pharmaceutical companies over the last few years. The fruit contains an exorbitant amount of ascorbic acid in the range of 1500–4500 mg/100 g, which is around 50–100 times that of orange or lemon. Having a reservoir of phytonutrients, the fruit exhibits high antioxidant capacity and several interesting biofunctional properties like skin whitening effect, anti-aging, and multidrug-resistant reversal activity. Countries like Brazil, realizing the potential of the fruit have started to exploit it commercially and have established a structured agro-industrial-based market. Despite possessing an enriched nutrient profile with potent ‘‘functional food’’ appeal, acerola is underutilized in large parts of the globe and demands greater attention. A comprehensive literature analysis was carried out concerning the latest frontiers on the compositional characteristics of the fruit. Emphasis has been given to newer dimensions of functional aspects of ascorbic acid and allied work and pectin and pectin methylesterase. The range of nutraceutical phytonutrients present in acerola and their biofunctional properties have been discussed. Recent advances in the value addition of the fruit highlighting the use of techniques like filtration, encapsulation, ultrasound, sonication, etc. are also elaborated. Furthermore, the potential use of acerola pulp in edible films and waste utilization for the development of valuable byproducts has been highlighted.

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Introduction

Acerola (Malpighia emarginata DC.) also known as Barbados cherry or West Indian cherry, belongs to the Malpighiaceae family. The fruit is known to be one of the richest natural sources of ascorbic acid in the world, whose vitamin C content is comparable to only Camu Camu (Mirciaria Dubai) (Delva and Schneider 2013a). The plant has synonyms like Malpighia glabra L., and Malpighia punicifolia L., but Malpighia emarginata DC. has been accepted as the present scientific name by the taxonomists (Assis et al. 2008).

The evergreen shrub of acerola which flourishes in warm and tropical climates bears a small trilobite cherry-like fruit (Mezadri et al. 2008; Delva and Schneider 2013b). It grows from South Texas, through Mexico and Central America to northern South America and throughout the Caribbean and has of late been introduced in the sub-tropical areas throughout the world including India (Assis et al. 2008). The tree followers from April to November and the fruit matures in 3–4 weeks after fall flowering. Fruits are small (1–4 cm diameter) weighing 2–15 g, whose skin color is green at the immature stage of ripening which changes to orange-red and a final bright red color on maturation (Supplementary Figure 1). Although the sweetness of the fruit varies according to the variety barring a few sweet varieties, most of them are quite tart and acidic.

Apart from containing an exorbitant amount of ascorbic acid the fruit also contains several phytonutrients like carotenoids, phenolics, flavonoids, and anthocyanins (Mezadri et al. 2008) and possesses numerous biofunctional properties. Therefore, value addition to this super fruit can be of great functional importance. This review discusses the current status of acerola in the world and India and summarizes the latest research publications and patents, along with their implications on the wholesome compositional characteristics, biofunctional properties, and value addition to the fruit.

Status in world

Asenjo and de Guzman of Puerto Rico were the first ones to point out the unusually high content of ascorbic acid in acerola, in the year 1946. Since then, over the years, the popularity of the fruit has increased and has at present been well established as a fruit of functional importance. Over the last few decades, Brazil has started to exploit acerola commercially and now is the largest producer of acerola, with 11,000 hectares of acerola plantation, producing 3000 kg/ha and a total of 32,990 tons/year (Pommer and Barbosa 2009). Brazil has also dominated in the marketing and export of processed products from acerolas like frozen fruit, juice, marmalade, frozen concentrate, jam, and liquor (Delva and Schneider 2013a). To preserve the genetic variability and provide evaluation and indication of promising genotypes of acerola, an Acerola Active Germplasm Bank (AGB) was established in June 1998, by the Federal Rural University of Pernambuco, Brazil (Lima et al. 2005). The fruit is also cultivated on a small scale in the American continent. In France, Germany, and Hungary, the fruit is used largely in juice form, whereas in the United States, it is utilized by the supplement and pharmaceutical industries as a rich source of ascorbic acid (Delva and Schneider 2013b). In the Chinese market too, acerola supplements are available.

