Asian Journal of Dairy and Food Research, volume 41 issue 3 (september 2022) : 249-255

Nutritional and Bioactive Properties of Rubus ulmifolius Schott (Blackberry): A Review

Ekta Singh Chauhan1,*, Urvashi Chauhan1
1Department of Food Science and Nutrition, Banasthali Vidyapith, Tonk-304 022, Rajasthan, India.
Cite article:- Chauhan Singh Ekta, Chauhan Urvashi (2022). Nutritional and Bioactive Properties of Rubus ulmifolius Schott (Blackberry): A Review . Asian Journal of Dairy and Food Research. 41(3): 249-255. doi: 10.18805/ajdfr.DR-1920.
Rubus ulmifolius Schott, commonly known as blackberry, has been widely used as a food source as well as in jams, juices, etc. for its purported medical benefits. It has also been extensively investigated for its nutritional and bioactive constituents, which might be responsible for these benefits. In general, the plant is rich in carbohydrates, lipids, vitamins and minerals. The primary carbohydrates are glucose and sucrose; while ascorbic acid has been reported to be the primary vitamin, contributing to the acidic nature of the fruits. The bioactive compounds identified in the various plant parts include polyphenols such as phenolic acids, flavonoids and anthocyanins and other chemicals in lesser amounts. The antioxidant and antimicrobial properties of various parts of the plant have been investigated. The antioxidant effect has been attributed both to the presence of ascorbic acid as well as the other polyphenolic compounds. An antimicrobial activity has also been reported against the common human pathogens. This review summarizes the prevailing literature on the nutritional and bioactive composition of the plant and the evidence for its antioxidant and antimicrobial properties. This review summarizes the prevailing literature on the nutritional and bioactive composition of the plant and the evidence for its antioxidant and antimicrobial properties.
Rubus ulmifolius Schott (wild blackberry or elm-leaf blackberry) is one of the natural products that have been widely investigated for its beneficial properties with respect to nutrition and health. The plant is a perennial shrub of the family Rosaceae (Sochor et al., 2018). It is native to Europe, North Africa and parts of Asia. The detailed taxonomy of the plant is outlined in Table 1. The plant flowers during the months of May and June following which the fruits ripen and their colour changes from green to black; hence the term called ‘blackberry’ (Bandeira Riedel et al., 2016). Apart from direct consumption, the deliciously flavoured fruits are also used in juices, jams and marmalades (da Silva et al., 2019; Peano et al., 2017).
 

Table 1: Classification of Rubus ulmifolius.


       
Rubus ulmifolius was used as a traditional medicine in Chile for its hypoglycaemic property (Lemus et al., 1999). It has been also used as antipyretic as well as carminative agent (Ahmad et al., 2013). In Italy, the plant has been served as a folk medicine for treating the diseases like haemorrhoids, intestinal inflammations, abscesses, ulcer, diarrhoea, red eyes, along with vaginal infections (Manganelli and Tomei, 1999). Rubus ulmifolius offers phenolic acid and flavonoids which provides antioxidant activity also (Ali et al., 2017).
       
This review describes the nutrients and the bioactive compounds identified in various parts of the Rubus ulmifolius Schott plant along with the antioxidant, antimicrobial and antipyretic activity of the plant.
 
Nutritional value
 
The fruits of Rubus ulmifolius are rich in various nutrients, as outlined in various studies (Table 2). Consumption of fresh fruits of berries such as Rubus is associated with a greater amount of nutritional content than that of processed or refined foods (Fuhrman, 2018; Moscato and Machin, 2018; Moubarac et al., 2017; Murray et al., 2013). These values tend to differ substantially in various studies probably due to the differences in the geographical location of the plant, the part of the plant selected for the study, as well as the extraction methods used (Faniadis et al., 2010). Similar variations are also reported with other berries of the Rubus genus (Yang et al., 2018; Uhler and Yang, 2018; Wajs-Bonikowska et al., 2017; Mazur et al., 2014; Krauze-Baranowska et al., 2014).
 

Table 2: Nutritional content of Rubus ulmifolius.


