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Chemical Composition and Biological Activities of Fragaria Genus
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This entry is adapted from the peer-reviewed paper 10.3390/molecules25030498

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

Giampieri et al. [3] reviewed the composition of the strawberry (Fragaria x ananassa), while Morales-Quintana and Ramos [4] reviewed the composition and potential applications of the Chilean strawberry (Fragaria chiloensis (L.) Mill.), while the functional properties of the berries, in general, and of the strawberries, in particular, were reviewed by Jimenez-Garcia et al. [5]. As resulting from various literature studies [3][4][5][6][7], the general composition of the strawberries (in terms of major components) can be summarized in Table 1 (with a general image provided in Figure 1).
Figure 1. Main components Fragaria species identified according literature data.
Table 1. Major (common) components in Fragaria L. aggregate fruits (adapted from [3][4][5][6][7]).
Table

Class

Compound

Ref.

Anthocyanins

Pelargonidin 3-glucoside, cyanidin 3-glucoside, cyanidin 3-rutinoside, pelargonidin 3-galactoside, pelargonidin 3-rutinoside, pelargonidin 3-arabinoside, pelargonidin 3-malylglucoside

[3][4][5]

Flavonols

Quercetin, kaempferol, fisetin, their glucuronides, and glycosides

[3][4][5][8]

Flavanols

Catechin, proanthocyanidin B1, proanthocyanidin trimer, proanthocyanidin B3

[3]

Ellagitannins

Sanguiin H-6, ellagitannin, ellagic acid, lambertianin C, galloylbis-hexahydroxydiphenoyl-glucose

[3]

Phenolic acids

4-coumaric acid, p-hydroxybenzoic acid, ferulic acid, vanillic acid, sinapic acid

[7]

Vitamins

Vitamin C, vitamin B9

[6]

Minerals

Mn, K, Mg, P, Ca

[3]

Others

Sugars (glucose, fructose, and sucrose), fibers

[3]
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 2. Composition of Fragaria species (as presented by original works published in the reviewed period; references presented in chronological order).
Table

Species

Plant Part, Other Variables

Identified Compounds and Main Findings

Identification Method

Ref.

F. chiloensis

Ripe fruits

Anthocyanins (cyanidin 3-O-glucoside, pelargonidin 3-O-glucoside cyanidin-malonyl-glucoside and pelargonidin-malonyl-glucoside); procyanidins, ellagitannins, ellagic acid and flavonol derivatives

HPLC-DAD, LC-ESI-MS

[9]

F. chiloensis

Leaves

Procyanidins, ellagitannins, ellagic acid and flavonol derivatives

HPLC-DAD, LC-ESI-MS

[9]

F. chiloensis

Rhizomes

Procyanidins, ellagitannins, ellagic acid and flavonol derivatives

HPLC-DAD, LC-ESI-MS

[9]

Fragaria × ananassa

Fruits

Anthocyanins (pelargonidin-3-glucoside, pelargonidin-3-rutinoside, cyanidin-3-rutinoside, pelargonidin-3,5-diglucoside, pelargonidin-3-(6-acetyl)-glucoside, 5-carboxypyranopelargonidin-3-glucoside, delphinidin-3-glucoside, peonidin-3-glucoside, cyanidin-3-galactoside), p-hydroxybenzoic acid, (+)-catechin, ellagic acid, p-coumaric acid, quercetin glucoside

LC-MS/MS, HPLC-UV/Vis

[10]

Fragaria × ananassa

Fruits, cultivar and seasonal variations

Vitamin C, β-carotene, total phenolics, total anthocyanins; genotype influence is stronger than the environmental influence

Colorimetric

[11]

Fragaria × ananassa

Fruits, different cultivars on different ripeness stage

Total vitamin C, total phenolics, total anthocyanins, total ellagic acid/pelargonidin-3-glucoside and cyanidin-3-glucoside; higher amounts in pink fruits compared with fully ripped fruits

Colorimetric/HPLC-DAD

[12]

Fragaria × ananassa

Fruits, different farming methods

Total phenolics/pelargonidin-3-glucoside and cyanidin-3-glucoside, vitamin C, higher in organic farming fruits

Colorimetric/HPLC-DAD

[13]

