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Molecules 2017, 22(6), 944; doi:10.3390/molecules22060944
Fruits of Black Chokeberry Aronia melanocarpa in the Prevention of Chronic Diseases
Institute for teacher training, Faculty of Central European Studies, Constantine the Philosopher University in Nitra, Drazovska 4, Nitra SK-949 74, Slovakia
Department of Food Analysis and Chemistry, Faculty of Technology, Tomas Bata University in Zlín, nám. T. G. Masaryka 5555, CZ-760 01 Zlín, Czech Republic
Department of Viticulture and Enology, Faculty of Horticulture, Mendel University in Brno, Valticka 337, CZ-691 44 Lednice, Czech Republic
Language Centre, Faculty of Humanities, Tomas Bata University in Zlín, nám. T. G. Masaryka 5555, CZ-760 01 Zlín, Czech Republic
Author to whom correspondence should be addressed.
Academic Editors: Dong-Kug Choi and Palanivel Ganesan
Received: 3 May 2017 / Accepted: 5 June 2017 / Published: 7 June 2017
In recent years, growing attention has been focused on the utilization of natural sources of antioxidants in the prevention of chronic diseases. Black chokeberry (Aronia melanocarpa) represents a lesser known fruit species utilized mainly as juices, purees, jams, jellies and wine, as important food colorants or nutritional supplements. The fruit is valued as a great source of antioxidants, especially polyphenols, such as phenolic acids (neochlorogenic and chlorogenic acids) and flavonoids (anthocyanins, proanthocyanidins, flavanols and flavonols), particularly cyanidin-3-galactoside and cyanidin-3-arabinoside, as well as (−)-epicatechin units. The berries of A. melanocarpa, due to the presence and the high content of these bioactive components, exhibit a wide range of positive effects, such as strong antioxidant activity and potential medicinal and therapeutic benefits (gastroprotective, hepatoprotective, antiproliferative or anti-inflammatory activities). They could be also contributory toward the prevention of chronic diseases including metabolic disorders, diabetes and cardiovascular diseases, because of supportive impacts on lipid profiles, fasting plasma glucose and blood pressure levels.
Keywords:black chokeberry; Aronia melanocarpa; bioactive compounds; chronic diseases; prevention
In recent years, the utilization of natural products has substantially increased following the trends of chronic diseases reduction. The small blueberry-sized black or dark violet color fruits of Aronia melanocarpa shrub are of great interest to researchers also because they have, similarly to other distinguished fruit types [1,2,3,4,5,6], one of the highest levels of antioxidants . Berry crops, especially those underutilized (elderberry, honeyberry and black chokeberry), are widely recognized as valuable source of bioactive compounds used as natural food colorants and for health-promoting activities . Our attention has been focused on chokeberries involved in numerous clinical studies due to their antioxidant properties related to the high phenolic content [9,10,11,12,13], especially anthocyanins [14,15] in the form of cyanidin derivatives . It should be emphasized, as well, that other than polyphenolic compounds, the berries are also rich in bioactive constituents, such as vitamins (vitamin C and vitamin E), mineral elements (potassium, calcium and magnesium), carotenoids, pectins, organic acids and carbohydrates present in smaller amounts . That is a reason why Aronia species are at the top of fruits and berry species and why they display the wide range of activities in relation to chronic diseases, especially heart and cardiovascular [18,19,20] ones, involving antiatherosclerotic, hypotensive and antiplatelet properties . Due to the presence of these bioactive compounds, the berries of Aronia exhibit also other biological, health-promoting effects both in vitro and in vivo, such as gastroprotective (stomach ulcers), hepatoprotective, antiproliferative activities (e.g., colon cancer), prevention and treatment of diabetes [21,22,23,24,25].
Aronia fruits, with the common name chokeberry, belong to the Aronia genus of the Rosaceae family, Maloideae subfamily. The genus is represented by two species utilized as fruits: Aronia melanocarpa (Michx.) Ell. (black chokeberry) and Aronia arbutifolia (L.) Pers. (red chokeberry). Both species are considered as noted ornamental landscape shrubs. Black chokeberry is nowadays a widely utilized crop for the production of natural food colorants  and due to its usage in processed products  and nutraceutical utilization in the form of nutritional supplements .
Black chokeberry originates from the eastern parts of North America. The fruits of A. melanocarpa have been applied already by Native Americans to cure colds. The center of Aronia melanocarpa is located in the northeastern states of the USA and the Great Lakes region, with a range extension into the higher altitude of the Appalachian Mountains. In the United States, there are primary cultivars available for the fruit production: ‘Viking’ and ‘Nero’ cultivars. In comparison to wild-type chokeberry fruits, the commercial cultivars are larger, sweeter and have a bigger production .
The cultivation of this crop for the food industry in Europe started in Russia in the early 1900s in the cold areas of Siberia, and afterwards, the plant was spread all over Russia. In the first half of the 20th century, the Aronia plant was introduced also to other European countries, such as Eastern European states (e.g., Poland with a current area around 1600 ha and a production of 14,000–15,000 t), Germany, Finland, Sweden and Norway . To the significant commercial black chokeberry cultivars besides ‘Viking’ (Finland) and ‘Nero’ (Czech Republic) belong some other cultivar types such as ‘Aron’ (Denmark), Polish ‘Galicjanka’, Swedish ‘Hugin’, Russian ‘Rubina’ or ‘Fertödi’ (Hungary).
Aronia fruits can ripen as early as mid-July, but they primarily ripen during the month of August . For the optimal harvest date, regarding the maximum reached levels of berry weight and anthocyanin content, choosing the early September days could be the most suitable .
The taste of mature black chokeberry fruits is sweet with the level of reduced sugars in chokeberry cultivars from 8% (‘Viking and Nero’) to about 12% (‘Hugin’) . For these berries, it is typical also a certain level of astringency, due to the tannin presence, so they are not so popular for eating as natural fresh fruits. At present, black chokeberries are therefore used mainly as ingredients in the processed form, separately or more often together with other fruits, to make juices , purees , jams, jellies, wine , syrups, teas, alcoholic or energizing drinks and flavorings for products, such as yogurts . Furthermore, by-products such as pomace are a great source of bioactive constituents, comparable to berries . The berries can be also utilized as food colorants [17,38]. For this purpose, solid-phase extraction (SPE) , supercritical fluid extraction (SFE) or ultrasound-assisted extraction (UAE) [40,41,42] are highly recommended.
This review aims to summarize particular phenolic components of the lesser known fruits of black chokeberry (Aronia melanocarpa), their bioavailability, antioxidative properties and health-promoting benefits in relation to chronic diseases. Also shown are the new trends of fruit utilization and its situation among other valuable sources of berry crop and lesser known fruit species.
2. Polyphenols as the Main Bioactive Compounds of Chokeberry Fruit
Nowadays, the A. melanocarpa fruit is valued as a great source of bioactive components, such as polyphenols. They are considered to be very important dietary antioxidants [43,44].
Antioxidants are the substances that can scavenge free radicals, instable and reactive forms with an unpaired electron in the outer orbit. Free radicals could cause cell damage to the human body, “oxidative stress” that leads to various chronic diseases, such as atherosclerosis, inflammation, cancer and neurodegenerative diseases. Some dietary antioxidants are capable of donating hydrogen radicals and, thus, may act as free radical scavengers. Therefore, these compounds may prevent some crucial points in disorders’ progress.
First of all, black chokeberry fruit has a high content of total polyphenol (TP). Total polyphenols in Aronia melanocarpa were determined in the range of 690–2560 mg gallic acid equivalents (GAE) in 100 g fw (fresh weight) [44,45,46,47].
It is also important to emphasize the remarkable position of black chokeberry fruit among other berry crops. The total polyphenols (TP) in A. melanocarpa berries were quantified as higher than for many other remarkable berries, including blueberries, red raspberries, red currant, strawberries and blackberries [44,46,48]. The comparison of TP content in various important fruit berries confirms that the amount of TP in A. melanocarpa berries is similar to black currant (Ribes nigrum) content, about 2–4-fold of the content in blackberry (Rubus fruticosus), 4-fold for blueberry (Vaccinium corymbosum), 3–8-fold for red raspberry (Rubus idaeus) and 10-times more than in strawberry (Fragaria ananassa). Red currants (Ribes rubrum) have about 2/3 of the black chokeberry TP content; lingonberry (Vaccinium vitis-idaea) has about 1/4; and cranberry (Vaccinium macrocarpon) approximately 1/8 of the A. melanocarpa fruit phenolics [43,45,46,47]. Tian et al.  compared and analyzed the TP content of 13 various berry crops by the HPLC method with DAD detection. The results of the experiment showed that the highest concentration of polyphenols was present in bilberry fruit (564 mg/100 g fw); the rest of the berry crops had a content of TP similar to black chokeberry (432 mg/100 g), lingonberry and hawthorn (440 mg/100 g).
To achieve a maximum yield of polyphenols in black chokeberry fruit, some factors must be taken into account. The content of total polyphenols (TP) and particular phenolic compounds of different types of berries depend on many factors, such as genetic attributes (cultivar, genotype, variety) or growing conditions (location, cultivation techniques, ripening stage), processing and storage [43,45,50,51]. The optimum for storage is a temperature of 3 °C, although after six months of storage at 3 °C, the content of total polyphenols decreases only by 30% . High variations and discrepancy in total polyphenolic content during different growing seasons are due to the different air temperatures, sunlight and rainfall intensity, as has been proven by Tolic et al. . Higher temperatures and bright sunshine hours caused the high content of TP correlated with anthocyanins.
To obtain a maximum yield of polyphenols, a fruit cultivar must be taken into account as a very important factor [45,47,53]. The cultivars such as ´Viking´ and ´Nero´ and even wild varieties have higher amounts of TP than cultivar ´Galicianka´ . Cultivar ´Hugist´ represents the best source of polyphenols (23.4 mg of gallic acid equivalents per g of fresh fruit weight) as has been proven by Ochmian et al. . Otherwise, the lowest value of TP was detected in ´Aron´ cultivar (15.86 mg of gallic acid equivalent per fw) . It should be considered that in the case of the determination of total polyphenols, different methods and conditions of plant growing must be taken into account as well. Moreover, the extraction process is important for the optimal results of polyphenol content and composition. Various solvents (type, concentration), particle size, solid–solvent ratio, pH and extraction time could have an impact. Among these variables, time was ascertained as not a statistically important factor for the extraction of polyphenols. As the optimal extraction conditions, maceration of 0.75 mm-sized berries by 50% ethanol, with a solid–solvent ratio of 1:20, was evaluated . Furthermore, the integrated extraction-adsorption process, simultaneous phenolics extraction and their purification in a single operation could be used for the enhancement of the extraction yields of phenolics and enrichment of the Aronia extracts in antioxidant phenolics up to 15 times .
The polyphenols content and polyphenolic profile of Aronia melanocarpa berries and different types of products, such as pomace or processed juice, were determined by several researchers [7,53]. The pomace has been identified as the product with the highest content of phenolics in comparison to juice or fruits. The average concentration of polyphenols in pomace was about five-fold higher compared to chokeberry juice.
The effect of different drying methods, such as freeze-drying, vacuum, convective drying and the microwave method, on the quality factors of chokeberry fruit was studied Samoticha et al. . The results showed that the quality of dried chokeberry depends on the method and conditions of fruit drying. The highest content of bioactive compounds they determined was in freeze-dried samples, compared with fresh fruits. The increase in air temperature during drying deteriorated dried product quality due to the content of phenolics.
A phenolic analysis of dried chokeberry, bilberry and black currant fruit teas, prepared by decoction and infusion, showed that the highest concentration of phenolics is in chokeberry teas, followed by bilberry and black currant teas . Optimization of the extraction process for maximal yield of total phenolics content by sonication was determined by Ramić et al. . Ultrasonic power, temperature (30–70 °C) and extraction time (30–90 min) were investigated. The most suitable conditions were evaluated as a power of about 200 W, temperature of 70 °C and 80 min of extraction.
To the most important polyphenols of black chokeberries belong phenolic acids and flavonoids such as anthocyanins, flavanols, flavonols and proanthocyanidins . As the most significant phenolic compounds were identified from the group of phenolic acids hydroxycinnamic acids, especially neochlorogenic acid, from anthocyanins, there were cyanidin-3-galactoside and cyanidin-3-arabinoside; from proanthocyanidins, procyanidin B1. Flavanols (epicatechin) and flavonols (mainly quercetin glycosides) are minor components of black chokeberry fruits [43,48].
