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).
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).
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).
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).
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 IC
50 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).