Fragaria × ananassa

Fruits, different cultivars (27) and ripening stages

Phenolic compounds (multiple classes, including anthocyanins, flavanols and ellagitannins); composition dependent on cultivar, cinnamic acid conjugates and anthocyanins levels increased with the ripening stage

HPLC-DAD-MS

[14]

Fragaria × ananassa, F. vesca

Fruits

Quercetin and isorhamnetin glycosides (higher levels in wild strawberry)

HPLC-DAD, LC-ESI-MS

[15]

Fragaria × ananassa, F. vesca

Fruits, different cultivars

Volatile esters (including ethyl acetate, hexyl acetate, methyl butanoate, ethyl butanoate, hexyl butanoate, methyl hexanoate, ethyl hexanoate, hexyl hexanoate); higher levels in cultivated strawberries.

GC-MS

[16]

F. vesca

Fruits, two different cultivars

Anthocyanins (cyanidin 3-O-glucoside, pelargonidin 3-O-glucoside, peonidin 3-O-glucoside, cyanidin 3-O-malonylglucoside, pelargonidin 3-O-malonylglucoside, peonidin 3-O-malonylglucoside), dihydroflavonol and flavonols (taxifolin 3-O-arabinoside, kaempferol 3-O-glucoside, quercetin 3-O-glucoside, quercetin-acetylhexoside, kaempferol 3-O-acetylhexosides), flavan-3-ols and proanthocyanidins (catechin, B type proanthocyanidin dimers, trimers, and tetramers), ellagic acid and derivatives (glycosylated, methyl pentoside, methylellagic acid methyl pentoside, ellagitannins), other compounds (benzoic acid, ferulic acid hexose derivative, citric acid, furaneol glucoside)

HPLC-DAD

[17]

Fragaria × ananassa, F. vesca

Fruits

Anthocyanins (cyanidin, pelargonidin), cyanidin glycosides (cyanidin 3-glucoside, cyanidin 3-arabinoside, cyanidin 3-sambubioside, delphinidin 3-galactoside, delphinidin 3-glucoside, delphinidin 3-malonylglucoside); higher levels of cyanidin glycosides in wild species

HPLC-DAD

[18]

F. vesca

Leaves

Ellagitannins (sanguiin H-2 isomer, sanguiin H-10 isomer, sanguiin H-6/agrimoniin/lambertianin A isomer, castalagin/vescalagin isomer, sanguiin H-10 isomer, sanguiin H-2 isomer, casuarictin/potentillin isomer)

LC-PDA-ESI-MS

[19]

Fragaria × ananassa

Fruits, different cultivars and production years

Vitamin C, anthocyanins (pelargonidin 3-glucoside, cyanidin 3-glucoside, pelargonidin 3-rutinoside), ellagic acid; strongly dependent on the cultivar and production year

HPLC-UV/Vis

[20]

Fragaria × ananassa

Fruits, at different ripening stage

Vitamin C, pelargonidin-3-rutinoside, ellagic acid, cyanidin-3-glucoside, quercetin (red fruits), neochlorogenic, pelargonidin-3-glucoside, pelargonidin-3-rutinoside, epicatechin, quercetin-3-β-d-glucoside, ellagic acid (green fruits)

LC-ESI-TOF

[21]

Fragaria × ananassa

Calyx (red and green)

Quercetin-3-β-d-glucoside, ellagic acid, kaempferol-3-O-glucoside, vitamin C (red), catechin, quercetin-3-β-d-glucoside, ellagic acid (green)

LC-ESI-TOF

[21]

Fragaria × ananassa

Flower

Catechin, quercetin-3-β-d-glucoside, ellagic acid, kaempferol-3-O-glucoside, vitamin C

LC-ESI-TOF

[21]

Fragaria × ananassa

Leaf

Procyanidin dimer and trimer, catechin, quercetin-3-β-d-glucoside, vitamin C, ellagic acid

LC-ESI-TOF

[21]

Fragaria × ananassa

Stolon

Neochlorogenic, procyanidin dimer, catechin, quercetin-3-β-d-glucoside, ellagic acid, vitamin C, kaempferol-3-O-glucoside

LC-ESI-TOF

[21]