       
The dry matter content in the has been reported in various studies to vary from 12% to 28%, the ash content around 3.5 g/100 g of dry matter and the pH between 3.3 to 3.7 is acidic with the presence of citric and other acids (Schulz and Chim, 2019; Contessa et al., 2013).
 
Carbohydrates
 
The studies on multiple berries with regards to their sugar content was reviewed by Lee (2015) and reported that the total sugars in the Rubus fruits range from 2.6-13.9 g per 100 g of the fruit, with the major sugars being glucose, sucrose, fructose and sorbitol (Table 2). Similarly, glucose and fructose were reported to have the highest concentrations and malic and citric acids are the major organic acids in the berries (Mikulic-Petkovsek et al., 2012).

Schulz and co-workers (2019) revealed that the mature blackberry fruits contained around 17.38 g/100 g of glucose and 22.52 g/100 g of fructose; while the fully mature blackberry fruits contained 19.12 g/100 g of glucose and 26 g/100 g of fructose.
 
Lipids
 
Blackberries are generally low in fat. However, 74 different lipid compounds are present in the Rubus ulmifolius fruit volatiles by solid-phase microextraction (D’Agostino et al., 2015). Ahmad et al., (2015) reported a total lipid content of 4.7% in the Rubus ulmifolius fruit. Moreover, linoleic acid is the most common lipid in the Rubus ulmifolius fruits (Morales et al., 2013).
 
Vitamins
 
The presence of Vitamin C in Rubus ulmifolius fruits from two different sites in Madrid, Spain was observed by Ruiz-Rodriguez and co-workers (2014), who reported that majority of the Vitamin C (60%) was present as ascorbic acid and dehydroascorbic acid.
 
Minerals
 
The concentration of minerals such as sodium, potassium, manganese, magnesium, calcium, etc. have been identified by different researchers. These have also been summarized in Table 2. According to Schulz et al., (2019), the concentrations of sodium, potassium and calcium decreased significantly while that of magnesium increased further with the ripening of the fruit. This reduction may be attributed to the utilization of the minerals during the process of ripening.
 
Bioactive compounds
 
The fruits of Rubus ulmifolius have been the subject of considerable attention on account of their rich anti-inflammatory as well as antioxidant properties, which was due to the presence of polyphenols, ascorbic acid and tannins (Barros et al., 2010). The nature of these bioactive compounds and their concentration has been the subject of intensive study and scrutiny by various researchers.
 
Phenolic compounds
 
Compounds with a phenolic structure such as flavonoids, phenolic acids, anthocyanins, hydroxycinnamic acids, ellagic acid, cyanidin-3-O-glucoside derivatives along with carotenoids have been reported in the literature in various berries such as blackberry and raspberry (Staszowska-Karkut and Materska, 2020; Oszmiañski et al., 2015; Amjad et al., 2013). In a recently published study by Candela et al., (2021), dihydroflavonol glycosides, quercetin and proanthocyanidins has been confirmed as the primary phenolic compounds.
 
Total phenols 
 
The total phenolic content has been reported in the total Rubus ulmifolius fruits in two edible stages (Della Betta et al., 2018; Contessa et al., 2013), hydroalcoholic extract of flowers and decoction from lyophilized flowers (Martins et al., 2014), polar and non-polar extracts of fruits (Akkari et al., 2016) and leaves (Tabarki et al., 2017).
 
Phenolic acids
The average concentration of phenolic acids in wild Rubus ulmifolius fruits at two different sites in Madrid and was found to be 414.34 mg/100 g; gallic acid being the predominant phenolic acid with a concentration of 268.72±183.35 mg/100 g (Ruiz-Rodriguez et al., 2014). Gallic acid concentration 481.71±0.81 µg/100 g was reported in the fruit by Schulz et al., (2019). Twenty-four phenolic compounds were identified in the phenolic extracts of Rubus ulmifolius flowers, out of which seven were phenolic acid derivatives, eleven as flavonoids and six were tannins (Martin et al., 2014). Ellagic acid was identified only in the decoction and not in the extract.
 