2.1. Phenolic Acids of Chokeberry Fruit
Generally, berries are a rich source of hydroxycinnamic acids, derivatives of slightly water-soluble cinnamic acid. The most abundant is chlorogenic acid, which is a complex of caffeic acid linked to quinic acid through an ester bond. Together with neochlorogenic acid , they are considered to be the major non-flavonoid polyphenolic compounds in chokeberries [3,61]. Rop et al.  confirmed the fact that chlorogenic and neochlorogenic acids are very important antioxidants by the experiments of five black chokeberry cultivars ´Aron´, ´Fertödi´, ´Hugin´, ´Nero´ and ´Viking´. Furthermore, Ochmian et al.  determined chlorogenic and neochlorogenic acids as significant phenolic acids in similar amounts in cultivars ´Hugin´, ´Nero´, ´Viking´ and ´Galicianka´. The content of chlorogenic acid, assessed by Jakobek et al. , was quantified as a little bit higher. Zheng and Wang  drew attention to caffeic acid and its derivative present in wild chokeberry and their importance on the total antioxidant capacity. The significant amount of caffeic acid and also ferulic acid was detected by Hakkinen et al. . The content of total phenolic acids is comparable to Saskatoon berries. The predominant phenolic acids are present as 3-O-caffeoylquinic acid, which makes up about 23% of the total phenolic content, and 5-O-caffeoylquinic acid, with about 11% . During the process of chokeberry juice pasteurization (80 °C), the most unstable among the phenolics were hydroxycinnamic acids with losses up to 59%. On the contrary, plasma-treated chokeberry juice showed an increased concentration of hydroxycinnamic acids by 23% .
2.2. Flavonoids of Chokeberry Fruit
The main flavonoid subgroups of black chokeberry fruits are represented by anthocyanins, proanthocyanins, flavonols and flavanols (catechins) [45,53]. Flavonol glycosides represent about 10% of total phenolics content with the predominance of quercetin 3-O-galactoside (Q-Gal) and quercetin 3-O-glucoside . Similarly to the content of total phenol, also flavonoid and proanthocyanidin contents of black chokeberry extracts are higher than those of other berry extracts such as blueberries, black currant, blackberry, bilberry, red currant, red raspberry and strawberry [44,46,48].
Much of the interest in Aronia melanocarpa fruit is focused on anthocyanins, glycosylated pigmented flavonoid compounds, and their content. Among all detected compounds in black chokeberry fruit, anthocyanins were established as very important compounds , sometimes dominating ones . Due to Oszmiański and Wojdylo , anthocyanins represent about 25% of all phenolic components; according to Jakobek et al. , this is up to 41%. The major anthocyanin of black, purple and red Aronia (Aronia melanocarpa, Aronia prunifolia, and Aronia arbutifolia) was identified as cyanidin-3-galactoside . Ochmian et al. [32,61] determined more than 50% of anthocyanins of the present polyphenols when even one concrete compound (cyanidin-3-O-galactoside) made up 50% of the determined phenolic compounds in four studied cultivars.
Semi-preparative HPLC, thin-layer chromatography and spectral techniques indicated cyanidin as a single aglycone and glucose, galactose, arabinose and xylose as associated sugars. The anthocyanin composition is represented almost exclusively by cyanidin glycosides, namely predominant compounds cyanidin-3-O-galactoside and cyanidin-3-O-arabinoside, further cyanidin-3-O-glucoside and cyanidin-3-O-xyloside [43,48,50,66]. Furthermore, in chokeberry teas (infusion and decoction), the main components are cyanidin-galactoside and cyanidin-arabinoside, while cyanidin-glucoside and cyanidin-xyloside are present in half the amount. The content of cyanidin glycosides in natural chokeberry juices is similar as in chokeberry decoctions . The major cyanidins were cyanidin-3-O-galactoside (222 mg/100 g) and 3-O-arabinoside (Cy-Ara, 159 mg/100 g) . Slimestad et al.  reported total anthocyanins content in chokeberries (481 mg/100 g fw after extraction by 0.1% hydrochloric acid in methanol) with the major anthocyanidins cyanidin 3-O-galactoside (65% of total anthocyanins) and cyanidin 3-O-arabinoside (30%). Compared to anthocyanin aglycons, cyanidin shows higher antioxidant activity with the order of antioxidant potency values: cyanidin > delphinidin > malvidin ≈ peonidin ≈ petunidin .
Numerous studies focused attention on the comparison of anthocyanins content in different types of berry crops. For example, among berry fruits, such as black currant (Ribes nigrum), red currant, (Ribes rubrum), gooseberries (Ribes grossularia), strawberry (Fragaria ananassa), blackberry (Rubus fruticosus) and red raspberry (Rubus idaeus), black chokeberry has the highest total anthocyanin concentration [44,46,66]. According to the studies of Baloghova et al. , there are no significant differences in anthocyanin content between fruits of black chokeberry and blueberry (Vaccinium corymbosum). The content of anthocyanins in chokeberry is also comparable to the elderberry (Sambucus nigra) variety ´Haschberg´; cultivar ’Rubini’ has a higher amount of anthocyanins .
The content of anthocyanins is species dependent; their highest content was confirmed in black chokeberry and the lowest in red chokeberry fruits . The black chokeberry anthocyanin content depends on cultivar, as well; higher total anthocyanin content was determined in cultivars “Viking” and “Nero”, similarly to the higher polyphenol content, compared to the wild type of black chokeberry .
Quite interesting findings of total anthocyanins content are about their amount in the fruit decoctions and infusions. Regarding three types of the fruits containing higher concentrations of anthocyanin colorants (chokeberry, bilberry, black currant), the highest amount was determined by Šavikin et al.  in the bilberry decoction and infusion. In chokeberry and black currant teas, there was a two-fold lower anthocyanin content than in bilberry samples. Compared with the content in dry fruits, 1–3% of total anthocyanins were extracted into teas.
Another important task in relation to berries’ utilization is the stability of anthocyanins.
First of all, the total yield of anthocyanins is significantly influenced by temperature. Wilkes et al.  examined the stability of anthocyanins during juice processing within six months of storage at 25 °C. Anthocyanins were extensively degraded by thermal treatment, and their concentration declined linearly. The lower storage temperature together with the pH value of black chokeberry juice led to the highest yield of anthocyanins in juice, as has been proven in the experiments of Howard et al. .
Secondly, the anthocyanin content in fruit is influenced by the extraction procedure. It has been proven that the most suitable procedure to obtain the highest yield of anthocyanins is the usage of acidified methanol as the extraction solvent . Park and Hong  investigated the content of anthocyanins of Aronia melanocarpa extracts depending on extraction solvents, such as hot water, 50% ethanol and 50% methanol. The total anthocyanin content of the extract yield was higher with 50% methanol solvent than with the usage of 50% ethanol or hot water as the medium. In order to isolate major anthocyanins from Aronia berries, an extraction with methanol containing trifluoroacetic acid could be performed, since direct alcoholic extractions provide very poor yield, not keeping anthocyanins in the stable flavylium cationic form . One of the most efficient extractants of anthocyanins is supposedly Na2SO3. The presence of a preserve sodium sulfate (IV) in Aronia solutions in the filtration process (nanofiltration) increases the efficiency of the process .
Furthermore, the investigation of the temperature effect in combination with other extraction conditions is important and interesting. The influence of temperature (20–70 °C), extraction time (0–240 min), solvent composition (0–50% ethanol in water) and ultrasound power (0–100 W) on anthocyanins yields was studied by Zeković et al.  and D’Alessandro et al. . Results showed that higher temperature and ethanol content in the solvent greatly improved the extraction yields. Ultrasound improved mainly the extraction kinetics. The ultrasound effect was higher in the beginning of the extraction process and at low temperatures.
In the study of Yong et al. , the influence of various storage conditions (different temperatures) in combination with different forms of extract (powder or solution) on extract stability was examined. In the solution, a decrease was detected after four weeks of storage under the same conditions. The storage over 40 °C caused the decrease of cyanidin-3-O-galactoside in both evaluated forms. The optimum temperature for storage, with respect to no changes in anthocyanins, was established at 4 °C.
In another study , the influence of blanching, freezing, maceration temperatures (2–50 °C) and enzyme treatment before juice pressing on anthocyanin content was examined. The results of the experiment showed that the best results were achieved by cold maceration of frozen berries without enzyme addition to the pomace. On the contrary, cold and hot maceration of fresh, not blanched, berries with enzyme gave the lowest yield of anthocyanins.
Kovačević et al.  monitored changes in anthocyanins subjected to the effect of cold atmospheric gas phase plasma. The results were compared with the control sample (untreated) and pasteurized chokeberry juice. The treatment of cold atmospheric gas phase plasma exhibited 23% loss of anthocyanins in comparison to untreated juice.
2.2.2. Flavonols and Flavanols, Proanthocyanins
Flavonols (quercetin glycosides) and flavanols (flavan-3-ols, epicatechin in proanthocyanidins) are also present in the berries, but only as minor components.
In the chokeberry fruit, a mixture of four different flavonols is present, mainly quercetin-3-galactoside (hyperoside), quercetin-3-glucoside (isoquercetin), quercetin-3-rutinoside (rutin) [32,44,74,75] and quercetin-3-robinobioside . Furthermore, quercetin 3-vicianoside was found in A. melanocarpa fruit, though in the lowest concentration . Further, another flavonol identified in Aronia, kaempferol, is present only in a much smaller amount .
In the chokeberry decoctions and infusions, rutin was assessed as the predominant compound, followed by hyperoside (half amount) and isoquercitrin (one third amount) . Generally, quercetin aglycons have been found in a wide range of lesser known fruit berries, such as bog whortleberry and lingonberry, where the contents were the highest, lower in cranberry, sweet rowan, rowanberry, sea buckthorn berry and crowberry . During the process of chokeberry juice pasteurization, the content of flavonols was increased by 5%, as has been reported by the study of Kovačević et al. .
Polymeric procyanidins, the chains of flavan-3-ol subunits, are a significant group of polyphenols in chokeberry. They are composed predominantly of (−)-epicatechin units. The units are connected mainly with C4-C6 and C4-C8 bonds (B-type bonds). Free epicatechin is also present in black chokeberries, although its concentration is significantly lower in comparison with polymeric procyanidins (catechins). The degree of polymerization of procyanidins varies from 2–23 units in the fruits. The degree of polymerization is important for their bioavailability as low molecular weight oligomeric procyanidins are absorbed intact in the gastrointestinal tract, but polymerization greatly impairs intestinal absorption [71,77].
Similar oligomeric proanthocyanidins were identified in wild and cultivated A. melanocarpa fruits; however, the higher flavonoid content was determined in the berries of wild Aronia. In genotypes of Aronia, the presence of about 64 different isomers, such as proanthocyanidin dimers consisting of catechin and/or epicatechin, depending on the structural stereochemistry and configuration, was identified .
Procyanidins in the chokeberries are present in the flesh by about 70%, 25% in the skin and 5% in the kernels . In bark and berries of the Aronia plant, there are important dimeric procyanidins B2 and B5 and trimeric procyanidin C1 .
Three A. melanocarpa cultivars ‘Moskva’, ‘Hugin’ and ‘Nero’ and also hybrid A. prunifolia were analyzed to determine the procyanidin concentration. The highest amount was found in A. prunifolia, slightly less in the ‘Nero’ cultivar and the least in the cultivar ‘Hugin’ and ‘Moskva’, with nearly half the content of procyanidin compared to A. prunifolia . Black, purple and red Aronia (Aronia melanocarpa, Aronia prunifolia and Aronia arbutifolia) and ‘Viking’ (Aronia mitschurinii) berries were quantified for procyanidin content. ‘Viking’ Aronia berries and the red variety had substantially more proanthocyanidins than the other fruits .
As Mayer-Miebach et al.  detected, there are no significant changes regarding procyanidins content during the commercial juice production. Squeezing increases the procyanidins content of the mash by about 30% as compared to the berries, maybe due to an enhanced extractability and subsequent release of monomeric units (predominantly epicatechin) and of oligo- and poly-meric procyanidins. Heating of mash or raw juice did not affect procyanidins; the content remained stable after heating chokeberry purees up to 100 °C within 20 min and holding for 15 min. A similar concentration of total procyanidins was determined for the raw juice, the decanted juice and the sterilized juice. The procyanidins content in the sterilized juice and in the berries was similar, but significantly lower than in the heated mash (about 20%). The procyanidins content in the pomace was significantly higher than in the berries (about 45%) and also higher than in the heated mash (about 10%).