Fragaria × ananassa

Stem

Procyanidin dimer, catechin, ferulic acid, quercetin-3-β-d-glucoside, ellagic acid

LC-ESI-TOF

[21]

Fragaria × ananassa

Crown

Procyanidin dimer and trimer, catechin, propelargonidin dimer, ellagic acid

LC-ESI-TOF

[21]

Fragaria × ananassa

Root

Procyanidin dimer and trimer, catechin, neochlorogenic, propelargonidin dimer

LC-ESI-TOF

[21]

Fragaria × ananassa

Fruits, different novel cultivars

Phenolic acids (p-coumaric acid, ellagic acid, ferulic acid derivative, p-coumaric acid derivatives), monomeric flavanols ((+)-catechin), flavonols (quercetin 3-O-glucoside, fisetin, quercetin 3-O-glucoside derivative), anthocyanins (cyanidin 3-glucoside, cyanidin 3-rutinoside, cyanidin pentoside, pelargonidin 3-galactoside, pelargonidin 3,5-diglucoside, pelargonidin 3-glucoside, pelargonidin 3-rutinoside, cyanidin 3-Oacetylglucoside, cyanidin hexoside, pelargonidin 3-O-monoglucuronide, pelargonidin derivatives)

HPLC-DAD, LC-ESI-QTOF

[22]

Fragaria × ananassa

Fruits, grown on different altitudes, on consecutive years

Hydroxybenzoic acid, p-coumaric acid, other hydroxycinnamic acids, (+)-catechin, (−)-epicatechin, procyanidins, flavonols, anthocyanins (cyanidin 3-glucoside, pelargonidin 3-glucoside, pelargonidin derivative); higher levels recorded at lower altitudes.

HPLC-DAD

[23]

Fragaria × ananassa

Fruits

Kaempferol 3-(6-methylglucuronide), quercetin 3-(6-methylglucuronide), isorhamnetin 3-(6-methylglucuronide), trichocarpin, 2-p-hydroxybenzoyl-2,4,6-tri hydroxyphenylacetate, 2-p-hydroxyphene thyl-6-caffeoylglucoside, zingerone 4-glucoside, b-hydroxypropiovanillone 3-glucoside, (+)-isolariciresinol 90-glucoside, (−)-isolariciresinol 90-glucoside, aviculin, (−)-secoisolariciresinol 4-glucoside, cupressoside A, cedrusin, icariside E4, dihydrodehydrodiconiferyl alcohol 90-glucoside, massonianoside A, urolignoside, (−)-pinoresinol 4-glucoside, 2,3”-epoxy-4-(butan-2-one-3-yl)-5,7,40-trihydroxy flavane 3-glucoside, kaempferol 3-(6-butylglucuronide), benzyl 2-glucosyl-6-rhamnosylbenzoate

1H NMR, 13C NMR, HMBC, HPLC-UV/Vis, LC-MS/MS, HR-ESI-MS,

[24]

F. vesca

Fruits, wild and cultivated, from different geographical areas

39 phenolic compounds (including cyanidin 3-O-glucoside, delphinidin-3-O-glucoside, pelargonidin-3-O-glucoside, pelargonidin-3-O-rutinoside, (+) catechin, (−) epicatechin, procyanidin B1 and B2, isoquercetin, gallic acid, p-coumaric acid, phloridzin); composition dependent on the geographical area

LC-ESI-Orbitrap-MS, LC-ESI-QTrap-MS, LC-ESI-QTrap-MS/MS

[25]

Fragaria × ananassa

Fruits, different cultivars

Cyanidin 3-O-glucoside, pelargonidin-3-O-glucoside, pelargonidin-O-rutinoside, total anthocyanins content, dependent on the cultivar

UPLC-PDA-ESI-MS, HPLC-DAD

[26]

F. vesca

Fruits

Volatile composition—one hundred compounds (including esters, aldehydes, ketones, alcohols, terpenoids, furans and lactones).

GS-MS

[27]

F. vesca

Leaves

27 metabolites (organic acids, flavonoids, catechin and its oligomers, ellagitannins), including quinic acid, chelidonic acid, quercetin derivatives, catechin and procyanidins, phloridzin, pedunculagin, methyl ellagic acid glucuronide.