In India, the cultivation of the fruit goes back to the year 1962, wherein it was cultivated in the gardens of Chennai and Mysore cities (The Wealth of India 1962). As of now, the fruit is grown as a backyard tree in the states of Tamil Nadu, Kerala, Maharashtra, and Karnataka. During 1995–1996, a few selections of plants were introduced in Andaman and Nicobar Islands that performed well due to the tropical and humid climate (Singh 2006). Acerola is an exotic fruit that has exceptional agro-industrial potential and represents an alluring economic prospect. Due to the lack of awareness of its nutritional value and cultivation, the crop has not yet gained popularity among Indian farmers and remains a lesser-known and underutilized fruit. India being a tropical country, well suited for the growth of the acerola crop holds immense potential for the commercial cultivation and exploitation of the fruit.

Fruit development and changes during fruit ripening

Acerola fruits show a biphasic pattern of growth, with an increase in most of its size in the first phase of growth and an equal weight gain in each growth phase of about 2 weeks duration. The development of full maturity of fruit with deep red color is reached after 24–26 days of anthesis. It is a climacteric fruit with a very high respiratory rate (900 ml CO2 kg-1 h-1 ) and a low rate of peak ethylene production (3 ll C2H4 kg-1 h-1 ). Fully mature acerola fruits are highly delicate with a shelf life of only 2–3 days at ambient temperature. The fruits have a high metabolic activity after harvest and are too perishable for the fresh market (Delva and Schneider 2013a).

The ripening of acerola involves a sequence of complex biochemical reactions. There is the hydrolysis of starch, conversion of chloroplast into chromoplast, production of carotenoids, anthocyanins, and other phenolic compounds, and the formation of volatile compounds (Vendramini and Trugo 2000). All these are important for the peculiar flavor and the final characteristics of the mature fruit.

Vendramini and Trugo (2000) analyzed the chemical composition of acerola fruit at three stages of maturity. They found that titrable acidity, sugars, and soluble solids increased and Vitamin C and protein decreased with ripening. Further, Lima et al. (2005) evaluated the total phenolic and carotenoid contents in 12 acerola genotypes at three stages of ripening and observed that the phenolics degrade and carotenoids are biosynthesized during fruit maturation. A lower total antioxidant activity was found in fruit ripening by Oliveira et al. (2012) due to the decrease in total vitamin C and total soluble phenols content. They further reported that on ripening there was a reduction in the activities of oxygen-scavenging enzymes and an increase in membrane lipid peroxidation, indicating that acerola ripening is characterized by progressive oxidative stress.

Composition of acerola

Acerola is a source of several macro and micronutrients, which are summarized in Table 1. Glucose, fructose, and a small amount of sucrose are the major sugars present in the mature acerola fruit. Among the organic acids, malic acid represents 32% of the total acids present in the mature fruit whereas citric acid and tartaric acid are present in minor amounts (Righetto et al. 2005). The physicochemical properties of acerola fruit and its nutritional value depend on several factors, including growing locations, environmental conditions, cultural practices, stage of maturation, processing, and storage (Delva and Schneider 2013a). The detailed composition of the fruit is discussed herein.

Ascorbic acid

Ascorbic acid is one of the most important water-soluble vitamins, essential for collagen, carnitine, and neurotransmitter biosynthesis. Most animals and plants can synthesize ascorbic acid, but humans are unable to synthesize it due to the non-functional enzyme L-guano-1,4,-lactone oxidase, which catalyzes the final step in the ascorbic acid biosynthesis in animals (Naidu 2003). Therefore, humans require it as an essential supplement in their diet. Acerola is a natural source of vitamin C, whose content ranges from 1000 to 4500 mg/100 g, which is around 50–100 times that of orange or lemon (Moreira et al. 2009; Almeida et al. 2014). The Recommended dietary allowances (RDA) of ascorbic acid for adults ([ 19 yr) are 75 mg/day for women and 90 mg/day for men (Naidu 2003). Therefore, the consumption of three acerola fruits per day could satisfy the vitamin C RDA for an adult (Matta et al. 2004). However, one should abstain from eating large amounts of fruit as extreme intake of vitamins can act as pro-oxidant and generate changes in DNA. To substantiate the hypothesis, Dusman et al. (2012), investigated the cytotoxic and mutagenic effects of acerola fruit pulp and vitamin C in animal and plant systems. Their study showed that fresh acerola pulp diluted in water at a concentration of 0.4 mg ml-1 and commercial frozen acerola pulp diluted at a concentration of 0.2 mg ml-1 inhibited cell division in Allium cepa L. In the Wistar rats, all treatments of acerola, either acute or subchronic, were found to be neither cytotoxic nor mutagenic.