2.2.3. Bioavailability of Black Chokeberry Polyphenols
The bioavailability of chokeberry components is discussed because of the efficiency of particular phenolic components in the organism. The antioxidants should be absorbed, transported, distributed and retained properly in the biological fluids, cells and tissues. Generally, the bioavailability of chokeberry phenolics seems to be quite low .
The metabolism of black chokeberry anthocyanins has been mostly studied in rat models. Despite the predominate position of anthocyanins among polyphenols, their absorption is very poor and low for the small intestine (in the case of cyanidin 3-glucoside 22.4%, cyanidin 3-galactoside 13.6%) and stomach, as well [80,81,82]. After absorption, anthocyanins are transported with the circular system to various organs and tissues, including the liver, heart, prostate, testes, brain and body fat, but they are mostly distributed to the urinary bladder and kidney of rats [83,84]. The low rate of absorption of anthocyanins and another polyphenolic compounds in black chokeberry fruit can be explained by their transformation, modification by methylation or conjugation with glucuronic acid [81,85,86]. For example, cyanidin 3-glucoside is methylated and glucuronidated, cyanidin 3-galactoside oxidized, and finally, all derivates (conjugates) are eliminated by the urinary system [82,86,87]. Another way is an extraction with the bile  or with the feces . On the other hand, anthocyanin conjugation is probably responsible for their metabolic activation and health benefits in relation to chronic diseases [17,87].
Other studies are focused on the metabolism of phenolic acids. Raimondi et al.  found that Bifidobacterium animalis is able to hydrolyze chlorogenic acid into caffeic acid by the presence of the intracellular enzyme feruloyl esterase. Chlorogenic acid is already metabolized in the digestive system thanks to colonic microflora to quinic acid and caffeic acid , which are then absorbed in the small intestine  and transported into the blood circulation . Metabolites of chlorogenic acid (dimethoxycinnamic acid, glucuronide derivatives and sulfated caffeoylquinic acid derivatives) are excreted mainly with the urine [17,92].
3. Antioxidant Activity of Chokeberry Fruit
The determination of antioxidant activity is one of the ways to define the protection ability against free radicals. It is characterized as the capability of the compound (or mixture of compounds) to inhibit the oxidative reaction of various biomolecules . In recent years, A. melanocarpa has been highlighted with the respect to its particularly great quantity of antioxidants. Aronia antioxidants are represented mainly by vitamin C and polyphenols, such as anthocyanins, phenolic acids, flavanols, flavonols and tannins [44,46,53].
The antioxidant effects of chokeberry extract could be evaluated by different in vitro assays, such as radical-scavenging activity by the DPPH test with 2,2-diphenyl-1-picrylhydrazyl, the TEAC method (Trolox-equivalent antioxidant capacity) and the ABTS radical (2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid)) or FRAP (ferric reducing antioxidant power) assay with the reduction of complexes of 2,4,6-tripyridyl-s-triazine (TPTZ) with ferric chloride hexahydrate (FeCl3·6H2O) .
In vitro investigations show an increase in antioxidant defense and a decrease in reactive oxygen species levels after incubation with chokeberry bioactive compounds [45,94,95]. Polyphenol compounds derived from the Aronia berries have been investigated and detected to have a distinct effect on the reduction of the plasma lipid peroxidation induced by ziprasidone in vitro .
In vivo studies of chokeberry bioactive compounds’ effect are limited. Chokeberry anthocyanins could decrease lipid peroxidation, as was shown in the animal model . The mechanisms of the in vivo antioxidant activity of phenolics after absorption spread out far beyond radical scavenging and include suppressing the formation of reactive oxygen species and reactive nitrogen species, inhibition of prooxidants and restoration of antioxidant enzymes, as well as probably cellular signaling to regulate the level of antioxidant compounds and enzymes .
Oszmiański and Wojdylo  determined the antioxidant activity of Aronia melanocarpa berries and their products such as pomace and processed juice. The results showed that the pomace has a much higher antioxidant activity than berries or juice. This fact is in accordance with the highest measured content of phenolics in pomace. Predominant polyphenols consisted of polymeric proanthocyanins together with (−)-epicatechin. The concentration of phenolic acids (chlorogenic and neochlorogenic acids) in juice was higher than in pomace. The comparative study of Rop et al.  confirmed the highest antioxidant activity in the same type of black chokeberry fruit product, pomace, followed by Aronia fresh berry fruits and juices.
The highest antioxidant activity of dried Aronia berries, with flavonoids as the predominant compounds, was reported by Tolić et al. . Dried berries were followed by fruit tea (dried and ground chokeberry pomace), powder samples from pulp, fruit and pomace, further capsules (chokeberry extract) that had about twice lower values of the antioxidant activity and juices with even seven-times less values compared to dried berries. Anthocyanins represented a significant fraction of total phenolics in powder and capsule samples.
The antioxidant activity values, similarly to the polyphenols content, are species dependent. The hybrid of A. prunifolia was found to have the highest antioxidant activity and to be the richest in polyphenols, proanthocyanidins and anthocyanins compared with A. melanocarpa cultivars ´Viking´ and ´Aron´ . In the case of the scavenging effect of A. melanocarpa cultivars ´Aron´, ´Fertodi´, ´Viking´, ´Hugin´ and ´Nero´ on reactive oxygen species, the significant variability of black chokeberry fruit methanolic extracts was evident .
In comparison with other well-known and lesser known fruit species, relatively higher values of antioxidant capacity were reported for chokeberry fruit [44,45,47]. Zheng and Wang  compared the antioxidant activity of wild chokeberry, blueberry (Vaccinium corymbosum), cranberry (Vaccinium macrocarpon) and lingonberry (Vaccinium vitis-idaea) fruit. The chokeberry had significantly higher antioxidant activity related to the higher content of anthocyanins and phenolics than the other three berries. The contribution of individual phenolics to the total antioxidant capacity was generally dependent on their structure and content in the berries. Phenolics such as quercetin and cyanidin, with 3′,4′-dihydroxy substituents in the B ring and conjugation between the A and B rings, had highly effective radical scavenging structures in the berries. Phenolic acids, such as caffeic acid, displayed high antioxidant activity, as well, probably due to their dihydroxylation in the 3,4 positions as hydrogen donors.
The antioxidant activity of A. melanocarpa fruit is mostly contributed by the polyphenolic compounds . Various types of phenolic compounds may contribute differently to the total antioxidant activity. Rugină et al.  found a positive correlation between antioxidant activity and total proanthocyanidin and anthocyanin content in berries of Aronia melanocarpa cultivars ´Viking´, ´Aron´ and hybrid Aronia prunifolia. In the case of cultivars ´Nero´, ´Aron´ and ´Fertodi´ cultivated in the Czech Republic , a higher correlation in the case of neochlorogenic acid than of chlorogenic acid was found. The correlations between antioxidant activity and cyanidin 3-arabinoside and (−)-epicatechin were even higher followed by cyanidin 3-galactoside.
The lipophilic and hydrophilic antioxidant capacities, measured by oxygen radical absorbance capacity in berries of black chokeberry, Ribes nigrum (black currant), Ribes rubrum (red currant), Ribes grossularia (gooseberries) and Sambucus nigra (elderberry), were provided by Wu . However, the lipophilic antioxidant capacity was quite low; the hydrophilic capacities for black currant, chokeberry and elderberry are among the highest of fresh berry fruits. The best linear relationship was observed with total phenolics, followed by total anthocyanins and proanthocyanidins.
4. Chokeberry Fruit and Its Health-Promoting Activity
The berries of A. melanocarpa belong to the group of fruits with one of the highest in vitro antioxidant activities due to the presence and high content of bioactive components, mainly polyphenols (phenolic acids, flavonoids, such as anthocyanins, proanthocyanidins, flavanols and flavonols). The high antioxidant activity of berries makes their effective utilization in the treatment of chronic diseases related to oxidative stress possible, especially diabetes, cardiovascular diseases and cancer. Except for the mentioned properties, numerous other positive medicinal and therapeutic benefits, namely immunomodulatory, antibacterial, hepatoprotective, gastroprotective and anti-inflammatory, have been demonstrated for black chokeberry extracts both in vitro, in cells or cell lines, and in in vivo studies in humans or animals [22,23,24,99,100,101,102,103].
4.1. Anti-Inflammatory Effect of Chokeberry Fruit as a Base in the Prevention of Chronic Diseases
The anti-inflammatory properties of black chokeberry fruit are related to the prevention of the development of chronic diseases, such as diabetes , cardiovascular diseases  and chronic problems with the immune system .
Nowadays, the fruit of black chokeberry is highlighted in relation to strengthening the human immune system. It can be explored by different mechanisms of action, such as inhibition of release of cytokine IL-6, IL-8 and TNF-α in the human monocytes and activation of NF-κB and prostaglandin E2 (PGE2) .
Berries of black chokeberry possess an immunomodulation effect. The complement-modulating activities, the inhibitory activities on nitric oxide production in LPS-induced RAW 264.7 mouse macrophages of procyanidins C1, B5 and B2 and anthocyanins of Aronia melanocarpa were examined by Ho et al. . Results of the experiment showed that procyanidins C1, B5 and B2 and anthocyanins are mainly responsible for the immunomodulation effect. Cyanidin 3-glucoside possessed stronger activity than the other anthocyanidins. Xu and Mojsoska  assessed the immunomodulation properties in lipopolysaccharide (LPS)-stimulated human monocytes mono mac 6. The isolated chokeberries anthocyanin fraction of six different anthocyanidins exhibited strong antioxidative capacity. However the immunomodulatory activity is not associated with Aronia anthocyanins; they had only a slight effect on reducing IL-10. Therefore, there are other Aronia bioactive compounds responsible for that attribute.
Martin et al.  characterized the anti-inflammatory effects of Aronia berries and their polyphenols using primary C57/BL6 mouse splenocytes. The berries of commercial Aronia cultivar 'Viking' and extracts inhibited LPS-stimulated IL-6. Aronia extracts inhibited IL-6 predominately in CD4-lymphocytes. Cyanidin 3-arabinoside and quercetin inhibited LPS-stimulated IL-6; moreover, quercetin also inhibited LPS-stimulated IL-10.
4.2. Gastroprotective and Antidiabetic Effect of Chokeberry Fruit
It is well known that oxidative stress and inflammatory processes play a key role in the development of diabetes and metabolic syndrome, as well [112,113]. Chokeberry fruits are known also for their gastroprotective effects as many flavonoids are noted for their antioxidant and anti-inflammatory properties .
Peptic ulcer is a complex disease that involves infection of the gastric mucosa. The aim of the study of Valcheva-Kuzmanova et al.  was to investigate the effect of A. melanocarpa fruit juice in a male Wister rat model of indomethacin-induced gastric mucosal damage and its possible interference with the gastric oxidative status. Gastric mucosal concentrations of malondialdehyde (MDA), reduced and oxidized glutathione and blood plasma concentrations of MDA were used as biochemical markers of oxidative stress. The results of the experiment showed that fruit juice reduced indomethacin-induced gastric mucosal injury. The gastroprotective effect of the juice was accompanied by a significant decrease in lipid peroxidation.
Beneficial effects of long-term consumption of chokeberry juice and other Aronia products on metabolic parameters including fasting plasma glucose and lipid profiles have also been reported [20,114,115,116]. The berries of black chokeberries effectively improve the glucose metabolism, so they seem to be a good choice in the treatment of diabetes. Chokeberries are a rich source of anthocyanins, which may contribute to the prevention of obesity, which is associated with the reduction of sugars and lipids absorption in the digestive system. Polyphenolic compounds of A. melanocarpa can have beneficial effects in reducing blood glucose levels due to inhibition of α-glucosidase and thus preventing the onset of diabetes by controlling postprandial hyperglycemia through the inhibition of α-glucosidase and α-amylase activities. Anthocyanins such as cyanidin 3-rutinoside could potentially inhibit intestinal α-glucosidase, retard the absorption of sugars [115,117,118] and be useful in the prevention and control of diabetes mellitus, as well . Worsztynowicz et al.  investigated the effect of black chokeberry extracts on the activity of porcine pancreatic α-amylase and lipase, which are key enzymes in the digestive system. An in vitro study demonstrated that methanolic, water and acetic chokeberry extracts caused inhibition of α-amylase and lipase. The methanolic and acetic extracts exhibited higher inhibitory activities. The most effective inhibitor of pancreatic α-amylase was chlorogenic acid. These findings seem to indicate the use of chokeberry contributing to its anti-obesity activities.