LC-ESI-Orbitrap-MS

[28]

Fragaria × ananassa, F. vesca

White-fruited mutants, different genotypes

Anthocyanins, flavonols, flavan-3-ols, hydroxycinnamic acids, and ellagic acid—derived compounds, dependent on genotype

LC-ESI-MS/MS

[29]

F. chiloensis

Fruits

Anthocyanins (cyanidin-3-O-glucoside, pelargonidin hexoside, cyanidin manlonyl hexoside, pelargonidin-malonyl hexoside), ellagitannins (ellagic acid hexoside, pentoside, rhamnoside), proanthocyanidin dimers, epicatechin, flavonols (quercetin pentoside, glucuronide)

HPLC-DAD, LC-ESI-MS

[30]

Fragaria × ananassa

Fruits, different cultivars

Anthocyanins, flavonoids, cinnamic acid derivatives, tannins and related compounds, triterpenoids; concentration dependent on the cultivar

UPLC-ESI-QTOF-MS/MS, HPLC-DAD

[31]

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 [32], as macerate for renal stones, or as tea (together with other medicinal plants) for treating stomach inflammations, sedation, or regulation of digestion [33]. 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 [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 antioxidant properties (Table 3) are among the most studied effects of Fragaria extracts.
Table 3. Antioxidant properties of different extracts obtained from Fragaria species (references presented in chronological order).
Table

Species

Extraction Method

Antioxidant Assay

Antioxidant Potential

Responsible Compounds

Ref.

Fragaria × ananassa, Camarosa var. fruits

Anthocyanins isolated using CCC

ORAC, FRAP

ORAC: 2.7–24.46 mmol Trolox/g; FRAP: 2.75–12.5 mmol Fe2+/g (depending on the fraction)

Anthocyanins

[10]

Fragaria chiloensis spp. chiloensis form chiloensis fruits

Methanol: formic acid (99:1 v/v) extraction

DPPH, SAS

DPPH assay: IC50 = 38.7 mg/L; SAS: 79.3%)

Aglycone and glycosylated ellagic acid and flavonoids

[9]

Fragaria chiloensis spp. chiloensis form chiloensis leaves

Methanol: formic acid (99:1 v/v) extraction

DPPH, SAS

DPPH assay: IC50 = 49.4 mg/L; SAS: 67.60%

Aglycone and glycosylated ellagic acid and flavonoids

[9]

Fragaria chiloensis spp. chiloensis form chiloensis rhizomes

Methanol: formic acid (99:1 v/v) extraction

DPPH, SAS

DPPH assay: IC50 = 64.8 mg/L; SAS: 55%

Aglycone and glycosylated ellagic acid and flavonoids

[9]

Fragaria x ananassa Osogrande var. frozen fruits

Acetone (80%) extraction

DPPH, FRAP

DPPH: 11.91–12.83 μmol BHT eq./g FW; best results for ripe fruits FRAP: 27.37–36.75 μmol FS eq./g FW; best results for green fruits

Total phenolic content, vitamin C

[12]

Fragaria x ananassa Camino Real var. frozen fruits

Acetone (80%) extraction

DPPH, FRAP

DPPH: 9.75–12.01 μmol BHT eq./g FW, FRAP: 24.13–28.49 μmol FS eq./g FW (best results for pink fruits)

Total phenolic content, vitamin C

[12]

F. vesca leaves

Methanol, ultrasounds extraction

DPPH, FRAP

DPPH: IC50 = 13.46 mg/L; FRAP: 0.878 mmol Fe2+/g DW

Total phenols, total tannins

[37]

F. vesca roots, wild-growing

Hydromethanolic extraction, infusion, decoction

DPPH, FRAP, β-Carotene bleaching inhibition, TBARS

IC50, mg/L: DPPH—50.03/50.56/50.62; FRAP—40.98/44.78/49.23; β-C bleaching—116.26/44.88/66.10; TBARS—35.76/4.76/6.14

Total phenolics, total flavan-3-ols, total dihydroflavonols,

[38]