It has been reported that the vitamin C of acerola is better absorbed by human beings than synthetic ascorbic acid (Assis et al. 2008). Uchida et al. (2011) studied the comparison between the absorption and excretion of ascorbic acid alone and acerola juice in healthy Japanese subjects. Their results indicated that some components of acerola juice favorably affected the absorption and excretion of ascorbic acid. Vitamin C is readily absorbed when the intake is up to 100 mg/day; and at elevated levels of intake (500 mg/day), the efficiency of absorption of ascorbic acid swiftly declines (Naidu 2003). A much detailed study on the absorption, bioavailability, and toxicological effect of ascorbic acid present in the food matrix of acerola is needed to ascertain the possible holistic health benefits of the fruit.

However, as ascorbic acid is highly unstable, its loss incurred in value-added products during processing should also be considered. Our group showed a * 18–29% retention of ascorbic acid in various ketchup formulations developed from acerola and tomato (Prakash et al. 2016). In another study, Moreira et al. (2009) reported a 6–15% loss of ascorbic during spray drying of acerola pomace extract.

Understanding the molecular mechanism of the genes responsible for the abundance of vitamin C in acerola can open up new avenues for the propagation of commonly cultivated crops with enriched vitamin C content in them. Several detailed studies on the expression patterns of genes of enzymes that are involved in various steps of the ascorbic acid synthesis in acerola through the Smirnoff– Wheeler (SW) pathway have been studied by Badejo and his Japanese group. However, more detailed studies are required to elucidate the precise molecular mechanism for elevated biosynthesis of ascorbic acid in the fruit (Badejo et al. 2008).

Phytonutrients

Phytochemicals are non-nutrients present in plants, which are known to have diverse biological activities and reduce the risk of many chronic diseases. The major group of phytochemicals includes carotenoids, phenolics, alkaloids, nitrogen-containing compounds, and organosulfur compounds. Acerola is one of the few fruits, apart from having an exorbitant content of ascorbic acid, also contains a plethora of other phytonutrients like phenolics, flavonoids, anthocyanins, and carotenoids in a fair amount. The fruit also contains pro-vitamin A, vitamins B1 and B2, niacin, albumin, iron, phosphorus, and calcium (Assis et al. 2000; Delva and Schneider 2013a). Aptly, acerola is considered a ‘‘super fruit’’.

Phenolic compounds are one of the key secondary metabolites having diverse structures that are present ubiquitously in plants. The major phenolics present in acerola are in the form of phenolic acids, flavonoids, and anthocyanins. The phytonutrient content varies depending on the variety, genotype, stage of maturity, and growing and processing conditions. Mezadri et al. (2008) evaluated the total phenolics in different commercial frozen pulps and crushed and squeezed juices and reported values of 452–751, 805–1050, and 973–1060 mg gallic acid equivalent per 100 g (GAE/100 g). The anthocyanins content in commercial pulps was around 2.7 mg/100 g cyanidin-3- glucoside while the content in crushed and squeezed juices ranged around 46.9–52.3 mg/L cyanidin-3-glucoside. The phenolic content in acerola pulp and juices is higher than the fruits like maqui, pineapple, mango, guayaba, etc., but the anthocyanins content is lower than other fruit juices rich in anthocyanins like strawberries or blood oranges (Mezadri et al. 2008) Prakash et al. (2016) developed ketchup from different blended proportions of acerola and tomato and found varied retention of color after blending and blending. 

Carotenoids are organic pigments present in many fruits and vegetables, which are known to possess several physiological functions. The carotenoid content in 12 different acerola genotypes harvested in the dry and rainy seasons was found in the range of 9.4–40.6 lg g-1 b carotene equivalents by Lima et al. 2005. Four major carotenoids b-carotene, lutein, b-cryptoxanthin, and carotene were identified in acerola by Rosso and Mercadante 2005.