Aronia extracts decrease risk factors related to insulin resistance by modulating multiple pathways associated with insulin signaling, adipogenesis and inflammation [116,120]. Aronia melanocarpa anthocyanins can normalize the carbohydrate metabolism in diabetic patients and in streptozotocin-diabetic rats . Clinical evidence showed that polyphenol-rich natural products modulate the carbohydrate metabolism by various mechanisms such as restoring beta-cells’ integrity and physiology and enhancing insulin releasing activity. Chokeberries, rich in polyphenols, may decrease the insulin response and therefore be a natural alternative for diabetes treatment . For an improvement of glucose metabolism, Simoneov et al.  recommended daily consumption of 200 mL Aronia juice for at least three month.
A diet rich in berries is believed to play a distinct role not only in the treatment, but also in the prevention of metabolic diseases. Vlachojannis et al.  studied the minimum recommended anthocyanin doses of chokeberry anthocyanins extract for the treatment of metabolic syndrome disorders. They investigated products containing chokeberry due to their usefulness as a functional food. The minimum anthocyanin dose for the treatment of metabolic syndrome disorders was estimated as 110 mg per day.
4.3. Cardioprotective Effect of Chokeberry Fruit
It is well known that chronic inflammatory disorders can lead to cardiovascular diseases characterized by elevated blood pressure, a high level of serum triglycerides and a low level of HDL cholesterol in plasma. In this way, chokeberry fruit derivatives can also have a beneficial effect on several mentioned risk factors for cardiovascular diseases [123,124,125,126]. The fruits are beneficial due to multiple mechanism of action-influence on lipid metabolism, peroxidation, process of inflammation, coagulation and oxidation, as well.
They effectively influence the lipid metabolism, as has been documented in numerous animal and human studies [123,127,128]. Kim et al.  found that Aronia extract decreased the expression of genes for cholesterol synthesis, uptake and efflux in a dose-dependent manner in humans. These genes included sterol regulatory element-binding protein 2, scavenger receptor class B Type 1 and ATP-binding cassette transporter A1. Aronia extract showed a decreasing of the expression of genes involved in lipid metabolism and lipoprotein assembly, which include fatty acid synthase and acyl-CoA oxidase. There was a significant increase in the levels of LDL receptors and cellular LDL uptake, meaning that cholesterol was taken into the cell, degraded and used in processes like membrane synthesis, steroid production or bile production.
Kardum et al.  examined the anthropometric parameters of twenty-nine women (aged 25–49) in relation to markers of lipid peroxidation, before and after 12 weeks of regular chokeberry juice consumption. They found a positive correlation between the regular consumption and marker of lipid peroxidation, further age, body mass index, waist circumference and body fat percent. In the study of Skoczyñska et al. , the positive effect of chokeberry juice consumption on lipid parameters was shown: the reduction of the total cholesterol level, LDL cholesterol and triglycerides and increased HDL cholesterol in men with mild hypercholesterolemia without pharmacological treatment. Furthermore, Kowalczyk et al.  observed the influence of Aronia anthocyanins extract from berries on selected parameters of oxidative stress in young men with hypercholesterolemia that have taken extracted anthocyanins of 240 mg daily for 30 days. Results showed that Aronia anthocyanins extract administration caused an increase of glutathione peroxidase and catalase activities in red blood cells. Anthocyanins from Aronia melanocarpa can be considered as potent inhibitors of LDL oxidation as a key mechanism of atherosclerosis. It seems that anthocyanins have influenced the blood pressure, endothelin, lipid peroxidation, serum lipids and oxidative status  of patients with metabolic syndrome that were treated with Aronia extract (3 × 100 mg/day) for two months. After the therapy period, there was a significant decrease of systolic blood pressure, LDL cholesterol, total cholesterol, triglycerides and enzyme catalase and a significant increase of enzyme.
Polyphenolic extract of A. melanocarpa berries presented strong anticoagulant properties, prolonged blood clotting times (APTT-activated partial thromboplastin time, PT-prolonged prothrombin time and TT-thrombin time), as well as decreasing the maximal velocity of fibrin polymerization in human plasma. The obtained results clearly indicate the in vitro anticoagulant properties of the berry extracts used .
Firstly, the antithrombotic effect is given by inhibiting platelet aggregation. The experiments of Olas et al.  showed that the extract from black chokeberries reduces in vitro some steps of platelet activation (platelets adhesion to collagen and platelet aggregation) and the production of reactive oxygen species (ROS) in resting blood platelets and platelets activated by a strong physiological agonist, thrombin. Berries of A. melanocarpa have been supposed to prevent thrombosis in pathological states where plasma procoagulant activity and oxidative stress are observed, in hyperhomocysteinemia. In the study of Malinowska et al. , the influence of Aronia extract on the clot formation (with human plasma and purified fibrinogen) and the fibrin lysis during the model of hyperhomocysteinemia was investigated. The in vitro study presented the modifications of human plasma total proteins and the oxidative stress in plasma after Aronia extract application. Ryszawa et al.  studied the effects of polyphenol-rich extracts of black chokeberries on platelet function in vitro and in vivo in subjects with significant cardiovascular risk factors, such as hypertension, hypercholesterolemia, smoking and diabetes mellitus. Results in vivo demonstrated that the extract caused a decrease in superoxide production only in patients with cardiovascular risk factors, whereas it was not observed in the group without risk factors for arteriosclerosis. The extract exerted anti-aggregatory effects on platelets in both studied groups. The antioxidant properties of the black chokeberry extract on oxidative/nitrative stress in human blood platelets were studied in vitro. The extract from A. melanocarpa significantly inhibited platelet protein carbonylation and thiol oxidation. Especially anthocyanidins, phenolic acids and quercetin glycosides have protective effects against peroxynitrite-induced nitrative damage of plasma fibrinogen and, therefore, may contribute to the prevention of peroxynitrite-related cardiovascular diseases . Furthermore, Bijak et al.  estimated the effect of Aronia berries’ extract against nitrative and oxidative damage induced by peroxynitrite. The extract significantly inhibited both the formation of the high molecular weight protein aggregates and nitration of the fibrinogen molecule.
Aronia fruits significantly inhibited the inflammatory processes in vessels,  and protected against atherogenic changes in aorta and coronary arteries, as was documented in the study of Daskalova et al. .
Chokeberry fruit extract has also a positive effect on blood pressure and is recommended as a nutritional supplement in the management of arterial hypertension. First, the mechanism of protection is the inhibition of angiotensin I-converting enzyme (ACE). Sikora et al.  analyzed the effects of two-month supplementation with chokeberry preparation on the activity of angiotensin I-converting enzyme (ACE) in patients with metabolic syndrome. Results showed a decrease in ACE activity after one (to 25%) and two months (to 30%) of the experiment. They documented significant positive correlations between the ACE activity and the systolic and diastolic blood pressure together with CRP. Bell et al. in two studies [133,134] examined the potential coronary vasoactive and vasoprotective properties of anthocyanin-enriched extract prepared from chokeberry. Chokeberry produced dose- and endothelium-dependent vasorelaxation. Vasorelaxation and its endothelium contribution were least for chlorogenic acid, further caffeic and ferulic acids and greatest for coumaric acid. Thus, anthocyanin-enhanced extracts produce endothelium-dependent relaxation in porcine coronary arteries.
Secondly, the polyphenolic fractions of berries (especially anthocyanins) efficiently decrease oxidative stress. The findings of Kim et al.  indicate that A. melanocarpa juice is a potent stimulator of the endothelial formation of NO in coronary arteries that involves the phosphorylation of eNOS via the redox-sensitive activation of the Src/PI3-kinase/Akt pathway mostly by conjugated cyanidins and chlorogenic acids. Ciociou et al.  estimated the influence of polyphenolic compounds in chokeberries on the parameters of oxidative stress in the model of arterial hypertension in a group of rats without adding extract and with the extract. The serous activity of glutathione-peroxidase has significantly lower values in the hypertensive group as compared to the group protected by polyphenols. The results revealed the normalization of the reduced glutathione concentration, as well as a considerable reduction in the malondialdehyde serum concentration in the group protected by polyphenols. Substances responsible for the mentioned activity are chlorogenic acid, kuromanin, rutin, hyperoside and quercetin. In vitro studies also demonstrated that the A. melanocarpa fruit extract inhibits 7β-hydroxycholesterol-induced apoptosis of endothelial cells .
4.4. Anticancer Effect of Chokeberry Fruit
There is epidemiology evidence indicating that a diet with a high consumption of fruits rich in antioxidants reduces the risk of certain cancer types. Therefore, some dietary antioxidants could be a good prevention of cancer incidence. Results of in vitro experiments proved that Aronia fruit has been successfully used as a dietary supplement in some cases of cancer . Moreover, several mechanisms of action have been identified for a chemopreventive effect of polyphenolic extract of black chokeberry fruit (prevention of oxidation, reduction of oxidative stress, induction of detoxication enzymes, induction of cell cycle arrest apoptosis, regulation of the host immune system, anti-inflammatory activity and changes in cellular signaling)  that can multiply their utilization in comparison to other berry crops.
The studies of in vitro experiments proved the efficiency of Aronia melanocarpa on the growth of human breast, leukemia, colon and cervical tumor cell lines.
Stanisavljević et al.  suggested that although a large proportion of chokeberry phenolics undergoes transformation during digestion, they are still potent as antioxidant and antiproliferative agents. The effect of the digested juice on Caco-2 cells proliferation was studied, and the reduction of the proliferative rate by approximately 25% was determined.
Ga̧siorowski et al.  established that anthocyanins extract isolated from fruits of Aronia melanocarpa inhibited the mutagenic activity of benzo(a)pyrene and 2-amino fluorene in the Ames test. They restrain the generation and release of superoxide radicals by human granulocytes, as well. The results suggest that the antimutagenic influence of anthocyanins is exerted mainly by their free radical scavenging action, as well as by the inhibition of enzymes activating promutagens and converting mutagens to the DNA-reacting derivatives.
Black chokeberry extract and other products may reduce the oxidative stress in breast cancer patients before and after surgery and during various phases of oncology treatment . In a model system in vitro , the commercial extract from berries of A. melanocarpa, due to the antioxidant action, significantly reduced the oxidative/nitrative stress in platelets from patients with invasive breast cancer after the surgery, as an increase of biomarkers of oxidative stress, such as a decrease of glutathione in platelets from patients with breast cancer, was observed.
The aim of Sharif et al.’s  study was to determine the anticancer effect of a polyphenol-rich Aronia melanocarpa juice, containing 7.15 g/L of polyphenols, in the acute lymphoblastic leukemia Jurkat cell line. The results of the experiment showed that the juice inhibited cell proliferation, which was associated with cell cycle arrest in the G (2)/M phase, and caused the induction of apoptosis. In a study performed by Sueiro et al. , black chokeberry fruits were extracted with aqueous acetone. The extract, some fractions and subfractions were screened in a murine leukemia cell assay and a human DNA catalytic topoisomerase II assay in order to gauge the cancer chemopreventive potential of each genotype. The results of the experiment showed that the anthocyanins extract of black chokeberry inhibited the generation and release of superoxide radicals by human granulocytes. Some of the subfractions extracted from wild and cultivated chokeberry showed >90% of inhibitory activity to leukemia cells at a concentration of 25 and 50 μg/mL.
Malik et al.  revealed that 24-h exposure of 50 μg monomeric anthocyanin/mL of Aronia extract to human colon cancer cells resulted in 60% growth inhibition. The treated cells showed a blockage at G1/G0 and G2/M phases of the cell cycle. In the study of Zhao et al. , chokeberry anthocyanin-rich extract was also investigated for its potential chemopreventive activity against colon cancer. The growth of colon cancer-derived and non-tumorigenic colonic cells exposed to the extract (10–75 μg of monomeric anthocyanin/mL) was monitored. Colon cancer cell growth was inhibited by 50% after 48 h of exposure to 25 μg/mL extract.
It is also interesting to compare the inhibition activity of different polyphenolic compounds present in black chokeberry fruit.