F. vesca roots, commercial

Hydromethanolic extraction, infusion, decoction

DPPH, FRAP, β-Carotene bleaching inhibition, TBARS

IC50, mg/L: DPPH—68.89/255.81/51.32; FRAP—327.75/78.99/67.92; β-C bleaching—68.34/23.44/114.67; TBARS—6.69/24.25/10.62

Total phenolics, total flavan-3-ols, total dihydroflavonols,

[38]

Fragaria × ananassa var. Amaou, fruits, at different ripening stage

Ethanol or water room temperature extraction

Modified ABTS assay

Ethanol: 150.5/151.9; water: 227.2/189.4 (red/green fruits) μmol TE/100 g FW

Total phenolic content

[21]

Fragaria × ananassa var. Amaou calyx (red and green)

Ethanol or water room temperature extraction

Modified ABTS assay

Ethanol: 241.1/1239.9; water: 1716.6/577.7 μmol TE/100 g FW (red/green calyx)

Total phenolic content

[21]

Fragaria × ananassa var. Amaou flower

Ethanol or water room temperature extraction

Modified ABTS assay

4234.4/387.5 μmol TE/100 g FW (ethanol/water)

Total phenolic content

[21]

Fragaria × ananassa var. Amaou leaves

Ethanol or water room temperature extraction

Modified ABTS assay

2401.7/241.1 μmol TE/100 g FW (ethanol/water)

Total phenolic content

[21]

Fragaria × ananassa var. Amaou stolon

Ethanol or water room temperature extraction

Modified ABTS assay

1089.4/1856.7 μmol TE/100 g FW (ethanol/water)

Total phenolic content

[21]

Fragaria × ananassa var. Amaou stem

Ethanol or water room temperature extraction

Modified ABTS assay

1338.6/1123.1 μmol TE/100 g FW (ethanol/water)

Total phenolic content

[21]

Fragaria × ananassa var. Amaou crown

Ethanol or water room temperature extraction

Modified ABTS assay

6213.3/128.7 μmol TE/100 g FW (ethanol/water)

Total phenolic content

[21]

Fragaria × ananassa var. Amaou root

Ethanol or water room temperature extraction

Modified ABTS assay

253.1/69.2 μmol TE/100 g FW (ethanol/water)

Total phenolic content

[21]

F. vesca vegetative parts (leaves and stems), wild-growing

Hydromethanolic and aqueous extracts; wild-growing infusion microencapsulated in alginate and incorporated in k-carrageenan gelatine

DPPH, FRAP, β-Carotene bleaching inhibition, TBARS

IC50, mg/L: DPPH—123.67/86.17/109.10; FRAP—81.40/62.36/77.28; β-C bleaching—56.71/12.34/13.40; TBARS—12.63/3.12/5.03 (hydromethanolic/infusion/decoction); Final formulation (mg/mL)—DPPH—2.74; FRAP = 1.23

Total phenolics, total flavan-3-ols, total dihydroflavonols,

[39]

F. vesca vegetative parts (leaves and stems), commercial

Hydromethanolic and aqueous extracts

DPPH, FRAP, β-Carotene bleaching inhibition, TBARS

IC50, mg/L: DPPH—139.33/121.94/118.89; FRAP—324.49/91.88/88.20; β-C bleaching—388.90/76.41/69.98; TBARS—24.36/23.07/17.52 (hydromethanolic/infusion/decoction).

Total phenolics, total flavan-3-ols, total dihydroflavonols,

[39]

Fragaria x ananassa cv. Falandi fruit

22 compounds isolated from ethanolic extracts

ABTS, DPPH, FRAP

Best results (IC50): ABTS—4.42 μM kaempferol 3-(6-methylglucuronide); DPPH—32.12 μM quercetin 3-(6-methylglucuronide); FRAP—0.05 mmol/g—urolignoside.