Flavonoids
 
The presence of flavonoids in the aerial parts of the plant has been confirmed in in vitro and in animal studies (Ali et al., 2017). In their study, Ruiz-Rodriguez et al., (2014) reported the 44 mg/100 g total flavonoids in Rubus ulmifolius fruit. The total flavonoids content was almost equal in both the hydroalcoholic extract of flowers and decoction from lyophilized flowers of Rubus ulmifolius evaluated (14.45± 0.44 mg/g and 13.38±0.05 mg/g) (Martins et al., 2014). Akkari et al., (2016) found that the total polyphenolic content was highest in the aqueous extracts of the Rubus ulmifolius fruits (28.06 mg QE/g of dry weight) and lowest in the hexanic extracts (0.71 mg QE/g of dry weight).
       
The studies also reported the content of flavonoids such as catechin, quercetin 3-O-glucoside, quercetin 3-O-rutinoside, kaempferol 3-O-glucoside and kaempferol 3-O-rutinoside in both the hydroalcoholic extract of the flowers as well as the decoction prepared from the lyophilized flowers (Table 3).
 

Table 3: Concentration of phenolic compounds in Rubus ulmifolius.


       
Schulz et al., (2019) identified that thirteen flavonoid compounds in Rubus ulmifolius fruits were present among which are quercetin, isoquercitin, kaempferol, catechin and epicatechin (Table 3). Quercetin 3-galactoside, quercetin 3-glucoside and quercetin-3-rutinoside are the major flavonoid compounds present in the Rubus ulmifolius wild fruits. Kaempferol-3-O-rutinoside and naringenin have been previously identified by Tabarki et al., (2017) as the dominant phenolic compounds in the extracts of Rubus ulmifolius leaves.
 
Anthocyanins
 
Anthocyanins are pigments responsible for imparting colours such as red, blue and purple to the fruits. The total anthocyanins in Rubus ulmifolius wild fruits was 141.89 mg /100 g with pelargonidin-3-rutinoside, cyanidin-3-glycoside and cyanidin-3-glucoside being the major compounds (Ruiz-Rodriguez et al., 2014).
       
More recently, six anthocyanins have been identified by Candela et al., (2021) in the Rubus ulmifolius fruit extract, the major constituents being cyanidin dihexoside and cyanidin dioxalylglucoside and others being pelargolidin and delphinidin. Anthocyanidins and proanthocyanidins have also been similarly reported in varying concentrations in other fruits of the Rubus genus as well.
 
Other compounds
 
Apart from the phenolic acids and flavonoids, lignin-derived aldehydes (sinapaldehyde, coniferaldehyde and syrinagldehyde) have also been reported in Rubus ulmifolius fruits in concentrations between 0.15 to 0.75 µg/g of the fruit (Schulz et al., 2019) along with hydrolysable tannins (203.39 mg/g) (Martins et al., 2014).
 
Bioactive effects
 
The major benefits of the Rubus ulmifolius plants that have been primarily explored include the antioxidant and antimicrobial activities.
 
Antioxidant activity
 
Antioxidant activities have been reported with various Rubus plants (Samaniego et al., 2020; Caidan et al., 2015; Skrovankova et al., 2015).
       
Ruiz-Rodriguez et al., (2014) measured the mean antioxidant activity of the Rubus ulmifolius wild fruits by using four different methods as mentioned in Table 4. The antioxidant activity of the hydroalcoholic extract of Rubus ulmifolius flowers was much greater than the decoction from lyophilized flowers (Martins et al., 2014).
 

Table 4: Antioxidant activity of Rubus ulmifolius.


       
The antioxidant activity of the Rubus ulmifolius leaves extracts obtained from four different sites in Tunisia was dependent upon the phenol content of the leaves (Tabarki et al., 2017) (Table 4).
       