Rugină et al.  studied polyphenolic fractions of Aronia melanocarpa cultivars Viking and Aron, and of Aronia prunifolia in relationship with their anticancer activity. Anthocyanin and non-anthocyanin compounds were extracted. The results of the experiment showed that cyanidin glycosides significantly inhibited HeLa human cervical tumor cell proliferation and increased the generation of reactive oxygen species after 48 h of the treatment. Anticancer activity of the extract was dependent on the extraction method. The cancer cell growth inhibition activity of the 50% ethanol extract on the HeLa cell line was significantly higher than that of hot water and of 50% methanol extracts . Summary of protective properties of black chokeberry fruit in relation to chronic diseases are summarized in Table 1.
Since a high intake of fruits is inversely related to the incidence of several degenerative and chronic diseases, the importance of a balanced diet in relation to human health has received increased consumer attention worldwide . Berry crops, especially lesser known species, are effective in the prevention of cardiovascular, cancer and metabolic disorders, as well .
Lesser known fruit species such as black chokeberry, Aronia melanocarpa, are coming into the focus of researchers and also the public, particularly due to their great antioxidative activity. They represent a very valuable fruit with a high level of polyphenolic compounds, especially anthocyanins (cyanidin-3-galactoside and cyanidin-3-arabinoside) and procyanidins ((−)-epicatechin units). The content of polyphenols and their exact composition are quite variable and dependent on the particular cultivar, level of fruit ripeness, the growing locality and climatic conditions. Although the bioavailability of polyphenols is poor, their biotransformation can cause the metabolic activation of health benefits.
Taking into account all of the facts, by the selection of optimal cultivars and growing conditions, polyphenols of A. melanocarpa represent a good choice for health-promoting activities including immunomodulatory, antibacterial, hepatoprotective, gastroprotective, cardioprotective, antidiabetic, anti-inflammatory and anticancer benefits.
This study was funded by the internal grant agency of Tomas Bata University in Zlín, Project No. IGA /FT/2017/006.
All authors designed the review. Tunde Jurikova, Jiri Mlcek, Sona Skrovankova and Daniela Sumczynski contributed to the writing of the manuscript. Jiri Sochor, Irena Hlavacova, Lukas Snopek and Jana Orsavova read and approved the final manuscript.
Conflicts of Interest
The authors declare no conflict of interest.
- Skrovankova, S.; Sumczynski, D.; Mlcek, J.; Jurikova, T.; Sochor, J. Bioactive Compounds and Antioxidant Activity in Different Types of Berries. Int. J. Mol. Sci. 2015, 16, 24673–24706. [Google Scholar] [CrossRef] [PubMed]
- Sochor, J.; Jurikova, T.; Pohanka, M.; Skutkova, H.; Baron, M.; Tomaskova, L.; Balla, S.; Klejdus, B.; Pokluda, R.; Mlcek, J.; et al. Evaluation of antioxidant activity, polyphenolic compounds, amino acids and mineral elements of representative genotypes of Lonicera edulis. Molecules 2014, 19, 6504–6523. [Google Scholar] [CrossRef] [PubMed]
- Jurikova, T.; Sochor, J.; Rop, O.; Mlček, J.; Balla, Š.; Szekeres, L.; Žitný, R.; Zitka, O.; Adam, V.; Kizek, R.; et al. Evaluation of polyphenolic profile and nutritional value of non-traditional fruit species in the czech republic-a comparative study. Molecules 2012, 17, 8968–8981. [Google Scholar] [CrossRef] [PubMed]
- Gazdik, Z.; Reznicek, V.; Adam, V.; Zitka, O.; Jurikova, T.; Krska, B.; Matuskovic, J.; Plsek, J.; Saloun, J.; Horna, A.; et al. Use of liquid chromatography with electrochemical detection for the determination of antioxidants in less common fruits. Molecules 2008, 13, 2823–2836. [Google Scholar] [CrossRef] [PubMed]
- Hosseinian, F.S.; Beta, T. Saskatoon and wild blueberries have higher anthocyanin contents than other manitoba berries. J. Agric. Food Chem. 2007, 55, 10832–10838. [Google Scholar] [CrossRef] [PubMed]
- Lavola, A.; Karjalainen, R.; Julkunen-Tiitto, R. Bioactive polyphenols in leaves, stems, and berries of saskatoon (Amelanchier alnifolia nutt.) cultivars. J. Agric. Food Chem. 2012, 60, 1020–1027. [Google Scholar] [CrossRef] [PubMed]
- Kapci, B.; Neradová, E.; Čížková, H.; Voldřich, M.; Rajchl, A.; Capanoglu, E. Investigating the antioxidant potential of chokeberry (Aronia melanocarpa) products. J. Food Nutr. Res. 2013, 52, 219–229. [Google Scholar]
- Vagiri, M.; Jensen, M. Influence of juice processing factors on quality of black chokeberry pomace as a future resource for colour extraction. Food Chem. 2017, 217, 409–417. [Google Scholar] [CrossRef] [PubMed]
- Tolić, M.T.; Krbavčić, I.P.; Vujević, P.; Milinović, B.; Jurčević, I.L.; Vahčić, N. Effects of Weather Conditions on Phenolic Content and Antioxidant Capacity in Juice of Chokeberries (Aronia melanocarpa L.). Pol. J. Food Nutr. Sci. 2017, 67, 67–74. [Google Scholar] [CrossRef]
- Rodriguez-Mateos, A.; Heiss, C.; Borges, G.; Crozier, A. Berry (poly) phenols and cardiovascular health. J. Agric. Food Chem. 2013, 62, 3842–3851. [Google Scholar] [CrossRef] [PubMed]
- Lee, J.E.; Kim, G.S.; Park, S.; Kim, Y.H.; Kim, M.B.; Lee, W.S.; Shin, S.C. Determination of chokeberry (Aronia melanocarpa) polyphenol components using liquid chromatography–tandem mass spectrometry: Overall contribution to antioxidant activity. Food Chem. 2014, 146, 1–5. [Google Scholar] [CrossRef] [PubMed]
- Bolling, B.W.; Taheri, R.; Pei, R.; Kranz, S.; Yu, M.; Durocher, S.N.; Brand, M.H. Harvest date affects Aronia juice polyphenols, sugars, and antioxidant activity, but not anthocyanin stability. Food Chem. 2015, 187, 189–196. [Google Scholar] [CrossRef] [PubMed]
- McGhie, T.K.; Walton, M.C. The bioavailability and absorption of anthocyanins: Towards a better understanding. Mol. Nutr. Food Res. 2007, 51, 702–713. [Google Scholar] [CrossRef] [PubMed]
- Sójka, M.; Kołodziejczyk, K.; Milala, J. Polyphenolic and basic chemical composition of black chokeberry industrial by-products. Ind. Crops Prod. 2013, 51, 77–86. [Google Scholar] [CrossRef]
- Wilkes, K.; Howard, L.R.; Brownmiller, C.; Prior, R.L. Changes in chokeberry (Aronia melanocarpa L.) polyphenols during juice processing and storage. J. Agric. Food Chem. 2013, 62, 4018–4025. [Google Scholar] [CrossRef] [PubMed]
- Jakobek, L.; Šeruga, M.; Krivak, P. The influence of interactions among phenolic compounds on the antiradical activity of chokeberries (Aronia melanocarpa). Int. J. Food Sci. Nutr. 2011, 62, 345–352. [Google Scholar] [CrossRef] [PubMed]
- Borowska, S.; Brzóska, M.M. Chokeberries (Aronia melanocarpa) and Their Products as a Possible Means for the Prevention and Treatment of Noncommunicable Diseases and Unfavorable Health Effects Due to Exposure to Xenobiotics. Compr. Rev. Food Sci. Food Saf. 2016, 15, 982–1017. [Google Scholar] [CrossRef]
- Kulling, S.E.; Rawel, H.M. Chokeberry (Aronia melanocarpa)—A Review on the characteristic components and potential health effects. Planta Med. 2008, 74, 1625–1634. [Google Scholar] [CrossRef] [PubMed]
- Sosnowska, D.; Podsędek, A.; Kucharska, A.Z.; Redzynia, M.; Opęchowska, M.; Koziołkiewicz, M. Comparison of in vitro anti-lipase and antioxidant activities, and composition of commercial chokeberry juices. Eur. Food Res. Technol. 2016, 242, 505–515. [Google Scholar] [CrossRef]
- Broncel, M.; Kozirog, M.; Duchnowicz, P.; Koter-Michalak, M.; Sikora, J.; Chojnowska-Jezierska, J. Aronia melanocarpa extract reduces blood pressure, serum endothelin, lipid, and oxidative stress marker levels in patients with metabolic syndrome. Med. Sci. Monit. 2010, 16, 28–34. [Google Scholar]
- Jurgoński, A.; Juśkiewicz, J.; Zduńczyk, Z. Ingestion of Black Chokeberry Fruit Extract Leads to Intestinal and Systemic Changes in a Rat Model of Prediabetes and Hyperlipidemia. Plant. Foods Hum. Nutr. 2008, 63, 176–182. [Google Scholar] [CrossRef] [PubMed]
- Valcheva-Kuzmanova, S.; Marazova, K.; Krasnaliev, I.; Galunska, B.; Borisova, P.; Belcheva, A. Effect of Aronia melanocarpa fruit juice on indomethacin-induced gastric mucosal damage and oxidative stress in rats. Exp. Toxicol. Pathol. 2005, 56, 385–392. [Google Scholar] [CrossRef] [PubMed]
- Ciocoiu, M.; Badescu, M.; Badulescu, O.; Tutunaru, D.; Badescu, L. Polyphenolic extract association with renin inhibitors in experimental arterial hypertension. J. Biomed. Sci. Eng. 2013, 6, 493–497. [Google Scholar] [CrossRef]
- Valcheva-Kuzmanova, S.; Belcheva, A. Current knowledge of Aronia melanocarpa as a medicinal plant. Folia Med. 2005, 48, 11–17. [Google Scholar]
- Kowalczyk, E.; Charyk, K.; Fijalkowski, P.; Niedworok, J.; Blaszczyk, J.; Kowalski, J. Protective influence of natural anthocyanins of Aronia melanocarpa on selected parameters of antioxidative status in experimental intoxication with sulphide-2-chloroethyl-3-chloropropyl. Pol. J. Environ. Stud. 2004, 13, 339–341. [Google Scholar]
- Howard, L.R.; Brownmiller, C.; Prior, R.L.; Mauromoustakos, A. Improved Stability of Chokeberry Juice Anthocyanins by β-Cyclodextrin Addition and Refrigeration. J. Agric. Food Chem. 2013, 61, 693–699. [Google Scholar] [CrossRef] [PubMed]
- Horszwald, A.; Julien, H.; Andlauer, W. Characterisation of Aronia powders obtained by different drying processes. Food Chem. 2013, 141, 2858–2863. [Google Scholar]
- Sikora, J.; Broncel, M.; Markowicz, M.; Chałubiński, M.; Wojdan, K.; Mikiciuk-Olasik, E. Short-term supplementation with Aronia melanocarpa extract improves platelet aggregation, clotting, and fibrinolysis in patients with metabolic syndrome. Eur. J. Nutr. 2012, 51, 549–556. [Google Scholar] [CrossRef] [PubMed]
- Andrzejewska, J.; Sadowska, K.; Klóska, L.; Rogowski, L. The effect of plant age and harvest time on the content of chosen components and antioxidative potential of black chokeberry fruit. Acta Sci. Pol. Hortorum Cultus 2015, 14, 105–114. [Google Scholar]