Individual compounds

[24]

Fragaria x ananassa cv. Albion, Aromas, Camarosa, Camino Real, Monte Rey, Portola, and San Andreas fruits

Ultrasonic extraction with acidified methanol

DPPH

IC50 (mg/mL) ranging from 76.73 (Camarosa)—100 (Camino Real)

Total anthocyanin content

[26]

F. vesca leaves native to Italy

Ultrasonic extraction with ethanol: water solvent (70:30, v/v)

TEAC

0.34–0.35 mg/mL Trolox eq., compared with quercetin (0.40)

Condensed tannins and flavonoid derivatives

[28]

Fragaria x ananassa cv. Tochiotome leaves

Supercritical CO2 extraction with different entrainers

DPPH

0.07 (simple supercritical extraction)—5.82 μmol BHT/g sample (with ethanol, dried at 40 °C)

Phenolic compounds

[40]

Fragaria × ananassa fruits (90 cultivars)

Ultrasonic aqueous methanol (70%) acidified with 1.5% formic acid, at room temperature

DPPH, ABTS

Average values (μmol Trolox/100 g):765.06 (DPPH), 1637.96 (ABTS)

Tannin-based compounds.

[31]

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 [32][33]. Most of the authors assign the anti-inflammatory properties to the presence of anthocyanins (the most representative being pelargonidin and cyanidin derivates) [41], molecules with known anti-inflammatory potential [42][43], demonstrated both in vitro and in vivo [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. [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. [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. [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. [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 [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. [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).
Table

Action

Plant

Extraction Method

Assay

Results

Responsible Compounds

Ref.

Anti-inflammatory on inflammatory bowel disease

Fragaria vesca leaves

Eth. extraction

MPO activity; GSH, SOD and CAT levels

Prevention of increase in colon weight and disease activity index, decrease in macroscopic and microscopic lesion score; significant improvement of MPO, CAT and SOD levels at 500 mg/kg 5 days oral treatment

Phenolic acids, flavonoids

[51]

Anti-inflammatory

Fragaria vesca leaves

Eth. extraction at room temperature, infusion

Nitric oxide production, western blot analysis (expression of pro-inflammatory proteins in lipopolysaccharide-triggered macrophages); nitric oxide scavenger activity

Inhibition of nitrite production on pre-treated cells (at 80 and 160 mg/L—31%/40%); 23% inhibition in culture media, at 160 mg/L

Phenolic content

[46]

Anti-inflammatory

Fragaria x ananassa, var. Alba fruits

Meth. extraction at room temperature, infusion

Determination of ROS intracellular levels, apoptosis detection, antioxidant enzyme activities, immunoblotting analysis, determination of mitochondrial respiration and extracellular acidification rate in cells

Reduction of intracellular ROS levels (significant at 100 mg/L), decreased apoptotic rate (significant at 50 and 100 mg/L); Increased ARE-antioxidant enzymes expression, reduced NO and inflammatory cytokines production (at 50 and 100 mg/L) to control levels

Vitamin C, anthocyanins, flavonoids

[52]

Anti-inflammatory, hepatoprotective

Fragaria chiloensisssp. Chiloensis fruits

Aq. extracts

Histological analyses, determination of transaminases, cytokines, F2-isoprostanes, and glutathione assays

maintained hepatocellular membrane, structural integrity, attenuated hepatic oxidative stress, and inhibited inflammatory response in LPS-induced liver injury; downregulation of cytokines (TNFa, IL-1β, and IL-6)

Phenolic content

[53]

Anti-inflammatory

Fragaria x ananassa var. Camarosa fruits

Ultrasonic-assisted, acidified meth. extraction, separation

In vivo: quantification of the leukocyte content, exudate concentration, MPO and ADA activities, nitric oxide products, TNF-α and IL-6 levels; in vitro: MTT assay, measurement of nitric oxide products, TNF-α and IL-6 levels, western blot analysis

Inhibition of the carrageenan-induced leukocyte influx to the pleural cavity; reduction of myeloperoxidase activity, exudate concentration, NO levels.