Schulz et al., (2019) reported the antioxidant activity of the mature and fully mature fruits of Rubus ulmifolius and observed that the antioxidant capacity was higher in the fully mature fruit, indicated by the values of 241.06/ μM Fe+2/ per g of dry matter by the FRAP assay and 28.22/ mg GAE/ per g of dry matter by the Folin-Ciocalteu assay (Table 4). The antioxidant activity of the crude methanolic extract was equivalent to that of ascorbic acid (Ali et al., 2017). Contrarily, the antioxidant activity of the methanolic extract of Rubus ulmifolius has been reported to be more than ascorbic acid (Hajaji et al., 2017).
 
Antimicrobial activity
 
The extracts of various parts of Rubus ulmifolius plants identified to have activity against microbes pathogenic to humans.
       
Biofilm formation by Staphylococcus aureus was inhibited by the butanolic extract of Rubus ulmifolius roots at concentrations from 50-200 µg/mL; that has been attributed to the presence of ellagic acid and its derivatives (Quave et al., 2012). It has also been identified that ellagic acid xyloside and ellagic acid rhamnoside in the leaf extracts of Rubus ulmifolius inhibit biofilm formation by Staphylococcus aureus (Fontaine et al., 2017). In another study, the structure of Rubanthrone A, an anthrone derived from the aerial parts of Rubus ulmifolius was shown to have an in vitro activity against Staphylococcus aureus at 4.5 mg/mL concentration (Flamini et al., 2012). The planktonic cultures of Streptococcus pneumoniae were completely eradicated at an in vitro concentration of 80 µg/mL of the butanolic extract on overnight incubation (Talekar et ., 2014).
       
In another study, the methanolic extract of Rubus ulmifolius was detected to have an activity against Entamoeba histolytica in vitro with IC50 value of 61.785 ± 1.322 μg/mL; as also against Staphylococcus aureus, Streptococcus agalectiae, Salmonella typhimurium, Escherichia coli and Candida albicans with MIC values between 2.29-4.76 mg/mL for these organisms (Hajaji et al., 2017).
       
Antimicrobial activity of the Rubus ulmifolius leaves extracts with MIC values between 6.25-25 mg/mL and inhibition zones between 8-16 mm in diameter against six different bacteria was observed and was higher in Gram-positive bacteria (Tabarki et al., 2017).
 
Antipyretic activity
 
In rats, pyrexia was induced by injecting 20% Brewer’s yeast at a dose of 1 ml/100 g body weight (Ali et al., 2011). The study comprised rats with a temperature rise of at least 0.5°C to 1°C.  Ali et al. (2017) conducted an experiment in which they divided the albino rats into 6 groups (GI - GVI) involving six rats in every group. The GI (control group) was given 2 per cent gum acacia orally. The GII group functioned as the control group, receiving paracetamol orally (33 mg/kg of body weight in 2% gum acacia). GIII and GIV were given 150 mg/kg and 300 mg/kg body weight of Rubus ulmifolius crude methanolic extract, respectively (per oral). GV and GVI, on the other hand, got 150 mg/kg and 300 mg/kg body weight of Rubus ulmifolius crude flavonoids extract, respectively.
       
Antipyretic activity was observed in GIII, GIV, GV and GVI. The extract of crude flavonoids caused an 85.83 percent drop in body temperature in a test dose of 300 mg. On the fourth hour after administration, crude methanolic extract of Rubus ulmifolius in a test dose of 300 mg lowered rectal temperature by 74%. Overall findings showed that Rubus ulmifolius crude methanolic extract and crude flavonoids rich extract had significant antipyretic effect. Moreover, the presence of phytochemicals like flavonoids, which have been shown to inhibit cyclooxygenases, is responsible for Rubus ulmifolius considerable antipyretic activity (Rust et al., 2008).
Rubus ulmifolius fruit offers good amount of nutrients like carbohydrates (mainly glucose and fructose), lipids, vitamin C and minerals (K and Ca). The different parts of the Rubus ulmifolius plant such as the fruits, leaves and flowers also contain various phenolic acids, flavonoids and anthocyanins. These compounds can be further explored for various health benefits such as antioxidant, antimicrobial and antipyretic activity. This plant can therefore, be incorporated as food supplements or further explored as phytopharmaceuticals for human ailments. However, further studies are warranted to explore this highly potential plant source, which has so far been relatively untapped. 
None.

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