- Janick, J.; Paull, R.E. Encyclopedia of Fruit and Nuts, 1st ed.; CABI: Wallingford, UK, 2008; pp. 622–624. [Google Scholar]
- Brand, M. Aronia: Native shrubs with untapped potential. Arnoldia 2010, 67, 14–25. [Google Scholar]
- Ochmian, I.; Grajkowski, J.; Smolik, M. Comparison of Some Morphological Features, Quality and Chemical Content of Four Cultivars of Chokeberry Fruits (Aronia melanocarpa). Not. Bot. Horti Agrobot. Cluj-Napoca 2012, 40, 253–260. [Google Scholar] [CrossRef]
- González-Molina, E.; Moreno, D.A.; García-Viguera, C. Aronia-enriched lemon juice: A new highly antioxidant beverage. J. Agric. Food Chem. 2008, 56, 11327–11333. [Google Scholar] [CrossRef] [PubMed]
- Georgiev, D.; Ludneva, D. Possibilities for production of nectars and purees from fruits of black chokeberry (Aronia melanocarpa). Acta Horticult. 2009, 825, 595–597. [Google Scholar] [CrossRef]
- Pogorzelski, E.; Wilkowska, A.; Kobus, M. Inhibiting effect of tannin in chokeberry must on the winemaking process. Pol. J. Food Nutr. Sci. 2006, 15, 49–53. [Google Scholar]
- Balcerek, M. Carbonyl compounds in Aronia spirits. Pol. J. Food Nutr. Sci. 2010, 60, 243–249. [Google Scholar]
- Mayer-Miebach, E.; Adamiuk, M.; Behsnilian, D. Stability of chokeberry bioactive polyphenols during juice processing and stabilization of a polyphenol-rich material from the by-product. Agriculture 2012, 2, 244–258. [Google Scholar] [CrossRef]
- Kmiecik, W.; Lisiewska, Z.; Jaworska, G. Effect of Aronia berry honey syrup used for sweetening jams on their quality. Mol. Nutr. Food Res. 2001, 45, 273–279. [Google Scholar] [CrossRef]
- Kraemer-Schafhalter, A.; Fuchs, H.; Pfannhauser, W. Solid-phase extraction (SPE)—A comparison of 16 materials for the purification of anthocyanins from Aronia melanocarpa var Nero. J. Sci. Food Agric. 1998, 78, 435–440. [Google Scholar] [CrossRef]
- Zeković, Z.; Pavlić, B.; Ramić, M.; Vladić, J.; Cvejin, A.; Vidović, S. Optimization of ultrasound-assisted extraction of anthocyanins from Aronia melanocarpa by-product from filter-tea factory. Ann. Fac. Eng. Hunedoara-Int. J. Eng. 2014, 12, 185–188. [Google Scholar]
- D’Alessandro, L.G.; Dimitrov, K.; Vauchel, P.; Nikov, I. Kinetics of ultrasound assisted extraction of anthocyanins from Aronia melanocarpa (black chokeberry) wastes. Chem. Eng. Res. Des. 2014, 92, 1818–1826. [Google Scholar] [CrossRef]
- D’Alessandro, L.G.; Kriaa, K.; Nikov, I.; Dimitrov, K. Ultrasound assisted extraction of polyphenols from black chokeberry. Sep. Purif. Technol. 2012, 93, 42–47. [Google Scholar] [CrossRef]
- Jakobek, L.; Drenjančević, M.; Jukić, V.; Šeruga, M. Phenolic acids, flavonols, anthocyanins and antiradical activity of “Nero”,“Viking”,“Galicianka” and wild chokeberries. Sci. Horticult. 2012, 147, 56–63. [Google Scholar] [CrossRef]
- Jakobek, L.; Šeruga, M.; Medvidović-Kosanović, M.; Novak, I. Antioxidant activity and polyphenols of Aronia in comparison to other berry species. Agric. Consp. Sci. 2007, 72, 301–306. [Google Scholar]
- Rop, O.; Mlcek, J.; Jurikova, T.; Valsikova, M.; Sochor, J.; Reznicek, V.; Kramarova, D. Phenolic content, antioxidant capacity, radical oxygen species scavenging and lipid peroxidation inhibiting activities of extracts of five black chokeberry (Aronia melanocarpa (michx.) elliot) cultivars. J. Med. Plants Res. 2010, 22, 2432–2437. [Google Scholar]
- Benvenuti, S.; Pellati, F.; Melegari, M.; Bertelli, D. Polyphenols, anthocyanins, ascorbic acid, and radical scavenging activity of Rubus, Ribes, and Aronia. J. Food Sci. 2004, 69, 164–169. [Google Scholar] [CrossRef]
- Zheng, W.; Wang, S.Y. Oxygen radical absorbing capacity of phenolics in blueberries, cranberries, chokeberries, and lingonberries. J. Agric. Food Chem. 2003, 51, 502–509. [Google Scholar] [CrossRef] [PubMed]
- Hwang, S.J.; Yoon, W.B.; Lee, O.-H.; Cha, S.J.; Dai Kim, J. Radical-scavenging-linked antioxidant activities of extracts from black chokeberry and blueberry cultivated in Korea. Food Chem. 2014, 146, 71–77. [Google Scholar] [CrossRef] [PubMed]
- Tian, Y.; Liimatainen, J.; Alanne, A.L.; Lindstedt, A.; Liu, P.; Sinkkonen, J.; Kallio, H.; Yang, B. Phenolic compounds extracted by acidic aqueous ethanol from berries and leaves of different berry plants. Food Chem. 2017, 220, 266–281. [Google Scholar]
- Wangensteen, H.; Bräunlich, M.; Nikolic, V.; Malterud, K.E.; Slimestad, R.; Barsett, H. Anthocyanins, proanthocyanidins and total phenolics in four cultivars of Aronia: Antioxidant and enzyme inhibitory effects. J. Funct. Foods 2014, 7, 746–752. [Google Scholar] [CrossRef]
- Jeppsson, N.; Johansson, R. Changes in fruit quality in black chokeberry (Aronia melanocarpa) during maturation. J. Hortic. Sci. Biotechnol. 2000, 75, 34–67. [Google Scholar] [CrossRef]
- Misiak, M.; Irzyniec, Z. Effect of the temperature and storage time on polyphenol content and antioxidant properties of freeze-dried chokeberries. Zesz. Nauk. Pol. Łódź Chem. Spoż Biotechnol. 2009, 73, 73–81. [Google Scholar]
- Oszmiański, J.; Wojdylo, A. Aronia melanocarpa phenolics and their antioxidant activity. Eur. Food Res. Technol. 2005, 221, 809–813. [Google Scholar] [CrossRef]
- Sainova, I.V.; Pavlova, V.G.; Alexieva, B.S.; Valkova, I.P.; Ilieva, I.N.; Nikolova, E.B. Attenuation of cellular oxidative stress by natural products and plant extracts after chemotherapeutic exposure. J. Biosci. Biotechnol. 2015, 1–7. [Google Scholar]
- Ćujić, N.; Šavikin, K.; Janković, T.; Pljevljakušić, D.; Zdunić, G.; Ibrić, S. Optimization of polyphenols extraction from dried chokeberry using maceration as traditional technique. Food Chem. 2016, 194, 135–142. [Google Scholar] [CrossRef] [PubMed]
- D’Alessandro, L.G.; Vauchel, P.; Przybylski, R.; Chataigné, G.; Nikov, I.; Dimitrov, K. Integrated process extraction–adsorption for selective recovery of antioxidant phenolics from Aronia melanocarpa berries. Sep. Purif. Technol. 2013, 120, 92–101. [Google Scholar] [CrossRef]
- Samoticha, J.; Wojdyło, A.; Lech, K. The influence of different the drying methods on chemical composition and antioxidant activity in chokeberries. LWT-Food Sci. Technol. 2016, 66, 484–489. [Google Scholar] [CrossRef]
- Šavikin, K.; Zdunić, G.; Janković, T.; Gođevac, D.; Stanojković, T.; Pljevljakušić, D. Berry fruit teas: Phenolic composition and cytotoxic activity. Food Res. Int. 2014, 62, 677–683. [Google Scholar] [CrossRef]
- Ramić, M.; Vidović, S.; Zeković, Z.; Vladić, J.; Cvejin, A.; Pavlić, B. Modeling and optimization of ultrasound-assisted extraction of polyphenolic compounds from Aronia melanocarpa by-products from filter-tea factory. Ultrason. Sonochem. 2015, 23, 360–368. [Google Scholar] [CrossRef] [PubMed]
- Hirth, M.; Preiß, R.; Mayer-Miebach, E.; Schuchmann, H.P. Influence of HTST extrusion cooking process parameters on the stability of anthocyanins, procyanidins and hydroxycinnamic acids as the main bioactive chokeberry polyphenols. LWT-Food Sci. Technol. 2015, 62, 511–516. [Google Scholar] [CrossRef]
- Ochmian, I.; Oszmiański, J.; Skupień, K. Chemical composition, phenolics, and firmness of small black fruits. J. Appl. Bot. Food Qual. 2009, 83, 64–69. [Google Scholar]
- Hakkinen, S.; Heinonen, M.; Karenlampi, S.; Mykkanen, H.; Ruuskanen, J.; Torronen, R. Screening of selected flavonoids and phenolic acids in 19 berries. Food Res. Int. 1999, 32, 345–353. [Google Scholar] [CrossRef]
- Kovačević, D.B.; Kljusurić, J.G.; Putnik, P.; Vukušić, T.; Herceg, Z.; Dragović-Uzelac, V. Stability of polyphenols in chokeberry juice treated with gas phase plasma. Food Chem. 2016, 212, 323–331. [Google Scholar] [CrossRef] [PubMed]
- Cretu, G.C.; Morlock, G.E. Analysis of anthocyanins in powdered berry extracts by planar chromatography linked with bioassay and mass spectrometry. Food Chem. 2014, 146, 104–112. [Google Scholar] [CrossRef] [PubMed]
- Taheri, R.; Connolly, B.A.; Brand, M.H.; Bolling, B.W. Underutilized chokeberry (Aronia melanocarpa, Aronia arbutifolia, Aronia prunifolia) accessions are rich sources of anthocyanins, flavonoids, hydroxycinnamic acids, and proanthocyanidins. J. Agric. Food Chem. 2013, 61, 8581–8588. [Google Scholar] [CrossRef] [PubMed]
- Wu, X.; Gu, L.; Prior, R.L.; McKay, S. Characterization of anthocyanins and proanthocyanidins in some cultivars of Ribes, Aronia, and Sambucus and their antioxidant capacity. J. Agric. Food Chem. 2004, 52, 7846–7856. [Google Scholar] [CrossRef] [PubMed]
- Slimestad, R.; Torskangerpoll, K.; Nateland, H.S.; Johannessen, T.; Giske, N.H. Flavonoids from black chokeberries, Aronia melanocarpa. J. Food Comp. Anal. 2005, 18, 61–68. [Google Scholar] [CrossRef]
- Baloghova, M.; Paulovicsova, B.; Turianica, I. Biological characteristics of selected berries. Acta Hort. Regio 2009, 12, 49–52. [Google Scholar]
- Veberic, R.; Jakopic, J.; Stampar, F.; Schmitzer, V. European elderberry (Sambucus nigra L.) rich in sugars, organic acids, anthocyanins and selected polyphenols. Food Chem. 2009, 114, 511–515. [Google Scholar] [CrossRef]
- Park, H.-M.; Hong, J.-H. Physiological activities of Aronia melanocarpa extracts on extraction solvents. Korean J. Food Preserv. 2014, 21, 718–726. [Google Scholar] [CrossRef]
- Bräunlich, M.; Slimestad, R.; Wangensteen, H.; Brede, C.; Malterud, K.E.; Barsett, H. Extracts, Anthocyanins and Procyanidins from Aronia melanocarpa as Radical Scavengers and Enzyme Inhibitors. Nutrients 2013, 5, 663–678. [Google Scholar] [CrossRef] [PubMed]
- Gilewicz-Lukasik, B.; Koter, S.; Kurzawa, J. Concentration of anthocyanins by the membrane filtration. Sep. Purif. Technol. 2007, 57, 418–424. [Google Scholar] [CrossRef]
- Yong, L.H. Effect of Storage Conditions on the Stability of the Extracts from Aronia melanocarpa Elliot. Res. J. Biotechnol. 2016, 11, 38–45. [Google Scholar]
- Bermúdez-Soto, M.J.; Tomás-Barberán, F.A.; García-Conesa, M.T. Stability of polyphenols in chokeberry (Aronia melanocarpa) subjected to in vitro gastric and pancreatic digestion. Food Chem. 2007, 102, 865–874. [Google Scholar] [CrossRef]
