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Fragaria genus (Rosaceae), commonly known as strawberry, represents one of the most important food plants all over the world, with a double global production compared with all other fruit berries combined. Usually appreciated because of their specific flavor, the strawberries also possess biological properties, including antioxidant, antimicrobial, or anti-inflammatory effects.
- Fragaria genus
- chemical composition
- biological properties
1. Introduction
The production of different fruits all around the world exceeds millions of tons, depending on geographical zones, consumption, and growing traditions, inevitably leading to large amounts of by-products and wastes. Fragaria genus (Rosaceae), commonly known as strawberry, represents one of the most important food plants all over the world, with a double global production compared with all other fruit berries combined [1]. Their widespread use, primarily because of their flavor, can also lead to considerable benefits to human health. Among other characteristics, nonvisual properties like taste, nutritional values, or aroma make these fruits to be in the top of consumer preferences [2].
Among the 247 varieties known and listed, only few present commercial interest: Fragaria x ananassa Duchesne (octoploid hybrid-containing 56 chromosomes, known as garden strawberry, native to northern America, cultivated all over the world), and, to a lesser extent, Fragaria vesca L. (diploid species, known as wild strawberry, native to Northern hemisphere) and Fragaria chiloensis (L.) Mill. (octoploid species, known as Chilean strawberry, native to northern, pacific and southern America) [1].
2. Composition of Fragaria L. Genus
Figure 1.
Main components
Fragaria
species identified according literature data.
Table 1.
Major (common) components in
|
Class |
Compound |
Ref. |
|---|---|---|
|
Anthocyanins |
Table 2.
Composition of
Fragaria
species (as presented by original works published in the reviewed period; references presented in chronological order).
|
Species |
Plant Part, Other Variables |
Identified Compounds and Main Findings |
Identification Method |
Ref. |
|---|
]. The following paragraphs presents the main biological properties of different Fragaria species, as emerging from the literature data published in the past decade. Particularly, the anthocyanins family represent the subject of several review papers published in the last years, dealing with their bioavailability and potential health benefits [63,64,65][34][35][36]. The following chapters includes only the studies regarding the biological activity of compounds or extracts obtained from Fragaria species (not studies presenting the activity of compounds that are found in those plants).
The presented composition varies with a series of factors, including the value of the cultivar, seasonal variation, and the degree of fruit ripeness. In the reviewed time period, several studies presented the evaluation of species belonging to Fragaria genus. Their main findings are presented in Table 2, while relevant studies are presented in the following paragraphs.
Table 3.
Antioxidant properties of different extracts obtained from
Fragaria
species (references presented in chronological order).
where:13C NMR—Carbon-13 nuclear magnetic resonance; GC-MS—gas chromatography–mass spectrometry; 1H NMR—proton nuclear magnetic resonance; HMBC —heteronuclear multiple bond correlation; HPLC-DAD—high-performance liquid chromatography with diode array detector; HPLC-UV/Vis—high-performance liquid chromatography equipped with UV/vis detector; HR-ESI-MS—high-resolution electrospray ionization mass spectrometry analysis; LC-ESI-MS(/MS)—liquid chromatography electrospray ionization (tandem) mass spectrometry analysis; LC-ESI-Orbitrap-MS—liquid chromatography electrospray ionization Orbitrap mass spectrometry; LC-ESI-QTrap-MS(/MS)—liquid chromatography electrospray ionization quadrupole ion trap mass spectrometry; LC–ESI–(Q)TOF—liquid chromatography electrospray ionization with (quadrupole) time-of-flight; LC-MS/MS—liquid chromatography–tandem mass spectrometry; LC-PDA-ESI-MS—liquid chromatography equipped with photodiode array detector coupled to mass spectrometry using the electrospray ionization interface; UPLC-ESI-QTOF-MS/MS—ultra-performance liquid chromatography equipped quadrupole time of flight coupled to tandem mass spectrometry using the electrospray ionization interface; UPLC-PDA-ESI-MS—ultra-performance liquid chromatography equipped with photodiode array detector coupled to mass spectrometry using the electrospray ionization interface.
3. Biological Activities of Fragaria Genus
3.1. Antioxidant Properties
Traditionally consumed in the form of fruits (as previously presented), Fragaria species have also found application in traditional medicine. For example, Fragaria vesca leaves and fruits were traditionally used for the treatment of external rashes, as well as internally, as blood purification and roborontarium, for the treatment of diarrhea [61][32], as macerate for renal stones, or as tea (together with other medicinal plants) for treating stomach inflammations, sedation, or regulation of digestion [62][33
where: ABTS—2,2′-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) assay; BHT—butylated hydroxytoluene; DPPH—reduction of 2,2-diphenyl-1-picrylhydrazyl; DW—dry weight; eq.—equivalents; FRAP—ferric reducing ability of plasma; FS—ferrous sulphate; FW—fresh weight; IC50—half maximal inhibitory concentration; ORAC—oxygen radical absorbance capacity; SAS—superoxide anion assay; TBARS—thiobarbituric acid reactive substances assay; TEAC—Trolox equivalent antioxidant capacity.