Pectin

Pectin, a methylated ester of polygalacturonic acid that constitutes about one-third of the cell wall dry substance in higher plants, has been successfully used for years in the food and beverage industry as a gelling agent, a thickening agent, and a colloidal stabilizer. In acerola, Assis et al. (2001) reported a yield of 4.51% pectin in the immature green stage of the fruit, which was found to decrease to 2.99% on fruit ripening. The yield is comparatively lesser than the other pectin-rich source like apple pomace (10–15%) and citrus peel (20–30%) (Srivastava and Malviya 2011).

Pectin methylesterase

The enzyme pectin methylesterase (PME), present in most plant tissues, removes methyl groups from cell wall pectic constituents during ripening, which can then be depolymerized by polygalacturonase, decreasing the intercellular adhesivity and tissue rigidity (Assis et al. 2001). PME activity was found to be highest (2.08 units g-1 /g) in the immature stage of acerola (Assis et al. 2001). In a different study, they reported that the acerola PME was very stable at 50 °C and needed 110 min for inactivation at 98 °C. These values were found to be much higher than those of citrus PME inactivation, which requires only 1 min at 90 °C for inactivation. The heat inactivation of acerola PME was found to be nonlinear, which suggested the presence of fractions of PME with different heat stabilities (Assis et al. 2000). Further, in a separate study, the same group partially purified and characterized the acerola PME and reported that the total and partially purified PME specific activity increased with temperature. The total acerola PME retained 13.5% of its specific activity after 90 min of incubation at 98°C. The Km values of 0.081 and 0.12 mg/ml were reported for the total and partially purified PME isoforms respectively (Assis et al. 2002).

Since immobilized pectic enzymes can be used for clarification of various fruit juices (Demir et al. 2001), the same group of researchers further went on to try acerola PME immobilization on different supports. They immobilized total and partially purified PME from acerola on porous silica particles and reported the efficiency value of 114 and 351% respectively (Assis et al. 2003). Later, they screened various supports viz. glass, Celite, chrysolite, agarose, concanavalin A Sepharose 4B, eggshell, polyacrylamide, and gelatin for the immobilization. Among them, the highest immobilization yields were obtained with concanavalin A Sepharose 4B (81.7%) and in gelatin water (78.0%) (Assis et al. 2004b).

In another study, they optimized the conditions for the production of low methoxyl pectin using PME from acerola immobilized in gelatin using factorial and response methodology. The optimum conditions of activity in immobilized enzymes were found to be at the NaCl concentration of 0.15 M and a pH of 9.0 (Assis et al. 2004a).

Novel compounds

Few novel compounds have been reported from acerola fruit and different parts of the tree. Leucocyanidin-3-O-b-D-glucoside, a novel flavonoid possessing a 4,200—glycosidic linkage was isolated from green mature acerola puree and named ‘‘aceronidin’’ by Kawaguchi et al. (2007). From the branches and roots of the acerola tree, Liu et al. (2013) isolated three novel norfriedelanes, A–C. Among them, Norfriedelin A (possessing an a-oxo-b-lactone group) and norfriedelin B (with a keto-lactone group) were shown to have significant acetylcholinesterase inhibitory effects. Later, the group identified three new tetranorditerpenes acerolanins from the aerial parts of the plants with a rare 2H-benz[e]inden-2-one substructure possessing cytotoxic activity (Liu et al. 2014).

Biological activities

The in vitro antioxidant activity of the acerola fruit, its various extracts, and purified phytonutrients have been carried out using different assays like DPPH, ORAC, TEAC, etc. by various researchers in the past few years. However, it is difficult to compare the results reported by different laboratories as many of them have not mentioned the variety used in the experimentation, and there are substantial differences in the methodology of sample preparation, extraction of antioxidants, selection of endpoints, and expression of results even for the same method. However, having a complex matrix of a range of antioxidants, the total antioxidant capacity of acerola is thought to be due to the synergistic action of its range of phytonutrients. Mezadri et al. (2008) reported that the contribution of ascorbic acid to the hydrophilic antioxidant activity in acerola fruits, commercial pulps, and juices ranged between 40 and 83%, while the remaining activity was due to polyphenols, mainly the phenolic acids. They reported that the antioxidant activity values obtained from acerola juice were more than those reported for other fruit juices particularly rich in polyphenols such as strawberry, grape, and apple juices. In a different study by Righetto et al. (2005), it was reported that the antioxidant activity of the acerola juices depended on the synergistic action of the constituents of different fractions, with the most significant components being phenolic compounds and vitamin C Delva and Schneider (2013b) evaluated the contribution of phenolic fractions in acerola towards antioxidant capacity and reported the following order: anthocyanins＜phenolic acids ＜ flavonoids.