- Määttä-Riihinen, K.R.; Kamal-Eldin, A.; Mattila, P.H.; González-Paramás, A.M.; Törrönen, A.R. Distribution and contents of phenolic compounds in eighteen Scandinavian berry species. J. Agric. Food Chem. 2004, 52, 4477–4486. [Google Scholar] [CrossRef] [PubMed]
- Häkkinen, S.H.; Kärenlampi, S.O.; Heinonen, I.M.; Mykkänen, H.M.; Törrönen, A.R. Content of the flavonols quercetin, myricetin, and kaempferol in 25 edible berries. J. Agric. Food Chem. 1999, 47, 2274–2279. [Google Scholar] [CrossRef] [PubMed]
- Niedworok, J.; Brzozowski, F. Badania nad biologicznymi i fitoterapeutycznymi właściwościami antocyjanin aronii czarnoowocowej E. Post. Fitot. 2001, 5, 20–24. [Google Scholar]
- Sueiro, L.; Yousef, G.G.; Seigler, D.; De Mejia, E.G.; Grace, M.H.; Lila, M.A. Chemopreventive Potential of Flavonoid Extracts from Plantation-Bred and Wild Aronia melanocarpa (Black Chokeberry) Fruits. J. Food Sci. 2006, 71, 480–488. [Google Scholar] [CrossRef]
- Denev, P.N.; Kratchanov, C.G.; Ciz, M.; Lojek, A.; Kratchanova, M.G. Bioavailability and antioxidant activity of black chokeberry (Aronia melanocarpa) polyphenols: In vitro and In vivo evidences and possible mechanisms of action: A review. Compr. Rev. Food Sci. Food Saf. 2012, 11, 471–489. [Google Scholar] [CrossRef]
- Talavera, S.; Felgines, C.; Texier, O.; Besson, C.; Lamaison, J.L.; R´em´esy, C. Anthocyanins are efficiently absorbed from the stomach in anesthetized rats. J. Nutr. 2003, 133, 4178–4182. [Google Scholar] [PubMed]
- Talavera, S.; Felgines, C.; Texier, O.; Besson, C.; Manach, C.; Lamaison, J.L.; Rem´esy, C. Anthocyanins and efficiently absorbed from the small intestine in rats. J. Nutr. 2004, 134, 2275–2279. [Google Scholar] [PubMed]
- Kay, C.D.; Mazza, G.; Holub, B.J. Anthocyanins exist in the circulation primarily as metabolites in adult men. J. Nutr. 2005, 135, 2582–2588. [Google Scholar] [PubMed]
- Felgines, C.; Texier, O.; Garcin, P.; Besson, C.; Lamaison, J.L.; Scalbert, A. Tissue distribution of anthocyanins in rats fed a blackberry anthocyanin-enriched diet. Mol. Nutr. Food Res. 2009, 53, 1098–1103. [Google Scholar] [CrossRef] [PubMed]
- Kirakosyan, A.; Seymour, E.M.; Wolforth, J.; McNish, R.; Kaufman, P.B.; Bolling, S.F. Tissue bioavailability of anthocyanins from whole tart cherry in healthy rats. Food Chem. 2015, 171, 26–31. [Google Scholar] [CrossRef] [PubMed]
- Lala, N.; Malik, M.; Zhao, C.; He, J.; Kwon, Y.; Giusti, M.M.; Magnuson, B.A. Anthocyanin-rich extracts inhibit multiple biomarkers of colon cancer in rats. Nutr. Cancer 2006, 54, 84–93. [Google Scholar] [CrossRef] [PubMed]
- Wiczkowski, W.; Romaszko, E.; Piskula, M.K. Bioavailability of cyanidin glycosides from natural chokeberry (Aronia. melanocarpa) juice and dietary-relevant dose of anthocyanins in humans. J. Agric. Food Chem. 2010, 58, 12130–12136. [Google Scholar] [CrossRef] [PubMed]
- Kay, C.D.; Mazza, G.; Holub, B.J.; Wang, J. Anthocyanin metabolites in human urine and serum. Br. J. Nutr. 2004, 91, 933–942. [Google Scholar] [CrossRef] [PubMed]
- Raimondi, S.; Anighoro, A.; Quartieri, A.; Amaretti, A.; Tomas-Barber´an, F.A.; Rastelli, G.; Rossi, M. Role of bifidobacteria in the hydrolysis of chlorogenic acid. Microbiologyopen 2015, 4, 41–52. [Google Scholar] [CrossRef] [PubMed]
- Tomas-Barber´an, F.; Garcia-Villabla, R.; Quartieri, A.; Raimondi, S.; Amaretti, A.; Leonardi, A.; Rossi, M. In vitro transformation of chlorogenic acid by human gut microbiota. Mol. Nutr. Food Res. 2014, 58, 1122–1131. [Google Scholar] [CrossRef] [PubMed]
- Couteau, D.; McCartney, A.L.; Gibson, G.R.; Williamson, G.; Faulds, C.B. Isolation and characterization of human colonic bacteria able to hydrolyse chlorogenic acid. J. Appl. Microbiol. 2001, 90, 873–881. [Google Scholar] [CrossRef] [PubMed]
- Stalmach, A.; Williamson, G.; Crozier, A. Impact of dose on the bioavailability of coffee chlorogenic acids in humans. Food Funct. 2014, 5, 1727–1737. [Google Scholar] [CrossRef] [PubMed]
- Zhong, S.; Liu, J.; Ren, X.; Zhang, J.; Zhou, S.; Xu, X.P. Pharmacokinetics and excretion of chlorogenic acid in beagle dogs. J. Pharm. Sci. 2008, 63, 520–524.
- Sochor, J.; Ryvolova, M.; Krystofova, O.; Salas, P.; Hubalek, J.; Adam, V.; Trnkova, L.; Havel, L.; Beklova, M.; Zehnalek, J.; et al. Fully automated spectrometric protocols for determination of antioxidant activity: Advantages and disadvantages. Molecules 2010, 15, 8618–8640. [Google Scholar] [CrossRef] [PubMed]
- Kedzierska, M.; Olas, B.; Wachowicz, B.; Glowacki, R.; Bald, E.; Czernek, U.; Szydlowska-Pazera, K.; Potemski, P.; Piekarski, J.; Jeziorski, A.; et al. Effects of the commercial extract of Aronia on oxidative stress in blood platelets isolated from breast cancer patients after the surgery and various phases of the chemotherapy. Fitoterapia 2012, 83, 310–317. [Google Scholar] [CrossRef] [PubMed]
- Malinowska, J.; Babicz, K.; Olas, B.; Stochmal, A.; Oleszek, W. Aronia melanocarpa extract suppresses the biotoxicity of homocysteine and its metabolite on the hemostatic activity of fibrinogen and plasma. Nutrition 2012, 28, 793–798. [Google Scholar] [CrossRef] [PubMed]
- Dietrich-Muszalska, A.; Kopka, J.; Kontek, B. Polyphenols from berries of Aronia melanocarpa reduce the plasma lipid peroxidation induced by ziprasidone. Schizoph. Res. Treat. 2014, 2014, 13–18. [Google Scholar]
- Tolić, M.-T.; Jurčević, I.L.; Krbavčić, I.P.; Marković, K.; Vahčić, N. Phenolic content, antioxidant capacity and quality of chokeberry (Aronia melanocarpa) products. Food Technol. Biotechnol. 2015, 53, 171–179. [Google Scholar] [CrossRef] [PubMed]
- Rugină, D.; Sconţa, Z.; Leopold, L.; Pintea, A.; Bunea, A.; Socaciu, C. Antioxidant activities of chokeberry extracts and the cytotoxic action of their anthocyanin fraction on hela human cervical tumor cells. J. Med. Food 2012, 15, 700–706. [Google Scholar] [CrossRef] [PubMed]
- Kokotkiewicz, A.; Jaremicz, Z.; Luczkiewicz, M. Aronia plants: A review of traditional use, biological activities, and perspectives for modern medicine. J. Med. Food 2010, 13, 255–269. [Google Scholar] [CrossRef] [PubMed]
- Jing, P.; Bomser, J.A.; Schwartz, S.J.; He, J.; Magnuson, B.A.; Giusti, M.M. Structure-function relationships of anthocyanins from various anthocyanin-rich extracts on the inhibition of colon cancer cell growth. J. Agric. Food Chem. 2008, 56, 9391–9398. [Google Scholar] [CrossRef] [PubMed]
- Ho, G.T.; Bräunlich, M.; Austarheim, I.; Wangensteen, H.; Malterud, K.E.; Slimestad, R.; Barsett, H. Immunomodulating activity of Aronia melanocarpa polyphenols. Int. J. Mol. Sci. 2014, 15, 11626–11636. [Google Scholar] [CrossRef] [PubMed]
- Xu, J.; Mojsoska, B. The immunomodulation effect of Aronia extract lacks association with its antioxidant anthocyanins. J. Med. Food 2013, 16, 334–342. [Google Scholar] [CrossRef] [PubMed]
- Zapolska-Downar, D.; Nowicka, G.; Sygitowicz, G.; Jarosz, M. Anthocyanin-rich aronox extract from Aronia melanocarpa protects against 7beta-hydroxycholesterol-induced apoptosis of endothelial cells. Ann. Nutr. Metab. 2008, 53, 283–294. [Google Scholar] [CrossRef] [PubMed]
- Appel, K.; Meiser, P.; Millán, E.; Collado, J.A.; Rose, T.; Gras, C.C.; Muñoz, E. Chokeberry (Aronia melanocarpa (Michx.) Elliot) concentrate inhibits NF-κB and synergizes with selenium to inhibit the release of pro-inflammatory mediators in macrophages. Fitoterapia 2015, 105, 73–82. [Google Scholar] [CrossRef] [PubMed]
- Martin, D.A.; Taheri, R.; Brand, M.H.; Draghi, A.; Sylvester, F.A.; Bolling, B.W. Anti-inflammatory activity of Aronia berry extracts in murine splenocytes. J. Funct. Foods 2014, 8, 68–75. [Google Scholar] [CrossRef]
- Savoia, D. Plant-derived antimicrobial compounds: Alternatives to antibiotics. Future Microbiol. 2012, 7, 979–990. [Google Scholar] [CrossRef] [PubMed]
- Joseph, S.V.; Edirisinghe, I.; Burton-Freeman, B.M. Berries: Anti-inflammatory effects in humans. J. Agric. Food Chem 2014, 62, 3886–3903. [Google Scholar] [CrossRef] [PubMed]
- Cisowska, A.; Wojnicz, D.; Hendrich, A.B. Anthocyanins as antimicrobial agents of natural plant origin. Nat. Prod. Commun. 2011, 6, 149–156. [Google Scholar] [PubMed]
- Liepiņa, I.; Nikolajeva, V.; Jākobsone, I. Antimicrobial activity of extracts from fruits of Aronia melanocarpa and Sorbus aucuparia. Environ. Exp. Biol. 2013, 11, 195–199. [Google Scholar]
- Bräunlich, M.; Økstad, O.; Slimestad, R.; Wangensteen, H.; Malterud, K.; Barsett, H. Effects of Aronia melanocarpa constituents on biofilm formation of Escherichia coli and Bacillus cereus. Molecules 2013, 18, 14989–14999. [Google Scholar] [CrossRef] [PubMed]
- Handeland, M.; Grude, N.; Torp, T.; Slimestad, R. Black chokeberry juice (Aronia melanocarpa) reduces incidences of urinary tract infection among nursing home residents in the long term-a pilot study. Nutr. Res. 2014, 34, 518–525. [Google Scholar] [CrossRef] [PubMed]
- Park, S.; Kim, J.I.; Lee, I.; Lee, S.; Hwang, M.-W.; Bae, J.-Y.; Heo, J.; Kim, D.; Han, S.-Z.; Park, M.-S.; et al. Aronia melanocarpa and its components demonstrate antiviral activity against influenza viruses. Biochem. Biophys. Res. Commun. 2013, 440, 14–19. [Google Scholar] [CrossRef] [PubMed]
- Zhu, W.; Jia, Q.; Wang, Y.; Zhang, Y.; Xia, M. The anthocyanin cyanidin-3-O-β-glucoside, a flavonoid, increases hepatic glutathione synthesis and protects hepatocytes against reactive oxygen species during hyperglycemia: Involvement of cAMP-PKA-dependent signalling pathway. Free Radic. Biol. Med. 2012, 52, 314–327. [Google Scholar]
- De Lira Mota, K.S.; Nunes Dias, G.E.; Ferreira Pinto, M.E.; Luiz-Ferreira, A.; Monteiro Souza-Brito, A.R.; Hiruma-Lima, C.A.; Barbosa-Filho, J.M.; Batista, L.M. Flavonoids with Gastroprotective Activity. Molecules 2009, 14, 979–1012. [Google Scholar] [CrossRef] [PubMed]
- Worsztynowicz, P.; Napierała, M.; Białas, W.; Grajek, W.; Olkowicz, M. Pancreatic α-amylase and lipase inhibitory activity of polyphenolic compounds present in the extract of black chokeberry (Aronia melanocarpa l.). Process Biochem. 2014, 49, 1457–1463. [Google Scholar] [CrossRef]