3.2. Anti-Inflammatory Properties
As previously stated, one of the traditional uses of Fragaria is as an anti-inflammatory agent [61,62][32][33]. Most of the authors assign the anti-inflammatory properties to the presence of anthocyanins (the most representative being pelargonidin and cyanidin derivates) [75][41], molecules with known anti-inflammatory potential [76[42][43],77], demonstrated both in vitro and in vivo [78,79][44][45]. Similar to the other biomedical potential, the anti-inflammatory action is also correlated with the composition of different Fragaria species. The traditional use of F. vesca as an anti-inflammatory agent was supported by the study of Liberal et al. [80][46]. The authors observed the decrease of a relevant mediator of the inflammatory response (nitric oxide) produced by macrophages, cultured in the presence of a NO-production inducing bacterial endotoxin (LPS). The ethanolic extract obtained from Fragaria vesca leaves, used at non-cytotoxic concentrations (80 and 160 mg/L), induced a 31%, and 40% inhibition, respectively. The authors assigned the NO decrease to a direct scavenging effect (as demonstrated by a 23% inhibition of the nitrite content in the culture media, correlated with the absence of a significant effect when quantifying the inducible nitric oxide synthase—iNOS and the pro-inflammatory cytokine IL-1β). The authors also observed a statistically insignificant increase in the phosphorylated IκBα (nuclear factor of kappa light polypeptide gene enhancer in B-cells inhibitor, alpha) content, suggesting either an increase of its expression or a decrease in its degradation. More than that, the authors observed an increased conversion of the microtubule-associated protein light chain LC3-I to LC3-II (a marker of autophagy), suggesting further anti-cancer properties. Methanolic extracts of Fragaria x ananassa, var.
3.3. Other Potential Applications
The anti-microbial properties were evaluated within the reviewed time period, especially for F. vesca. Hydromethanolic extracts obtained from leaves and roots of Fragaria vesca L. were evaluated by Gomes et al. [85][47] as antimicrobial agents a series of S. aureus strains. The results suggested a weak antimicrobial potential of the extracts (5–9 mm inhibition halos in the qualitative assays), which did not qualify the extracts for quantitative determinations. Superior results in terms of antimicrobial properties were obtained by Cardoso et al. [86][48]. Using hydroalcoholic extracts, the authors observed good antimicrobial properties of the crude extract against a series of Helicobacter pylori isolates (inhibition zones ≥ 15 mm) at a 25 mg/mL concentration. The ellagitannin-enriched fraction was efficient against all isolates at lower concentrations (7.5 mg/mL), which led the authors to assume that the ellagitannins were the main class of compounds responsible for the anti-microbial properties. As the H. pylori represents a pathogen involved in several gastric pathologies (including gastritis, gastroduodenal ulcer disease, gastric adenocarcinoma and mucosa-associated lymphoid tissue lymphoma), the authors proposed the wild strawberry extract as a potential candidate for human health applications.
The anti-allergenic potential of several compounds (linocinnamarin, 1-O-trans-cinnamoyl-b-d-glucopyranose, p-coumaric acid, cinnamic acid, chrysin, kaempferol, catechin, and trans-tiliroside) isolated from Fragaria x ananassa var. Minomusume fruits were evaluated by Ninomiya et al. [87][49], through the determination of their inhibitory effects on antigen-stimulated degranulation in rat basophilic leukemia RBL-2H3 cells. Among the studied compounds, linocinnamarin (95% inhibition of control at 100 μM) and cinnamic acid (approx. 80% of control at 100 μM) were the most efficient in degranulation suppression (through direct inactivation of spleen tyrosine kinase), being proposed as promising tools for alleviating symptoms of type I allergy.
The commercially-available strawberry freeze-dried powder was demonstrated by Abdulazeez [88][50] to reverse alloxan-induced diabetes (results not presented in Table 4 as authors used commercial powder product); in a similar study, Yang et al. [12][4] evaluated the potential anti-diabetic application of new and known compounds isolated from strawberry fruits (as presented in Section 2) by determining the α-glucosidase inhibitory activity. The best results were obtained for cupressoside A (IC50 = 25.39 μM), kaempferol 3-(6-methylglucuronide) (IC50 = 65.22 μM), and 2-p-hydroxybenzoyl-2,4,6-tri hydroxyphenylacetate (IC50 = 97.81 μM), with very good results obtained for a newly proposed structure (kaempferol 3-(6-butylglucuronide)-IC50 = 107.52 μM); results superior to the positive control (acarbose-IC50 = 619.94 μM) were also obtained for five other compounds.
Table 4.
Main biological activities presented in the literature (references listed in chronological order).
where: ADA—adenosine-deaminase; Akt—Protein Kinase B; aq.—water (aqueous); CAT—catalase; COX-2—cyclooxygenase-2 enzyme; ERK—extracellular signal-regulated kinase; eth—ethanol; GSH—glutathione; HepG2—human liver cancer cell line; IC50—half maximal inhibitory concentration; IL-1β—Interleukin 1 beta cytokine protein; IL-6—interleukin 6; iNOS—inducible nitric oxide synthase; meth.—methanol; MPO—myeloperoxidase; MTT—3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide; NFκB—nuclear factor kappa-light-chain-enhancer of activated B cells; NO—nitric oxide; PGE2—Prostaglandin E2; PI3K—phosphatidylinositol 3-kinase; RBL—rat basophilic leukemia cells; ROS—reactive oxygen species; SOD—superoxide dismutase; TNF-α—tumor necrosis factor alpha;.
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