Phenolic compounds, anthocyanins (particularly pelargonidin-3-O-glucoside)

[54]

Anti-inflammatory, wound healing

Fragaria x ananassa var. San Andreas fruits

Ultrasound-assisted extraction, acidified meth.: aq. (80:20); separation of different fractions

MTT assay, ROS, NO levels, effects on inflammatory markers and on skin fibroblast migration

ROS reduction, suppression of IL-1β, IL-6 and iNOS gene expressions; enhanced skin fibroblast migration

Polyphenolic compounds, especially anthocyanins

[55]

Anti-microbial

Fragaria vesca leaves and roots

Centrifugation extraction with meth.: aq. (80:20)

Disc diffusion assay

6–9 mm inhibition zones for leaves, 5–9 mm for roots (depending on S. aureus strain)

Phenolic compounds

[47]

Anti-microbial

Fragaria vesca leaves

Hydroalcoholic extraction, separation

Disc diffusion assay

Good inhibition potential at 25 mg/mL, better effect for the ellagitannin-enriched fraction

Ellagitannins

[48]

Anti-allergenic

Fragaria x ananassa var. Minomusume fruits

Methanol fraction of fruits juice (obtained by squeezing)

Antigen-stimulated degranulation in RBL-2H3 cells

degranulation suppression (95–60% inhibition for linocinnamarin, cinnamic acid, chrysin, kaempferol, trans-tiliroside)

Best results - phenylpropanoid glycoside

[49]

Anti-diabetic

Fragaria x ananassa var. Falandi fruits

Compounds isolated from eth. extracts

α-glucosidase inhibitory activity

IC50 values better than the positive control (acarbose) for nine compounds (537.43 to 25.39 μM)

Individual compounds

[24]

Anti-obesity, anti-allergy, skin-lightening

Fragaria ×ananassa var. Amaou, entire plant (red fruit, green fruit, red calyx, green calyx, flower, leaf, stolon, stolon leaf, stem, crown and root)

Eth. or aq. room temperature extraction

Anti-lipase assay, adipocyte differentiation inhibition assay, melanogenesis inhibition assay, β-hexosaminidase inhibition assay, tyrosinase inhibition assay

Crown, stolon leaf and flowers extracts exhibited the highest effects

Total phenolic content

[21]

Antihyperuricemic

Fragaria x ananassa cv. Tochiotome leaves

Supercritical CO2 extraction with different entrainers

Uric acid production in AML12 hepatocytes

Reduction of uric acid at 100 mg/mL (96 mmol/2 h/mg protein), compared with the control (16,096 mmol/2 h/mg protein)

Kaempferol, quercetin

[40]

Cytotoxic, anti-proliferative

Fragaria x ananassa fruits

Meth. extraction

Ex vivo: cell viability assay; in vivo: developing tumor size determination

Cytotoxic on cancer cells, blocked the proliferation of tumor cells

Phenolic compounds

[56]

Antineoplastic

Fragaria x ananassa var. Pajaro fruits

Acidified hydro-eth. extraction

Transglutaminase assay and polyamine detection, immunoblot analysis

reduction of cell proliferation, lowering of the intracellular levels of polyamine, enhancement of tissue transglutaminase activity

Anthocyanins

[57]

Cytotoxic

Fragaria vesca L. leaves

Hydroalcoholic extract at room temperature, ellagitannins-enriched fraction

Effects on HepG2 cells—cell viability assessment, cell proliferation, cell cycle and cell death analysis, Western blot analysis, proteasome chymotrypsin-like activity

Inhibition of HepG2 cell viability IC50 = 690 mg/L (extract)/113 mg/L (fraction); fraction induced necrosis and apoptosis, influenced the cellular proteolytic mechanisms

Ellagitannins

[19]

Chemopreventive

Lyophilized Fragaria x ananassa fruits

Ultrasound-assisted extraction with acidified acetone

Histological studies, Western blot analysis, PGE2 measurement, and nitrate/nitrite colorimetric assay

Decreased tumor incidence, decreased levels of TNF-α, IL-1β, IL-6, COX-2 and iNOS, inhibition of the phosphorylation of PI3K, Akt, ERK, and NFκB

anthocyanins, ellagitannin/ellagic acid/ellagic acid derivatives flavonols

[58]

Cytotoxic

Fragaria x ananassa leaves

Hydroalcoholic extracts (meth., eth., isopropanol) from in vitro cell suspension

Cell proliferation, cell viability

Under 50% viable cells for colorectal adenocarcinoma and colon adenocarcinoma upon treatment with extracts containing 0.29 mM ethoxy-dihydrofuro-furan

Polyphenols

[59]

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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Radu Claudiu Fierascu
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Georgeta Temocico
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Irina Fierascu
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Alina Ortan
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Narcisa Elena Babeanu
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