In an extensive study by Motohashi et al. (2004), acerola fruit was fractionated using column chromatography with various organic solvents, and a range of biofunctional properties were investigated viz. radical generation, superoxide anion scavenging activity, tumor-specific cytotoxic activity, anti-HIV activity, antibacterial activity, antifungal activity, anti-Helicobacter pylori activity, and MDR reversal activity. They reported that a few acetone and hexane fractions showed higher cytotoxic activity against tumor cell lines than against normal cells. Their most important finding was the MDR reversal activity of a few hexane fractions, which inhibited the Pgp function in the MDR cancer cells, more effectively than the positive control, verapamil. Thus, the authors interestingly stated that the tumor-specific cytotoxic activity and MDR reversal activity of Barbados cherry suggest its possible application in cancer chemotherapy and prevention.

Using acerola fruit juice as an active ingredient, a bacteriostatic agent against thermo-resistant and acid-resistant bacteria was patented by Tanada et al. (2007). Apart from these, several other biological activities like hepatoprotective, anticarcinogenic activity, antihyperglycemic effect, anti-genotoxicity activity, etc. have also been studied in acerola, which is summarized in Table 2.

Value addition and techniques for value addition

Acerola, possessing high nutritional attributes, has a short shelf life with a low sensorial appeal (Sousa et al. 2010). Being highly perishable and acidic, the fruit is by and large consumed after being processed, in the form of pulps and juices. The fruit is commercially processed into puree, juice, or juice concentrates and is perfect for the preparation of jams, jellies, fruit juices, and supplements. The fruit can also be used to prepare a range of other products like ice cream, gelatin, juice, soft drinks, nectar, gum, fruit conserved, nutraceuticals, yogurts, and sodas. It is also used in the fortification of infant foods and for the production of nutritional and pharmacological products (Badejo et al. 2008). Of late, many new and diversified products have appeared in the Brazilian market like blends of acerola and cashew, acerola and orange, and blends with guarana, powdered refreshments, and concentrated juices (Matta et al. 2004).

Powder

Several researchers have attempted to prepare ascorbic acid-rich powder from acerola. In 1961, Morse and Habra in a patent claimed to prepare a vitamin C concentrate in the form of powder from acerola with enhanced stability, excellent color, and reduced ascorbic acid oxidase content which can be directly administered in small doses into the human body. The steps involved in the invention included fermentation and solvent precipitation of the insoluble solids. Later, in another invention, they produced a substantially non-hygroscopic powder containing high ascorbic acid content, with an excellent shelf life (a year or more without refrigeration) and pleasant flavor. For the production of the said powder, the inventors prepared a single-strength juice, brought its pH around 7 or 7.5 using the suitable base, and allowed it to precipitate. The juice was then filtered, concentrated, and dried in a powder form (Morse and Habra 1963). Still, later, a method for preparing acerola fruit powder comprising 51–60 mass percent of acerola cherry juice solids and 40–49 mass percent of oxidized starch was described by Chai et al. in a patent published in 2014. Their method comprised preparing a concentrate of acerola cherry juice, adding oxidized starch to the concentrate, and spray-drying it.

Blends

Blending different fruit juices offers advantages over conventional juices in terms of nutritional and sensorial quality by combining different aromas and flavors (Lima et al. 2009; Matsuura et al. 2004). Since, acerola can easily be blended with more flavorful juices (Lima et al. 2009); few studies have focused on the formulation of blended products from acerola and the study of its physicochemical, microbial, and sensorial attributes. Some examples include—the preparation of nectar from the cashew apple, papaya, guava, acerola fruit, and passion fruit with added caffeine (Sousa et al. 2010), nectar from acerola pulp, papaya pulp, and passion fruit juice (Matsuura et al. 2004) and preparation of beverage from whey butter cheese and acerola juice (Cruz et al. 2009).

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