- Qin, B.; Anderson, R.A. An extract of chokeberry attenuates weight gain and modulates insulin, adipogenic and inflammatory signalling pathways in epididymal adipose tissue of rats fed a fructose-rich diet. Br. J. Nutr. 2012, 108, 581–587. [Google Scholar] [CrossRef] [PubMed]
- Simeonov, S.B.; Botushanov, N.P.; Karahanian, E.B.; Pavlova, M.B.; Husianitis, H.K.; Troev, D.M. Effects of Aronia melanocarpa juice as part of the dietary regimen in patients with diabetes mellitus. Folia Med. 2002, 44, 20–23. [Google Scholar]
- Adisakwattana, S.; Yibchok-Anun, S.; Charoenlertkul, P.; Wongsasiripat, N. Cyanidin-3-rutinoside alleviates postprandial hyperglycemia and its synergism with acarbose by inhibition of intestinal α-glucosidase. J. Clin. Biochem. Nutr. 2011, 49, 36–41. [Google Scholar] [CrossRef] [PubMed]
- Valcheva-Kuzmanova, S.; Kuzmanov, K.; Tancheva, S.; Belcheva, A. Hypoglycemic and hypolipidemic effects of Aronia melanocarpa fruit juice in streptozotocin-induced diabetic rats. Meth. Find. Exp. Clin. Pharm. 2007, 29, 101–106. [Google Scholar] [CrossRef] [PubMed]
- Sikora, J.; Broncel, M.; Mikiciuk-Olasik, E. Aronia melanocarpa elliot reduces the activity of angiotensin i-converting enzyme-in vitro and ex vivo studies. Oxid. Med. Cell. Longev. 2014, 2014, 1–7. [Google Scholar] [CrossRef] [PubMed]
- Dragan, S.; Andrica, F.; Serban, M.-C.; Timar, R. Polyphenols-rich natural products for treatment of diabetes. Curr. Med. Chem. 2015, 22, 14–22. [Google Scholar] [CrossRef] [PubMed]
- Vlachojannis, C.; Zimmermann, B.F.; Chrubasik-Hausmann, S. Quantification of anthocyanins in elderberry and chokeberry dietary supplements. Phytother. Res. 2015, 29, 561–565. [Google Scholar] [CrossRef] [PubMed]
- Skoczyñska, A.; Jêdrychowska, I.; Porêba, R.; Affelska-Jercha, A.; Turczyn, B.; Wojakowska, A.; Andrzejak, R. Influence of chokeberry juice on arterial blood pressure and lipid parameters in men with mild hypercholesterolemia. Pharmacol. Rep. 2007, 59, 177–182. [Google Scholar]
- Kowalczyk, E.; Fijalkowski, P.; Kura, M.; Krzesinski, P.; Blaszczyk, J.; Kowalski, J.; Smigielski, J.; Rutkowski, M.; Kopff, M. The influence of anthocyanins from Aronia melanocarpa on selected parameters of oxidative stress and microelements contents in men with hypercholesterolemia. Pol. Merkur Lekarski 2005, 19, 651–653. [Google Scholar] [PubMed]
- Kim, B.; Park, Y.; Wegner, C.J.; Bolling, B.W.; Lee, J. Polyphenol-rich black chokeberry (Aronia melanocarpa) extract regulates the expression of genes critical for intestinal cholesterol flux in caco-2 cells. J. Nutr. Biochem. 2013, 24, 1564–1570. [Google Scholar] [CrossRef] [PubMed]
- Zapolska-Downar, D.; Bryk, D.; Małecki, M.; Hajdukiewicz, K.; Sitkiewicz, D. Aronia melanocarpa fruit extract exhibits anti-inflammatory activity in human aortic endothelial cells. Eur. J. Nutr. 2012, 51, 563–572. [Google Scholar] [CrossRef] [PubMed]
- Valcheva-Kuzmanova, S.; Kuzmanov, K.; Mihova, V.; Krasnaliev, I.; Borisova, P.; Belcheva, A. Antihyperlipidemic effect of Aronia melanocarpa fruit juice in rats fed a high-cholesterol diet. Plant Foods Hum. Nutr. 2007, 62, 19–24. [Google Scholar] [CrossRef] [PubMed]
- Kardum, N.; Konić-Ristić, A.; Šavikin, K.; Spasić, S.; Stefanović, A.; Ivanišević, J.; Miljković, M. Effects of polyphenol-rich chokeberry juice on antioxidant/pro-oxidant status in healthy subjects. J. Med. Food 2014, 17, 869–874. [Google Scholar] [CrossRef] [PubMed]
- Bijak, M.; Bobrowski, M.; Borowiecka, M.; Podsędek, A.; Golański, J.; Nowak, P. Anticoagulant effect of polyphenols-rich extracts from black chokeberry and grape seeds. Fitoterapia 2011, 82, 811–817. [Google Scholar] [CrossRef] [PubMed]
- Olas, B.; Wachowicz, B.; Nowak, P.; Kedzierska, M.; Tomczak, A.; Stochma, A.; Oleszek, W.; Jeziorski, A.; Piekarski, J. Studies on antioxidant properties of polyphenol-rich extract from berries of Aronia melanocarpa in blood platelets. Acta Physiol. Pol. 2008, 59, 823–835. [Google Scholar]
- Ryszawa, N.; Kawczynska-Drozdz, A.; Pryjma, J.; Czesnikiewicz-Guzik, M.; Adamek-Guzik, T.; Naruszewicz, M.; Korbut, R.; Guzik, T.J. Effects of novel plant antioxidants on platelet superoxide production and aggregation in atherosclerosis. J. Physiol. Pharmacol. 2006, 57, 611–626. [Google Scholar] [PubMed]
- Daskalova, E.; Delchev, S.; Peeva, Y.; Vladimirova-Kitova, L.; Kratchanova, M.; Kratchanov, C.; Denev, P. Antiatherogenic and cardioprotective effects of black chokeberry (Aronia melanocarpa) juice in aging rats. Evid. Based Complement. Alternat. Med. 2015, 2015, 717439. [Google Scholar] [CrossRef] [PubMed]
- Bell, D.R.; Burt, T.D. Phenolic acids contained in anthocyanin enriched extracts from elderberry, bilberry and chokeberry possess endothelium dependent and independent vasorelaxation properties in porcine coronary arteries. FASEB J. 2007, 21, A366. [Google Scholar]
- Bell, D.R.; Gochenaur, K. Direct vasoactive and vasoprotective properties of anthocyanin-rich extracts. J. Appl. Physiol. 2006, 100, 1164–1170. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.H.; Auger, C.; Kurita, I.; Anselm, E.; Rivoarilala, L.O.; Lee, H.J.; Lee, K.W.; Schini-Kerth, V.B. Aronia. melanocarpa juice, a rich source of polyphenols, induces endothelium-dependent relaxations in porcine coronary arteries via the redox-sensitive activation of endothelial nitric oxide synthase. Nitr. Oxide. 2013, 35, 54–64. [Google Scholar] [CrossRef] [PubMed]
- Ciocoiu, M.; Badescu, L.; Miron, A.; Badescu, M. The involvement of a polyphenol-rich extract of black chokeberry in oxidative stress on experimental arterial hypertension. Evid.-Based Complet. Altern. 2013, 2013, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Matés, J.M.; Segura, J.A.; Alonso, F.J.; Márquez, J. Oxidative stress in apoptosis and cancer: An update. Arch. Toxicol. 2012, 86, 1649–1665. [Google Scholar] [CrossRef] [PubMed]
- Stanisavljević, N.; Samardžić, J.; Janković, T.; Šavikin, K.; Mojsin, M.; Topalović, V.; Stevanović, M. Antioxidant and antiproliferative activity of chokeberry juice phenolics during in vitro simulated digestion in the presence of food matrix. Food Chem. 2015, 175, 516–522. [Google Scholar] [CrossRef] [PubMed]
- Ga̧siorowski, K.; Szyba, K.; Brokos, B.; Oszmiański, J. Antimutagenic activity of anthocyanins isolated from Aronia melanocarpa fruits. Cancer Lett. 1997, 119, 37–46. [Google Scholar] [CrossRef]
- Olas, B.; Kedzierska, M.; Wachowicz, B.; Stochmal, A.; Oleszek, W.; Jeziorski, A.; Piekarski, J.; Glowacki, R. Effect of Aronia on thiol levels in plasma of breast cancer patients. Open Life Sci. 2010, 5, 38–46. [Google Scholar] [CrossRef]
- Sharif, T.; Stambouli, M.; Burrus, B.; Emhemmed, F.; Dandache, I.; Auger, C.; Etienne-Selloum, N.; Schini-Kerth, V.B.; Fuhrmann, G. The polyphenolic-rich Aronia melanocarpa juice kills teratocarcinomal cancer stem-like cells, but not their differentiated counterparts. J. Funct. Foods 2013, 5, 1244–1252. [Google Scholar] [CrossRef]
- Malik, M.; Zhao, C.; Schoene, N.; Guisti, M.M.; Moyer, M.P.; Magnuson, B.A. Anthocyanin-rich extract from Aronia meloncarpa e. Induces a cell cycle block in colon cancer but not normal colonic cells. Nutr. Cancer 2003, 46, 186–196. [Google Scholar] [CrossRef] [PubMed]
- Zhao, C.; Giusti, M.M.; Malik, M.; Moyer, M.P.; Magnuson, B.A. Effects of commercial anthocyanin-rich extracts on colonic cancer and nontumorigenic colonic cell growth. J. Agric. Food Chem. 2004, 52, 6122–6128. [Google Scholar] [CrossRef] [PubMed]
- Giampieri, F.; Forbes-Hernandez, T.Y.; Gasparrini, M.; Alvarez-Suarez, J.M.; Afrin, S.; Bompadre, S.; Quiles, J.L.; Mezzetti, B.; Battino, M. Strawberry as a health promoter: An evidence based review. Food Funct. 2015, 5, 1386–1398. [Google Scholar] [CrossRef] [PubMed]
- Kresty, L.A.; Mallery, S.R.; Stoner, G.D. Black raspberries in cancer clinical trials: Past, present and future. J. Berry Res. 2016, 6, 251–261. [Google Scholar] [CrossRef] [PubMed]
Table 1. Summary of the protective effects of black chokeberry fruit in relation to chronic diseases.
|Effect||Mechanism of Action||Study Model||Sources|
|Anti-inflammatory||Inhibition of release IL-6,IL-8,IL-10 TNF-α Activation NF-κB, cytokines, PGE2||Human monocytes, mouse macrophage cells, murine splenocytes||[102,104,105]|
|Inhibition on nitric oxide production||Mouse macrophage|||
|Antidiabetic||Reduction of gastric mucosal demage||Wister rat model|||
|Inhibition of α-glucosidase, lipase and amylase||In vitro model studies||[115,117]|
|Modulation of multiple pathways associated with insulin signaling||Rats on fructose-rich diet, in vivo, in vitro studies||[118,119]|
|Restoring of beta cells integrity||In vivo models||[116,120,121]|
|Cardioprotective||Lipid metabolism–decrease of cholesterol synthesis||Caco-2-cells|||
|-Inhibition of LDL oxidation, lipid peroxidation||Patients with metabolic syndrome|||
|-Increase activity of glutathione peroxidase and catalase, reduction of LDL cholesterol -Inhibition of platelet aggregation, protein carbonylation and thiol oxidation||Mens with hypercholesterolemia|||
|Anticoagulant, antithrombotic -Decrease in fibrin polymerization||Human plasma||[23,25,123]|
|-Inhibition of platelet aggregation, protein carbonylation and thiol oxidation||Human plasma, purified fibrinogen||[95,120,129,130,131]|
|Decrease blood pressure|
|-inhibition of angiotensis I-converting enzyme ACE||Patients with metabolic syndrome|||
|Protection of coronary arteries|
|Coronary vasoactive, vasoprotective effect||Caco-2-cells|
|Decrease oxidative stress—stimulation of endothelial formation of NO||Porcine coronary arteries|
|Anticancer||Inhibition of oxidation||Caco-2-cells line|||
|Reduction of oxidative stress||Human granulocytes, HeLa cervical tumor line, murine leukemia cells, brest cancer patients||[94,98,130,139,141]|
|Induction of apoptosis||Lymphoblastic leukemia Jurkat cell line|||
|Blockage at G1/G0 and G2/M phases of cell cycle||Human colon cancer|||
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